Forthcoming Current Anthropology Wenner-Gren Symposium Curren t Supplementary Issues (in order of appearance)

     

Humanness and Potentiality: Revisiting the Anthropological Object in the Anthropolog y Current Context of New Medical Technologies. Klaus Hoeyer and Karen-Sue Taussig, eds. Alternative Pathways to Complexity: Evolutionary Trajectories in the Anthropology Middle Paleolithic and Middle Stone Age. Steven L. Kuhn and Erella Hovers, eds.

THE WENNER-GREN SYMPOSIUM SERIES

Previously Published Supplementary Issues December 2012 HUMAN BIOLOGY AND THE ORIGINS OF HOMO Working Memory: Beyond Language and Symbolism. omas Wynn and Frederick L. Coolidge, eds. GUEST EDITORS: SUSAN ANTÓN AND LESLIE C. AIELLO

Engaged Anthropology: Diversity and Dilemmas. Setha M. Low and Sally Early Homo: Who, When, and Where Engle Merry, eds. Environmental and Behavioral Evidence

V Dental Evidence for the Reconstruction of Diet in African Early Homo olum e Corporate Lives: New Perspectives on the Social Life of the Corporate Form. Body Size, Body Shape, and the Circumscription of the Genus Homo Damani Partridge, Marina Welker, and Rebecca Hardin, eds. Ecological Energetics in Early Homo

5 Effects of Mortality, Subsistence, and Ecology on Human Adult Height 3 e Origins of Agriculture: New Data, New Ideas. T. Douglas Price and Plasticity in Human Life History Strategy Ofer Bar-Yosef, eds. Conditions for Evolution of Small Adult Body Size in Southern Africa

Supplement Growth, Development, and Life History throughout the Evolution of Homo e Biological Anthropology of Living Human Populations: World Body Size, Size Variation, and Sexual Size Dimorphism in Early Homo Histories, National Styles, and International Networks. Susan Lindee and Ricardo Ventura Santos, eds. Male Life History, Reproductive Effort, and Evolution of the Genus Homo Evolution of Cooperation among Mammalian Carnivores How Our Ancestors Broke through the Gray Ceiling 6 The Capital Economy in Hominin Evolution Origins and Evolution of Genus Homo Current Anthropology is sponsored by e Wenner-Gren Foundation for Anthropological

Research, a foundation endowed for scientific, Page s educational, and charitable purposes. e Foundation, however, is not to be understood as

endorsing, by virtue of its financial support, any of S267–S496 the statements made, or views expressed, herein.

Sponso r e d b y the W enne r - G r e n F o u n d a tion f o r Anth r opologic a l Rese a r c h

THE UNIVERSIT Y O F CHICA G O PRESS Wenner-Gren Symposium Series Editor: Leslie Aiello Wenner-Gren Symposium Series Managing Editor: Victoria Malkin Current Anthropology Editor: Mark Aldenderfer Current Anthropology Managing Editor: Lisa McKamy Book Reviews Editor: Holley Moyes Corresponding Editors: Claudia Briones (IIDyPCa-Universidad Nacional de Rı´o Negro, Argentina; [email protected]),Anne de Sales (Centre National de la Recherche Scientifique, France; [email protected]), Michalis Kontopodis (Humboldt Univ- ersita¨t zu Berlin, Germany; [email protected]), Jose´ Luis Lanata (Universidad Nacional de Rı´o Negro San Carlos de Bariloche, Argentina; [email protected]), David Palmer (Hong Kong University, China; [email protected]), Zhang Yinong (Shanghai University, China; [email protected])

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Human Biology and the Origins of Homo

Leslie C. Aiello Human Biology and the Origins of Homo: Wenner-Gren Symposium Supplement 6 S267 Introduction Leslie C. Aiello and Susan C. Anto´n Human Biology and the Origins of Homo:An Introduction to Supplement 6 S269 Setting the Stage Susan C. Anto´n Early Homo: Who, When, and Where S278 Richard Potts Environmental and Behavioral Evidence Pertaining to the Evolution of Early Homo S299 Food, Morphology, and Locomotion Peter S. Ungar Dental Evidence for the Reconstruction of Diet in African Early Homo S318 Trenton W. Holliday Body Size, Body Shape, and the Circumscription of the Genus Homo S330 Herman Pontzer Ecological Energetics in Early Homo S346 Body Size and Growth Andrea Bamberg Migliano and Myrtille Guillon The Effects of Mortality, Subsistence, and Ecology on Human Adult Height and Implications for Homo Evolution S359 Christopher W. Kuzawa and Jared M. Bragg Plasticity in Human Life History Strategy: Implications for Contemporary Human Variation and the Evolution of Genus Homo S369

http://www.journals.uchicago.edu/CA Susan Pfeiffer Conditions for Evolution of Small Adult Body Size in Southern Africa S383 Gary T. Schwartz Growth, Development, and Life History throughout the Evolution of Homo S395 J. Michael Plavcan Body Size, Size Variation, and Sexual Size Dimorphism in Early Homo S409 Richard G. Bribiescas, Peter T. Ellison, and Peter B. Gray Male Life History, Reproductive Effort, and the Evolution of the Genus Homo: New Directions and Perspectives S424 Models for Cooperation, Sociality, Life History, Body Size, and Brain Size Jennifer E. Smith, Eli M. Swanson, Daphna Reed, and Kay E. Holekamp Evolution of Cooperation among Mammalian Carnivores and Its Relevance to Hominin Evolution S436 Karin Isler and Carel P. van Schaik How Our Ancestors Broke through the Gray Ceiling: Comparative Evidence for Cooperative Breeding in Early Homo S453 Jonathan C. K. Wells The Capital Economy in Hominin Evolution: How Adipose Tissue and Social Relationships Confer Phenotypic Flexibility and Resilience in Stochastic Environments S466 New Perspectives on the Evolution of Homo Susan C. Anto´n and J. Josh Snodgrass Origins and Evolution of Genus Homo: New Perspectives S479 Current Anthropology Volume 53, Supplement 6, December 2012 S267

Human Biology and the Origins of Homo Wenner-Gren Symposium Supplement 6

by Leslie C. Aiello

Human Biology and the Origins of Homo is the 143rd Wenner- human evolution. The concluding paper by Anto´n and Snod- Gren Symposium and the sixth to be published as an open- grass (2012) draws from the wealth of ideas in this collection access supplement of Current Anthropology. The symposium and provides a fresh perspective on three important shifts in was organized by Susan C. Anto´n (New York University) and human evolutionary history: (1) the emergence of Homo;(2) Leslie C. Aiello (Wenner-Gren Foundation) and was held the transition between non-erectus early Homo and H. erectus; March 4–11, 2011, at the Tivoli Pala´cio de Seteais in Sintra, and (3) the appearance of regional variation in H. erectus.It Portugal (fig. 1). concludes with a new positive feedback model for the origin Wenner-Gren symposia are intensive week-long workshop and evolution of Homo that involves critical elements such meetings that traditionally focus on big questions in the field as cooperative breeding, changes in diet, body composition, of anthropology, and the origin of Homo is currently one of and extrinsic mortality risk that drive life history. the biggest questions in the field of hominin paleontology. This symposium builds on the long history of the Wenner- Although Homo erectus has been known since the 1890s (Pith- Gren Foundation with hominin evolution. Foundation in- ecanthropus erectus; Dubois 1894) and Homo habilis was an- terest began in the 1940s with “The Early Man in Africa” nounced almost 50 years ago (Leakey, Tobias, and Napier program (1947–1955) that was initiated by Fr. Teilhard de 1964), new fossil discoveries in the last decade have compli- Chardin to call attention to the extraordinary significance of cated our understanding of early Homo and challenged our the human origins in southern Africa, to date the southern long-held assumptions about its similarities and differences Africa cave deposits, and to facilitate multidisciplinary team to the australopiths as well as to later members of our genus. research. The “Origins of Man” program followed (1965– This necessarily influences our interpretations for the origin 1972), under the guidance of Walter William (Bill) Bishop, and evolution of Homo and also highlights the need for a new C. K. (Bob) Brain, J. Desmond Clark, Francis Clark Howell, framework for interpretation of the hard evidence. Louis Leakey, and Sherwood Washburn, and the Foundation continues to be an enthusiastic supporter of human origins The purpose of this symposium was to meet this challenge. research (see Wood 2011 for a history of this support). The aims were to assess what is currently known about the Since the late 1950s, the Foundation has held a number of fossil evidence and the environmental context of early Homo paleoanthropological symposia that have led to landmark and to set the stage for integrated, multidisciplinary studies publications. These include Social Life of Early Man (Wash- to provide a framework for interpretation of the hard evi- burn 1961), African Ecology and Human Evolution (Howell dence. The basic premise of the meeting was that it is essential and Bourlie`re 1963), Classification and Human Evolution to have a solid understanding of how and why modern hu- (Washburn 1964), Background to Evolution in Africa (Bishop mans and other animals vary in order to understand the and Clark 1967; Clark 1967), Man the Hunter (Lee and Devore adaptive shifts involved with the evolution of Homo. Partic- 1968), Calibration of Hominoid Evolution: Recent Advances in ipants in the symposium included paleoanthropologists, hu- Isotopic and Other Dating Methods as Applicable to the Origin man biologists, behavorialists, and modelers, and, to our of Man (Bishop and Miller 1972), After the Australopithecines: knowledge, this is the first time that such a varied multidis- Stratigraphy, Ecology, and Culture Change in the Middle Pleis- ciplinary group has gathered to focus attention on a major tocene (Butzer and Isaac 1975), Earliest Man and Environments question in hominin evolution. in the Lake Rudolf Basin: Stratigraphy, Paleoecology, and Evo- The collection of papers is introduced by Aiello and Anto´n lution (Coppens et al. 1976), and Early Hominids of Africa (2012), who summarize the current state of our knowledge (Jolly 1978). about the origin of Homo, integrate the varied contributions, To continue this tradition, the Wenner-Gren Foundation and give a taste of the potential that this approach has for is always looking for big questions and innovative new di- rections in all areas of anthropology for future Foundation- Leslie C. Aiello is President of the Wenner-Gren Foundation for sponsored and Foundation-organized symposium meetings Anthropological Research (470 Park Avenue South, 8th Floor North, and eventual CA publication. We encourage anthropologists New York, New York 10016, U.S.A.). to contact us with their ideas for future meetings. Information

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0001$10.00. DOI: 10.1086/667709 S268 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 1. Participants in the symposium “Human Biology and the Origins of Homo.” Front: Laurie Obbink, Susan Anto´n, Leslie Aiello, Rick Potts, Andrea Migliano, Jonathan Wells, Peter Ungar. Middle: Katie MacKinnon, Jennifer Smith, Karin Isler, Karen Steudel, Susan Pfeiffer. Back: Josh Snodgrass, Trent Holliday, Gary Schwartz, Tom Schoenemann, Herman Pontzer, Carel van Schaik, Mike Plavcan, Chris Kuzawa, Chris Rainwater, Rick Bribiescas. A color version of this photo appears in the online edition of Current Anthropology. about the Wenner-Gren Foundation and the Symposium pro- Clark, J. Desmond, ed. 1967. Atlas of African prehistory. Chicago: University of Chicago Press. gram can be found on the Foundation’s Web site (http:// Coppens, Yves, Francis Clark Howell, Glynn L. Isaac, and Richard E. F. Leakey, wennergren.org/programs/international-symposia). eds. 1976. Earliest man and environments in the Lake Rudolf Basin: stratig- raphy, paleoecology, and evolution. Prehistory Archeology and Ecology Series. Chicago: University of Chicago Press. Dubois, Eugene. 1894. Pithecanthropus erectus, eine menschenaehnliche Uber- egangsform aus Java. Batavia: Landesdruckerei. Howell, Francis Clark, and Franc¸ois Bourlie`re, eds. 1963. African ecology and References Cited human evolution. Viking Fund Publications in Anthropology, no. 36 (Wen- Aiello, Leslie C., and Susan C. Anto´n. 2012. Human biology and the origins ner-Gren Foundation for Anthropological Research). Chicago: Aldine. of Homo: an introduction to supplement 6. Current Anthropology 53(S6): Jolly, Clifford J. ed. 1978. Early hominids of Africa. New York: St. Martin’s. S269–S277. Leakey, Louis S. B., Phillip V. Tobias, and John R. Napier. 1964. A new species Anto´n, Susan C., and J. Josh Snodgrass. 2012. Origins and evolution of genus of the genus Homo from Olduvai Gorge. Nature 202:7–9. Homo: new perspectives. Current Anthropology 53(S6):S479–S496. Lee, Richard B., and Irven DeVore, eds. 1968. Man the hunter. Chicago: Aldine. Bishop, Walter William, and J. Desmond Clark, eds. 1967. Background to Washburn, Sherwood L., ed. 1961. Social life of early man. Viking Fund evolution in Africa. Chicago: University of Chicago Press. Publications in Anthropology, no. 31 (Wenner-Gren Foundation for An- Bishop, Walter William, and J. A. Miller, eds. 1972. Calibration of hominoid thropological Research) Chicago: Aldine. evolution: recent advances in isotopic and other dating methods as applicable ———. 1964. Classification and human evolution. Viking Fund Publications to the origin of man. Edinburgh: Scottish Academic Press. in Anthropology, no. 37 (Wenner-Gren Foundation for Anthropological Butzer, Karl W., and Glynn L. Isaac, eds. 1975. After the australopithecines: Research) Chicago: Aldine. stratigraphy, ecology, and culture change in the middle Pleistocene. New York: Wood, Bernard. 2011. Wiley-Blackwell encyclopedia of human evolution. Chich- de Gruyter. ester, UK: Wiley-Blackwell. Current Anthropology Volume 53, Supplement 6, December 2012 S269

Human Biology and the Origins of Homo An Introduction to Supplement 6

by Leslie C. Aiello and Susan C. Anto´n

New fossil discoveries relevant to the origin of Homo have overturned conventional wisdom about the nature of the australopiths and early Homo, and particularly Homo erectus (including Homo ergaster). They have eroded prior assumptions about the differences between these genera and complicated interpretations for the origin and evolution of Homo. This special issue surveys what is now known about the fossil evidence and the environmental context of early Homo. It also moves beyond the hard evidence and sets the stage for integrated, multidisciplinary studies to provide a framework for interpretation of the hard evidence. The underlying premise is that to understand the adaptive shifts at the origin of Homo, it is essential to have a solid understanding of how and why modern humans and other animals vary. Contributors to this issue include paleoanthropologists, human biologists, behavorialists, and modelers. We tasked each with bringing her or his special expertise to bear on the question of the origins and early evolution of Homo. The papers in this collection are a product of a week-long Wenner-Gren symposium held in March 2011, and this introduction integrates this work and its significance for Homo.

What We Once Knew . . . phasized by the diminutive size of the most complete Aus- tralopithecus skeleton (A.L. 288-1; Lucy), on the one hand, The origin of Homo holds particular sway for us and has often and the surprisingly large size of the most complete H. erectus been seen as the point in our evolution when the balance tips skeleton (KNM-WT 15000; Nariokotome boy), on the other from a more ape-like to a more human-like ancestor. By the (e.g., Ruff 1993). The comparisons between H. erectus and turn of this century, a conventional wisdom had grown up Homo sapiens were so strongly drawn that the inclusion in around the origin of Homo and particularly Homo erectus that the genus of some of the earliest species, such as H. habilis cast this species as the first hominin to take important bio- and H. rudolfensis, was seriously questioned on the basis of logical and behavioral steps in the direction of modern hu- their more australopith-like postcranial skeleton, among other mans (Anto´n 2003; Shipman and Walker 1989). Homo erectus things (Wood and Baker 2011; Wood and Collard 1999, 2007). was envisioned as a large-brained, small-toothed, long-legged, The fossil record never ceases to upset conventional wis- narrow-hipped, and large-bodied hominin with relatively low dom, and over the past 2 decades, new discoveries from East sexual dimorphism. By virtue of a higher-quality, perhaps and South Africa, Georgia, and even Indonesia have chal- animal-based diet, H. erectus is said to have ranged farther, lenged these stark distinctions between Australopithecus and cooperated more, and quickly dispersed from Africa (Aiello H. erectus and within non-erectus early Homo. In particular, and Key 2002; Anto´n, Leonard, and Robertson 2002; Mc- new small-bodied and small-brained finds from the Republic Henry and Coffing 2000; Walker and Leakey 1993). The pau- of Georgia and Kenya call to question claims for universally city of early Homo fossils of Homo habilis sensu lato (including large size in H. erectus (e.g., Gabunia et al. 2000; Potts et al. Homo rudolfensis) meant that comparisons of Australopithecus 2004; Simpson et al. 2008; Spoor et al. 2007) and focus our ((Paranthropus) were made to H. erectus (including Homo attention instead on the range of variation within that taxon. ergaster) rather than to other early Homo. And the distinctions This variation in H. erectus has most often been referred to between Australopithecus and Homo were perhaps overem- as sexual dimorphism and/or regional/climatic adaptations (Anto´n 2008; Spoor et al. 2007), although short-term accom- modations and phenotypic plasticity are likely to have played Leslie C. Aiello is President of the Wenner-Gren Foundation for an important role (see Anto´n 2013). And larger-sized, longer- Anthropological Research (470 Park Avenue South, New York, New legged Australopithecus have been found (Haile-Selassie et al. York 10016, U.S.A. [[email protected]]). Susan C. Anto´n is a Professor in the Center for the Study of Human Origins, Department 2010), as have members of that genus who may share some of Anthropology, New York University (Rufus D. Smith Hall, 25 postcranial characteristics with Homo (Asfaw et al. 1999; Ber- Waverly Place, New York, New York 10003, U.S.A. [susan ger et al. 2010; Kibii et al. 2011; Kivell et al. 2011; Zipfel et [email protected]]). This paper was submitted 12 XII 11, accepted 8 al. 2011). Additionally, new fossil remains of non-erectus VII 12, and electronically published 27 IX 12. Homo and new work on previously known remains emphasize

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0002$10.00. DOI: 10.1086/667693 S270 Current Anthropology Volume 53, Supplement 6, December 2012 the diversity of the early members of the genus and the ways We argue that understanding the response of extant organ- in which they differ from Australopithecus (Blumenschine et isms, especially humans, in shifting environments provides al. 2003; Spoor et al. 2007). an ideal basis for understanding the integration of biocultural Yet despite this increased appreciation of variation in early responses to environmental constraints. The application of fossil Homo, little time has been spent evaluating the rela- these data in light of the known fossil record can help us to tionships between morphology and behaviors in extant taxa, understand these past populations, their constraints and adap- especially modern humans, in different ecological circum- tive strategies. By mining the rich data sets of our subspe- stances. We maintain that these are the data that are essential cialties, we sought to forge a stronger and more nuanced to create a more nuanced understanding of the implications understanding of the adaptive shifts that can—or cannot— and expectations of anatomical changes at the origin of our be inferred at the base of our genus and to set out a series genus—an understanding that goes beyond simple assump- of hypotheses and predictions to be tested against future fossil tions of sexual or climatic variation. and archaeological data. The results of an intense 5-day Wen- ner-Gren Symposium in Sintra, Portugal, in March 2011 and Topic and Rationale our follow-up analyses are presented in this special issue.

The increasing number of early Homo fossil finds and their Setting the Stage diversity in size and shape suggest that this discussion sur- rounding the origin and evolution of early Homo is likely to We begin the volume, as we did the symposium, by reassessing form a major focus for the next decade of paleoanthropo- the fossil foundation of what we now know regarding genus logical work. As such, our goal was to bring together human Homo. Anto´n (2012) provides an overview of the genus and biologists, behaviorists, modelers, and fossil experts to inte- its species and the differences between Australopithecus and grate the rich extant data sets with the new details of the fossil Homo. The first recognizable members of the genus Homo record. Understanding the adaptive shifts at the origin of appear at approximately 2.3 Ma, suggesting that the genus Homo is dependent on a solid understanding of how and why evolved earlier, but substantial fossil evidence does not appear modern humans vary and particularly on the relationship until about 2.0 Ma. Her paper focuses our attention on the between human behavior, human morphology, and human importance of individual fossil data points for understanding lifestyle and life history variation. diversity within and between groups, and she concludes that Among the highly variable features in living humans are a strong case can be made for at least three different morphs features such as body size and aspects of life history that between 2.0 and 1.5 Ma: an 1813-group, a 1470-group, and separate us from other primates. In many cases, human var- Homo erectus (including Homo ergaster). She avoids the use iation in, for example, growth rates, fertility, and perhaps even of taxonomic names for the 1813-group and 1470-group be- lifespan, can be traced to such environmental or behavioral cause of uncertainty over group affiliation of type specimens factors as nutritional sufficiency and unavoidable (extrinsic) for early Homo species (e.g., Homo habilis and Homo rudol- mortality. Such phenotypic plasticity provides a more rapid fensis; Leakey et al. 2012). Her paper also provides an intro- response to environmental challenges than does genetic duction to what is now known about the distinct features change, but the fact that genetic change can follow has been that separate the three different morphs from each other and long suggested in human biology (e.g., Kuzawa and Bragg from Australopithecus (see Anto´n 2012, tables 1–8, and Anto´n 2012). Thus, understanding the causes of human phenotypic and Snodgrass 2012, tables 1–6, for membership of these plasticity can provide important clues to understanding both morphs and distinguishing morphological and inferred be- within and between species variation in the morphology of havioral features). Additionally, she suggests that, on average, our hominin ancestors. early Homo is larger of body and brain than Australopithecus, Unavoidably, the biology of early Homo will be unlike that and H. erectus is larger than other early Homo. That said, the of ourselves, however—and therefore, primate and mam- surprising facts, particularly to those who have been involved malian trends are also important to understand. And because in paleoanthropology for a considerable time, are the degree at some point cooperation in hunting or breeding became of diversity within the morphs and that, in some ways, the important to survival, considering how both carnivory and morphs are more similar to each other than was previously cooperation influence life history, body size, and body shape imagined. For example, all early Homo, including H. erectus, and whether they leave a detectable signal are important con- may exhibit substantial amounts of sexual dimorphism, and siderations as well. H. erectus is less fully modern in body proportions than has We set out, then, to probe the meaning of the newly iden- been previously claimed. These themes and their implications tified ranges of variation in size and shape in early Homo are further plumbed in the contributions by Holliday (2012), based on empirical evidence of how extant humans, non- Pontzer (2012), and Plavcan (2012). human primates, and social carnivores respond energetically, Fossils cannot be understood and interpreted without their physiologically, and socially to changes in resource availability context, and Potts (2012) provides an overview of the envi- and to stress from climatic, environmental, and other factors. ronmental and archaeological background for the evolution Aiello and Anto´n Origins of Homo S271 of Homo in eastern Africa between 3.0 and 1.5 Ma. He con- pelvis demonstrate that its bi-illiac breadth was broad and cludes that there were major episodes of moist-arid variability australopith-like (Simpson et al. 2008; but see Ruff 2010). during this period, superimposed on an overall drying trend. Because locomotor efficiency is primarily a function of relative The first appearance of Homo at approximately 2.3 Ma (Kim- limb length (Pontzer 2012), and because limb length is al- bel et al. 1996; and of the Oldowan at approximately 2.58 lometrically related to body size in all hominins, larger-bodied Ma; Semaw et al. 2003; but see McPherron et al. 2010) as individuals of any taxon would be more efficient in walking well as the proliferation of the genus after 2.0 Ma coincide and running, with faster optimal speeds and increased ab- with particularly high levels of climate variability, suggesting solute speed. Long leg length and arm length also have ther- that adaptive plasticity in its broadest developmental, physi- moregulatory advantages in hot climates, which would be a ological, and behavioral manifestations was integral to the distinct advantage either during locomotion or at rest. evolution of Homo. For example, stone tools, which have a Given the similar scaling relationships between limb lengths strong stratigraphic persistence in the archaeological record and body size across hominins, Holliday concludes that there after 2.0 Ma, provide an efficient behavioral mechanism to is little evidence of a major locomotor shift between Aus- enhance foraging ability, enabling predictable returns in a tralopithecus and early Homo (including H. erectus), a point changing environment. But they also pose an energetic chal- that is shown by the analyses presented by Pontzer (2012) as lenge of material transport over distances as great as 1–13 km well. However, they note that a significant difference remains by about 2.0 Ma (Braun et al. 2008). between these genera in terms of mean body size; early Homo is approximately 33% larger than Australopithecus, and H. Food, Morphology, and Locomotion erectus is approximately 15% larger than other early Homo, even when the recently discovered small H. erectus fossils (e.g., One means of offsetting the energetic cost of tool and raw from Georgia, Kenya, Tanzania, and perhaps Ethiopia) and material transport as well as increased body and brain size is large Australopithecus are included in estimates. dietary expansion to higher-quality food resources, which Despite having similar proportions as earlier hominins, a might involve access to animal resources (as well as a wider number of symposium contributions emphasize that larger range of plant food; Aiello and Wells 2002; Aiello and Wheeler size itself has important energetic, locomotor, and survival 1995; Leonard and Robertson 1997). Such resources would consequences for Homo. Holliday (2012) and Pontzer (2012) also serve to buffer environmental instability and resulting point out that across mammals, larger body size equates with changes of food resources across space and over time (Potts a larger home range size, which would be exaggerated further 2012). Some direct evidence for a dietary shift in early Homo if Homo was also more carnivorous (Anto´n, Leonard, and (including even more substantial changes in Homo erectus) Robertson 2002). Pontzer (2012) develops the implications relative to the diet of Australopithecus is provided by Ungar of this by demonstrating that across mammals there is no (2012), who reviews dental macro and micro anatomy and selection for greater locomotor efficiency (as proxied by wear. In particular, all early Homo teeth are most similar to changes in limb proportions) in those species with larger extant animals that do not use fracture-resistant foods. In home range sizes. Instead, species that travel farther adopt a other words, the genus seems not to have used particularly high-throughput strategy (increased daily energy expenditure hard-brittle foods or especially tough foods. However, within in relation to body size and a correspondingly greater repro- early members of the genus, there are some differences that ductive investment), resulting in greater lifetime reproductive suggest a broader subsistence base for H. erectus that included output. This suggests that in Homo, as in other far-ranging more tough foods than other early Homo. This dental evidence mammals, there must have been an increased energy budget is consistent with increased meat eating (or eating other non- to provide for increased brain and body growth and repro- brittle foods) and tool use in food preparation (perhaps even duction. Outside of a more calorie-rich diet at the carnivorous cooking) over the condition in Australopithecus,witha end of the omnivorous spectrum, Pontzer (2012) argues that broader range of foods eaten by H. erectus than other early an increased daily energy expenditure would suggest greater Homo. These results could be a hard tissue signal of dietary food availability, perhaps implying the origins of food sharing. and behavioral plasticity to temper environmental vacillation. These results are consistent with the symposium papers on Like the dietary results, other papers suggest that some living humans and extant carnivores by Migliano and Guillon adaptations once thought to appear with H. erectus arise at (2012), Kuzawa and Bragg (2012), and Smith and colleagues the origin of the genus or even earlier. Holliday (2012) pro- (2012). vides new analyses and an overview of our current knowledge of body size and body proportions. The unexpected outcome Body Size and Growth is that our prior understanding that H. erectus was unique among the early hominins in having long legs and a narrow, While height in humans is influenced by a number of en- heat-adapted body is wrong. Leg length scales with body mass, vironmental and idiosyncratic factors (see references in Ku- and large-bodied australopiths have long, human-like legs and zawa and Bragg 2012; Migliano and Guillon 2012), it is human-like thoraces, while new analyses of the H. erectus achieved through a combination of speed and duration of S272 Current Anthropology Volume 53, Supplement 6, December 2012 growth, which is in turn dependent on resource availability sidering especially the regional variation in H. erectus derived and mortality probability (Kuzawa and Bragg 2012; Migliano from these principles are developed in detail in the concluding and Guillon 2012). This may provide a clue for possible in- paper of this issue (Anto´n and Snodgrass 2012). terpretations of size variation in Homo. In human popula- Although more data are sorely needed, what we know about tions, the greater the probability of mortality, the earlier is the tempo and mode of growth in the early hominins, based the age of maturity (and the shorter the period of growth), on rates of dental maturation, is summarized by Schwartz to ensure maximum reproductive output. Based on the anal- (2012). These data suggest that both Australopithecus and early ysis of small-scale human societies, Migliano and Guillon Homo have more rapid maturation than Homo sapiens,which (2012) demonstrate that the main determinant in height var- could reflect environments of higher extrinsic mortality. How- iability in humans is the probability of mortality—the lower ever, there are probably differences between the genera as well. the mortality probability, the taller the populations. They also Dental eruption in Australopithecus and Paranthropus is com- show that environment has an important effect, although diet parable to, or faster than, Gorilla gorilla beringei, the fastest is not significant in their analyses. This probably results from of the living great apes. Dental eruption in H. erectus is equiv- data limitations in their large comparative analysis. alent to Pongo pygmaeus pygmaeus, the slowest of the living Kuzawa and Bragg (2012) emphasize this nutritional side great apes, and just below the large range of eruption ages in of the equation and argue that nutritional abundance is as- modern humans. The somewhat extended developmental sociated with a faster growth rate, earlier maturity, and larger schedule of H. erectus relative to Australopithecus is consistent adult sizes. Because males are affected more than females, with mortality reduction and increased body size. There is sexual size dimorphism is increased with greater nutritional still much to learn, but one definite conclusion of Schwartz’s abundance. Nutritional stress has the opposite effects—slower synthesis is that the full suite of modern human life history growth, later maturity, and reduced size dimorphism. If mor- with extended periods of growth and development was not tality rates were high and precluded later maturity, smaller present in early Homo, including H. erectus, and possibly did body size would be expected. not appear in its modern form until much later in time. Pfeiffer’s (2012) work on the bioarchaeological record of While these papers address size differences between human the small-bodied KhoeSan, however, reminds us of the mul- populations and what we know about the tempo of hominin tifactorial effect on size and of the issue that small size may maturation, Plavcan (2012) raises the important issue of sex- be the default in the absence of selective factors for larger ual size dimorphism. He provides a detailed overview of what size. That is, bigger may not always be better. In her particular is currently known (and knowable) about sexual size dimor- case study she finds no evidence for the traditional drivers of phism in hominins and living primates and provides a num- small size: nutritional insufficiency, early maturation, high ber of caveats in relation to interpretation of the evidence. It extrinsic mortality, or climate change. In light of this, she has long been assumed that sexual dimorphism is a feature suggests instead that the long-term relaxation of selection for observable in hominins that can be directly and causally re- large size was allowed due to the relative isolation of the lated to social behavior across primates, and particularly to KhoeSan and therefore an absence of competition with large- male competition over mates (Leigh 1992; Plavcan 2001; Plav- sized human populations. This might favor increasingly large can and van Schaik 1997a, 1997b). However, Plavcan cautions male size and shape changes to the pelvis that accommodated that although all highly dimorphic primate species are po- relatively large infants in small mothers, which might oth- lygynous, the inverse relationship is not straightforward, and erwise favor large females. It is important, then, to consider any hominin inferences can only be made with extreme cau- the multiple and sometimes conflicting causes for size change tion. in light of their influence on developmental plasticity. A particularly important aspect of his research is the focus At present we lack the detailed data from the fossil record on female size. He argues that female size represents the op- to assess intraspecific differences in growth and development timum for the particular environment, and male size repre- with the aim of inferring the possible roles of nutrition, mor- sents a trade-off between the costs of deviating from this tality probability, or other factors in shaping the observed size optimum and the benefits of larger size in mate competition. differences in the hominins. However, because the size varia- Female size change alone does not result in marked changes tion, particularly in Homo erectus, is similar to that found in in dimorphism across extant species. Although there is some modern humans (Migliano and Guillon 2012), there is every variation within species, without a change in mating com- reason to assume that similar factors were in play and that size petition, which drives male size increase or decrease, an in- differences in the hominins also reflect an adaptive plasticity crease in female size should simply be tracked by an equivalent similar to that observed in modern humans. Migliano and increase in male size. Beyond this, he notes that size variation Guillon (2012), Kuzawa and Bragg (2012), and Bribiescas and within H. erectus is “unremarkable” relative to human levels colleagues (2012) also emphasize the important role of behav- and that our understanding of sexual size dimorphisms re- ior, and particularly cooperation, in buffering both nutritional quires better understanding of temporal changes in male and sufficiency and mortality probability, thereby setting the stage female size relative to each other in both humans and non- for body size increase. A series of alternative scenarios for con- human primates. He makes a specific call for further system- Aiello and Anto´n Origins of Homo S273 atic research on intraspecific geographic and sexual variation cus and early Homo was a common theme that developed in primates. from a variety of perspectives throughout the symposium. The evolution of male life history trade-offs has not been Many of the previously mentioned papers suggest that the a major focus in hominin evolution, outside of the relatively abilities to maximize food and to limit predation are critical simple association between reduced dimorphism and a move to increasing body and brain size. Food sharing and conse- away from polygynous social systems and strong size-driven quent group cooperation are means of achieving this. In light mating competition. However, Bribiescas and colleagues of the several lines of evidence pointing toward the impor- (2012) argue that it is central to the evolution of Homo. tance of sociality and cooperation, several symposium par- Consistent with Plavcan’s interspecific analyses demonstrating ticipants explored the correlates of such behavior in extant no correspondence between reduced dimorphism and any organisms as well as the concept of cooperation as a means particular social system, Bribiescas and colleagues (2012) of expanding an organism’s “capital.” point to the fact that humans, with their relatively reduced Nonhuman primates provide the logical starting point be- dimorphism, are unique among the apes not only in the cause of their close phylogenetic relationship to humans. They degree of their paternal parenting behavior but also in its demonstrate the roots of human evolutionary plasticity par- variation. There is variation in the amount of time and energy ticularly in dietary/niche expansion, extended life history, and invested and in the type of offspring care, provisioning, and increasing social complexity with extensive cooperation and other involvement. Paternal parenting behavior is dependent communication (Anto´n and Snodgrass 2012). These abilities on context, including the availability of other caregivers such provide the basis for the elaborate niche construction ob- as grandmothers or siblings. served in humans that involves accelerating biocultural com- The important point is the move away from energy in- plexity and an increasing reliance on cooperation in all aspects vestment in large male size that permits not only energy al- of hominin life (Fuentes, Wyczalkowski, and MacKinnon location to parenting behavior but also to other aspects of 2010; Odling-Smee, Laland, and Feldman 2003). life history including fertility and longevity. One particularly However, primates are not the only models for hominin novel aspect of their work is the argument that increased male behavior, and useful insights can be drawn from, for example, fertility at older ages may have contributed to the emergence other large-brained animals such as dolphins, cooperative of female longevity and the evolution of the female postre- breeders among all orders, and large-bodied mammal species productive lifespan and increased female reproductive effort that inhabit woodland and savanna environments. In the late through grandmothering and child care. This provides an 1960s, Schaller and Lowther (1969) wrote a now classic paper alternative, or perhaps complementary, explanation to the on the relevance of carnivore behavior to the study of early Grandmothering Hypothesis (Hawkes et al. 1998, 2011; Ka- hominins. Their basic premise was that to understand sociality chel, Premo, and Hublin 2011a, 2011b; O’Connell, Hawkes, in hominins, it would be productive to draw inferences from and Blurton Jones 1999). animals that are ecologically similar, such as social carnivores, It is now clear that we cannot be sure whether there was as well as animals that were closely related, such as the pri- any significant difference in dimorphism between Australo- mates. At the time, this work represented a major innovation pithecus and Homo (either early Homo or H. erectus; Anto´n in the interpretation of early hominin behavior. Smith and 2012; Holliday 2012; Plavcan 2012; Pontzer 2012). However, colleagues (2012) take up where Schaller and Lowther left off if we could be sure that dimorphism was reduced in H. erectus, more than 40 years ago to demonstrate commonalities in we would have direct evidence of a change in mating behavior behavior and morphology between humans and the Carni- leading to a reduction of sexual selection acting on male size, vora. Sociality among carnivores is the exception rather than and likely involving a major change in social organization the rule, but significant features related to sociality and co- involving increased levels of cooperation and allocare, and operation in the Carnivora include cursorial hunting of large perhaps increased longevity. Given the importance of under- game in open habitats, a relatively tall body build (shoulder standing the relationship between male and female size, it height in relation to body mass), reduced sexual dimorphism, would be useful to expend the effort to understand more larger brains, a high reproductive output (in this case larger critically the relationship between skeletal and body mass di- litters), allocare of infants, increased weaning age, and larger morphism and how it varies among modern human popu- population density. Many of these features (with the possible lations. exception of reduced sexual dimorphism) are reminiscent of the morphology of Homo and may help to infer behavior and Models for Cooperation, Sociality, Life life history of early Homo (including Homo erectus). Indeed, History, Body Size, and Brain Size many of these features in social carnivores help to reinforce the inferred relationships between dietary change, morphol- Although we cannot be confident that there was a change in ogy, and cooperation reached by other symposium partici- sexual size dimorphism associated with the evolution of pants using other data sets. Homo, the idea that cooperation and food sharing may have Brain size expansion in Homo may provide another, in- been major distinguishing factors between the Australopithe- dependent avenue for inferring the presence of cooperative S274 Current Anthropology Volume 53, Supplement 6, December 2012 breeding. Isler and van Schaik (2012) draw on their previous differences in life history strategies among human popula- work on the Expensive Brain Hypothesis (Isler and van Schaik tions, and it has been correlated with large brain sizes across 2009) and on a large comparative mammalian database to mammals (Navarrete, van Schaik, and Isler 2011). It is thus underscore the relationship between brain size increase and important to develop creative ways to infer adiposity from cooperation in the form of allocare. They argue that across fossil record. mammals, large brain size is generally correlated with a re- Storing energy in generalized currencies (social relation- duction in population growth rate. This correlation is driven ships and adipose tissue) means that various aspects of life by the extended ontogenetic periods necessary for the growth history (growth, reproduction, and immunity) can be of larger-bodied and larger-brained offspring and the corre- “funded” according to the state of the environment and over- spondingly longer interbirth intervals required. Allocare pro- all energy availability (Wells 2012). If conditions demand it, vides extra resources to the mother, resulting in early weaning one aspect may be prioritized at the expense of others, re- of the infant and a shorter interbirth interval. An important sulting in the life history variation and its outcomes in features aspect of their work is the prediction based on extant primates such as growth rates, adult body size, fertility, and possibly that a mean endocranial capacity of 600–700 cc would be the lifespan that are observed in modern humans (Bribiescas, “gray ceiling” beyond which cooperation in the form of allo- Ellison, and Gray 2012; Kuzawa and Bragg 2012; Migliano care would be essential if the population were to grow fast and Guillon 2012). The symposium provided a vehicle for enough to replace itself and avoid extinction. The great apes bringing together the disparate data sets of our subdisciplines seem to be at the very farthest extension of this relationship, into a framework that suggests ways in which variation is just barely allowing population replacement without allocare. produced, organized, and interrelated in the extant world. The fact that the mean brain size of the largest-bodied Aus- tralopithecus species (478 cc in Australopithecus afarensis;Hol- What We Know Now and What We Hope to loway, Broadfield, and Yuan 2004) converges on that of mod- Know in the Future ern apes suggests that cooperative breeding probably had not yet appeared in these early hominins. However, by the time The final paper of the volume takes up the challenge of using of H. erectus, with brain sizes uniformly over 700 cc, repro- this framework to generate means of assessing the variation ductive cooperation would seem to have been a necessity. observed in the fossil record and the biocultural relationship Allocare is undoubtedly a key element that enabled hom- between hominin morphology, hominin behavior, and the inins to break through the gray ceiling, but it is only one fluctuating environment of the African Pliocene and Pleis- element of capital in hominin evolution (Kaplan, Lancaster, tocene (Anto´n and Snodgrass 2012). What we know is that and Robson 2003; Kaplan et al. 2000). Wells (2012) sees capital early Homo existed in a highly variable environment (a non- as a key and integrating concept that brings together many equilibrium ecosystem) that may have placed adaptive plas- of the themes of intraspecific and interspecific variation and ticity at a premium. The type of body size variation observed plasticity that emerged from the symposium. He defines cap- in early Homo is consistent with the range observed in modern ital as a generalized energy currency that can be expended in humans that is mediated by life history differences in growth a variety of ways to increase adaptive flexibility. This results and development that are dependent on energy availability in the fact that humans are “uniquely under-committed” to and mortality probability (Kuzawa and Bragg 2012; Migliano any specific niche. and Guillon 2012; Migliano, Vinicius, and Lahr 2007). Dietary Wells (2012) talks about social capital as well as physical differences, involving increased dietary breadth and a more capital. Social capital is facilitated by larger brain sizes, stored carnivorous diet, are also evident between these hominins and in social relationships and variably expended to achieve pred- are consistent with greater adaptive plasticity than inferred ator protection or to enable food security (particularly for the australopiths. Comparative studies suggest that larger- through sexual division of labor and allocare). Physical capital bodied hominins would have had to adopt a high energy is stored within the body as adipose tissue or extracorporeally throughput strategy, and this, together with the increase in in food hoards and similarly used to avoid predators and brain size, would presuppose increased cooperation in the provide sufficient nutrition. Because it is difficult to assess form of allocare and sexual division of labor. The increased from the fossil record, adipose tissue has received relatively cooperation and sociality would also be significant in group little attention in human evolution. Yet it is a major feature protection in a relatively dangerous terrestrial environment distinguishing us (and our sexual dimorphism; see Anto´nand and create a relatively safe “niche” that would be consistent Snodgrass 2012; Plavcan 2012) from nonhuman primates and with later maturation (and perhaps increased longevity) that one that buffers the costs of reproduction against food short- begins to be evident in the dental maturation evidence for ages in fluctuating environments (Knott 1998; Kuzawa 1998). Homo erectus in relation to the other early hominins. It also is the source of signaling molecules responsible for These results provide the basis for a model for the evolution energy trade-offs between competing biological functions of Homo involving an integrated feedback loop that drove life such as growth, immune function, and reproduction (Wells history evolution and contributed to cultural change (Anto´n 2009). It may be one of the major factors responsible for and Snodgrass 2012). The central elements of this model are Aiello and Anto´n Origins of Homo S275 cooperative behavior, diet, cognitive abilities, and extrinsic test these predictions. For example, to understand the factors mortality risk. This model also generates a number of testable surrounding the evolution of Homo, it will be essential to hypotheses (e.g., to explain size variation in the hominins), target intra- and interpopulational research on energetic and but each requires additional data from both the fossil and the life history variation in various climatic, nutritional, and mor- modern records to test. Increased body size across genera may tality environments. We need to tease out the complex in- be hypothesized to signal either decreased extrinsic mortality, terrelationships among these and other variables to under- increased nutritional sufficiency, or both. On the one hand, stand the fundamental correlates of body size, brain size, and specific predictions are made about rates of growth, timing sexual dimorphism (Kuzawa and Bragg 2012; Smith et al. of weaning, and timing of growth cessation in each scenario— 2012). Among many other things, we want to know, for ex- so additional growth data, especially from dental development ample, how skeletal dimorphism tracks body mass dimor- and especially for the earliest Homo, are needed. But beyond phism across populations, especially in humans (Plavcan simply “finding more fossils,” additional means of assessing 2012), and how individual skeletal features are influenced in “hard tissue” growth in extant populations in ways that are males and females in differing circumstances (Bribiescas, El- comparable to fossil samples are needed—and the need to lison, and Gray 2012; Kuzawa and Bragg 2012). consider intrapopulational variation among extant primate Our thinking about the origins of Homo has continued to and nonprimate mammals to the level that it is done in human change since Homo habilis was announced (Leakey, Tobias, populations is also required. There are issues of scale and and Napier 1964), the almost complete Nariokotome H. comparability in our data sets that can only be remedied by erectus skeleton was discovered (Brown et al. 1985), and long-term analyses of extant populations. Dmanisi and other material changed our ideas about variation The increase in brain and body size between other early in H. erectus (Gabunia et al. 2000; Potts et al. 2004; Simpson Homo and H. erectus again suggests decreased extrinsic mor- et al. 2008; Spoor et al. 2007). New fossils will undoubtedly tality and/or increased nutrition. These features may reflect continue to be uncovered. However, this material cannot be adaptations to the higher mortality rates in terrestrial envi- interpreted in a vacuum, and the more we know about intra- ronments and perhaps cooperative hunting—as shown in the and interspecific variation in modern humans and other an- social carnivores. The extended developmental schedule of H. imals, the stronger the foundation we have for a rich under- erectus is consistent with mortality reduction, possibly as the standing of our evolutionary past. result of behavioral changes involving some form of coop- eration. Here, along with additional fossil data and more com- parable data sets, a key endeavor will be mining the rich social carnivore data sets and creating new ones that consider aspects Acknowledgments of morphology, behavior, and variation. Regarding extrinsic We would like to thank the Wenner-Gren Foundation for the mortality, new ways can and should be developed to inter- opportunity to hold this symposium and to publish the results rogate the archaeological and extant records for predator load as an open-access supplementary issue of Current Anthro- and the degree to which this can be assessed for different pology. We would also like to thank all of the participants for hominin species. Novel means should also be developed for lively and stimulating discussion and debate over a 6-day assessing the ways in which population variation and physical period in March 2011 at the Tivoli Pala´cio de Seteais Hotel character development (including size and dimorphism) are in Sintra, Portugal. This experience will be fondly remem- influenced by the high degree of climate variability that char- bered for a long time to come. We would like to give special acterized this period of evolutionary history. thanks to Chris Rainwater (New York University), who served For example, it has been hypothesized for the small-sized as the rapporteur for the meeting; to Emily Middletown (New Dmanisi sample that nutritional insufficiency and perhaps York University), who provided invaluable assistance in help- isolation resulted in short-term accommodations or adapta- ing to edit and prepare all of the manuscripts for publication; tions (e.g., Anto´n 2003, 2013; see also Migliano and Guillon and to Lisa McKamy and the editorial and production staff 2012). If this is the case, one would expect lower growth rates at the University of Chicago Press for their help in bringing and a longer period of maturation in relation to larger-bodied this issue to fruition. The meeting would not have been as H. erectus. Alternatively, if the short stature was due to a high successful as it was without the deft organizational skills of mortality environment, one would expect the smaller speci- Laurie Obbink, the Wenner-Gren Foundation Conference As- mens to have more rapid growth rates and a shorter period sociate, and for this we are most grateful. of maturation. Clearly this requires greater detail than we currently possess regarding H. erectus growth, but it provides a place to start. References Cited While we end, as many such symposia do, with a decided Aiello, Leslie C., and Catherine Key. 2002. Energetic consequences of being plea for more fossil remains in different localities, we hope a Homo erectus female. American Journal of Human Biology 14:551–565. Aiello, Leslie C., and Jonathan C. K. Wells. 2002. Energetics and the evolution to move beyond that to an agenda of integrated and multi- of the genus Homo. 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Early Homo Who, When, and Where

by Susan C. Anto´n

The origin of Homo is argued to entail niche differentiation resulting from increasing terrestriality and dietary breadth relative to the better known species of Australopithecus (A. afarensis, A. anamensis, A. africanus). I review the fossil evidence from ∼2.5 to 1.5 Ma in light of new finds and analyses that challenge previous inferences. Minimally, three cranial morphs of early Homo (including Homo erectus) exist in eastern Africa (1.9–1.4 Ma), with at least two in southern Africa. Because of taphonomic damage to the type specimen of Homo habilis,inEastAfrica two species with different masticatory adaptations are better identified by their main specimen (i.e., the 1813 group and the 1470 group) rather than a species name. Until recently, the 1470 group comprised a single specimen. South African early Homo are likely distinct from these groups. Together, contemporary early H. erectus and early Homo are bigger than Australopithecus (∼30%). Early H. erectus (including recently discovered small specimens) is larger than non-erectus Homo (∼15%–25%), but their size ranges overlap. All early Homo are likely to exhibit substantial sexual dimorphism. Early H. erectus is less “modern” and its regional variation in size more substantial than previously allowed. These findings form the baseline for understanding the origin of the genus.

The origins of the genus Homo and the factors that may have Schrenk, Kullmer, and Bromage 2007; Stringer 1986; Wood led to its appearance remain murky. In the past two decades, 1991) even if there is little agreement as to their composition. the idea of increased behavioral flexibility in our early fore- Any understanding of the origin and evolution of Homo must bears (Potts 1988) and increased diet quality and ranging build from the primary data of the fossil record. To frame what (Anto´n, Leonard, and Robertson 2002; Shipman and Walker comes later in this special issue, here I discuss how the genus 1989) have become cornerstones of how we understand the may be defined relative to other hominin genera. And within origin and evolution of Homo before we left Africa. These our genus I consider the morphology, location, and age of the ideas in turn have emphasized the importance of enlarging individual representatives of early Homo up to and including brain and body size, decreases in sexual dimorphism, some- H. erectus. The taxa of interest here are those commonly referred what expanded ontogenetic periods, increases in energetic re- to as Homo habilis sensu lato and H. erectus sensu lato (table quirements, and increased cooperation during the first million 1; fig. 1). The former group is often split into multiple taxa, years or so of our history (Aiello and Key 2002; Dean and usually H. habilis and Homo rudolfensis, but others, such as Smith 2009; Dean et al. 2001). Yet more recent fossil finds Homo microcranous (for KNM-ER 1813) and Homo gauten- call into question some of these trends. New fossils in East gensis (for Stw 53) have also been suggested. The H. erectus Africa, Georgia, and Indonesia suggest large ranges of size and group is also sometimes split into Homo ergaster for the early perhaps shape variation in Homo erectus sensu lato and hint African and Georgian material and H. erectus for the Asian, at local adaptation and short-term accommodation as an im- although a consensus seems to be building for recognizing just portant yet underappreciated contributor to the morpholog- one species, H. erectus (Anto´n 2003; Baab 2008; Rightmire ical picture seen in the fossil record (Anto´n et al. 2007; Potts 1990). Given this flux in species composition, I advocate that et al. 2004; Rightmire, Lordkipanidze, and Vekua 2006; Simp- particular attention must be paid to individual fossil data and son et al. 2008; Spoor et al. 2007). Although the record is ranges of variation in size and shape in order to build an explicit patchier, there is also considerable variation among earlier picture of what we can and cannot know about fossil taxa and Homo, and arguably several species are represented (Curnoe how what we think we know changes depending on the in- 2010; Leakey, Tobias, and Napier 1964; Leakey et al. 2012; cluded data points of a taxon.

Susan C. Anto´n is Professor of Anthropology at the Center for the Recognizing Early Homo Study of Human Origins, Department of Anthropology, New York University (25 Waverly Place, New York, New York 10003, U.S.A. [[email protected]]). This paper was submitted 12 XII 11, A biological genus comprises closely related species, and al- accepted 9 VII 12, and electronically published 3 XII 12. though the protocol for doing this is not strictly codified in

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0003$10.00. DOI: 10.1086/667695 Anto´n Early Homo: Who, When, and Where S279

Table 1. Fossils attributed as type specimens to named species of early Homo

Umbrella species and Country type specimen Species name Publication of type Homo habilis sensu lato: OH 7 Homo habilis Leakey, Tobias, and Napier 1964 Tanzania KNM-ER 1470 Homo rudolfensis Alexeev 1986 Kenya KNM-ER 1813 Homo microcranous Ferguson 1995 Kenya Stw 53 Homo gautengensis Curnoe 2010 South Africa Homo erectus sensu lato: Trinil 2 (Pithecanthropus) erectus Dubois 1894 Indonesia Zhoukoudian 1 Sinanthropus pekinensis Black 1927 China Ngandong 1 Homo soloensis Openoorth 1932 Indonesia Perning 1 Homo modjokertensis Von Koenigswald 1936 Indonesia Swartkrans 15 Telanthropus capensis Broom and Robinson 1949 South Africa Ternifine 1 Atlanthropus mauritanicus Arambourg 1954 Algeria OH 9 Homo leakeyi Heberer 1963 Tanzania KNM-ER 992 Homo ergaster Groves and Mazek 1975 Kenya Dmanisi 2600 Homo georgicus Gabunia et al. 2002 Georgia Note. Species listed by umbrella taxon in chronological order of publication. The most commonly used species appear in bold. zoological nomenclature, it has been argued that a genus and Baker 2011) proposed to remove two species, Homo ha- “should be defined as a species, or monophylum, whose mem- bilis and Homo rudolfensis, from the genus and place them bers occupy a single adaptive zone” (Wood and Collard 1999: into Australopithecus. Their criteria for distinguishing species 66). Such a definition combines the cladistic requirement of of Homo from those of Australopithecus were based on finding monophyly for genera with a means of deciding (the adaptive six classes of characteristics that were more similar to the zone) where to recognize the base of the genus. Such a def- condition in Homo sapiens than to that of Australopithecus inition is thus both prudent and pragmatic if somewhat prob- africanus (the type species of each genus). The first criterion lematic to apply. The main problem is how to assess the is monophyly. The last is an extended period of growth and “adaptive zone,” especially in light of the probability that the development. The remaining four criteria are more explicitly full suite of characters associated with such a zone is likely related to the adaptive zone; three to reconstructions of body to have evolved in a mosaic fashion rather than appearing mass, shape, and proportions and one to jaw and tooth pro- full blown at the base of the genus. portions as scaled to body-size-adjusted brain size. Three of Several morphological differences distinguish fossil mem- the six are not assessable in H. rudolfensis. And those that are bers of the genus Homo from those of Australopithecus and assessable in H. rudolfensis or H. habilis are contested (see Paranthropus,1 including reduction in tooth and jaw size, re- Holliday 2012). That aside, judging inclusion in a genus based organization of craniofacial morphology, and perhaps changes on the association with its most derived member would seem in body shape and size (Kimbel 2009; Rightmire and Lord- to preclude the possibility of mosaic evolution in its earlier kipanidze 2009; Wood 2009). And these physical differences members. Thus, the specific ways in which H. rudolfensis and have been taken to suggest underlying adaptive shifts at the H. habilis are like other members of the genus, such as relative origin of the genus Homo, most or all of which have energetic brain size, are trumped by their dissimilarity to H. sapiens. and life history implications (e.g., McHenry and Coffing While monophyly must be maintained and identifying 2000). Thus, the adaptive zone of Homo has been variously adaptive zones will always be somewhat subjective, I favor defined, implicitly or explicitly, to relate either to cranial ex- recognizing and fully weighting the incipient characters of the pansion and masticatory diminution (e.g., Kimbel 2009; Kim- adaptive zone; Wood and Baker (2011) refer to this as a bel, Johanson, and Rak 1997; Kimbel et al. 1996; Leakey, “bottom-up” approach. Genus Homo is recognized, then, on Tobias, and Napier 1964) and/or to increased locomotor ef- the basis of the following mostly derived craniodental char- ficiency and ranging (Wood 2009; Wood and Collard 1999) acters relative to Australopithecus as have been outlined and relative to Australopithecus. more fully described by others. Using the above definition of a genus, Wood and Collard 1. Cranial expansion. Size-adjusted capacity relative to orbit (1999; see also Collard and Wood 2007; Wood 2009; Wood size is above 2.7 (Collard and Wood 2007; Wood and Collard 1999). In addition or independently, there may be evidence 1. While it is recognized that Australopithecus may be paraphyletic, of endocranial expansion or asymmetry relative to Austral- for the purposes of the comparisons in this paper, the genus is considered opithecus (LeGros Clark 1964; Rightmire and Lordkipanidze to exclude Paranthropus species but to include the best represented species commonly assigned to Australopithecus, that is, A. anamensis, A. afarensis, 2009). A. garhi, A. africanus, and A. sediba. When the data for specific com- 2. Shape of the face and palate. The palate is deep and broad. parisons come from a single species, that species is indicated by name. The anterior maxillary profile, as seen from above, is round Figure 1. Temporal and geographic distribution of early Homo and early Homo erectus localities and some important specimens discussed in the text. On the far left is the geomagnetic polarity timescale, with normal periods in black and reversed in white. Radiometric time is indicated in millions of years on the far right. Within regional columns, solid lines on either side of site names indicate time spans suggested by multiple individuals from a site; dashed-and-dotted lines indicate possible time range around a single or a few specimens. In the Africa columns, sites are grouped from left to right as South Africa, Malawi, Kenya, Tanzania, and Ethiopia; A.L. p Afar Locality; OG p Olorgesailie; OH p Olduvai Hominid; numbers on the Koobi Fora lines p KNM-ER numbers; WT p West Turkana specimen numbers; Stw p Sterkfontein. The recently described specimens of the 1470 group of early Homo are KNM-ER 60000, 62000, and 62003 (Leakey et al. 2012). Anto´n Early Homo: Who, When, and Where S281 to square (not triangular). The subnasal prognathism is mild, of Homo (Curnoe 2010; Dean and Wood 1982; Kimbel and the nasoalveolar clivus is sharply angled to the nasal floor, Rak 1993; Moggi-Cecchi, Tobias, and Beynon 1998). These and the nasal margin is everted (Kimbel 2009; Kimbel, Jo- include the cranial base, Sts 19, and juvenile cranial fragments, hanson, and Rak 1997; Kimbel et al. 1996). Stw 151, from Sterkfontein. However, both are commonly 3. Size and shape of the dentition. The canine crown is attributed to Australopithecus africanus (Dean and Wood symmetrical. Premolars lack substantial molarization in 1982; Spoor 1993). crown and root form (buccolingually narrow) but are not It is unclear which species is directly ancestral to Homo sectorial. The molars, especially the first, are somewhat me- (Kimbel 2009). However, the origin of the lineage is likely to siodistally elongated but may retain a large crown-base area. be at 2.5 Ma or earlier given that by 2.3 Ma there is incipient M2 is “rhomboidal” in shape (dominated by mesial cusps; evidence of two dental morphs. Based on the current record, Bromage, Schrenk, and Zonneveld 1995; Johanson et al. 1987; the earliest accepted Homo appear to be in the northern part Kimbel 2009; Kimbel, Johanson, and Rak 1997; Kimbel et al. of eastern Africa; however, this does not preclude an ancestor 1996; Wood 1991). from another part of the continent. Postcranial differences are not used here to distinguish Homo and Australopithecus because few postcranial remains Non-erectus Early Homo (2.0–1.44 Ma) are certainly associated with species-diagnostic cranial re- mains of early Homo. Additionally, those that are do not Members of “non-erectus” Homo are better represented after support a major locomotor difference between H. habilis 2 Ma and range in age from about 2.0 to 1.44 Ma (Feibel, sensu lato on the one hand and H. erectus (p ergaster)on Brown, and McDougall 1989; Spoor et al. 2007). They are the other (see Holliday 2012 contra Wood and Collard 1999). best known from Kenya and Tanzania, although at least one Using this standard, H. habilis and H. rudolfensis are recog- South African morph also appears to be present (Curnoe nized as Homo because both differ in distinct craniodental 2010; Grine 2005; Grine et al. 2009; Hughes and Tobias 1977; ways from Australopithecus (see below). In these differences, Moggi-Cecchi, Grine, and Tobias 2006). H. habilis and H. rudolfensis trend toward the condition in later members of genus Homo. Early Homo: Taxa, Individuals, and Anatomy

Homo before 2 Ma Homo habilis (Leakey, Tobias, and Napier 1964) was the first non-erectus species of early Homo to be recognized, and for A small number of fossil remains of older than 2 Ma in East many scholars it represents a single species that is larger Africa satisfy the above criteria; however, none of these can brained and smaller toothed than Australopithecus yet smaller be confidently attributed to species (fig. 1). The oldest fossil brained and slightly larger toothed than early African Homo Homo is likely to be the A.L. 666 maxilla from Hadar, Ethiopia, erectus. Apart from size, the teeth differ in shape from Aus- which is minimally 2.33 Ma (Kimbel et al. 1996). This spec- tralopithecus and Paranthropus in the ways discussed in the imen differs from Australopithecus in the anatomical suites of definition above, among others. For a time, all other early, characters mentioned in items 2 and 3 above. A similarly aged relatively small-brained African Homo specimens were isolated molar from West Turkana, Kenya, is also likely early lumped into this species (e.g., Boaz and Howell 1977; Hughes Homo (Prat et al. 2005). Both have some affinities with later and Tobias 1977; Johanson et al. 1987; Leakey, Clarke, and early Homo from Kenya, such as KNM-ER 1813. Isolated Leakey 1971; Wood 1991). dental remains from the Omo, Ethiopia (2–2.4 Ma), also likely The discussion in the mid-1980s regarding whether the H. represent early members of Homo and bear some similarities habilis hypodigm varied too much to constitute a single spe- to later teeth of KNM-ER 1802 from Kenya (Suwa, White, cies is well known (Lieberman, Pilbeam, and Wood 1988; and Howell 1996). The Uraha-501 (UR-501) mandible from Stringer 1986; Wood 1985). The debate has focused heavily Malawi has been argued to be of similar or slightly older age; on issues of brain size, with the most complete of the Koobi its age, based on faunal correlations, may be as young as 1.9 Fora specimens, KNM-ER 1470 and 1813, representing the Ma or as old as 2.5 Ma (Bromage, Schrenk, and Zonneveld extremes of cranial capacity (750 vs. 510 cm3). For those who 1995; Kimbel 2009). The inclusion of UR-501 in Homo is include these fossils in a single species, the size and shape based on both molar and premolar morphology (item 3) and differences between the two are explained as sexual dimor- mandibular anatomy. This specimen has strong morpholog- phism (Howell 1978; Tobias 1991); however, the very different ical affinities of the symphysis and corpus with the KNM-ER facial structures are more problematic than is absolute size 1802 mandible (Schrenk, Kullmer, and Bromage 2007). These for the inclusion of both specimens in a single species (Leakey similarities suggest the two are likely to belong to the same et al. 2012; Wood 1991, 1992). species of Homo, whatever that may be. Subsequently, these fossils have been used as type specimens In South Africa, fewer fossils from the period 2.6 to 2.0 for other species. In 1986, KNM-ER 1470 became the type Ma or older have been suggested to represent either early of Australopithecus rudolfensis (Alexeev 1986); Wood (1991, Homo or a species of Australopithecus derived in the direction 1992) provided substantial anatomical reasoning to support Table 2. Elements commonly associated with KNM-ER 1470 as Homo rudolfensis

Specimens Element Main attributes and reasons for previous association with KNM-ER 1470a Type specimen: KNM-ER 1470 Cranium ϩ partial tooth roots Large cranial vault (750 cm3); flat face with anterior placement of zygomatic takeoff (mesial end M1); P3 with three roots “incompletely divided double root”; P4 probably double rooted (Wood 1991: 74). Craniodental specimens: KNM-ER 1590 Upper dentition and cranial fragments Large vault size and shape and large tooth crown size (Wood 1991:251). However, root form cannot be compared as these are yet to form in this subadult, and crown form is not preserved in 1470. This specimen formed the basis for arguments of large crown size in H. rudolfensis (see Leakey et al. 2012). KNM-ER 3732 Partial calotte and left zygoma Large vault size, size and robusticity of the frontal bone’s contribution to the face, and the anterior inclination of the malar region (Wood 1991:251). However, no teeth are present and supraorbital and orbital region differs from 1470. Zygomatic and palatal portions are incompletely preserved. Does not add to our knowledge of crown morphology. KNM-ER 3891 Cranial fragments including maxilla fragments Anterior takeoff of the zygomatic at distal P4; three-rooted P3 and P4; large entoglenoid (although construction differs from that of 1470; Wood 1991:135, 251). This fragmentary specimen may affili- ate with 1470 but does not add to our knowledge of crown morphology or cranial size. Mandibulodental specimens:b KNM-ER 819 Mandible fragment Similar in size and shape to 1802, sharing everted base and P roots. Superficial resemblance to Paran- thropus boisei, but lacks extreme specializations (Wood 1991:251). Ties to KNM-ER 1802 but not necessarily 1470 (see Leakey et al. 2012). KNM-ER 1482 Mandible Similar in size and shape to 1802. Similar superficial association with P. boisei as above (Wood 1991: 251). Ties to 1470 (see Leakey et al. 2012). KNM-ER 1483 Mandible fragment Large corpus size, and symphysis align with mandible 1802, but premolar roots are simpler (Wood 1991:251). Ties to KNM-ER 1802 less strong for corpus shape and premolar form. KNM-ER 1801 Mandible fragment Similarities to KNM-ER 1802 in corpus, symphysis, P roots and M3 (Wood 1991). Homo ϩ Australo- pithecus boisei-like features affine it with 1802 (Wood 1991:189). Ties to 1470 (Leakey et al. 2012). KNM-ER 1802 Mandible Mandibular robusticity and dental size and root complexity consistent with the inference that 1470 was adapted to a heavy masticatory pattern (Wood 1991:251). No direct tie to KNM-ER 1470; but, as noted by Wood, Stringer argued, “The anterior placement of the root of the ascending ramus and extramolar sulcus may be consistent with KNM-ER 1470 zygoma position” (Stringer 1986).How- ever, see Leakey et al. (2012). UR-501 Mandible Mandibular morphology similar to KNM-ER 1802 with especial reference to the broad Ps and plate- like P roots (Bromage, Schrenk, and Zonneveld 1995). Strong ties to KNM-ER 1802 but not neces- sarily 1470. Postcranial specimens: KNM-ER 813 Talus More similar to human than australopithecine tali (Wood 1992). Tie to KNM-ER 1470 is based on presumed size. Could be other early Homo. KNM-ER 1472 Femur Larger size and more humanlike anatomy than femora from Olduvai (Wood 1992). Tie to KNM-ER 1470 is based on presumed size. Could be other early Homo. KNM-ER 1481A, B Femur/tibia Larger size and more humanlike anatomy than femora from Olduvai (Wood 1992). Tie to KNM-ER 1470 is based on presumed size. Could be other early Homo. Note. The list of referred specimens is taken from the most commonly followed delineation of H. rudolfensis, that presented by Wood (1991, 1992), with the additional inclusion of UR-501, the mandible from Malawi that is considered nearly identical to but with smaller premolars than KNM-ER 1802 (Bromage, Schrenk, and Zonneveld 1995). a Main attributes or reason for association with KNM-1470 as provided by original author. Italicized comments provided by Anto´n and/or Leakey et al. (2012). b Note added in proof: I consider the newly described cranial (KNM-ER 62000) and mandibular (KNM-ER 60000 and 62003) specimens to associate with KNM-ER 1470 to the exclusion of KNM-ER 1802 for the reasons articulated by Leakey et al. (2012). Anto´n Early Homo: Who, When, and Where S283 the specific designation and its association with genus Homo. ER 1590 and KNM-ER 1802 have become the de facto ex- He also suggested the possibility that a number of other cra- amples for H. rudolfensis maxillary and mandibular dental nial, mandibular, dental, and postcranial remains from Koobi morphology, respectively (e.g., Schrenk, Kullmer, and Brom- Fora might be included as well (see table 2). In 1995, KNM- age 2007; Spoor et al. 2007; Wood and Richmond 2000). ER 1813 became the type specimen of Homo microcranous While parsimony may suggest that this KNM-ER 1802/UR- (Ferguson 1995). Because the issue of affinity of OH 7, and 501 group of mandibles may go with the 1470 face, there is hence the H. habilis name, has never been adequately ad- no particular anatomical argument that they must.2 dressed (see below), it is most prudent to set it aside for the Alternatively, because of the better preservation of KNM- moment and work from the specimens that are more com- ER 1813, the 1813 morph can be extended to include other plete. So as not to confound the argument, I will refer here maxillae from Kenya and Tanzania (e.g., OH 13, OH 62, OH to these specimens and any associated fossils as the 1813 and 65, KNM-ER 1805). OH 65 was initially aligned with KNM- 1470 groups, respectively. The main specimens assigned to ER 1470 largely on the basis of size and malar position (Blu- these groups and their earlier attributions are listed in table menschine et al. 2003; Clarke 2012). However, zygomatic root 3. position, midfacial prognathism, anterior maxillary contours, As was argued in the initial proposal for two taxa, there arcade shape, and tooth position differ so markedly between are important differences in facial structure and perhaps den- the two as to preclude their inclusion in the same group to tal size between the two specimens (Wood 1991, 2009). Re- the exclusion of the 1813-group specimens (see Rightmire gardless of how it is hafted to the vault (Bromage et al. 2008), and Lordkipanidze 2009; Spoor et al. 2007).3 Thus, if two the KNM-ER 1470 face is quite flat, with a forward-facing morphs are accepted, OH 65 must be placed with the 1813 malar region and relatively deep and tall zygomatics that are group. Because KNM-ER 1813 also retains some maxillary anteriorly inclined. The anterior tooth row and the maxillary teeth, the maxillary dental anatomy of the group is known bone that holds it are somewhat retracted and narrow across and can be compared for consistency with those dentitions the canines (Wood 1985, 1991). Although the anatomy shows that are housed in the maxilla mentioned above. And because superficial similarities to the Paranthropus face, zygomatic some of these other maxillae have associated mandibles (e.g., position causes the facial flatness in Paranthropus, whereas OH 13; KNM-ER 1805), the mandibular dental anatomy and the midface itself is flat in KNM-ER 1470. Wood suggested bony morphology can be directly seen and linked to isolated additional parallels between the two, including postcanine mandibles. The 1813 group can thus be formed on the basis megadontia (albeit less marked in KNM-ER 1470). He thus of direct anatomical ties. described the 1470 morph as a large-brained but large-toothed The affinity of the type of H. habilis,OH7,toeitherof early Homo. Alternatively, the KNM-ER 1813 face is more these groups remains unclear. OH 7 is a difficult type from conservative in its structure, with a moderately prognathic which to judge the anatomy of the species because it com- midface, a rounder anterior maxilla, and somewhat more pos- prises a subadult, a partial mandible that is also deformed teriorly positioned but more vertical zygomatic arches. The taphonomically, a set of parietals that indicate approximate KNM-ER 1813 face also houses relatively smaller teeth. vault size but provide little definitive anatomy, and some iso- If we accept that the structural differences in the face in- lated hand bones presumed to be the same individual. The dicate two different species, the constituents of the groups scenario that has found the most favor links OH 7 with the can only be built based on direct anatomical associations 1813 group, thus named H. habilis (e.g., Schrenk, Kullmer, between other fossils and either 1470 or 1813. KNM-ER 1470, and Bromage 2007; Wood 1991). The 1470 group (which while preserving a face and vault, lacks maxillary dental crown according to those authors includes the 1802/UR-501 man- morphology and does not preserve a mandible. Table 2 de- dibles) is then H. rudolfensis. OH 7 has often been suggested lineates the specimens typically associated with KNM-ER 1470 to align with the 1813 group on dental crown anatomy, al- (aka Homo rudolfensis) and the original reason for so doing (mostly after Wood 1991, 1992). The large size of the vault, 2. Note added in proof: Recently described Kenyan fossils (KNM-ER tooth roots, and flat anterior face suggested that large indi- 60000, 62000, 62003) confirm facial differences between KNM-ER 1470 viduals with a “heavy” masticatory pattern might be the best and 1813 but not absolute molar size differences. These fossils also seem fit. However, there are no discrete, derived anatomical ar- to exclude the 1802 group of mandibles from the 1470 group (Leakey guments beyond vault size and inferred dental size for linking et al. 2012). 3. The main issue here is the contention that OH 65’s lower nasal KNM-ER 1470 with KNM-ER 1590, until recently the only region; roots of the zygoma; and broad, flat, nasoalveolar clivus were complete maxillary dentition assigned to H. rudolfensis.Al- most similar to KNM-ER 1470’s. However, this is not the case. OH 65 ternatively, the table highlights the strong arguments, includ- is much more prognathic subnasally and has more posteriorly positioned ing premolar root form, for linking some of the mandibular zygomatic roots than does KNM-ER 1470. Additionally, OH 65’s na- remains (e.g., KNM-ER 819, UR 501) with one another and soalveolar clivus is arched at the alveolar margin where 1470 is flat, and its canine alveoli are not part of the anterior tooth row, whereas those with the more complete mandible KNM-ER 1802. However, of 1470 are. In short, OH 65 is a large version of KNM-ER 1813 and there are again no linkages between these mandibles and shows none of the structural features that are critical to erecting the 1470 KNM-ER 1590 or 1470 except for size. Despite this, KNM- morph. ; ?1813 group b b Homo Homo Homo Homo Homo Homo Homo Homo Homo Homo 1813 group H. habilis (Blumenschine et al. 2003; Clarke onneveld 1995) 1802 group H. habilis condition (Moggi-Cecchi, Tobias, and Beynon 1998) ? (Suwa, White, and Howell 1996) Early Homo (Kimbel et al. 1996) Early (Prat et al. 2005) Early (Alexeev 1986) 1470 group H. habilis H. habilis H. rudolfensis (Wood 1991) Early (Wood 1991) Early (Wood 1991) Early (Wood 1991) 1802 group (Bromage, Schrenk, and Z (Wood 1991)(Wood 1991) Early Early (Wood 1991)(Wood 1991) 1802 group 1802 group (Johanson et al. 1987) 1813 group (Leakey et. al. 1989) Early (Leakey, Tobias, and Napier 1964) Early (Leakey, Clarke, and Leakey 1971) 1813 group (Wood 1991) 1813 group (Leakey, Tobias, and Napier 1964) 1813 group (Leakey, Tobias, and Napier 1964) (Howell 1978; Wood 1991) 1813 group (Spoor et al. 2007) 1813 group (Wood 1991:270) 1813 group by original attribution and species group in this paper rudolfensis sp. indet. (Hill et al. 1992), Hominidaesp. gen. (Kimbel sp. and indet. Rak (Martyn 1993) and Tobias 1967) ? ? sp. aff. sp. aff. sp. aff. ) A. ( 2012) Homo H. habilis H. habilis H. habilis H. habilis H. habilis H. rudolfensis H. habilis H. habilis Homo Homo H. H. rudolfensis H. rudolfensis H. rudolfensis H. habilis H. rudolfensis H. rudolfensis H. rudolfensis H. habilis Homo Homo Homo H. rudolfensis H. rudolfensis H. habilis ϩ mandible partial skeleton ϩ ϩ cranial fragments maxilla dentition Similar to 1470, which they include in fragmentary skeleton ϩ ϩ ϩ ϩ attributed to earliest or early cranial fragments fragments Mandible Mandible Mandible partial Maxilla fragment : c b b erectus Homo a OH 65 Maxilla OH 62 Maxilla KNM-ER 3735 Cranial fragments KNM-ER 42703 OH 16 Maxillary and mandibular teeth OH 24 Cranium trampled KNM-ER 1805 Calvaria OH 13 Maxilla, mandible, teeth, cranial KNM-ER 1590 Cranial fragments/teeth OH 7 Mandible KNM-BC 1 Temporal KNM-ER 3732 Partial cranium Stw 151 Cranial fragments—juvenile Derived toward an early KNM-ER 1470 Cranium Sts 19 Cranial base KNM-ER 3891 Cranial fragments/maxilla KNM-ER 819 Mandible fragment KNM-ER 1482 KNM-ER 1813 Cranium A.L. 666-1 Palate KNM-WT 42718 Molar Omo E-G teeth Miscellaneous teeth KNM-ER 1483KNM-ER 1802 Mandible fragment Mandible KNM-ER 1801 KNM-ER 1501 Mandible partial UR-501 East Africa: South Africa: East Africa: 2.0 Ma: 2.0–1.5 Ma non- Table 3. Main fossil specimens Specimen1 Element Common attribution Species/group

S284 erectus erectus aff. aff. Homo Homo Homo 0000, 62000, 62003) are H. erectus H. erectus H. erectus H. erectus H. erectus ?Early Homo H. erectus H. erectus H. erectus H. erectus Homo Homo H. erectus H. erectus H. erectus H. erectus (Grine 2001) (Kimbel, habilis aff. H. erectus sp. indet. (Grine 2001) Australopithecus africanus (Curnoe 2010) Homo Homo sp. indet. (Grine 2001) Homo H. gautengensis (Howell 1978); (Rightmire 1979) (Curnoe and Tobias 2006) Early newly described KNM-ER 60000, 62000, and 62003. H. habilis (Clarke, Howell, and Brain 1970); (Kuman and Clarke 2000) Early H. erectus ; Gabunia et al. 2000; Rightmire and Lordkipanidze 2009) H. habilis erectus ergaster (Wood 1991) (Wood 1991) (Wood 1991) (Hughes and Tobias 1977); some view as H. ergaster p erectus erectus erectus habilis (Heberer 1963); (Walker, Zimmerman, and Leakey 1982) (Leakey and Walker 1985) (Rightmire 1979) (Asfaw et al. 2002) (Asfaw et al. 1992) (Howell 1978; Robinson 1961); (Robinson 1961); (Leakey and Walker 1985) ( (Spoor et al. 2007) (Walker and Leakey 1993) aff. aff. aff. (Howell 1978); aff. possibly aff. sp. indet. aff. (Kuman and Clarke 2000) or type of Johanson, and Rak 1997; Tobias 1991; Walker 1981); Homo Homo Homo H. erectus Homo H. erectus Homo Homo H. leakeyi H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus Homo H. erectus H. erectus H. erectus teeth ely belong to the 1470 group along with teeth ϩ ϩ cranial fragments ϩ skeleton ϩ mandible, partial Reconstructed partial cranium Calvaria Cranial fragments Calvaria Mandible partial Partial mandible -like: ey et al. (2012), KNM-ER 1482 and 1801 lik c Homo erectus c d c c c KNM-ER 820KNM-ER 992KNM-ER 1808 Mandible—subadult Mandible Skeleton KNM-ER 730 Occipital, parietal, frontal, SK 27 Crushed cranium (juvenile) KNM-ER 3733 Cranium OH 12 Stw-80 Mandible partial, crushed SK-45 Partial mandible KNM-ER 3883 Cranium Stw-53 Daka KGA 10-1 SK-15 SK-847Dmanisi (multiple) Partial face Crania, mandibles, postcrania KNM-ER 42700 Calvaria KNM-WT 15000 Skull OH 9 East Africa South Africa: South Africa: Georgia: May be older than 2.0 Ma. Following Leak May be younger than 2.0 Ma. Is or may be younger than 1.5 Ma. 2.0–1.5 Ma not included, but see Leakey et al. (2012). Note. Most isolated teeth, mandible fragments,a and specimens youngerb than 1.5 Ma arec omitted. Newly describedd specimens from the 1470 group (KNM-ER 6

S285 S286 Current Anthropology Volume 53, Supplement 6, December 2012 though it should again be noted that no dental remains are langes, which presumably indicate some arboreal behavior firmly associated with the 1470 group (the calvaria retains (Tocheri et al. 2007). However, other aspects of especially the only partial roots), and it is unclear, therefore, how or whether thumb suggest precision grip abilities more derived toward the groups differ in dental occlusal anatomy or size. Alter- human than ape capabilities (Susman and Creel 1979). The natively, OH 7’s roughly estimated cranial capacity (690 cm3; sizes and proportions of the limbs of the associated skeletons Tobias 1991) perhaps aligns it with KNM-ER 1470. If OH 7 are discussed below. is so placed, that group (p KNM-ER 1470 only ϩ OH 7) then becomes H. habilis, leaving the 1813 group as H. mi- Non-erectus Early Homo: Size and Proportions crocranous. Present data are, in my opinion, insufficient to choose between these scenarios or to show to which the 1802/ Given that at least two different facial morphs seem to coexist UR-501 group links. While future evidence may prove con- in time and space in East Africa, what can be said about size vincing, it is also possible that 1802/UR-501 represents a third and shape of non-erectus Homo? As currently constructed, the morph and that the affinities of OH 7 are with any of the 1470 group has a larger cranial capacity (750 cm3) than does three (see also Leakey et al. 2012). the 1813 group (510–675 cm3) with the caveat that OH 7 has It is generally agreed that there is some fossil evidence for not been assigned to either group (tables 5, 6). Additionally, at least one member of non-erectus early Homo in South more fragmentary remains, such as the OH 65 maxilla, con- Africa; however, there is no consensus concerning which spe- form well to the shape of the KNM-ER 1813 palate and teeth cies are present or whether these also occur in East Africa but are quite a bit bigger and could (but are not required to) (see also Grine 2005; Grine et al. 2009). The remains in ques- imply a larger cranial capacity for that group. Similarly, KNM- tion date (roughly) between 2.0 and 1.5 Ma and come from ER 1590, a fragmentary juvenile specimen whose parietals Sterkfontein, Swartkrans, and Drimolen. The Swartkrans re- suggest a large cranial capacity, has been included by some mains are most frequently linked with H. erectus and are in the 1470 group based on size and the presumption that discussed below. The Sterkfontein remains include isolated this group is large and the 1813 group small, but it could teeth, two partial mandibles, and the cranium Stw 53, whose instead affiliate with the 1813 group if size differences are not taxonomic identification and reconstruction is heavily con- substantiated. Yet even without such size extension of the 1813 tested (e.g., Curnoe 2010; Curnoe and Tobias 2006; Grine group, brain size among the well-preserved early Homo in- 2001; Grine et al. 2009; Kuman and Clarke 2000). The Sterk- dividuals (KNM-ER 1805; OH 13, 16, 24) is fairly continu- fontein cranial remains have been variously affiliated with ously distributed between the two end members, KNM-ER Homo (aff. habilis or sp. indet.; Kuman and Clarke 2000 for 1813 and 1470 (table 6). Such distribution suggests that av- the mandibles; Curnoe and Tobias 2006; Grine et al. 2009) erage ranges of cranial capacity will vary depending on who or Australopithecus (Kuman and Clarke 2000 for StW 53; is included in each group. On the basis of facial morphology, Clarke 2012). The isolated teeth from Sterkfontein and Dri- KNM-ER 1805 and OH 13 and 24 should be included in the molen lend strong support to the identification of an as yet 1813 group (OH 16 does not preserve facial anatomy), and unnamed early non-erectus Homo in South Africa (Grine et thus the upper end of this group is as much as 670 cm3, al. 2009). Because they do not affiliate strongly with the East substantially larger than KNM-ER 1813. Regardless of African teeth, following Grine (2001; Grine et al. 2009) they whether there is one or more species of early non-erectus are considered here simply as early non-erectus Homo. Homo, brain size across the entire group ranges from 510 to Postcranial remains of early East African Homo are few, 750 cm3. and fewer still are certainly associated with one of the cranial Dental size cannot be compared between the groups be- morphs (table 4). OH 7 has a partial hand. The OH 62 partial cause only the 1813 group has complete teeth that are certainly skeleton can be associated with the 1813 group on the basis associated with it; however, dental size can be assessed across of maxillary morphology. The KNM-ER 3735 fragmentary the entire early Homo sample and for the 1813 group alone skeleton is Homo, based on anatomy of the posttoral sulcus, (table 7). KNM-ER 1470 has been inferred to be large toothed mandibular fossa, and zygomatic, but of uncertain affinity. on the basis of preserved tooth roots. However, this inference Isolated elements of the lower limb—such as OH 8 (foot), is overstated given that especially the postcanine roots are OH 35 (distal tibia), and various hind limb fragments from observed low on the root and in oblique section. The max- Koobi Fora—have been tentatively assigned to Homo.How- illary dental metrics generally quoted for this species are from ever, for these isolated remains there is always some question KNM-ER 1590, which has extremely large teeth but as dis- as to which hominin they belong (see Gebo and Schwartz cussed above has no firm anatomical tie to KNM-ER 1470. 2006; Wood and Constantino 2007). If OH 8 is early Homo, Similarly, the mandibular dental metrics are from KNM-ER the ankle and “close-packed” arches may indicate a pattern 1802, which has large teeth but also has no firm anatomical of bipedalism similar to Homo sapiens (see Harcourt-Smith tie to KNM-ER 1470. Thus, the argument that the 1470 group 2007; Harcourt-Smith and Aiello 2004), although primitive is large toothed is circular because it is made on the basis of elements are retained as well. The OH 7 hand retains the specimens that have been placed in the group because of large primitive condition of the carpals and curvature of the pha- dental size resulting in the conclusion that the group has large Table 4. Main postcranial specimens attributed in this paper to earliest or early Homo in Africa and Georgia by original attribution and species group used in this paper

Body mass Specimen Element Common attribution Species/group estimate (kg)a East Africa: KNM-ER 1472 Femur Homo rudolfensis (Wood 1992) ?Early Homo 49.6 KNM-ER 1481A, B Femur, tibia H. rudolfensis (Wood 1992) ?Early Homo 57 KNM-ER 3228 Os coxae Homo ?erectus (Rightmire 1990) or H. rudolfensis (McHenry and Coffing 2000) Early Homo 63.5 OH 35 Tibia, distal H. habilis Early Homo 31.8 OH 62 Maxilla ϩ fragmentary skeleton H. habilis (Johanson et al. 1987) 1813 group ? OH 28 Os coxae H. erectus (Rightmire 1990) H. erectus 54 OH 34 Femur H. erectus (Rightmire 1990) H. erectus 51 KNM-ER 736 Femur H. erectus (Rightmire 1990) H. erectus 68.4 KNM-ER 737 Femur H. erectus (Rightmire 1990) H. erectus ? KNM-ER 1808 Multiple cranial and postcranial elements H. erectus (Walker, Zimmerman, and Leakey 1982) H. erectus 63.4 KNM-WT 15000 Skeleton ϩ skull H. erectus (Walker and Leakey 1993) H. erectus 51 Gona Pelvis H. erectus (Simpson et al. 2008) ?Homo 39.7 South Africa: SK-1896 Femur, distal Homo aff. erectus (Susman, de Ruiter, and Brain 2001) Homo aff. erectus 57 SK-2045 Radius, proximal Homo aff. erectus (Susman, de Ruiter, and Brain 2001) 53–58 SKX-10924 Humerus, distal (small) Homo aff. erectus (Susman, de Ruiter, and Brain 2001) Homo aff. erectus (30) SKW(SKX) 34805 Humerus, distal (large) Homo aff. erectus (Susman, de Ruiter, and Brain 2001) H. aff. erectus ? Georgia: Dmanisi (small) Multiple elements H. erectus (p H. ergaster; Gabunia et al. 2000; Rightmire and Lordkipanidze H. erectus 40.7 2009) Dmanisi (large) Multiple elements H. erectus (p H. ergaster; Gabunia et al. 2000; Rightmire and Lordkipanidze H. erectus 48.8 2009) Note. Only those bones useful in establishing stature or body weight are listed. Hand and foot elements excluded. a In addition to sources in a previous column of this table, body mass estimates follow table 8, Holliday (2012), Pontzer (2012), and Ruff, Trinkaus, and Holliday (1997). S288 Current Anthropology Volume 53, Supplement 6, December 2012

Table 5. Comparative brain and body size of Australopithecus and Homo

South Africa East Africa South Africa East Africa/Georgia Early A. sediba A. africanus A. afarensis non-erectus Homo H. aff. erectus Early H. erectus Brain sizea 420 (MH 1) 571 (Stw 505) 550 (A.L. 444-2) 510 (1813) . . . 638 (D3444) 485 (Sts 5) 485 (A.L. 333-45) 580 (1805) 655 (D2282) 443 (MLD 37/38) 400 (A.L. 162-28) 595 (OH 24) 690 (42700) 385 (Sts 60) 630 (OH 16) 727 (OH 12) 410 (Sts 71) 660 (OH 13) 775 (D2880) 680 (OH 7) 804 (3883) 750 (1470) 848 (3733) 909 (15000) 995 (Daka) 1,067 (OH 9) Mean 420 454–461 478 629 . . . 810 (w/Dmanisi) 863 (East Africa only) CV . . . 15.9 15.7 12.2 . . . 17.8 (w/Dmanisi) 15.9 (East Africa) Body mass/femur lengthb 35.7 (MH 2) 45.4/433.5 (Stw 99) 50.1/382 (A.L. 333-3) 63.5 (3228) 57 (SK 1896) 68.4 (736) 31.5 (MH 1) 41.3 (Stw 443) 48.2 (A.L. 333x-26) 49.6/401 (1472) 53–58 (SK 2045) 63.4/485 (1808) 40.7 (Stw 311) 45.6/375 (A.L. 827-1) 57/396 (1481) [30] (SKX 10924) 54/456 (OH 28) 38.4 (Sts 340) 45.4 (KSD-VP-1/1) 31.8 (OH 35) 51/429 (15000) 37.9 (Stw 389) 42.6 (A.L. 333-7) 31 (OH 8) 51/432 (OH 34) 34.2 (Stw 25) 41.4 (A.L. 333-4) —/315 (OH 62) 48.8 (Dmanisi large) 32.7 (Stw 392) 40.2 (A.L. 333-w-56) 40.7 (Dmanisi small) 32.5 (TM 1513) 33.5 (A.L. 333-8) 39.7 (Gona) 30.5 (Stw 102) 28/281 (A.L. 288-1) 30.3/276 (Sts 13, 34) 27.1 (A.L. 129a) 27.5 (Stw 347) 23.3 (Stw 358) Mean body mass 33 34 40 44 44 52 (w/Dmanisi) 55 (East Africa only) CV body mass/ femur length 9/— 18.7/— 20.2/16.3 33/13 32/— 19.3/8.7 (w/Dmanisi) 18.8/5.8 (East Africa) Note. Specimen numbers are in parentheses. Brain size in cm3; mass in kilograms; femur length in millimeters. a Endocranial capacity for A. sediba from Berger et al. (2010), for A. africanus from Neubauer et al. (2012), for A. afarensis from Holloway and Yuan (2004), and individually for Homo as indicated in table 6 of this paper. b Body mass estimates follow Pontzer (2012) and tables 4 and 8 of this paper. Femur length CVs are raw values not corrected for dimensionality. teeth. Across all of early Homo, then, molar size is somewhat al. 2007). There is also some evidence of difference between diminished over the condition in Australopithecus and some- the 1802 group and the 1813 group in both dental and man- what, but not significantly, larger than the condition in early dibular morphology. The former have relatively broader pre- H. erectus (table 5; Anto´n 2008). There is some suggestion molars with greater talonid development and differently that there may be a large-toothed morph, but it is unclear shaped roots, and the base of the mandible is everted and the whether this morph belongs to the 1470 group or not (see symphysis more vertical than the apparent condition in the note in table 7). 1813 group (Anto´n 2008; Schrenk, Kullmer, and Bromage Dental proportions and occlusal morphology can also be 2007, table 9.1); however, it is unclear to what extent these described for the 1813 group, which differs from Australo- differences may reflect intraspecific idiosyncratic variation in pithecus and H. erectus. Whether this morphology is unique mandibular size and robusticity. to this group of early Homo is unknown. The 1813 group Body size cannot be compared between the groups because shows buccolingual narrowing of its cheek teeth, especially only the 1813 group has associated postcranial remains (i.e., the molars, relative to Australopithecus, and its M2s are mostly OH 62 on maxillary form; table 3). OH 62 has been inter- rhomboidal in form. The third molar is large relative to M2, preted as small bodied and with relatively long and strong however, in contrast to the condition in H. erectus (Spoor et arms, but the specimen is very fragmentary (Haeusler and Table 6. Size comparisons of individual fossils of Homo habilis sensu lato and early Homo erectus sensu lato

Mass (kg) Group (1813 Geological Presumed Brain Mean body mass (kg) Range body mass (kg) from a b 3 c c 1 2 Specimen or 1470) age (Ma) sex size (cm ) from orbit area (k/a) from orbit area (k/a) postcrania M area M1 area M area M2 area Homo habilis s.l.: KNM-ER 1813 Homo microcranous 1813 1.9 Female 510 34.9/31.0 24.3–50/36.9–35.5 . . . 1,560 . . . 1,640 . . . KNM-ER 1805 1813 1.9 Male 580 ...... 1,770 . . . 1,730 . . . OH 24 1813 1.8 Female 595 30.3/36.3 21.1–43.4/31.5–41.8 . . . 1,790 . . . 1,890 . . . OH 16 ? 1.8 ? 625–638 ...... 2,010 1,870 2,020 2,330 OH 13 1813 1.6 Female 650–675 ...... 1,640 1,510 1,810 1,700 OH 7 Homo habilis ? 1.8 Male 647–690 ...... 1,760 ... 2,110 KNM-ER 60000 1470 1.8 ? ...... 1,460 . . . 1,790 KNM-ER 1590 ? 1.85 ? ...... 2,090 . . . 2,570 . . . KNM-ER 62000 1470 1.9 Female ...... 1,850 . . . 2,016 . . . KNM-ER 1470 Homo rudolfensis 1470 2.03 Male 750 45.5/77.4 33.8–69.9/64.1–93.6 ...... Homo erectus s.l.: DmanisiD3444 1.7 Male 638 ...... D2282/D211 1.7 Female 655 ...... 1,560 1,550 1,560 1,420 KNM-ER 42700 1.55 Female 690 ...... OH12 1.2 Male 727 ...... D2280 1.7 Male 775 ...... KNM-ER 3883 1.5 Male 804 57.4/83 39.9–57.5/68.2–101 kg ...... KNM-ER 3733 1.8 Female 848 59.2/88.8 41–85.3/72.5–108.7 kg ...... 1,860 . . . KNM-WT 15000 1.5 Male 909 59.9/ . . . 41.5–86.4/ . . . 51 1,490 1,410 1,500 1,520 Daka 1.0 ? 995 ...... OH9 1.5 Male 1,067 ...... Note added in proof. Data from recently described fossils from the 1470 group (Leakey et al. 2012) are included here but could not be included in text discussion. a Species names for which these serve as type specimens are noted by the specimen number. b The sex of all specimens is unknown. These estimates represent the most frequent inferences and should be considered uncertain at best. c Body mass estimates from orbital area are from k p Kappelman (1996) and a p Aiello and Wood (1994). S290 Current Anthropology Volume 53, Supplement 6, December 2012

Table 7. Dentognathic summary statistics for Homo habilis sensu lato and early Homo erectus from Africa and Georgia

Africa Africa and Georgia KNM-ER 1590 KNM-ER 1802 1813 group Homo habilis sensu lato Early Homo erectus

M1 buccolingual . . . 130 119.3/6.7 (3) 123.8/9.0 (8) 119.2/7.6 (5)

M1 mesiodistal . . . 148 137.6/0.6 (3) 138.5/6.1 (8) 132.2/6.5 (5)

M1 area . . . 1,920 1,610/118 (3) 1,705/181 (8) 1,592/131 (6) M1 buccolingual 148 . . . 132.3/2.9 (6) 134.9/6.0 (8) 129.2/6.8 (4) M1 mesiodistal 142 . . . 128.3/5.1 (6) 132.3/8.7 (8) 126.2/3.8 (5) M1 area 2,090 . . . 1,695/88 (6) 1,784/181 (8) 1,630/127 (5)

Corpus height M1 . . . 38 29.3/2.7 (3) 32.6/4.3 (11) 29.4/2.9 (6)

Corpus breadth M1 . . . 23 18.3/2.3 (3) 20.8/3.68 (10) 20.1/0/9 (6) Symphyseal height . . . 36 25 33.2/6.0 (5) 33.4/2.6 (4) Symphyseal depth (labiolingual) . . . 24.5 18 21.7/3.2 (5) 18.5/2.4 (4) Note. Individual fossils KNM-ER 1590 and 1802 and the 1813 group are also presented. Measurements in millimeters; mean/SD; (n). Note added in proof. Teeth of the 1470 group are now known from recently described fossils, and, while dental proportions differ, teeth are not always large. See Leakey et al. (2012) for discussion. New fossils are not included in these statistics, but see table 6 for some raw measures.

McHenry 2004; Richmond, Aiello, and Wood 2002; see also wrist bones, if they are of the same taxon (Tocheri et al. 2007). Holliday 2012). KNM-ER 3735 is larger than OH 62 but more Alternatively, hind-limb elongation remains debated because fragmentary and is not definitively assigned to either subgroup of uncertainties in reconstructions of long bone lengths from (Haeusler and McHenry 2007; Leakey et al. 1989). The range the highly fragmentary OH 62 and KNM-ER 3735. At least of body weights in these two specimens is 30–46 kg (66–101 one set of researchers argues that hind-limb elongation may lb.), respectively (tables 5, 8; Johanson et al. 1987; Leakey et have been present (Haeusler and McHenry 2004; Reno et al. al. 1989). Inferred stature is very approximately 118–145 cm 2005; but see Korey 1990; Richmond, Aiello, and Wood 2002). (311–48). Three other relatively large femora may be as- And the relatively long distal tibia of OH 35 may support signed to Homo sp. and would support the larger end of this this idea (Harcourt-Smith 2007). However, others have re- size range (149 cm/57 kg; Holliday 2012) if their attribution constructed the lengths differently and found the primitive is correct. However, two of the femora (KNM-ER 1472 and condition (i.e., long humerus, short femur; Richmond, Aiello, 1481) are often attributed either to the 1470 group (because and Wood 2002). More recent work, however, suggests that they are large; Wood 1992) or H. erectus (because they are hind-limb length proportions do not actually differ between somewhat flattened in the subtrochanteric area and are large; Australopithecus and Homo (see Holliday 2012; Pontzer 2012). Kennedy 1983a, 1983b; but see Trinkaus 1984), and they are So, while strength proportions appear to link OH 62 with also attributed to H. habilis sensu stricto by others (e.g., Australopithecus rather than later Homo, hind-limb elongation Schrenk, Kullmer, and Bromage 2007). One large partial os relative to body size would appear to be the same in all genera. coxae (KNM-ER 3228) has a geological age of 1.95 Ma. This It will be clear from the small number of fossils in each specimen is usually considered Homo and possibly H. erectus group and the disagreement about taxonomic assignments (Anto´n 2003; Rightmire 1990), although McHenry and Coff- that assessing sexual dimorphism will be nearly impossible ing (2000) suggest it may represent a large-bodied non-erectus for early Homo. Ideally, we should identify males and females Homo (their H. rudolfensis). Based on estimates of femoral by focusing on discrete characters that are independent of head size, a body mass estimate of 60–65 kg has been sug- overall body size, such as canine size and robusticity, and then gested (Ruff, Trinkaus, and Holliday 1997). Collectively, these assess male and female mean values from these independently remains suggest that the largest end of the non-erectus early assigned subgroups. The 1813 group is the only one in which Homo body size range is just under 5 ft. tall (150 cm), and it is possible to try to assess sexual dimorphism in this way, the average weight is 44 kg (range 31–65; tables 4–6, 8; see but such characters are few. Historically, the development of Holliday 2012; Pontzer 2012). cranial crests in KNM-ER 1805 over the condition in KNM- There is much discussion as to whether the limb propor- ER 1813 has been used to suggest the former is male and the tions of early Homo are as or even more primitive than Aus- latter female (Wood 1991:84). None of the other known spec- tralopithecus afarensis and therefore whether they differentiate imens in the group exhibit crests, leaving KNM-ER 1805 as early Homo from H. erectus. Based on cross-sectional strength the only male candidate at the moment. Cranial capacity dif- measures, the OH 62 humerus is relatively stronger compared fers little between the two specimens (510 vs. 580 cm3). How- with its femur than is true of recent humans and is like those ever, molar occlusal areas are larger in KNM-ER 1805. Yet of Pan (Ruff 2010; see also Richmond, Aiello, and Wood they are no larger than, say, OH 24, which lacks crests and 2002). Thus, OH 62, but not later Homo, likely participated is thus a presumed female. Here we face the issue of the in substantial arboreal locomotion as well as terrestrial (bi- possibility of large females and small males and the inadequate pedal) locomotion. This would be supported by the OH 7 sampling of the fossil record. For the postcranial skeleton, if Anto´n Early Homo: Who, When, and Where S291

Table 8. Body size in East African adult early non-erectus Homo and early East African and Georgian Homo erectus individuals and isolated elements

Africa Georgia Inferred Early Homo Early Homo Adult H. erectus H. erectus H. erectus H. erectus adult adult isolated adult adult isolated adult Taxon OH 62 KNM-ER 3735 Homo sp.a KNM-ER 1808b individualsc elementsd individualse 775–638 1,067–690 עBrain size (cc) ...... 510–750 . . . 909 x p 629 x p 863 x p 686 Femur length (mm) [280–374] . . . 350 (1503) 480 ...... 386 400 (1472) 395 (1481) ...... x p 383.75 x p 498 x p 454.5 . . . 473 Range (n) [280–374] (1) . . . 350–400 (4) 480 (1) 480–517 (2) 430–500 (4) 386 (1) 466–480 (2) Stature (cm): Mean 118 . . . 145 173 179 174 155 170 Range (n) ...... 173–185 (2) 161–186 (4) 145–166 168–173 (2) Body mass (kg): Meanorbit ...... 36.9k ...... 58.8k ... 48.2 a 85 a Femur head mass estimates ...... 49.6 (1472) 63.4 51 (15000) 49.6 (D4507) 57 (1481) Mean postcrania 33 46 48 59 64.5 (2) 54.75 48.8 large 63 57 (2) 40.2 small Range (n) ...... 21–77 . . . 63–68 (2) 51–68 (4) 40–49.6 (3) 55–63 (2) a KNM-ER 1503 is assigned to either Homo habilis or Australopithecus boisei, as are most specimens of this age from Koobi Fora (McHenry 1991); “k” and “a” refer to orbitally estimated mean body masses from Kappelman (1996) and Aiello and Wood (1994); femur head estimates from Holliday (2012); parenthetical number next to femur value is the specimen number providing that value. Square brackets are estimates. b KNM-1808 mean body mass values from Ruff and Walker (1993), top, or Ruff, Trinkaus, and Holliday (1997), bottom. c Adult individuals are KNM-1808, and adult estimates for KNM WT 15000 femur, stature, and body mass following either Ruff and Walker (1993), top, or Graves et al. (2010); Ohman et al. (2002) provide even smaller stature estimates for KNM-WT 15000. d Femora: KNM-ER 736 and 737, OH 28 and 34. e Mass data are for large and small adult individuals (see Pontzer 2012), and range estimates include other elements (Holliday 2012). the small OH 62 skeleton is female and the larger KNM-ER significantly greater (table 5). Plavcan (2012) provides a fuller 3735 is male, then if they are typical of their sexes, sexual discussion of the options for considering size dimorphism in dimorphism in body mass could be as much as 1.5 (male/ these taxa. female weight dimorphism as compared with chimpanzees at about 1.3 and H. sapiens about 1.1). Alternatively, one could Homo erectus sensu lato (1.9–? Ma) use CVs from the certain members of the 1813 group, al- though this may give an artificially low value because it is not In the early part of its range with which we are concerned, clear how to handle some of the larger specimens, such as Homo erectus overlapped for nearly half a million years with KNM-ER 1590. And using the overall CV also implicitly as- other groups of early Homo in Africa, principally the 1813 sumes that size differences and sex differences are the same group, whose last appearance datum is 1.44 Ma (fig. 1; see thing. In the absence of discrete characters to indicate sex, Spoor et al. 2007). The earliest H. erectus (at about 1.8–1.9 this may be a necessary assumption, but it is worth noting Ma) are found in Koobi Fora, Kenya, and the species persists the confounding issue (see also Plavcan 2012). CVs for upper in Africa until about the Brunhes-Matuyama boundary (0.78 and lower first molar area are 5.2 and 7.3, respectively, and Ma; fig. 1; Asfaw et al. 2002; Feibel, Brown, and McDougall CVs for capacity are 9.9. These values are lower than those 1989; Potts et al. 2004). Homo erectus is best known from for early African and Georgian H. erectus, particularly for Kenya and Tanzania, although Ethiopian and South African cranial capacity. If we take instead all the early non-erectus specimens also exist (e.g., Asfaw et al. 2002; Robinson 1953). Homo, regardless of group affiliation, the cranial CVs are still The earliest African H. erectus quickly dispersed into Asia by lower than those for H. erectus, but their body mass CVs are 1.7–1.8 Ma (Gabunia et al. 2000; Swisher et al. 1994). The S292 Current Anthropology Volume 53, Supplement 6, December 2012 species persists in Asia and Island Southeast Asia through at Georgia, Kenya, Tanzania, and perhaps Ethiopia suggest sub- least the middle if not the late Pleistocene (Indriati et al. 2011; stantial overlap in absolute size with earlier Homo species Shen et al. 2009; Swisher et al. 1996).4 Given interest here in (tables 5–7; Anto´n 2004; Gabunia et al. 2000; Potts et al. 2004; the origin and evolution of Homo, I consider only the early Rightmire 1979; Simpson et al. 2008; Spoor et al. 2007; Vekua African and Georgian record. et al. 2002). Although absolutes of size do not differ, some proportions Homo erectus: Taxa, Individuals, and Anatomy do, and so individuals of H. erectus are relatively easy to differentiate from all other early Homo on the basis of cra- Like Homo habilis, H. erectus sensu lato is an umbrella taxon niodental remains. Early H. erectus tends to have somewhat that may include nested sets of other taxa (table 1). Those smaller occlusal areas and fewer roots than other early Homo who split the larger taxon in two usually refer to the African/ but relatively larger crowns and more complex roots (espe- Georgian members as Homo ergaster based on the type spec- cially premolar) than do modern humans (table 7; Gabunia 5 imen KNM-ER 992 (Groves and Mazek 1975). Most recently, et al. 2000, 2001; Indriati and Anto´n 2008). Crowns, especially Homo georgicus (Gabunia et al. 2002) was named to accom- molars, tend to be buccolingually narrower compared with modate morphology in the Georgian remains that is argued length and less bulbous than in early Homo, with cusp apices to combine more primitive traits (especially of the face and closer to the outer margins of the tooth than in other early brain size) than in the earliest African H. erectus. However, Homo (Anto´n 2008; Indriati and Anto´n 2008). Homo erectus this variation is easily encompassed within early African H. also shows size reduction along the molar row with the third erectus (Anto´n 2003; see also Baab 2008; Rightmire and Lord- molar reduced or similar in size to M2 (Spoor et al. 2007). kipanidze 2009), which also shows clear signs of size-related And early H. erectus jaws are relatively more lightly built with shape changes with cranial capacity (Anto´n et al. 2007; Spoor narrower extramolar sulci than in early Homo (Grine 2001). et al. 2007). And the derived characters shared by the Georgian The H. erectus symphysis is thinner (anteroposterior), the and recently discovered small-brained African specimens genioglossus pit is relatively lower, and the postincisive plane, unite them taxonomically (Spoor et al. 2007). For the purpose although obliquely oriented, is not quite so pronounced as of discussion here, it makes little difference whether the Far in other early Homo (Anto´n 2008). East Asian and African/Georgian hominins are seen as re- Although general vault thickness scales with cranial capacity gional demes of one species, as two distinct species, or even in H. erectus and other early Homo, H. erectus shows species- multiple species, although I favor the former interpretation typical examples of thickening (Anto´n et al. 2007; Spoor et (table 3; Anto´n 2003). al. 2007). These include (1) essentially continuous supraor- As will be clear from the discussion of the genus, H. erectus bital tori of variable thickness associated with a posttoral shelf/ is now considered to take the first major anatomical and sulcus that may be continuous, (2) occipital tori that are behavioral steps in the direction of a “modern human” body continuous but somewhat variably expressed, often contin- plan (Anto´n 2003; Anto´n et al. 2007; Walker and Leakey uous with the angular tori and mastoid crests and often as- 1993). Although the species was not identical to Homo sapiens sociated with a supratoral sulcus, (3) angular tori, and (4) in size or shape, H. erectus bodies and brains were larger and midline (sagittal, bregmatic, and frontal) keels. their teeth and especially jaws were somewhat diminished in Homo erectus also differs from other early Homo and mod- size, on average, compared with those of earlier members of ern humans in other aspects of the cranium. The occipital Homo (Anto´n 2008). However, their teeth were larger and squama is relatively short, and the petrous temporal is more their brains smaller than in later Homo. Their lower-limb sagittally oriented and angled relative to the tympanic portion skeleton was relatively elongated compared with body mass (i.e., petrotympanic angle reduced; Rightmire and Lordki- over the condition in Pan, and their upper limbs were some- panidze 2009; Weidenreich 1943; although the base of earlier what foreshortened over the condition in Australopithecus and Homo is not well known). The glenoid fossa is relatively perhaps other early Homo (Holliday 2012; Pontzer 2012). broader anteroposteriorly (compared with mediolaterally) That said, newly discovered small-sized individuals from than in other early Homo (Spoor et al. 2007). The face is described as more similar in proportions to modern humans 4. Throughout the paper I use the traditional chronological delineation than with other early Homo (Bilsborough and Wood 1988; of the Plio/Pleistocene boundary as occurring at 1.8 Ma, the onset of Wood and Richmond 2000); however, the positioning and severe northern hemispheric glaciation. 5. While this is the most common nomen, it should be noted that form of the zygomatics and supraorbital torus is more similar many of the often included specimens represent types for earlier named to the 1813 group than to KNM-ER 1470, as is relative facial species (i.e., Homo (T.) capensis [Swartkrans 15; Robinson 1953]; Homo breadth, which is greatest at the midface in 1470 but at the (At.) mauritanicus [Ternifine 1; Arambourg 1954], and Homo leakeyi [OH superior face in the other groups. 9; Heberer 1963]; table 1); thus, the earliest of those included should While there again is some difference of opinion as to tax- provide the group name. This has not been the case, however, because these earlier types were not included when the species was named and onomic affinities of the South African fossils, craniodental are not consistently included in Homo ergaster by all scholars (e.g., Wood remains from Swartkrans are likely to represent either H. 1991:276). erectus (as discussed above) or something very erectus-like. Anto´n Early Homo: Who, When, and Where S293

Two mandibles, SK 15 and SK 45, were the first at Swartkrans differences are smaller between early H. erectus and the 1813 to be recognized as Homo (originally as Telanthropus capensis; group (excluding KNM-ER 1802 and 1590) and are not sta- Broom and Robinson 1949; Grine 2001; Grine et al. 2009; tistically significant for individual teeth in any event (Anto´n Robinson 1961). The most compelling evidence, however, is 2008). Relative molar cusp proportions and molar size rela- the SK 847 partial face that shows strong affinities with early tionships do, however, sort early H. erectus from early Homo East African H. erectus (Anto´n 2003; Clarke, Howell, and (Grine et al. 2009; Spoor et al. 2007). Brain 1970; Kimbel, Johanson, and Rak 1997; Walker 1981). Body size range is quite substantial as well (tables 4, 5, 8). Given this strong resemblance, the postcranial remains at South African and East African H. erectus are similar in size, Swartkrans that differ from those of Paranthropus are most although there are only a few South African remains for which usually assigned to Homo aff. erectus (Susman, de Ruiter, and body size can be estimated. The Georgian remains are 17%– Brain 2001). 24% smaller (40–50 kg, 146–166 cm) on average than early The postcranial record for early East African H. erectus is East African H. erectus (51–68 kg, 160–185 cm) depending far better than that of other early Homo.InAfrica,asingle on whether the Gona pelvis is included. This difference may well-preserved skeleton, KNM-WT 15000, is the main data be the result of a categorization bias in Africa that has tended point, but this information is augmented by a second partial to place smaller isolated postcrania into early Homo and larger skeleton, KNM-ER 1808, and a number of large isolated el- into H. erectus. The Gona pelvis (Simpson et al. 2008), if ements (tables 4, 8). We should be cautious that the isolated substantiated as H. erectus, would lower the body size range elements could, however, represent other early Homo.Ad- for Africa to perhaps as little as 120 cm/39.7 kg. In light of ditionally, in Georgia both adult and subadult skeletal ele- the small-headed remains from Ileret (Spoor et al. 2007), ments, some associated, are known. Although little that is Olorgesailie (Potts et al. 2004), and Olduvai Gorge (OH 12; species specific can be attributed to the postcrania of H. Anto´n 2004), a small-bodied H. erectus in Ethiopia seems erectus, there is much that differs from Australopithecus.For plausible. However, the Gona pelvis is not associated with example, H. erectus has enlarged articular surface areas of long cranial remains, and Ruff (2010) argues that the pelvis is more bones, thick cortical bone particularly in the lower limb, and likely Australopithecus or Paranthropus. Without Gona, early an anteroposteriorly flattened (platymeric) femur (Weiden- H. erectus stature estimates range from 145 to 185 cm (53– reich 1941), deep trochlea of the distal femur (Tardieu 1998, 61) and body mass estimates from 40 to 68 kg (88 to 150 1999), double meniscal attachments of the proximal tibia (but lb.). It should be noted, however, that although the remains see Dugan and Holliday 2009), reoriented pelves that are per- are fragmentary, Susman, de Ruiter, and Brain (2001) have haps less broad (but see Holliday 2012) but certainly more suggested that female Homo aff. erectus at Swartkrans may be capacious (Ruff 2010), a marked iliac pillar (i.e., acetabulo- as small as 30 kg (table 4). cristal buttress), and medial torsion of the ischial tuberosity Several lines of evidence suggest that early H. erectus was (Day 1971; Rose 1984). Thus, postcranially, H. erectus differs an accomplished striding biped with little arboreal locomotion from modern humans mostly in primitive characters, some in its repertoire. Hind-limb elongation is present in the as- of which are derived relative to nonhuman primates and oth- sociated skeletons from Africa (McHenry and Coffing 2000) ers of which may originate at the origin of Homo (e.g., Mc- and Georgia (Lordkipanidze et al. 2007). Whether this elon- Henry, Corruccini, and Howell 1976; Trinkaus 1984). Alter- gation began with H. erectus, at the base of the genus, or even natively, a number of aspects of the postcranial skeleton— at the base of the hominins, is a matter of debate (see Holliday including most of the hand and foot—are better known in 2012; Pontzer 2012), although it now seems likely that this other early Homo than in H. erectus. is a hominin adaptation. However, the forelimb is at least somewhat reduced in length compared with overall body size in H. erectus and with the condition in Australopithecus and Homo erectus: Size and Proportions perhaps early Homo. Cross-sectional properties of the hind Early H. erectus from Georgia and East Africa are moderately limb and forelimb indicate different patterns of strength be- bigger brained than other early Homo in East Africa. Adult tween Australopithecus afarensis and early H. erectus (Ruff cranial capacity ranges from 638 cm3 to a maximum of 1,067 2008, 2009), suggesting that like humans, H. erectus was a cm3 (tables 5, 6; Holloway 1983; Spoor et al. 2007; Vekua et predominantly terrestrial biped. The foot of H. erectus,which al. 2002). Several characters scale with cranial capacity, in- is recently known from Dmanisi, supports this notion by cluding cranial vault shape; smaller crania are more globular showing evidence of both transverse (metatarsal torsion) and (see Anto´n et al. 2007; Spoor et al. 2007). Although their longitudinal (first metatarsal base width) arches (Lordkipan- ranges overlap, the Georgian sample is smaller (638–775 cm3) idze et al. 2007; Pontzer et al. 2010). The hand skeleton is than the African (690–1,067), which may speak to issues of largely unknown. resource scarcity, extrinsic mortality, or climatic adaptation The shoulder and trunk appear to exhibit both primitive (seasonality). and derived conditions. The shoulder girdle retains an inter- Dental and mandibular size are smaller in early H. erectus mediate condition: The glenoid fossa of the scapula is oriented than in the entire early Homo group (table 7). However, the more superiorly (Dmanisi and KNM-WT 15000), the clavicle S294 Current Anthropology Volume 53, Supplement 6, December 2012 is relatively short compared with body size (proxied by hu- theless, they do not suggest a reduction of dimorphism in H. meral length), and humeral torsion is not as great as in mod- erectus over other groups. ern humans. Thus, the scapula was likely placed relatively less Given that by 1.8 or 1.9 Ma H. erectus coexists with two dorsally than in recent humans (Larson et al. 2007), which groups of early Homo, the origin of the taxon must predate has implications for throwing and possibly suggests less sta- this by some time. Craniofacial affinities are strongest with bility while running (Larson 2009). Like Australopithecus,the the 1813 group, suggesting that the A.L. 666 maxilla is one lumbar vertebral bodies of both Dmanisi and Nariokotome possible source population. are small relative to body weight, unlike the condition in modern humans (Latimer and Ward 1993; Lordkipanidze et Summary of Shifts in Homo al. 2007). Additionally, the African remains may suggest the primitive condition of diaphragmatic placement (Williams Early Homo appears in the record by 2.3 Ma. By 2.0 Ma at 2011) even though they appear to retain five lumbar vertebrae, least two facial morphs of early Homo (1813 group and 1470 as is the modal condition in humans (Haeusler, Martelli, and group) representing two different adaptations are present (ta- Boeni 2002; Haeusler, Schiess, and Boeni 2011; Williams ble 3). The 1813 group survives until at least 1.44 Ma. Early 2011). Homo erectus represents a third more derived morph yet and Other thoracic and pelvic features appear derived. The tho- one that is of slightly larger brain and body size but somewhat rax is broad superiorly and narrow inferiorly (based on the smaller tooth size. South African remains of early Homo are angulation of KNM-WT 15000’s ribs to thoracic vertebrae; present; however, they likely represent a separate species from Jellema, Latimer, and Walker 1993). This shape suggests that those in East Africa (see Grine et al. 2009). H. erectus had a relatively small gut (Aiello and Wheeler 1995), Small cranial remains from Georgia and Africa provide which has implications for diet quality and possible foraging evidence of substantial individual and perhaps populational shifts. Additionally, a number of pelvic features of H. erectus size variation within early H. erectus and indicate overlapping have been argued to be more similar to H. sapiens than to A. ranges of brain size with other early Homo. However, even afarensis and possibly H. habilis (Ruff and Walker 1993). with these new discoveries, H. erectus had a larger range (638– 1,067) and average (x p 810 cm3) of cranial capacity than did However, some of these features are from os coxae of indef- other early Homo (510–750,x p 629 cm3; Anto´n et al. 2007). inite species attribution, such KNM-ER 3228, and may also Currently, the overlap of cranial ranges is greater than is the be seen in non-Homo pelves such as the A. sediba adult, MH body size overlap; however, this may reflect sampling bias 2. Furthermore, Holliday (2012) contends that pelvic nar- between cranial and postcranial remains. rowing is not seen until H. sapiens. Although the fossil evidence is limited, average body and Until recently, sexual dimorphism was thought to be brain size increase appears to be an important shift between smaller in H. erectus than in Australopithecus because of dif- early Homo and Australopithecus and again between H. erectus ferentially large H. erectus females (Aiello and Key 2002; Leon- (sensu lato) and other early Homo (H. habilis sensu lato). ard and Robertson 1997; McHenry 1992; McHenry and Coff- Holliday (2012) and Pontzer (2012) document ∼33% increase ing 2000; Ruff 2002; but see Susman, de Ruiter, and Brain in average mass estimates between the genera Australopithecus 2001). Current evidence suggests, however, that cranial and and early Homo (all taxa from 2.0 to 1.5 Ma inclusive of H. body mass dimorphism may have been as large as in earlier erectus) and about a 10% increase between early non-erectus hominins (Pontzer 2012; Spoor et al. 2007). However, this Homo and Australopithecus. Body size estimates from post- conclusion is dependent on the frame of comparison. Plavcan cranial specimens that can be certainly assigned to H. erectus (2012) shows that there is a significant temporal component- from Africa and Georgia yield adult stature estimates between to-size variation in Homo. And he shows that when compared about 145 and 185 cm and adult body mass estimates of with intraspecific variation in extant apes, H. erectus size var- between 40 and 65 kg (tables 5, 8; Graves et al. 2010; Lord- iation (and perhaps dimorphism) is not particularly remark- kipanidze et al. 2007; McHenry 1992, 1994; Ruff and Walker able. To complicate matters, the assemblages make clear that 1993). The lower end of the range may decrease to as little not all small-sized individuals are females. In the small-sized as 120 cm and 30 kg if the Gona pelvis and Swartkrans post- Dmanisi population, some cranially robust probable male re- crania are certainly assigned to H. erectus. The sparser evi- 3 mains (D3444; 638 cm ) are absolutely small (Lordkipanidze dence for early non-erectus Homo overlaps the lower end of 3 et al. 2006). Similarly, at Olduvai, OH 9 (1,067 cm )andOH this range (118–150 cm and 30–60 kg) but is about 15% 12 (727 cm3) differ greatly in size but not robusticity (i.e., smaller than the combined early H. erectus mean (Georgia ϩ cranial thickness, superstructure development), which I in- Africa) and 37% smaller than the early African H. erectus terpret as within-sex variation. Nonetheless, cranial and body mean. Dimorphism as proxied by CVs seems no less than mass CVs are similar to one another (around 15%–19%) and earlier Australopithecus, but the variables used and the scale not substantially different than species of Australopithecus or of comparison seem to influence the results (table 5; and see early Homo (12%–20%; table 5). Given small and uncertain Plavcan 2012). samples, the values should not be weighed too heavily; none- Average differences in body size have implications for life Anto´n Early Homo: Who, When, and Where S295 history and ranging that may be of particular importance to Asfaw, Berhane, William H. Gilbert, Yonas Beyene, William K. Hart, Paul R. Renne, Giday WoldeGabriel, Elizabeth S. Vrba, and Tim D. White. 2002. niche differentiation in Africa. The overall larger size of early Remains of Homo erectus from Bouri, Middle Awash, Ethiopia. Nature 416: H. erectus and their different patterns of postcranial strength 317–320. if not length may indicate larger home range sizes and perhaps Baab, Karen L. 2008. The taxonomic implications of cranial shape variation in Homo erectus. Journal of Human Evolution 54:827–847. more open habitat for H. erectus, all of which may entail Berger, Lee R., Darryl de Ruiter, Steven E. 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Environmental and Behavioral Evidence Pertaining to the Evolution of Early Homo

by Richard Potts

East African paleoenvironmental data increasingly inform an understanding of environmental dynamics. This un- derstanding focuses less on habitat reconstructions at specific sites than on the regional trends, tempo, and amplitudes of climate and habitat change. Sole reliance on any one indicator, such as windblown dust or lake sediments, gives a bias toward strong aridity or high moisture as the driving force behind early human evolution. A synthesis of geological data instead offers a new paleoenvironmental framework in which alternating intervals of high and low climate variability provided the dynamic context in which East African Homo evolved. The Oldowan behavioral record presents further clues about how early Homo and Homo erectus responded to East African environmental change. Shifting conditions of natural selection, which were triggered by climatic variability, helped shape the adaptability of Oldowan hominins. Together, the behavioral and environmental evidence indicates the initial adaptive foundation for the dispersal of H. erectus and the persistence of Homo. In particular, overall dietary expansion made possible by the making and transport of stone tools compensated for increased locomotor and foraging costs and provided effective behavioral-ecological responses to resource instability during the early evolution of Homo.

The interval from ∼3.0 to 1.5 million years ago (Ma) broadly paleoenvironmental research has changed in recent years to- defines when Homo originated and Homo erectus first evolved ward a focus on environmental dynamics, that is, the nature and dispersed beyond Africa (Anto´n 2003; Anto´n and Swisher and tempo of environmental change that resulted from cli- 2004; Kimbel 2009; Kimbel et al. 1996; Pickering et al. 2011). mate variability, specifically the nonlinear interaction of in- Despite small samples of hominin fossils, particularly in the solation cycles, and the episodic effects of faulting and vol- interval between 3 and 2 Ma, there is a growing body of canism (e.g., deMenocal 1995, 2004; Feibel 1997; Potts 1998a, African climatic and paleohabitat data relevant to the early 2007; Trauth et al. 2010). The interaction of these factors is evolution of Homo (e.g., Cerling et al. 2011; deMenocal 2011; especially apparent in the paleoenvironmental records of the Potts 2007; Trauth et al. 2007). This time interval in Africa East African Rift System. also preserves the oldest definite stone tool flaking and the Throughout the period of hominin evolution, environ- spread of innovations such as carcass processing, overall di- mental dynamics inevitably altered the local and regional etary expansion, and the transport of resources across ancient abundance of water, vegetation, and food sources. This re- landscapes (de Heinzelin et al. 1999; Domı´nguez-Rodrigo et shaping of the overall landscape and of the time and space al. 2005; Plummer 2004; Potts 1991; Semaw et al. 2003). The distribution of resources had a pervasive influence on eco- goals of this paper are (1) to characterize the paleoclimate logical opportunities, competition, mortality, and reproduc- and overall environmental dynamics in which early Homo tive success. It also stimulated repeated population divergence evolved, (2) to consider how well the prevailing environ- and coalescence, the subsequent degree of allopatry of pop- mental hypotheses of human evolution explain the adapta- ulations, and thus eventual speciation in hominins and other tions of early Homo, and (3) to examine archaeologically vis- organisms (e.g., Potts 1996b, 1998b; Vrba 1985, 1995b). ible behaviors as part of the emerging adaptability of Homo. A rich array of paleoenvironmental data sets offers time Paleoenvironmental research on human evolution has long sequences of regional resource opportunities and stresses that emphasized the reconstruction of habitat, where the aim is influenced the prospects for lineage divergence and the ben- to portray the main type of vegetation or climatic condition efits and costs of adaptive strategies (ecological, social, de- in which early hominins lived. However, the leading edge of velopmental, and reproductive) associated with the origin and early evolution of Homo. Although the fossil records of south- Richard Potts is Director of the Human Origins Program, National ern and other regions of Africa offer a rich body of evidence Museum of Natural History, Smithsonian Institution (P.O. Box of hominin evolution, Plio-Pleistocene climate and vegetation 37012, Washington, DC 20013-7012, U.S.A. [[email protected]]). This data for these parts of the continent typically offer only short- paper was submitted 12 XII 11, accepted 10 VII 12, and electronically term snapshots or combine lengthy or unknown periods of published 27 XI 12. time (i.e., they are highly time averaged); in addition, they

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0004$10.00. DOI: 10.1086/667704 S300 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 1. Oxygen isotope curve (d18O) for the past 10 Myr (data from Zachos et al. 2001). Arrow 1, beginning around 6 Ma, warm- cold climate fluctuation became more dramatic; compare pre– with post–6 Ma intervals. Arrow 2, beginning 3.0–2.8 Ma, glacial fluctuations strengthened and included the onset of Northern Hemisphere glaciations. Note that the interval 3.0–2.4 Ma was characterized by both overall cooling and an increase in the amplitude of oscillation. Arrow 3, from the mid-Pliocene through the Pleistocene, the range of climate variability increased dramatically; this observation suggests that organismal features that heightened the ability to adjust to ecological dynamics and uncertainty (i.e., adaptability) were at a premium. The genus Homo, and eventually the adaptations characteristic of Homo sapiens, evolved during the strongest fluctuations. A color version of this figure is available in the online edition of Current Anthropology. are patchily distributed in time and space and often less pre- ∼100,000-yr [100-kyr] and ∼413-kyr periods), “obliquity” cisely calibrated than those in East Africa. For this combi- (the angle of Earth’s axis of rotation relative to the sun; ∼41- nation of reasons, the Plio-Pleistocene environmental syn- kyr period), and “precession” (an effect of Earth’s axial wobble thesis developed here is mainly drawn from and is relevant that creates a progression of the seasons relative to how close to the fossil-rich, well-calibrated stratigraphic records of East the planet is to the sun; ∼19–23-kyr periods). Interactions Africa. among these cycles and with millennial-scale and shorter-term sources of variability create a dynamic system of insolation Environmental Dynamics in Which amplification and damping prone to both predictable cycles Early Homo Evolved and nonlinear threshold-type change, especially over the course of the past 3 million years (Myr), since the onset of In this paper, climate and vegetation data for the interval Northern Hemisphere glaciation. from 3.0 to 1.5 Ma come from several main sources: stable Measurement of stable oxygen isotopes (d18O) in ocean isotopes, eolian dust and plant biomarker records, northeast benthic foraminifera provides a global record of the trend, African sapropels, and East African lake sediments. By com- amplitude, and periodicity in temperature and glacial ice var- bining the variety of environmental data sets, I briefly sum- iability (fig. 1). Because glaciation also lowers sea level world- marize here four principal developments in the East African wide, glacial conditions (high d18O) can also reduce the mois- and global environmental system during the evolution of early ture (largely originating from the ocean) that reaches Homo and Homo erectus. continental interiors. Between 2.8 and 2.4 Ma, an important shift took place in The Gradual Onset of Continental Ice Sheets (∼3.1–2.5 Ma) the dominant period of climate oscillation, from the 19–23- Denotes the Development of a Periodically Cooler, kyr mode to the 41-kyr mode, evident in d18O variability. This Drier, and Glaciated Planet shift in the dominant periodicity coincided with an increase Heating of Earth’s surface, the amount and distribution of in climate variability. Another notable shift in the dominant moisture, and the strength of ocean currents that redistribute mode, from 41- to 100-kyr periodicity, occurred around 0.8 heat are all influenced by solar insolation—the amount of Ma, accompanied again by an increase in amplitude. The solar radiation reaching marine and land surfaces (Ruddiman evolution of mid- and late Pleistocene Homo, including Homo 2001). Insolation is regulated by three large-scale orbital cy- sapiens, was associated with the highest-amplitude fluctua- cles: “eccentricity” (the shape of Earth’s orbit around the sun; tions in marine d18O (fig. 1). Potts Environments of Early Homo S301

A Net Increase in Aridity and C4 Grasses Occurred over the third type of data set that focuses on East African aridity. Past 4 Myr, with a Large Increase Possibly ∼2.8 Ma and Paleosols can preserve organic residues and carbonate deposits Another ∼1.8 Ma that form under certain environmental conditions. The d13C of these ancient soil components has been used to infer the Continental sedimentary records indicate considerable drying relative proportions of C (wooded) and C (grassy) signals of East Africa and expansion of grasslands around 2.8–2.5 3 4 of vegetation that grew in a limited area (∼10 m2) averaged Ma and between 2.0 and 1.7 Ma. These aridity pulses and over many years (e.g., Ambrose and Sikes 1991; Cerling 1992; the timing of substantial increases in grass abundance have Kingston 2007). best been documented by three types of data: eolian dust Figure 2 illustrates d13C data over the past 7 Myr, based on obtained from deep-sea cores off the northeast coast of Africa the data set compiled by Kingston (2007). An overall increase (deMenocal 1995, 2004), molecular plant biomarkers ob- in C biomass occurs within a mixed vegetation setting tained from these same drill cores (Feakins, deMenocal, and 4 throughout the time period of human evolution. Compilation Eglinton 2005), and the isotopic composition of East Africa of d13C data from Turkana and Olduvai (Cerling 1992; Cerling soil carbonates associated with early hominin sites (e.g., Cer- and Hay 1986; Wynn 2000), in particular, indicates a long- ling 1992; Cerling et al. 2011). term trend toward aridity and open habitat in East Africa. Drill cores obtained from the Atlantic and northwest Indian However, inspection of broader compilations (e.g., Cerling et Oceans have provided nearly continuous records of the pro- al. 2011; Kingston 2007; Levin et al. 2004; see fig. 2) suggests duction and atmospheric transport of mineral dust from the the wide range of vegetation settings that accompanied the African continent. Large rainfall seasonality generates the aridity trend, even from 3.0 to 1.5 Ma, the period with the dust. Summer eolian dust plumes in northeast Africa, which strongest turn from wooded to grassland settings. A d13C anal- are tied to Indian Ocean monsoonal surface winds, are ex- ysis of soil carbonates from Gona, Ethiopia, also indicates an ported to the Arabian Sea and the Gulf of Aden (Clemens overall expansion of C4 grass biomass from 4.5 to 1.5 Ma, 1998; deMenocal 2004). Measurement of wind-borne dust in although considerable heterogeneity in the vegetation is evi- drill cores from these areas shows that large-amplitude aridity dent throughout the sequence (Levin et al. 2004). While the cycles were associated with the onset of Northern Hemisphere onset of a “savanna” ecosystem consisting of more grass than glacial cycles around 2.8 Ma and that major shifts in wind- trees is evident in the Middle Awash of Ethiopia by around blown dust variability occurred at 2.8–2.6 Ma, 1.8–1.6 Ma, 2.6 Ma (Quade et al. 2004), the oldest isotopic evidence of and again at 1.0–0.8 Ma (deMenocal 1995, 2004, 2011). On open grassland in East Africa is from ∼2.0 Ma at the site of this basis, deMenocal has emphasized the importance of the Kanjera South, Kenya (Plummer et al. 2009). aridity trend in African climate, which was superimposed on wet-dry cycles. Fossil pollen recovered from terrestrial settings ∼ and marine drill cores are consistent with the substantial arid- Deep Lakes Formed in East Africa between 2.7 and 2.5 Ma ∼ ity intervals, especially between 1.8 and 1.6 Ma. Drier vege- and between 1.9 and 1.7 Ma as End Members of Strong tation is recorded in Rift Valley lowlands and across northwest Moist-Arid Oscillations ∼ Africa by 2.4 Ma, and arid vegetation intensified 1.8 Ma Sedimentary sequences preserving evidence of hominins and (Bonnefille 1995; Leroy and Dupont 1994). other fauna include deposits, most notably lake sediments, Deep-sea records of African dust are complemented by the that are sensitive indicators of past climate. In recent years, analysis of terrestrial plant biomarkers, which are derived Trauth and colleagues have produced an analytical synthesis from waxy lipids abraded from plant leaf surfaces and trans- of lake deposits in East African basins. They conclude that ported by wind to marine sediments. Molecular biomarkers long phases of high moisture characterized East Africa at three in deep-sea cores offer a rich record of terrestrial vegetation. important times—2.7–2.5 Ma, 1.9–1.7 Ma, and 1.1–0.9 Ma— A study by Feakins, deMenocal, and Eglinton (2005) shows and that these times were critical intervals in human evolution that long-chain n-alkanoic acids from the leafy waxes provide (Trauth et al. 2005). In publications since 2005, these re- a reliable indicator of terrestrial vegetation. Carbon isotopic searchers have placed greater emphasis on the fact that the (d13C) analysis of these molecules sampled through time from prolonged high-moisture phases actually occurred during Site 231 in the Gulf of Aden demonstrates the expansion of “periods of extreme climate variability” (Trauth et al. 2007: grasslands across northeast Africa from the Miocene through 475) related to Earth’s eccentricity cycle (i.e., its modulation early Pleistocene. As with the eolian dust record, the analysis of precession, especially at the ∼413-kyr period; Trauth et al. of plant biomarkers shows considerable variability in any 2007). In other words, cycles of deep lakes and strong aridity given time interval; however, an emphasis on the average (fig. occurred during those ∼200-kyr-long intervals. 3 in Feakins, deMenocal, and Eglinton 2005) indicates a sub- The most precisely dated evidence of periodic lake diato- 40 39 stantial shift toward C4 grasses relative to C3 woody vegetation mites is from the Tugen Hills, where Ar/ Ar dates and orbital between 3.4 and 2.4 Ma, with an ongoing trend toward grass- tuning of the sedimentary sequence point to five deep-lake dominated habitat registered at 1.7 Ma. cycles over a period of ∼100–115 kyr between ∼2.68 and 2.58 Study of paleosols (buried ancient soils) has produced the Ma (Deino et al. 2006; Kingston et al. 2007). As to the period S302 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 2. Stable carbon isotope data (d13C) for the past 7 Myr, based on the data set compiled by Kingston (2007). An overall 13 increase in C4 biomass occurred. Although some d C data sets from Turkana and Olduvai indicate a strong aridity trend and grassland expansion associated with the evolution of early Homo and Homo erectus, a wider data set sampling many East African sites demonstrates the considerable heterogeneity of vegetation throughout the key time interval. A color version of this figure is available in the online edition of Current Anthropology. between 1.9 and 1.7 Ma, the major lake phase postulated by at odds with the general aridity trend emphasized by Trauth et al. (2005, 2007) corresponds to the Lorenyang Lake deMenocal (1995, 2004) in his study of the windblown dust of the Koobi Fora Formation, Turkana basin, and Beds I and record. In fact, an alternative view concerning the timing of lower II, Olduvai Gorge. Analyses of the Lorenyang Lake (a East African aridity is offered by Trauth, Larrasoan˜a, and precursor to the present Lake Turkana) indicate a period of Mudelsee (2009). Their statistical reanalysis of eolian dust data relative stability surrounding a large lake from ∼2.0 to 1.85 indicates that significant aridification of East Africa did not Ma followed by stronger fluctuations between low and high begin ∼2.8 Ma. Rather, heightened aridity is evident only in lake levels and substantial change in landscape features be- times of highly variable climate (strong wet-dry oscillations) tween 1.85 and 1.7 Ma (Feibel, Harris, and Brown 1991; Joor- in East Africa, especially ∼1.8 Ma, with a further drying trend dens et al. 2011; Lepre et al. 2007; Quinn et al. 2007). At that began ∼1.5 Ma and reached a peak starting ∼1.0 Ma, Olduvai, Ashley (2007) postulates five episodes of lake ex- again associated with magnified wet-dry fluctuation (see also pansion and contraction between ∼1.85 and 1.74 Ma as pre- Owen, Potts, and Behrensmeyer 2009). cessionally controlled climate affected the amount of rainfall and the profile of resources available to organisms. Deino Several Very Long Periods (Lasting ∼130–330 Kyr Each) of (2012) has refined the Bed I Olduvai chronology and shows Magnified Moist-Arid Variability Occurred in the Period a more complex picture of wet-dry cycles in relation to orbital between 3.0 and 1.5 Ma precession. These interpretations of strong wet-dry variability are consistent with a synthesis of fossil pollen, stable isotopes, A strong stepwise increase in monsoonal variability (moist- microfauna, and other evidence from this oldest part of the arid fluctuation) occurred in northeast Africa ∼3 Ma. This Olduvai sequence (Potts and Teague 2010). increase in moisture variability is recorded in the Mediter- The manifestation of large, deep lakes in East Africa appears ranean record of sapropels, which are dark, organic-rich sed- Potts Environments of Early Homo S303 imentary layers deposited periodically on the sea floor as the result of heightened runoff of the surface water from the Nile catchment. The succession of Pliocene and Pleistocene sap- ropels suggests that climate variability in the northeast quad- rant of the African continent has been sensitive to orbital precession, with moist-arid cycles recorded nearly every 19– 23 kyr (deMenocal 2004; Rossignol-Strick 1983). Sapropel studies have thus documented that African monsoonal cli- mate is driven largely by precession. Geochemical studies in- dicate that the humid period in each cycle may have ranged from ∼4 to 12 kyr in duration (Wehausen and Brumsack 1999). Furthermore, according to Mediterranean sapropel records, a relatively low level of monsoonal variability was expressed from ∼4.4 to 3.0 Ma, followed immediately by a sharp ex- pansion in the range of fluctuation. This expansion coincides with the last appearance datum (LAD) of Australopithecus afarensis and the current first appearance data (FAD) for Par- anthropus, ∼2.7 Ma, and Homo (sensu stricto), arguably by ∼2.4 Ma. While the rhythm of low-latitude climate variability is or- bital precession with periods of ∼19 and 23 kyr, the amplitude of tropical moist-dry variability is strongly affected by orbital eccentricity with its dual periods of ∼100 and ∼413 kyr. The intersection of the precession and eccentricity curves (essen- tially the interaction of four sine waves) results in a predicted sequence of high and low climate variability for African low latitudes. This predictive framework of alternating high- and Figure 3. Alternating high– and low–climate variability intervals low-amplitude climate variability “packets,” each lasting 104– from ∼3.2 to 1.4 Ma. Low variability is defined by mean orbital 105 years, is evident in the eolian dust records of deMenocal eccentricitye ≤ 0.0145 or 1 standard deviation (SD) below mean (1995) and is recognized by other authors (e.g., Campisano e for the past 5 Myr (R. Potts and P. deMenocal, unpublished data). The time interval, duration, and mean e for each interval and Feibel 2007; Deino et al. 2006; Kingston 2007; Trauth et are shown. SDs of dust flux measured in Arabian Sea core 721 al. 2007). (deMenocal 1995) test the validity and robustness of this high-/ The recognition of high- and low-variability intervals offers low-variability framework. Asterisks indicate that the direction a novel framework in which to examine East African climate of change in the SD matches (13 out of 17 pairs of intervals change. Figure 3 shows the time intervals in the period from [76%]) the predicted widening and narrowing of climate vari- 3.0 to 1.5 Ma that are defined by high or low eccentricity. ability from one interval to the next. Boldface indicates intervals During high eccentricity, moist-arid variability is most pro- in which low variability dominates for more than 30,000 years or high variability dominates for more than 100,000 years. Note nounced (i.e., a high–climate variability interval), whereas that the critical interval ∼2.85–2.08 Ma (highlighted) exhibits the relatively stable climate occurs at low eccentricity. High var- lengthiest eras of both high and low climate variability, that is, iability dominates this key interval, and three of the most prolonged intervals of wide fluctuation interspersed with rela- prolonged periods of high climate oscillation in tropical Africa tively stable climate. A color version of this figure is available in over the past 5 Myr are predicted for this interval, with du- the online edition of Current Anthropology. rations of 326 kyr (∼2.79–2.47 Ma), 288 kyr (∼2.37–2.08 Ma), and 192 kyr (∼1.89–1.69 Ma). 2.7 to 1.5 Ma; the intensity of this reflectance records the Figure 4 shows a broader time perspective by showing the strengthening and reduction in moist-arid variability. Analysis eight longest eras of high climate variability, based on orbital- of sapropel color (spectral reflectance) confirms that mon- eccentricity values, during the past 5 Myr, that is, the pre- soonal intensity was magnified in alternating “packets” of high diction of when moist-arid variability prevailed for the longest and low climate variability as predicted by eccentricity-mod- periods in East Africa. Several important FADs and LADs in ulated precession over long periods of time. The bottom of African human evolutionary history are situated in these in- figure 5 situates the oldest known Oldowan archaeological tervals. It should be noted, however, that the dates of these occurrence (Gona) in a high-variability interval. Oldowan first and last appearances are likely to shift as new fossil and sites throughout the period occurred in both moist and arid archaeological discoveries are made. environments and in prolonged eras of high or low climate Figure 5 shows a plot of sapropel spectral reflectance from variability. S304 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 4. Longest-duration high–climate variability intervals (the longest time intervals of predicted high climate variability in East Africa over the past 5 Myr). The intervals range from 326 to 192 kyr in duration. These are the most prolonged eras of environmental instability in East African hominin evolutionary history. Several of the most prominent events in hominin evolution appear to have occurred in these intervals. FAD p first appearance datum; LAD p last appearance datum.

This synthesis of environmental data sheds light on the driver of evolutionary change across a wide range of taxa, larger physical and biotic context of hominin populations in that is, a concentrated pulse of extinction and speciation and beyond the localities that have produced fossils so far. events in lineages that, in Africa, favored cool- and arid- Over the past three decades, a small number of key hypotheses adapted taxa at the expense of warm- and moist-adapted have proposed critical linkages between climate, resources, lineages, particularly evident in bovids and rodents. Cooling ecological and social interactions, natural selection, and spe- thus set the climatic and ecological contexts in which the ciation. These hypotheses offer robust and testable ideas re- genus Homo (as well as Paranthropus) originated, around 2.5 garding the environmental factors involved in the evolution Ma, or more broadly between 2.8 and 2.4 Ma (Vrba 1988). of early Homo. In a more speculative development, Vrba (1994) posited that cooling produced conditions that favored the retention of Environmental Drivers of Evolution in Early juvenile neurocranial traits through neotenic processes, which Homo: Cooling, Aridity, Moisture, promoted brain enlargement in Homo. Warmth, or Variability? The environmental hallmarks and data sets reviewed in the Aridity preceding section have led researchers to propose a variety of The long-term aridity trend in Africa was established by tec- environmental explanations concerning the origin of Homo tonic uplift, with the formation of the East African Rift System and the early evolution of Homo erectus. The following sum- having a dominant effect in that portion of the continent marizes the most prominent hypotheses. (Sepulchre et al. 2006). Aridity, the expansion of open habitat, and, ultimately, the formation of grasslands were parallel Cooling trends. Vrba’s most influential papers seemed to consolidate This idea has been around the longest, probably as a result the savanna hypothesis of early human evolution: global cool- of the fact that glacial climate has, since the 1800s, been ing led to African drying and the spread of grass-dominated understood as an important context of human evolution. The habitats. The savanna hypothesis is the long-established idea causal influence of climate cooling on African hominin evo- that dry, open, grassy settings provided the stage on which lution was formalized by Vrba in her influential turnover- the human evolutionary drama unfolded. In a series of work- pulse hypothesis (Vrba 1985, 1988, 1995a, 1995b) and habitat shops and conferences organized by Vrba (e.g., Vrba et al. theory (Vrba 1992). Vrba proposed that global cooling was a 1995), a number of researchers offered paleontological and Potts Environments of Early Homo S305

Figure 5. Sapropel variability, showing the presence of alternating intervals of high and low climate variability, from 2.7 to 1.5 Ma (right to left). Spectral reflectance is a measure of dark versus light color, with higher values for lighter stratigraphic layers (arid times, prevalent during less variable periods) and lower values for darker strata (moist times, especially prevalent during high moist- arid variability). Variability, noted in the upper right, provides examples of well-defined time periods of high and low climate fluctuation. Malapa, SK, ST, Wonderwerk, and A.Hanech are key southern and northern African Oldowan sites and age estimates. The remaining points and age estimates represent key East African Oldowan archaeological sites, starting with the oldest documented so far (OGS-6/7 at Gona, ∼2.58 Ma). Spectral reflectance data are from ODP Site 967A (Hilgen et al. 1999; P. deMenocal, personal communication). A color version of this figure is available in the online edition of Current Anthropology. climate data sets that fell in line with Vrba’s idea that some- Moisture thing important happened in African climate and mammalian In considerable contrast, Trauth, Maslin, and colleagues (Mas- evolution between 2.8 and 2.4 Ma. Among those data sets lin and Trauth 2009; Trauth et al. 2005, 2007, 2010) have was deMenocal’s eminent analysis of eolian dust input from argued that lengthy periods of high moisture and climate- northeast Africa to the Arabian Sea and the Gulf of Aden. driven production of deep lakes were the primary drivers of His efforts (e.g., deMenocal 1995) drew further attention to Pliocene and Pleistocene human evolution in East Africa. the East African drying trend with a proposal that there was They envisioned three main intervals of climatic moisture that a stepwise increase in dust production on the African con- were associated with key events in human evolution. Specifi- ∼ tinent and dust input to nearby deep-sea records 2.8–2.5 cally, they considered earliest Paranthropus and Homo to be Ma. The conclusion reached by deMenocal and others is that associated with the first moisture phase, from 2.7 to 2.5 Ma; Homo arose as an integral part of the arid- and grassland- they placed the earliest H. erectus, its dispersal beyond Africa, adapted African biota and that the major adaptations of Homo and the origin of the Acheulean in the second phase, from (e.g., stone tools, meat eating, brain size increase, geographic 1.9 to 1.7 Ma; and they asserted that the extinction of Par- dispersal) were responses to the increase in aridity. The use anthropus and further expansion of H. erectus matched up by deMenocal of Cerling’s East African compilation of pa- with the third moisture phase, from 1.1 to 0.9 Ma. As noted leosol d13C, which portrays an increase in grass proportions above, this hypothesis actually emphasizes that lake devel- over time, adds evidence to the aridity hypothesis. A com- opment was part of a highly variable climate system; thus, parison of paleosol d13C for the entire Turkana basin and the these authors actually consider the moisture hypothesis as a lower Awash basin, Ethiopia, by Levin et al. (2011) confirms subset of the variability selection hypothesis (Trauth et al. an overall increase in C4 (grass) vegetation in floodplain set- 2005, 2007; see “Variability,” below). tings between 4 million and 700,000 years ago. Trauth et al. (2010) expanded the moisture hypothesis by S306 Current Anthropology Volume 53, Supplement 6, December 2012 combining tectonic evidence for north-south rift formation The variability selection idea points to this spectrum of in East Africa with lake history to postulate that large lakes environmental dynamics in creating a signal that can prompt imposed a barrier to populations on opposite sides (east vs. adaptive change. It seeks to answer how a population of or- west) of those lakes, whereas lake contraction and drying of ganisms can change over time via a process of adaptation to the rift floor created refugia on opposite rift shoulders. This the variability—that is, to the temporal range—of environ- sequence thus promoted vicariance and allopatric speciation. mental dynamics in adaptive settings. Furthermore, it posits The authors thus consider large lakes as “amplifiers” that drive that adaptation to environmental dynamics fosters plasticity, evolutionary change. adaptive versatility, or—perhaps the most encompassing term at many levels of biological organization—adaptability (Potts 1998b, 2002, 2007; see fig. 6). Warmth Based on evidence that well-defined eras of pronounced This hypothesis derives largely from Passey et al. (2010), who climate variability occurred between 3.0 and 1.5 Ma, coupled document what they consider to be extraordinarily persistent with episodic revisions of landscapes due to tectonic events, high-temperature soils in the Turkana basin, Kenya, over the the idea is that African environmental dynamics created highly past 4 Myr. Soil carbonates were analyzed using an innovative diverse conditions of natural selection that led to positive method known as the “clumped-isotope thermometer” (Ghosh selection for genetic combinations favoring adaptability and et al. 2006:1441) to investigate the temperature history of the thus the ability of certain organisms to adjust to environ- Turkana basin. This method uses the distribution of 13C-18O mental change, move to new habitats, and respond in novel bonds in paleosol carbonates as a proxy for soil temperature ways to their surroundings. Adaptive change in response to during carbonate formation. For the Turkana basin, the results environmental dynamics thus engendered responsiveness at indicate persistent hot temperatures above 30ЊC and often many biological levels—from molecular, cellular, and physi- above 35ЊC for the past 4 Myr, similar to those in the present ological to developmental, social, and ecological dimensions Turkana area, which is one of the hottest places on Earth. of life (Potts 2002). The possibility presented by the variability Although Passey et al. (2010) note that these surprising tem- selection hypothesis is that the evolution of early Homo and perature estimates apply only to periods of soil carbonate for- H. erectus was embedded in environmental instability and can mation, they claim that such periods make up most of the past be explained by selection that improved the ability of certain several million years in the Turkana basin. The authors link hominin populations (ultimately species) to adjust to varia- this finding to the evolution of human thermophysiology, spe- tion in their adaptive setting. cifically, the change in body proportions associated with early Variability selection as a viable process of evolutionary H. erectus and “a long-standing human association with mar- change has recently been tested by Grove (2011), who used ginal environments” (Passey et al. 2010:11245). a single-locus genetic model originally suggested in Potts (1996a, 1996b, 1998b). In Grove’s simulations, “versatilist” alleles that build genetic combinations favoring plasticity were Variability unable to increase when the fluctuating environment was While recognizing that environmental variability is more than modeled as a sine wave. However, in an empirical environ- mere noise in an overall trend, each of the previous four ment based on d18O for the past 5 Myr, variability selection hypotheses emphasizes mainly one dimension of the global was inevitable as versatile strategies of adaptation and behav- or African environmental system and treats it as the dominant ioral plasticity were favored (Grove 2011). This test of vari- adaptive challenge and evolutionary force relevant to the evo- ability selection as an evolutionary process aligns with points lution of early Homo and H. erectus. An integrated treatment made by deMenocal (2011): in a situation where seasonal- to of the environmental data sets, however, begs the question as orbital-scale fluctuation is regular or even in tempo and am- to what the principal environmental signal in this dynamic plitude, variability alone is unlikely to have served as a se- era of Earth’s climate history truly was. Was it cooling or lection agent; however, progressively larger degrees of envi- warmth, aridity or monsoons? The variability hypothesis, also ronmental variability, evident as an overall trend in the d18O known as variability selection, cuts across this possible im- curve (see fig. 1) and in particular intervals during the Pli- passe by highlighting not any one trend, habitat, or extremity ocene and Pleistocene (figs. 3, 4), may result in new adap- of climate oscillation but rather the evolutionary effect of tations that promote adaptable behavior, including successful environmental dynamics itself (Potts 1996a, 1996b,1998a, responses and dispersal to novel environments. 1998b, 2007). It is the variability across a large set of envi- ronmental axes that led to highly varying adaptive conditions Geographic Variation and the Possible over time and space: warm-cool, wet-dry, high or low resource Role of Refugia abundances, concentrated or patchy resource distributions, high or low parasite loads, high or low predation risks, dense According to several recent studies, the expression of climatic or dispersed species populations, and strong or weak inter- conditions varied considerably across different areas of East species competition. Africa. The Omo-Turkana basin has especially contributed to Potts Environments of Early Homo S307

Figure 6. Three possible outcomes of population evolution in a time series of environmental dynamics typical of the Plio-Pleistocene. The ability to move and track habitat change geographically (narrow lines) or to expand the degree of adaptive versatility is important for any lineage to persist. Extinction occurs if species populations have specific dietary/habitat adaptations (i.e., a narrow band of “adaptive versatility”; highlighted bands) and cannot relocate to a favored habitat. In the hypothetical situation (rightmost band) where adaptive versatility expands, migration and dispersal may occur independently of the timing and direction of environmental change. The evolution of adaptive versatility is the impetus behind the variability selection idea. A color version of this figure is available in the online edition of Current Anthropology. this emerging picture of geographic variation. In a study of period. In other words, for about 150,000 years the eastern soil d13C and d18O by Levin et al. (2011) encompassing ∼5,000 Turkana basin served as a refugium for hominins and other km2, the northern floodplains of the ancestral Omo River permanent water-dependent fauna. This refugium was buf- ∼ between 2.9 and 2.0 Ma were dominated by woody C3 veg- fered from severe lake level fluctuations and drought that etation indicative of a seasonally moist, riparian woodland, affected other regions of East Africa. at the same time as the broader southern floodplains had The idea that an area on the order of 102–103 km2 was drier, less productive soils populated by grassy C4 vegetation. protected over the long term from extreme fluctuations is an The Awash basin, by comparison, was more arid than the important consideration. Could the reliable resources of a Omo-Turkana basin, and it supported a greater proportion refugium have provided a more significant context for the of C4 vegetation during this same interval (Levin et al. 2011). evolution of early Homo or Homo erectus than climate-driven These comparisons suggest that different regions, both be- extremes of food and water fluctuation over the broader East tween and within basins, manifested varied degrees of sen- African region? sitivity to the large-scale climate shifts that affected East Africa This question cannot yet be answered; however, the moist, overall during the late Pliocene. wooded refugium suggested by Joordens et al. (2011) appears Furthermore, a study by Joordens et al. (2011) introduces not to have extended past 1.85 Ma. Isotopic comparison the intriguing idea of a habitat refugium as a magnet for across the Omo-Turkana basin indicates a major restructuring hominin populations during the Plio-Pleistocene. The authors of hydrology and vegetation toward arid C4 habitats beginning develop a new type of climate record, a strontium isotopic no later than 1.9 Ma (Levin et al. 2011). In fact, Quinn et al. (87Sr/86Sr) indicator applied to lake fish fossils. Their study (2007) characterize the entire period from 2.0 to 1.75 Ma as demonstrates, first, that precessional moist-arid variation did one of important vegetational change in the Turkana basin, indeed affect the lake that existed in the Turkana basin be- trending from relatively closed savanna woodland toward tween 2.0 and 1.7 Ma but, second, that the basin retained open, low-tree shrub savanna. These authors also note that permanent water and moist wooded habitats throughout the the shift in average floral composition between 2.0 and 1.75 period from ∼2.0 to 1.85 Ma. The authors show that hominin Ma coincides with high species turnover, the principal finding fossils occur during both wet and dry phases of the long-term by Behrensmeyer et al. (1997). Furthermore, this finding is monsoonal cycles and further suggest that hominins were consistent with the study by Lepre et al. (2007) at East Tur- drawn to continuously well-watered habitats over this long kana, which detects evidence of heightened environmental S308 Current Anthropology Volume 53, Supplement 6, December 2012 variability from 1.87 to 1.48 Ma; high wet-dry monsoonal African dust variability (deMenocal 1995, 2004), and evidence variability is predicted for much of this period (fig. 3). of species turnover in the Turkana basin (Behrensmeyer et al. 1997). Reed (1997) concludes that the climatic and eco- ∼ Do Environmental Drivers Serve as Adequate logical transition at 1.8 Ma corresponds to the early evo- Evolutionary Explanations? lution of Homo erectus, and thus only with this later species of Homo (after 2.0 Ma) do we have a hominin adapted to In brief, the answer to this question is “no” or, at least, “not arid and open landscapes. if any given environmental hypothesis invokes a fairly sim- A different finding by Bobe and Eck (2001) came from plistic notion of correlation.” Tests of correlation seek to de- measuring the relative abundances of bovids recovered from termine how key evolutionary events map onto large-scale the Omo Shungura Formation between 3.4 and 1.9 Ma. The environmental patterns. The value of correlation hypotheses results indicate a climatic shift toward increased aridity be- is that they usually integrate all the evidence from paleoan- ginning ∼2.8 Ma and intensifying by 2.3 Ma, an age for ar- thropological sites pertinent to a particular evolutionary event idification considerably earlier than that reached by Reed and then examine how well the patterning of evolutionary (1997). Later analysis of bovids, suids, and cercopithecids in change matches global or continental environmental trends. the Turkana basin (Bobe and Behrensmeyer 2004) gave evi- Information from deep-sea cores has proved especially useful dence of (1) an initial increase in grassland-adapted mammals in testing correlation hypotheses. Such tests do not, however, at ∼2.5 Ma, (2) fluctuation in the abundance of arid and formally establish which particular environments hominins moist taxa until ∼2.0 Ma, and then (3) a strong excursion actually encountered in their local settings or the processes toward open-country grazers at ∼1.8 Ma. On the basis of by which hominin populations responded to novel survival these findings, Bobe and Behrensmeyer (2004) favor a com- challenges in those settings. bination of explanations that invoke both aridity and vari- Two additional factors, discussed below, have become crit- ability selection as evolutionary drivers in the Turkana basin ical in developing environmental explanations for the evo- between 2.5 and 1.8 Ma. lution of early Homo: evidence of evolutionary change in In a more refined analysis, Bobe et al. (2007) confirmed contemporaneous large mammals and the development of that the abundance of grazing bovids underwent an overall compelling, testable models that specify how particular types increase in the Turkana basin between 3.0 and 1.0 Ma. How- of environmental change can incite evolutionary change. ever, different patterns of fluctuation in the percentage of grazers occurred in different parts of this large basin; in fact, grazing bovids underwent an overall decline in West Turkana Faunal Change Can Test the Causes of Evolutionary between 3.0 and 1.5 Ma. According to the authors, the overall Change in Homo trend nonetheless indicates that East African landscapes in- The study of faunal communities can provide an important habited by bovids and hominins became more open, arid, test of how environmental dynamics influenced the evolution and seasonal; the moist and more vegetated end of the habitat of Homo. Each lineage represents a natural experiment in how spectrum became particularly limited after 2.0 Ma. They cau- external environment may have prompted certain evolution- tioned, however, that different patterns of faunal change in ary changes. Responses across an array of large mammals— separate parts of the same region point to the difficulty of for example, the success of arid-adapted taxa over moist- establishing definitive correlations between climatic and fau- adapted ones, the emergence of dental hypertrophy in mul- nal change. tiple animal lineages, an increase in body size across carniv- Several other notable studies occur in a compendium fo- orous taxa, or a widening of geographic ranges across a variety cused on the African Pliocene faunal evidence (Bobe, Alem- of taxa—can offer clues as to the nature of the adaptive chal- seged, and Behrensmeyer 2007). Frost (2007), for example, lenges and the conditions that shaped human evolution, in- examined evolutionary change in the Cercopithecidae and cluding the origin and early evolution of the genus Homo. found no support for a turnover pulse from 2.8 to 2.5 Ma, For these tests to be effective, the relevant faunal lineages the time range predicted by Vrba (1995b) for speciation and must occur in the same times and places in which hominins extinction caused by global cooling and the spread of grass- lived and evolved. This point has been recognized for some land habitats in Africa. Frost did find, however, a clustering time, particularly for the interval between about 3.6 and 1.8 of first and last appearances of monkey lineages ∼2.0 Ma, Ma. which could be associated with a number of environmental Analysis of a wide range of large mammal fossil assemblages happenings at that time, including East African aridification. from eastern and southern Africa by Reed (1997), for ex- In a study of evolutionary change in Plio-Pleistocene car- ample, showed that grazing adaptations fluctuated within nar- nivores (members of the Carnivora), Lewis and Werdelin row limits (10%–25%) between 3.6 and ∼2.0 Ma. Only by (2007) noted that the earliest known appearance of stone tools about 1.8 Ma did an increase in the percentage of grazing ∼2.6 Ma had no obvious effect on the carnivore guild. How- species occur, exceeding 30%. Reed’s finding corresponds well ever, a drop in carnivore speciation rate and a rise in their to information from d13C (Cerling 1992; Levin et al. 2011), extinction rate after 1.8 Ma and a pronounced decrease in Potts Environments of Early Homo S309 carnivore lineages after 1.5 Ma could be ascribed to the emer- influenced speciation and adaptive shifts in early Homo gence of H. erectus, climate change, and a drop in overall prey (deMenocal 2011). The work has hardly begun to relate even species richness. the most highly resolved climate records to shifts in season- From these examples and others (e.g., Behrensmeyer et al. ality, landscapes, and resource abundances, that is, the things 1997; Reed 2008; Vrba 1995a), it is evident that most of what that matter to organisms. So, for example, are evolutionary is termed “hominin paleoecology” to date has involved either transitions driven largely by stresses associated with resource the analysis of lineage turnover or habitat reconstruction. scarcity, opportunities related to resource abundance, or un- Questions about which species commonly occurred together certainties linked to seasonal unpredictability and longer-term and which taxa had particularly strong associations with hom- landscape remodeling? Were adaptations in early Homo largely inins have yet to gain much attention, even though such habitat specific (e.g., solutions to a well-defined and consistent studies would truly reflect “paleoecology” in terms of docu- set of environmental problems), or did they reflect increases menting species co-occurrences and potential interactions. in behavioral plasticity and adaptability (e.g., solutions to Such studies would offer the strongest clues regarding the highly dynamic settings and environmental novelty)? adaptive milieu that influenced early hominin populations. Furthermore, it is hard to say whether significant evolu- Some notable exceptions exist, however, drawn mainly from tionary shifts were initiated in highly localized settings (e.g., the late Pliocene Turkana basin and the mid-Pleistocene Olor- refugia), where intra- and interspecific interactions played a gesailie basin (Bobe and Behrensmeyer 2004; Bobe, Behrens- prominent role, or over much of an evolving lineage’s geo- meyer, and Chapman 2002; Potts 2007). These studies suggest graphic range, where broader climatic and tectonic effects may the fluidity of species composition in faunal communities have been important. Finally, were adaptations in early Homo dated between 2.8 and 1.8 Ma (Turkana basin) and between a response largely to external (climate- and tectonism- 1.0 and 0.6 Ma (Olorgesailie basin). These findings are con- mediated) factors or to social and competitive factors that sistent with environmental variability’s role in causing the were consistent across a diverse spectrum of habitats? It is assembly and disassembly of ecological communities and the counterproductive to frame this last matter as an either/or continual shifting of the adaptive conditions associated with question; rather, it is better to see environmental, resource, the evolution of Homo. social, and competitive factors as interrelated and potentially reinforcing rather than at odds with one another in explaining how evolutionary change occurred. An Understanding of Evolutionary Processes Is Also Vital

Any evolutionary explanation must posit explicitly what evo- Archaeological Behaviors and the Emerging lutionary processes were at work in order to evaluate the Adaptability of Homo feasibility of each explanation and to lay out potential tests of the explanation. Vrba (1985, 1992, 1995b) has been explicit The behavioral and ecological adaptations of hominins, on this point by asking what evolutionary mechanisms are viewed through the archaeological record, offer their own involved in translating from external environment to evolu- direct clues as to the nature of responses by early Homo and tionary responses. She posits, for example, that cooling re- Homo erectus to environmental challenges and can thus point sulted in directional selection and adaptive evolutionary re- to whether and how cooling, warming, aridity, moisture, or sponses to cooler, drier habitat and in speciation that favored variability influenced evolutionary change. This section iden- organisms possessing such adaptations. Other researchers im- tifies certain key adaptations evident in the behavioral record plicitly invoke habitat-specific directional selection as the pri- of artifacts, sites, and archeofaunas and examines them in the mary adaptive process, although very little attempt is made light of the changes in the East African environmental system to state how directional selection related to aridity, moisture, between 3 and 1.5 Ma. or high temperature translated into evolutionary change at the critical junctures in the environmental system. Transporting Rocks and the Oldest Known Stone The idea of variability selection has followed Vrba’s lead Toolmaking, ∼2.6–2.0 Ma by focusing on an evolutionary process as the foundation for explaining hominin and faunal evolution. As noted above, During this interval, groups of one or more hominin species variability selection makes a specific connection between (1) began to seek out rocks across distances of up to several evidence of increased environmental variability, (2) the effect kilometers to flake and to assist in processing food. From an of this increase on resources and adaptive settings at various adaptive-strategy standpoint, this behavior is more peculiar temporal scales, and (3) the evolutionary change that may than is commonly perceived, largely because the costs of learn- result from the inconsistency of natural selection over time, ing about and keeping track of good-quality stone, walking which is posited to favor adaptive versatility over habitat- considerable distances to get it, and carrying rocks of up to specific solutions to survival problems. several kilograms across the landscape were likely quite high, A focus on evolutionary processes leads to many questions especially since rocks by themselves have no caloric or nu- as to how climate and overall environmental change actually tritional value. It is not the manipulation and flaking of stone S310 Current Anthropology Volume 53, Supplement 6, December 2012 that is unexpected in hominins so much as the dedication to foraging adaptability in the face of Plio-Pleistocene environ- transporting sufficiently large amounts of rock, detectable to- mental dynamics. day as concentrations, over considerable distances from places An important further implication regarding stone transport where that rock naturally occurred. concerns its effect on the energetic costs of locomotion. This Between ∼2.6 and 2.3 Ma, the use of flaked stone tools in topic has not received much consideration since a “null acquiring food entailed relatively short-distance transport of model” of Oldowan stone and food transport costs was de- resources, typically tens to hundreds of meters (e.g., Delagnes veloped in Potts (1988). In light of current ideas about lo- and Roche 2005; Goldman-Neuman and Hovers 2009; Semaw comotor costs (e.g., Bramble and Leiberman 2004), the point et al. 2003). Longer-distance transport is well documented to consider is that the cost of stone transport for particular later. By 2.0–1.95 Ma, at the site of Kanjera South (Braun et activities must be factored into interpretations about endur- al. 2008), hominin toolmakers were moving certain types of ance running versus walking in early Homo. stone over total distances of at least 12–13 km from their Based on weights of Oldowan tools from Bed I Olduvai closest rock sources. The energetic and potential social bene- (e.g., Potts 1988, 1991), an estimate of the minimum weight fits of processing particular foods using stone tools obviously of the basic Oldowan equipment—a single hammerstone plus compensated for the costs of rock transport involved in such a number of basalt/trachyte/phonolite cores sufficient to yield cumulative distances. enough sharp flakes (minimally 50–100) to cut the hide and The question, then, is “Under what environmental and disarticulate a fleshed wildebeest-sized ungulate—would selective conditions did this complex of activities—rock trans- come to ∼4–9 kg. (An average of ∼6 flake scars per Oldowan port, precise flaking, and mental mapping of stone and food core would require at least 8–16 cores [for ∼50 to ∼100 flakes], distributions—catch on and become conspicuous in the rep- assuming that all flake scars define usable flakes, plus one ertoire of certain hominin populations?” The oldest known hammerstone, with calculated weights of 375–500 g per core site that preserves stone flaking—Gona, Ethiopia—is asso- and an average of 0.5–1 kg per hammerstone [Potts 1991].) ciated with d13C evidence of a prominent grassy component Repeated trials in an East African field situation (Olorgesailie, in a mixed vegetation setting (Quade et al. 2004). On this Kenya), involving well-conditioned individuals carrying 5–10 basis, it could be claimed that stone toolmaking was an ad- kg of rocks in backpacks over uneven terrain from outcrops aptation associated with aridity and increasingly open vege- 5 km away, suggest that running is feasible for 100 m or so tation. before the rate of fatigue strongly urges the desire to walk, However, as noted above, this oldest archaeological site is which can be accomplished comfortably for the entire trial situated in a period of pronounced moist-arid variability. Fig- distance. While this does not cast doubt on whether early ure 5, furthermore, opens the question as to why Oldowan Homo or H. erectus ran long distances, it is reasonable to ask tool behavior eventually spread across East Africa and else- what the individual might accomplish after such a run if a where and became an important behavior in the genus Homo. minimal butchery tool kit involving 8–16 sizeable rocks were The emergence of the Oldowan and its dispersal in an era of not also transported. Social running is feasible, although it widely shifting environments and diverse food regimes points would be speculative at best to wonder whether each indi- to an interpretation that contrasts with the long-standing arid- vidual runner would carry a similarly sized tool kit. Or per- ity-grassland explanation. It is feasible that stone tools suc- haps running in order to capture and butcher animals was ceeded largely because carrying stone made it possible to bring not the point. Adequate quantitative experiments yielding re- tools and foods that required tool processing together in the alistic expectations about the addition of stone transport to same places—and to do this consistently across diverse hab- locomotor costs have yet to be carried out (see Pontzer 2012). itats, even as the distribution and abundance of food resources varied over time and place. Stone transport not only incurred Dietary Expansion Involving Access to large energetic costs but also enabled consistent and predict- Meat/Marrow Resources able returns in response to a varying environment. As a result, the effort involved in making sharp edges and using rocks Because of the relative rarity and unpredictability of prey for crushing provided a resilient means of processing a species and animal tissues across the landscape relative to changeable array of foods across a wide range of habitats. plant foods, carnivory typically leads to larger foraging dis- By ∼2.0–1.95 Ma, therefore, we see definitive evidence of tances and substantially increased energy budgets (Carbone, persistent Oldowan toolmaking (and stone transport) in an Teacher, and Rowcliffe 2007; Kelt and Van Vuren 1999; Nagy, arid grassland setting recorded at Kanjera South (Plummer Girard, and Brown 1999). That Oldowan hominins coupled et al. 2009) and in a nearly contemporaneous moist, wooded these latter costs with the added costs of transporting the habitat recorded at FwJj20, East Turkana (Braun et al. 2010). rocks needed to process carcasses is reason to suspect that In this light, the Oldowan repertoire of behavior emerged as the survival and energetic returns on accessing animal tissues a characteristic of the genus Homo (even if adopted initially were substantial. Access to nutritious resources in mammalian by non-Homo populations) because it enabled dietary and bones and organs as well as to a wider range of plant foods Potts Environments of Early Homo S311 is likely to have played a fundamental role in offsetting the well dissected (Binford 1981; Potts 1988), the repetitive act costs of transporting stone. of carrying and aggregating rich packets of fatty tissue and The expansion in diet implied by access to animal fat and protein almost certainly had important social implications protein is also thought to have played a role in a number of (see below). adaptive changes in the evolution of Homo (Aiello and The spread or elaboration of this behavior (the transporting Wheeler 1995; Anto´n, Leonard, and Robertson 2002; Plum- of food) is not well calibrated, but its appearance by ∼2Ma mer 2004; Shipman and Walker 1989). The possible stature falls in an era when stable and highly variable climate regimes increase in early Homo and by 1.9–1.7 Ma in some popula- alternated with one another, evident in the predictive frame- tions of H. erectus could have had the dual advantage of work of East African monsoonal variability (fig. 3) and in the increasing the foraging range and facilitating the search for sapropel record (fig. 5). Ultimately, this strategy of dual trans- carcasses, while animal protein and fatty tissues could have port of stone and food resources was expanded to diverse fueled body and brain growth. These foraging strategies ap- habitats populated by Oldowan toolmakers, including early pear to have been advantageous in an arid, open habitat. At Homo and H. erectus, and was elaborated in the relatively the same time, the expansion of diet to include animal foods variable settings of East Africa between 1.9 and 1.5 Ma as well was an advantageous buffer against changing templates of as across the diverse habitats of northern and southern Africa food resources across an array of habitats. That is, the adop- and from the Caucasus to eastern Eurasia (Potts and Teague tion of animal foods likely offered a useful means of ecological 2010). and dietary adjustment even if meat/fat acquisition was not the goal of all or most occasions of stone tool use. This Oldowan Behavior and Its Implications concerning approach to buffering environmental instability would have Mortality in Early Homo proved equally useful when moving through unfamiliar hab- itats, thus facilitating range expansion and dispersal (Anto´n, It is commonly assumed that the venture into the ecological Leonard, and Robertson 2002). domain of large African carnivores, made possible by profi- As hominins ventured farther into the ecological arena of cient stone flaking, entailed substantive risks of injury and large carnivores, seeking out and carrying portions of animal death and probably led to a marked rise in extrinsic mortality carcasses had its risks (Blumenschine 1991; Donadio and in Oldowan toolmakers. There is evidence, for example in Buskirk 2006). These risks were conceivably lowered when Bed I Olduvai (Domı´nguez-Rodrigo, Barba, and Egeland prey density was high and competition for meat relatively low. 2007; Potts 1988), of substantive carnivore involvement in Evidence from a variety of sites—Kanjera South, FwJj20 in bone assemblages where aggregations of stone tools also occur, East Turkana, and FLK Zinj at Olduvai—implies, however, which is indicative of a spatially focused overlap where tool- that by 2.0–1.8 Ma, the success of Oldowan toolmakers in making hominins and meat-eating carnivores conducted their competing for animal tissues applied across a broad spectrum business. The overlap of carnivore tooth marks and tool of environmental conditions and probably a variety of eco- butchery marks, first reported in Bed I Olduvai (Potts and logically competitive situations. This could mean that early Shipman 1981), might at first suggest a powerful way to in- Homo and especially H. erectus succeeded in the carnivore vestigate whether carnivores or hominins held the upper hand end of an omnivorous dietary spectrum not solely in arid, in their competitive interactions over carcasses. Such tooth/ grassland habitats but across the gamut of arid-moist con- cut mark overlaps appear to be quite rare, however, and are ditions and the changing template of seasonality associated unlikely to produce definitive, statistically robust results across with high climate variability. a variety of sites. Furthermore, no systematic study has yet been carried out comparing the frequency of carnivore tooth marks on bones of Australopithecus, early Homo, and early Delayed Consumption of Food: An Extraordinary H. erectus; the findings of such a study would not necessarily Development in Hominin Behavior with Broad measure carnivore-caused mortality but may imply how com- Implications regarding Sociality monly carnivores had access to hominin bones and the degree Relatively dense concentrations of butchered faunal remains of overlap and potential risk that hominins incurred before associated with plentiful tools made from rocks 2–13 km from and after the emergence of stone tool flaking. their sources are known by ∼2.0–1.8 Ma (Braun et al. 2008, The assumption that stone tool–assisted carnivory incurred 2010; Plummer 2004; Plummer et al. 2009). These sites appear higher mortality costs thus has yet to be demonstrated. This to reflect a critical step in foraging and sociality, namely, a point leaves open the reasonable possibility that episodic and delay in eating the marrow- and meat-rich carcass portions eventually persistent stone toolmaking and carnivory oc- that were transported. This behavior is odd, given the em- curred only when the mortality costs due to predation had phasis on “eat-as-you-go” foraging in almost all animals ex- decreased, compared with that for earlier pre-Oldowan hom- cept when provisioning young. Although Isaac’s (1984) em- inins (Lewis and Werdelin 2007). We may call this the phasis on home bases involving male-female division of labor, “decreased-mortality hypothesis” of Oldowan behavior, which pair bonding, and other elements of human behavior has been sees carnivory as an integral yet variably expressed aspect of S312 Current Anthropology Volume 53, Supplement 6, December 2012 the adaptive repertoire in early Homo and H. erectus. Such a sponse solely to arid, hot, open landscapes (see also Anto´n decrease could have been sustained by shifts in social group- 2012; Anto´n and Snodgrass 2012; Kuzawa and Bragg 2012; ing, cooperation, vigilance, and signaling, that is, a variety of Migliano and Guillon 2012). feasible behavioral changes that could have negated the sup- posed rise in mortality risk due to predation (Gursky-Doyen Persistence and Spread of Oldowan Behaviors and Nekaris 2006). Conditions favoring such social-based Beginning by 2.0 Ma strategies likely had to be met as Oldowan hominins carried carcass parts and invested in strategies of food and stone An important shift in the archaeological record of Oldowan transport that repeatedly concentrated social encounters in behavior appears to be focused in the interval from about 2.0 certain spots on the landscape, whether through central-place to 1.8 Ma. Before 2.0 Ma, archaeological sites (defined by or multiple-place foraging (Isaac 1984; Potts 1988, 1991). clusters of stone artifacts) are distributed over time in an A decrease in extrinsic mortality due to predation could have episodic pattern. That is, within a given stratigraphic se- provided the context in which intrinsic mortality (due to aging) quence, sites typically occur within a very confined strati- became a more prominent factor in life history (Kuzawa and graphic interval and a narrow and repetitive range of geo- Bragg 2012). In other words, decreased mortality due to pre- logical settings. By contrast, after 2.0 Ma, Oldowan behavior dation served as either a release or the impetus for the pro- becomes considerably more persistent, with clusters found longation of maturation and an increase in longevity. The latter more frequently across consecutive layers within a given strat- effects, furthermore, would have improved the opportunities igraphic sequence. In addition, Oldowan tools are found for alloparenting by older siblings and postreproductive adults. throughout a varied spectrum of habitats and over wider This train of cause and effect is currently speculative yet has geographic areas both within Africa and, for the first time, the following potentially testable implications: (1) taphonomic in Eurasia. indicators of decreased hominin-carnivore interaction (at odds In the series of 2.58-Ma sites from Gona, Ethiopia, for with the usual assumption of increased predation risk due to example, the three most studied lithic assemblages (EG-10, overlapping carnivory); (2) prolongation of dental develop- EG-12, and OGS-7) come from the same stratigraphic inter- ment/maturation (see Schwartz 2012), correlated with de- val, described by Stout et al. (2010) as within the second creased hominin-carnivore interaction; and (3) body size in- fining-upward sequence above the base of the Busidima For- crease, which is predicted to accompany decreased extrinsic mation. Each of about a dozen Gona sites, distributed from mortality (see Kuzawa and Bragg 2012; Migliano and Guillon ∼2.58 to 2.53 Ma and from ∼2.17 to 2.0 Ma, occurs in fining- 2012; Pontzer 2012). upward sediments overlying large cobble conglomerates (Quade et al. 2008). Site location thus seems to have been conditioned by proximity to conglomerates, which were the Increase in Body Size sources for on-site or very localized (e.g., ∼20-m distance in An increase in body size in early H. erectus is documented by the case of OGS-7) stone flaking (Stout et al. 2005, 2010). fossils such as KNM-WT 15000 (∼1.53 Ma) and KNM-ER Oldowan tools associated with the Hata Member at Bouri, 1808 (∼1.7 Ma). The robust innominate KNM-ER 3228 (Ruff dating to ∼2.5 Ma, are described as rare and scattered surface et al. 1993) dated ∼1.92 Ma (Joordens et al. 2011) and femora artifacts with no concentrations observed. Several mammalian (e.g., KNM-ER 1481) dated ∼1.89 Ma from the Turkana basin bones bearing cut marks and hammerstone impact scars have (Ruff and Walker 1993) further suggest that body enlargement also been described from surface and excavated finds within had begun by at least 1.9 Ma, although the taxon in which a single stratigraphic horizon across more than 2 km of out- this occurred is as yet unknown (see Holliday 2012; Pontzer crop (de Heinzelin et al. 1999). 2012). It seems unlikely, however, that the body size increase The next-oldest archaeological sites documented so far— in Plio-Pleistocene Homo was registered across all populations from Hadar and Omo, Ethiopia, and Lokalalei, West Turkana, or environmental contexts. Since several intervals of height- Kenya—are dated between ∼2.36 and 2.32 Ma. The two Hadar ened moist-arid fluctuation (with intervening low-variability sites known so far (within the Makaamatilu basin), A.L. 894 periods) characterized the time between 2.0 and 1.7 Ma, it is and A.L. 666, are separated vertically by ∼2 m within the possible that the increase in body size reflects the importance lowermost portion of the Busidima Formation (Goldman- of plasticity in body growth trajectories. This proposed rise Neuman and Hovers 2011). Five archaeological sites reported in plasticity would have made feasible a broader spectrum of in Omo Shungura Member F are distributed though ∼35-m body sizes, from small to large, in response to resource avail- thickness of Member F; here, the repetitive characteristic is ability and other environmental factors. Evidence of small that all of the Member F sites occur within small channel individuals of early H. erectus (sensu lato) at Dmanisi (Lord- deposits or associated floodplain silts of a braided stream (de kipanidze et al. 2007; Pontzer et al. 2010) may indicate that la Torre 2004; Howell, Haesaerts, and de Heinzelin 1987). In the apparent evolution of large body size in this species ac- the West Turkana sequence, two sites, the slightly older Loka- tually reflects the evolution of plasticity in body growth in lalei 1 and the younger Lokalalei 2C, are almost contempo- accord with a variability selection scenario rather than a re- raneous (Delagnes and Roche 2005), and the next Oldowan Potts Environments of Early Homo S313 occurrences reported so far in the basin are more than 300,000 of the Oldowan within highly dynamic East African environ- years younger, in the Upper Burgi Member at East Turkana. ments between 2.6 and 2.0 Ma and appears to have been in There is little doubt that Oldowan assemblages dated be- place by the time of the aridity pulse in East Africa. tween 2.6 and 2.0 Ma provide solid evidence of intentional flaking, selective use of raw materials, and a well-developed Adaptability as a Framework for the Analysis of sense of fracture mechanics and planning during the process Adaptations in Homo of stone flaking (e.g., Delagnes and Roche 2005; Goldman- Neuman and Hovers 2011; Stout et al. 2005). The boundary This analysis of the environmental and behavioral adaptations defined here beginning ∼2.0 Ma, nonetheless, marks a later of early Homo and H. erectus point to the importance of interval of Oldowan sites that occur in a wider variety of adaptability in diet, foraging, and mobility, that is, resilience geological, geographical, and environmental contexts. For ex- in the face of moist or arid habitats, abundant or scarce re- ample, excavations at Kanjera South, Kenya, have uncovered sources, and large lakes or dry landscapes. The picture that a continuous stratigraphic distribution of Oldowan artifacts emerges is one of shifting variability in the ecological milieu on the order of 102–103 years long, dated between 2.0 and superimposed on an overall drying trend across the time in- 1.95 Ma, associated with evidence of persistent carnivory terval from 3 to 1.5 Ma. If this current understanding of (across multiple stratigraphic layers) in the form of cut and environmental dynamics is correct, it suggests that adapta- percussion marks on small and medium-sized mammalian bility may be expected in many aspects of the biology of early skeletal remains (Ferraro 2007; Plummer 2004; Plummer et H. erectus and possibly its immediate precursor, especially a al. 2009). M. D. Leakey’s excavations in Bed I Olduvai, fur- novel degree of developmental and physiological plasticity and thermore, documented a nearly continuous distribution of a spectrum of life history trajectories that promoted the fine Oldowan stone tools from ∼1.85 to 1.70 Ma (Deino 2012; tuning of biological adaptations in Homo to the dynamics of Hay 1976; Leakey 1971). The temporal distribution of sites its surroundings (Potts 2002). The idea that particular com- in figure 5, moreover, illustrates the expansion of Oldowan binations of genes favoring plasticity can be filtered and se- sites within and beyond East Africa starting ∼2 Ma, after a lected because of the instability of conditions of natural se- noticeable sampling hiatus between roughly 2.3 and 2.0 Ma. lection, especially in times of increased seasonal- to In South Africa, new age estimates and a synthesis of data orbital-scale climate variability, is consistent with the hypo- (Herries, Curnoe, and Adams 2009; Herries and Shaw 2011) thetical process of variability selection (e.g., deMenocal 2011; indicate that the oldest currently documented Oldowan tools Grove 2011; Potts 1996a, 1996b, 1998b; Trauth et al. 2007, in this part of Africa are between 2.0 and 1.78 Ma, including 2010). Sterkfontein M5A (1.8–1.5 Ma), Wonderwerk Cave (1.95– 1.78 Ma), Malapa (∼1.98 Ma), and Swartkrans M1 (∼2.0 Ma, Conclusion although this date is considered relatively poorly constrained). A few final points arise from this analysis of the East African This revised chronology for the oldest archaeological finds in environmental and behavioral contexts of early Homo and South Africa, along with the presence of a sequence of stone Homo erectus. They are as follows. tool layers dated ∼1.8MaatAı¨n Hanech, Algeria (Sahnouni et al. 2002), further suggests that the making of stone tools Building a Synthesis of Environmental Data had become a regular part of the behavioral repertoire of dispersing populations of Homo by ∼2.0 Ma. The sequence A growing array of environmental indicators—exemplified by of Oldowan sites now documented at Dmanisi between 1.85 d18O, d13C, eolian dust, plant biomarkers, lake sediments, and and 1.78 Ma and the archaeological sequence beginning by sapropels—offers insights into the evolutionary context of 1.66 Ma in the Nihewan basin, China, further confirms the Plio-Pleistocene Africa. On first inspection, these records ap- persistence of hominin toolmakers across a wide variety of pear to contradict one another. Eolian dust and d13C (in- climatic and ecological settings (Ferring et al. 2011; Zhu et cluding its application to plant biomarkers) appear to be most al. 2004). sensitive to the arid aspects of climate variability. This makes It is unclear whether the stratigraphic persistence of the sense, given that the most arid times in Africa would correlate Oldowan within East Africa beginning roughly 2 Ma and its with strongest dust productivity and would lead to the pre- spread to other regions can be attributed to the emergence cipitation of carbonate nodules in soils, the primary focus of of H. erectus or whether these phenomena are the product of stable carbon isotope analyses. During times of large or deep two contemporaneous Oldowan toolmaking species, Homo lakes, when aquatic deposits are dominant, soils and terrestrial habilis and H. erectus. It does, nonetheless, denote a shift in fossil animals (whose teeth also provide d13C data) are often the regularity of Oldowan toolmaking from ∼2.0 to 1.8 Ma, not even recorded in sedimentary exposures. In a parallel vein, the persistence of Oldowan hominins across numerous en- analyses that focus on lake sediments are sensitive to the vironmental transitions within East Africa, and the spread of wettest times. Deep-sea d18O offers a picture of global ocean these populations into novel environments and diverse cli- temperature and tends to highlight global cooling and a trend matic regimes. All of this occurred after the early development toward rising amplitude in cold-warm or glacial-interglacial S314 Current Anthropology Volume 53, Supplement 6, December 2012 oscillation over the past 6 Myr. Passey et al.’s (2010) paleo- rent FADs for these events occur during intervals of strong temperature proxy based on d13C of Turkana basin paleosols climate variability, which, along with local tectonic and vol- is at odds with the global picture of overall cooling and pro- canic events, caused substantial modifications to resource nounced temperature variability. This apparent contradiction landscapes. The growing body of data from East African hom- may result from the special conditions under which carbonate inin-occupied basins confirms that landscapes and resources precipitates in paleosols, and thus Passey’s method may sam- underwent recurrent, high-amplitude alterations during the ple primarily the arid and hot end member in the range of focal time interval. Within this dynamic context, of growing environmental variability. Finally, sapropels capture an in- interest is the presence of refugia that offered basic needs of triguing pattern in wet-dry climate variability that does not water and food options during eras of strong climate vari- appear in the global ocean record—that is, an alternation ability throughout East Africa. between high and low climate variability—rather than a con- tinual rise in variability. Evolutionary Interpretations That Emphasize Adaptive The sapropel record in particular appears to offer a prom- Versatility Are Well Supported ising way of examining the entire moist-arid spectrum of northeast African climate. The records of sapropels, eolian The environmental and behavioral evidence summarized here dust, plant biomarkers, and lake sediments, furthermore, can highlights the importance of ecological adaptability and phys- all be reconciled with one another through the high/low cli- iological plasticity as an element, perhaps even the central mate variability framework described in this paper. As noted issue, in the evolution of Homo. An evolved responsiveness by Feakins, deMenocal, and Eglinton (2005) with regard to to environmental variability would seem to have played a biomarker isotopes, the overall aridity trend in Africa seems central role in the adaptive and phylogenetic history of Plio- to be made up of high and low variability intervals; this means Pleistocene Homo. It is important, nonetheless, to recognize that an overall aridity trend can be seen as a matter of sam- that Pleistocene Homo underwent critical behavioral, ecolog- pling: “The data . . . suggest that changes in northeast African ical, and life history transitions over the past 1 Myr. It is thus vegetation were primarily related to the amplitude of sub- sensible to avoid the temptation of attributing all that is im- tropical orbital insolation variations, since large-amplitude portant in the adaptive history of Homo sapiens to the origin vegetation variability ca. 3.7 and ca. 1.4 Ma coincided with of the genus or of its longest-enduring lineage, H. erectus. high orbital precession variability, and low variability ca. 2.4 Ma occurred during a precessional minimum” (Feakins, deMenocal, and Eglinton 2005:979–980). Likewise, dust rec- Acknowledgments ords show that alternating high and low climate variability is a crucial, newly recognized dimension in tropical African en- I am grateful to the following colleagues for their collabo- vironment pertinent to hominin evolution. ration and shared data over the past decade: Kay Behrens- The current limitation of the sapropel, dust, and biomarker meyer, Chris Campisano, Andy Cohen, Alan Deino, Peter records as applied to questions of human evolution is that deMenocal, Tim Eglinton, Sarah Feakins, Craig Feibel, Bernie they are focused exclusively in eastern and northeastern Af- Owen, and Tom Plummer. I also thank Jennifer Clark for rica. Development of long-term stratigraphic records of cli- assistance with the figures and John Kingston for enabling matic, environmental, and ecological dynamics in other the use of his data compilation in figure 2. Research reported regions of Africa remains a critical need. here was supported by the Peter Buck Fund for Human Or- igins Research, the Ruth and Vernon Taylor Foundation, Na- tional Science Foundation Hominid Program grant BCS- Evolutionary Interpretations That Emphasize Habitat or 0128511, and the Smithsonian Institution’s Human Origins Resource Stability Lack Support Program. Logistical support and collaboration with the Na- At present, the most impressive feature of East African climate tional Museums of Kenya have provided a strong base for records during the evolution of early Homo and H. erectus is several of the studies reported here. I am grateful to Leslie the series of lengthy eras of pronounced moist-arid variability. 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Dental Evidence for the Reconstruction of Diet in African Early Homo

by Peter S. Ungar

The reconstruction of diet is important for understanding the paleoecology and evolution of early hominins. This paper reviews and colligates the fossil evidence for diets of early Homo (Homo habilis, Homo rudolfensis, Homo erectus), particularly that related to tooth size, shape, structure, and wear. Technological innovations and new finds have led to improved understandings of feeding adaptations and food preferences in the earliest members of our genus. Differences in dental topography between these species and the australopiths, for example, have been doc- umented, as have differences in microwear textures between H. habilis and H. erectus. These and other lines of evidence suggest a probable shift in diet in early Homo, and especially H. erectus, compared with their australopith forebears, with a broadened subsistence base to include foods with a wider range of fracture properties. Studies to date also make clear that while much remains to be done, early hominin teeth hold the potential to provide more detail about diet and confidence in our reconstructions as samples increase, our understanding of functional mor- phology improves, and other methods of analysis are applied to the fossils we have.

Introduction to the same adaptive zone as later members of the genus (see Mayr 1950). Wood and Collard (1999) later challenged this, suggesting, in part on the basis of presumed dietary adap- Diet is the most direct connection an organism has with its tations, that the shift really began with Homo erectus. They environment. Changing environments, with associated new even proposed that both H. habilis and Homo rudolfensis be challenges and opportunities, have surely driven changes in transferred to the genus Australopithecus on this basis (see early hominin diets and with them the evolution of our genus. Anto´n 2012; Holliday 2012). There are many ideas concerning the role of diet changes in Models for key changes in the evolution of human diet can the transition to early Homo. These include elegant and well- be viewed as hypotheses, some of which may be testable using reasoned models based on nutritional studies combined with the fossils themselves (Ungar, Grine, and Teaford 2006). There direct analogy to living peoples or nonhuman primates or on are many potential lines of evidence to examine, including contextual evidence such as archeological remains and pa- dental microwear and the sizes, shapes, internal architecture, leoenvironmental indicators (e.g., Aiello and Wheeler 1995; and chemical compositions of the teeth and jaws (see Ungar Isaac 1978; O’Connell, Hawkes, and Jones 1999; Wrangham and Sponheimer 2011 for review). This paper will review four et al. 1999; Zihlman and Tanner 1978). Some have suggested of the more commonly examined lines of evidence—tooth that meat eating was key to human evolution, and others have size, shape, structure, and microwear—and what these might opined that plant foods such as underground storage organs tell us about diets of the earliest members of our genus. The were more important. Yet others have proposed that food focus will be on early Homo (i.e., fossils often attributed to preparation with tools and cooking were critical elements for H. habilis, H. rudolfensis, and H. erectus) from Africa and the evolution of human diet. whether these provide evidence for dietary differences among Another issue that has been raised revolves around where these species and between them and the australopiths (Aus- to draw the line between australopith-like and humanlike tralopithecus spp., Paranthropus spp.). While data are ex- diets. Leakey, Napier, and Tobias (1964) drew that line with tremely limited and interpretations must be considered ten- Homo habilis. By including this presumed-toolmaking hom- tative, the fossil evidence is consistent with a broadening of inin in Homo, these authors recognized H. habilis as belonging the subsistence base by early Homo and especially H. erectus to include more tough foods. Peter Ungar is Distinguished Professor and Chair, Department of Anthropology, University of Arkansas (Old Main 330, Fayetteville, Tooth Size Arkansas 72701, U.S.A. [[email protected]]). This paper was submitted 12 XII 11, accepted 14 V 12, and electronically published Tooth size has been considered an important proxy for early 23 VIII 12. hominin diets since Robinson (1954) noted variation among

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0005$10.00. DOI: 10.1086/666700 Ungar Diet in Early Homo S319 species more than half a century ago. He argued that the paring gibbons to siamangs and chimpanzees to gorillas. Pri- large, flat premolars and molars of Paranthropus robustus were mates feeding on large, husked fruits benefit from larger in- well suited to crushing and grinding tough vegetation, whereas cisors to process them, whereas those that feed on smaller the larger front teeth and smaller cheek teeth of Australo- objects (e.g., berries, leaves) do not require big front teeth. pithecus africanus are consistent with “a more nearly omniv- Larger incisors also increase functional life given wear asso- orous diet, which may have included a fair proportion of ciated with increased use. These results have been more or flesh” (Robinson 1954:328). He also noted that “Telanthropus” less confirmed in subsequent studies of anthropoids, although (Homo erectus) from Swartkrans evinced more humanlike the importance of comparing closely related species has been dental proportions with smaller molars than either of the noted; for example, independent of diet, platyrrhines as a australopiths from South Africa. And Leakey, Napier, and group have smaller incisors than do catarrhines (Eaglen 1984; Tobias (1964) included small molars relative to Australo- see also Ungar 1996). Further, the relationship between diet pithecus as part of their revised diagnosis of the genus Homo and incisor size in strepsirhines is not nearly as clear (Eaglen when they first described Homo habilis. 1986). Groves and Napier (1968) followed with a comparative So where do early hominins, and especially early Homo study of incisor-to-molar row-length ratios (incisor-molar in- species, fit in incisor size studies? This is not an easy question dex). They found that fruit-eating chimpanzees have relatively to answer. Efforts to compare incisor sizes (usually measured larger incisors and smaller molars than do more folivorous as mesiodistal diameters of I1s) of early hominins are com- gorillas, with orangutans intermediate in both incisor-molar plicated by small samples (Ungar, Grine, and Teaford 2006). index and diet. Relatively large incisors were thought to be We can count the number of I1s reported for some hominin adapted to husking and ingesting fruits, whereas larger molars taxa with the fingers of one hand, which presents a formidable -for ex 20%ע were associated with grinding coarse vegetation. They then challenge given typical size variation of about reported that Australopithecus had a similar incisor-molar in- tant hominoids (Plavcan 1990). An even greater challenge is dex to the gorilla, and Paranthropus had an even smaller value. the paucity of associated craniodental and postcranial remains Homo habilis had an incisor-molar index in the range of available on which to base body-mass estimates. Indeed, as chimpanzees and orangutans. Smith (1996) has noted, confidence intervals for recon- Jolly (1970) soon after proposed his seed-eater hypothesis structed weight averages of most hominin species are so great wherein, and by analogy with the modern gelada, the large that our allometric studies must be approached with caution molar teeth and smaller incisors of Paranthropus were inter- if not skepticism. McHenry’s (1994) average body weight es- ע kg for males and 31.5 22.6 ע preted as adaptations to consume small tough seeds. Aus- timate for H. habilis is51.6 tralopithecus and especially H. habilis were said to have moved 22.5 kg for females. And for Homo rudolfensis,wehaveno from grass seeds to the consumption of more meat and gath- idea about body size because there are no published postcra- ered vegetable foodstuffs given that “the trend to back-tooth nial bones definitively associated with this hominin, though dominance has been partially reversed” (Jolly 1970:23). While it is common to assign KNM-ER 1472 and KNM-ER 1481 a specialization on grass seeds by earlier hominins has since (from Koobi Fora, Kenya) to it (Kimbel 2009; Wood 1992). been considered unlikely (Dunbar 1976), this idea has been In this light, the value of placing estimates for individual influential in stimulating further research, especially that using hominin species on a regression plot of tooth size against extant analogues as models for early hominin diets. And the body mass for extant primates is not entirely clear. idea that some hominins (i.e., Paranthropus boisei) regularly Despite these constraints, however, it may still be “heuris- consumed C4 resources, such as tropical grasses, has recently tically interesting” (McHenry and Coffing 2000) to compare received support from other studies (e.g., Ungar and Spon- incisor size with estimated body weights, understanding that heimer 2011). results must be considered tentative at best. Figure 1 repre- sents a regression of I1 breadth for a variety of extant catar- rhines with 95% confidence limits as indicated. This confirms Incisor Allometry that relative incisor size does indeed reflect diet differences Most of the work that followed considered front teeth and among living Old World higher primates. Average values for back teeth separately, as it would otherwise be unclear on hominins (both incisor size and body weight estimates) are which part of the dentition selection has acted. Hylander’s plotted for comparison. Data for Australopithecus anamensis, (1975) study of anthropoid incisors provides a case in point. Australopithecus afarensis, and Australopithecus africanus fall He found that residuals from a regression line of incisor row on or near the regression line connecting gibbons and gorillas, width (taken as a proxy for incisor size) plotted against body suggesting moderate incisor size. Australopithecus spp. have mass predict diet such that frugivorous cercopithecines have neither the large incisors of chimpanzees and orangutans nor relatively larger front teeth than do folivorous colobines (see the small ones of extant folivorous colobines. Homo habilis, also Goldstein, Post, and Melnick 1978). Frugivorous squirrel and H. rudolfensis both have enlarged incisors relative to Aus- monkeys also have relatively larger front teeth than do more tralopithecus spp., and relative incisor size in H. erectus is folivorous howlers, and the same pattern holds when com- intermediate between those of H. habilis and H. rudolfensis S320 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 1. Incisor allometry. The dashed lines indicate 95% confidence limits of the least squares regression. This figure is modified from Teaford, Ungar, and Grine (2002) with original data and taxonomic attributions from Coffing et al. (1994), Jungers (1988), Leakey et al. (1995), Ungar and Grine (1991), and Wood (1991). on the one hand and Paranthropus and modern humans on Homo habilis s.l. and H. erectus, particularly when specimens the other. If these values are accurate, they suggest an increase from outside of Africa are incorporated into analyses. in incisor size with the earliest members of the genus Homo The traditional explanation for megadontia in the australo- followed by a decrease in H. erectus and ultimately Homo piths, and especially Paranthropus, has been that enlarged sapiens. It should be reiterated, however, that tiny samples cheek teeth provide more surface area to process larger quan- (n p 2 each for H. habilis and H. erectus,forn p 1 H. ru- tities of lower-quality and mechanically challenging foods. dolfensis) and uncertain weight estimates remain a serious While Pilbeam and Gould (1974) suggested that differences limitation (see Teaford, Ungar, and Grine 2002). in tooth size between hominins could be explained by met- abolic scaling (i.e., larger species might need relatively larger Molar Allometry teeth given metabolic requirements), Kay (1975, 1985) has shown that for primates with given food preferences, tooth Studies of molar allometry face the same limitations as those size scales isometrically with body size. Thus, differences in for incisors (small samples, questionable weight estimates) relative tooth size between hominins probably do reflect dif- but are also challenged by uncertain form-function relation- ferences in diet, especially given the likely overlap in body ships. That said, molar size has been considered an important indicator of adaptive zone (e.g., Leakey et al. 2001; Wood and mass between hominin species (Jungers 1988; McHenry and Collard 1999), and many have suggested an increase in molar Coffing 2000). Indeed, Lucas (2004) has argued from a bio- size over time in the australopiths followed by a decrease over mechanical perspective that cheek-tooth size should relate to time in the genus Homo (e.g., see Brace, Smith, and Hunt the external properties of foods, including ingested particle 1991; McHenry and Coffing 2000; Teaford and Ungar 2000). size, shape, and abrasiveness. A diet dominated by smaller As illustrated in figure 2, this holds whether we consider particles or thinner ones with less volume (sheets or rods) absolute cheek-tooth surface area or a megadontia quotient should select for larger teeth to increase the probability of that incorporates reconstructed body size. There has been little fracture. Likewise, abrasive foods should select for larger teeth agreement, however, as to with whom the decrease in me- to increase surface area for wear. gadontia starts. According to Wood and Collard (1999), H. But what would explain decreasing molar sizes in the genus habilis and H. rudolfensis retain australopith-size teeth, and Homo? Several hypotheses have been proposed. The tradi- molar reduction begins with H. erectus. According to Mc- tional explanation is that tooth size decreases as selective pres- Henry and Coffing (2000), however, H. habilis and especially sures to maintain larger teeth are relaxed; foods processed H. rudolfensis show some reduction of occlusal area relative with tools and by cooking require less chewing (e.g., see Brace, to body size when compared with the australopiths. And as Smith, and Hunt 1991). Reduction in cheek-tooth size has Anto´n (2008) has noted, there is substantial overlap between been attributed to mutation, drift, or even selection given Ungar Diet in Early Homo S321

Figure 2. Cheek-tooth occlusal areas and megadontia quotients of early hominins. Occlusal areas (the sum of the products of mesiodistal and buccolingual diameters of P4,M1, and M2) are presented above (A), and megadontia quotients (occlusal areas divided by 12.15 # body mass0.86) are illustrated below (B). The values in these graphs are from McHenry and Coffing (2000), and taxonomic attributions are as presented by those authors. savings of energy and raw materials (Brace 1963; Jolly 1970; and Hanna 2005). This does not hold for cercopithecoids, Smith 1982). Another popular idea is that decreased chewing however, as colobines have smaller molars than cercopithe- resulting from tool use led to a reduction of mechanical cines (Kay 1977). It is also unclear why for many primate stresses on the mandible that are necessary for alveolar bone species, males have relatively smaller cheek teeth than females growth (Oppenheimer 1964). Teeth would have evolved to (Harvey, Clutton-Brock, and Kavanagh 1978). Because rela- become smaller to avoid dental crowding, which can lead to tive molar size does not track broad diet category the same impaction, malocclusion, and a predisposition for periodontal way in all groups of extant primates, it is difficult to use this disease (see Calcagno and Gibson 1991; Jungers 1978; Sofaer, trait to retrodict diets of fossil hominins, at least until we can Bailit, and MacLean 1971). Lucas et al. (2009) suggested yet explain differences between higher-level taxa in the patterns another possibility related to the notion that tooth size affects observed (Kay and Cartmill 1977). the rate of food processing. Smaller cheek teeth could slow So what might explain the unexpected results for cerco- down oral processing to avoid a “potential avalanche of food” pithecoids? Perhaps the tendency toward smaller teeth in co- given the consumption of items requiring less chewing, such lobines relates to the need to avoid dental crowding given as meat or plant parts prepared with tools or by cooking. shorter faces. Of course, this raises the question of whether We may be able to gain some insights by considering re- tooth size drives jaw length or whether it is the other way lationships between occlusal surface area and diet in living around (Brace, Smith, and Hunt 1991). Perhaps there is a primates. Given that leaves are tough and that thin sheets modular developmental link between jaw length and molar require thorough chewing, they should select for larger teeth, size (see Vinyard and Hanna 2005). Indeed, Workman et al. and indeed folivores do have longer molars than closely re- (2002) found that for mice, many quantitative trait loci af- lated frugivores for most primate groups (Kay 1977; Vinyard fecting tooth size and jaw shape are the same. This may have S322 Current Anthropology Volume 53, Supplement 6, December 2012 implications for fossil hominins, for which associations be- and Ungar 1997). The fact that teeth change shape as they tween jaw length and tooth size have been noted for some wear must also be considered; shearing crests can be difficult time (Sofaer 1973). And as McCollum and Sharpe (2001) to measure when the landmarks used to define them are have argued, there is likely a developmental link between tooth obliterated with use. As such, whole-surface characterizations form and skull form. Until we have a better understanding of dental topography can be especially valuable for distin- of relationships between tooth size and function in living guishing species on the basis of diet. Indeed, dental topo- primates, however, we are probably best off using other lines graphic analysis has shown that folivorous monkeys and apes of evidence to infer the diets of fossil hominins. have, at a given stage of gross wear, steeper sloping surfaces with greater occlusal relief than do closely related frugivores Occlusal Morphology (Bunn and Ungar 2009; M’Kirera and Ungar 2003; Ungar and Bunn 2008; Ungar and M’Kirera 2003). As Aristotle noted more than 2 millennia ago in De partibus So what about early hominins? Are there differences in animalium, “teeth have one invariable office, namely the re- shearing-crest lengths or slope and relief between early Homo duction of food” (in Ogle’s translation, 1912). Teeth are tools and the australopiths that preceded them? While hominin to burst cell walls and to fracture and fragment foods to species have been distinguished on the basis of occlusal form increase the surface area exposed to digestive enzymes. And (see Bailey and Wood 2007 and references therein), little re- because natural selection theory dictates that animals should search to date has focused on the functional morphology of evolve the best tools possible for the job, teeth should be their crown shapes. Studies of shearing-crest length do not formed in a manner suited to overcoming the mechanical work well with early hominins because their molars typically defenses of the particular foods that an animal eats (Ungar have bulbous cusps that lack distinct crests for measurement. 2010). Also, because crest lengths are difficult or impossible to mea- Dental functional morphologists consider two basic types sure on worn or damaged teeth, there is an insufficient sample of mechanical defense: stress limited and displacement limited of early Homo specimens for such analyses, especially given

(see Lucas 2004; Ungar and Lucas 2010). Foods protected by that studies typically focus on a single tooth type (e.g., M2s) stress-limited defenses tend to be strong and stiff; it requires for comparability of results. Still, it has been noted that while substantial force per unit area to initiate a crack in them. early Homo species did not have the long sharp crests seen These foods are also often brittle, so they do not require a in extant folivores, their cheek teeth do appear to be less great deal of work to spread a crack once it starts. Examples bunodont than those of australopiths (Teaford, Ungar, and include hard-brittle nuts and bone. Foods protected by dis- Grine 2002; Wood and Strait 2004). placement-limited defenses, on the other hand, are tough or This has been confirmed with a dental topographic analysis ductile; initiating a crack in such foods is often less of a (Ungar 2004, 2007) of early Homo from Africa, though the challenge than propagating it. Examples include many leaves paucity of available specimens, even worn ones, has made it and animal flesh. Some foods, such as softer fruits, are in- necessary to combine early members of the genus into a single termediate in their fracture properties, and many are com- sample (see table 1 for taxonomic attributions of individual posites with individual elements varying in their mechanical specimens). Results of comparisons of dental topography of defenses. Different dental tool kits are most appropriate for M2s of early Homo with Australopithecus afarensis and extant efficient processing of these different types of food. Hard- chimpanzees and gorillas are illustrated in figure 3. The com- object feeders, for example, should have blunt but dome- bined early Homo sample falls between the two African apes shaped cusps to concentrate force on a small area while at in average surface slope and topographic relief for all but the the same time protecting the tooth itself from fracture. These most worn specimens, and relief is significantly less than that should oppose concave surfaces formed by basins or staggered of gorillas. On the other hand, the average occlusal slope for cusps to prevent energy loss due to the spread or movement early Homo is significantly greater than that for A. afarensis. of food. Folivores and other tough-food feeders, in contrast, Degree of difference in surface slope and occlusal relief values would be better served by shear-like offset opposing blades at given stages of wear for the two hominin samples are on or crests acting as wedges to create tension at the tips of the same order as or slightly less than those between gorillas advancing cracks. and chimpanzees. This suggests a degree of difference in di- Studies of dental morphology have borne out these pre- etary adaptation between early Homo and A. afarensis com- dictions. Folivorous and insectivorous primates tend to have parable with or slightly less than that seen between the extant longer shearing crests relative to tooth length than do closely African apes (with appropriate caveats for sample size and related frugivorous species (Kay and Covert 1984; Strait 1993). combining samples). Further, among frugivores, hard-object feeders have the short- So what do differences in occlusal topography between early est shearing crests (Meldrum and Kay 1997). As with studies Homo and Australopithecus mean in terms of dietary adap- of incisor size, shearing-crest lengths need to be compared tations? Chimpanzees and gorillas consume many foods in among closely related species as, for example, cercopithecoids common where the two are sympatric; they differ mostly at have longer crests than platyrrhines independent of diet (Kay times of fruit scarcity, when gorillas fall back on tougher, more Ungar Diet in Early Homo S323

Table 1. Specimens of early Homo used in analyses

Analysis Species Occlusal morphology Microwear texture Homo erectus KNM-ER 806, KNM-ER 992, KNM-WT 15000, OH 22 KNM-BK 8518, KNM-ER 807, KNM-ER 820, KNM-ER 992, KNM-ER 1808, KNM-WT 15000, OH 60, SK 15 Homo habilis OH 16 OH 4, OH 7x, OH 15, OH 16, OH 41, OH 65, OH 67, OH 69, OH 70, Stw 15 Homo rudolfensis KNM-ER 1506, KNM-ER 1802 Homo sp. KNM-ER 3734 Note. Analyses are described in the text. Attributions follow authors referenced in each section (see Anto´n 2012 for additional discussion).

fibrous plant parts such as leaves and stems, whereas chim- differences in preferred foods or fallback items, though dental panzees continue to exploit available ripe, succulent fruits microwear (see below) may provide additional evidence to (e.g., Remis 1997; Tutin et al. 1991). It may be that early help us resolve this. Homo and A. afarensis diets likewise differed subtly, with sub- stantial overlap in food types, or at least in their fracture Dental Structure properties. The blunt-cusped molars of Australopithecus would have been somewhat better suited to crushing hard- Studies of early hominin dental structure are beginning to brittle foods because crown shape would have made these experience a renaissance of sorts given both new methods of teeth resistant to fracture under heavy stress (Berthaume et characterization and new theories for interpreting it. Research al. 2010). Early Homo cheek teeth have less bulbous cusps has focused on the thickness of the enamel cap and on the and more sloping occlusal surfaces that would have allowed layout of its microstructure (see Swain and Xue 2009; Teaford them to shear or slice tough items more efficiently. This of 2007b for review). course does not tell us whether differences in dental-dietary adaptations between early Homo and the australopiths reflect Enamel Thickness For more than half a century, the australopiths have been recognized to have had a relatively thick cap of enamel cov- ering their teeth (e.g., Robinson 1956). Simons and Pilbeam (1972) suggested that this was an adaptation to lengthen the use life of the dentition given rapid wear with the consump- tion of tough, grit-laden foods on the ground (see also Macho and Spears 1999). Kay (1981) countered that there is no ten- dency among living apes or Old World monkeys for terrestrial species to have thicker enamel than arboreal ones. And the fact that orangutans, the most arboreal of the great apes, not only have thicker tooth enamel (at least by traditional mea- sures) than African apes but tend to have less worn teeth than chimpanzees or gorillas suggests that this trait need not be a compensatory mechanism for increased wear (Dean, Jones, and Pilley 1992; but see Kono 2004). The alternative explanation is that thickened enamel in early hominins provided structural reinforcement to strengthen teeth against breakage given forces generated by a diet of hard foods (Kay 1981). Tooth and food are in a “death match” as nature selects for strength in both—teeth must break foods without themselves being broken (Ungar 2008). And indeed, primates that consume hard objects tend to have thicker molar enamel than do closely related forms that eat Figure 3. Dental topographic analysis data. Mean occlusal relief softer foods (Dumont 1995). This makes sense, especially (A) and slope (B) values by wear stage (see Ungar 2004) for taxa as indicated in the legend. The data illustrated are from Ungar given that tooth crowns are bilayered with hard-brittle enamel (2004), with early Homo specimen attributions as indicated in overlaying more compliant dentin; hard-object feeders should table 1. have thicker enamel because heavy loads would make thin S324 Current Anthropology Volume 53, Supplement 6, December 2012 coats more prone to flex and cause tensile stresses leading to even has implications for crown sculpting with wear, as prisms cracks in teeth (Lucas et al. 2008). aligned parallel to an abrasion vector are more resistant than The relationship between enamel thickness and diet is not those perpendicular to it—witness the enamel ridges on the a simple one, however. It has become increasingly clear that occlusal surfaces of rhinoceros teeth resulting from differing the distribution of enamel covering a tooth, not just its av- prism orientations (Rensberger and Koenigswald 1980). Finite erage thickness, is important for understanding function (e.g., element modeling has recently been applied to better under- Macho and Thackeray 1992; Schwartz 2000). Dental sculpting stand effects of prism orientation on surface stresses and wear provides a case in point. Many mammals have teeth that resistance (Shimizu, Macho, and Spears 2005). actually require wear to function properly (see Fortelius 1985; As with studies of enamel thickness, though, only limited Ungar 2010). Because enamel is harder than dentin, wear can work has been published on the functional implications of cause a sharp edge to form where the two tissue types meet enamel microstructure variation in early hominins (Macho on the occlusal surface (Kono 2004; Shimizu 2002; Ungar and and Shimizu 2009; Macho et al. 2005). While this research M’Kirera 2003). Thinner enamel can result in quicker dentin documents variation between species, it has been limited to exposure to facilitate fracture of tough foods. Thus, the mor- naturally fractured surfaces of australopith teeth; no such phology of the enamel-dentin junction (EDJ) can literally functional studies have yet been published for early Homo. guide wear to sculpt occlusal surfaces. Exciting new studies There remains a great deal of background work to be done, using x-ray microcomputed tomography (micro-CT) to map but the potential of dental microstructure for functional stud- the distribution of enamel across tooth crowns show great ies is clear. Phase contrast x-ray synchrotron microtomog- promise to help us better understand both form and function raphy, which allows imaging of dental microstructure with (e.g., Gantt et al. 2006; Kono 2004; Kono and Suwa 2008; submicron resolution, offers a particularly promising ap- Olejniczak et al. 2008b; Smith and Tafforeau 2008). proach (Tafforeau and Smith 2008). While researchers have begun to map enamel distribution and EDJ morphology in fossil hominins (Olejniczak et al. Dental Microwear 2008a; Suwa et al. 2009), such studies have not yet been extended to early Homo. Nevertheless, there has long been Tooth size, shape, and structure can all potentially tell us the general impression among researchers that early members something about hominin dietary adaptation. That said, mor- of our genus had thinner enamel than did the australopiths phological specializations should reflect mechanically chal- (see Wallace 1975). Beynon and Wood’s (1986) measurements lenging foods rather than those that require little work to of naturally fractured specimens from East Africa support this fracture if both are needed for survival, regardless of which assertion in that Homo erectus has the absolutely thinnest is eaten more frequently (e.g., Constantino et al. 2009; Ungar enamel of Plio-Pleistocene hominins they analyzed. On the 2004; Wood and Strait 2004). It should not matter what your other hand, a recent study of enamel thickness across the teeth look like if you eat gelatin most of the time, but if you genus using micro-CT on intact specimens indicates sub- have to crush hard nuts 5 days out of the year to survive, stantial variation in early Homo molar teeth. Indeed, some your teeth had better be able to crush hard nuts. Dental specimens from South Africa have average and relative enamel adaptations can tell us something about the capabilities of thickness values comparable to those of Paranthropus (Smith teeth but not how frequently they were used on given types et al. 2012). Further study and comparisons among taxa will of food. This is an important distinction, as a tooth may be hopefully provide new insights into the functional implica- overbuilt for most of the foods an animal eats. tions of enamel thickness and distribution in early Homo. In contrast to adaptive lines of evidence, dental microwear reflects the fracture properties of foods that animals eat on a day-to-day basis. Dental microwear analysis is the study of Enamel Microstructure microscopic patterns of wear that form on teeth as the result It is also clear that the physical properties of enamel can vary of food acquisition and processing. The basic idea is that hard- across a tooth crown (Cuy et al. 2002). This is due in part brittle items crushed between lower and upper teeth should to chemical composition but also in large measure to mi- create pits, whereas tough foods sheared as opposing surfaces crostructure. Enamel prisms and crystallites within them can slide past one another should result in scratches. And nu- be arranged in many different ways to limit the development merous studies have shown that hard-object feeding primates and spread of cracks through a crown. For example, layers tend to have molar microwear surfaces dominated by large of prisms can decussate or wiggle about in waves between the pits, folivores have more scratches, and soft-fruit eaters or EDJ and crown surface. Adjacent layers can interweave and mixed feeders are intermediate (e.g., see Teaford 1991, 2007a; be stacked horizontally, vertically, or in a zigzag fashion to Ungar et al. 2007). Studies also show that microwear features prevent the spread of cracks and strengthen a tooth are replaced as they wear away and that patterns can change (Koenigswald and Clemens 1992; Maas and Dumont 1999; over the course of days, weeks, or months (Teaford and Oyen Rensberger 2000). This has important implications for struc- 1988). As such, if we have sufficient numbers of individuals tural integrity of enamel under different loading regimes. It sampled over time, we should be able to infer something Ungar Diet in Early Homo S325 about dietary preferences and perhaps even foraging strategies Discussion of a fossil species. The combination of adaptive evidence and microwear may then provide important insights not just into The most obvious conclusion we can draw from a review of the fossil evidence for diet in African early Homo is that there diet but into how nature selects for tooth size, shape, and is not much of it, and what we do have is not very compelling. structure (Ungar 2009). We lack the large samples of teeth for individual species that Microwear research on early hominins at first focused on are available for Australopithecus afarensis and the South Af- the australopiths (e.g., Grine 1981; Ryan 1981; Walker 1981), rican australopiths. The fossil record for postcranial remains, but studies have recently been expanded to include early especially those associated with teeth, is even worse. These do Homo. Ungar et al. (2006) found that a sample of Homo not engender confidence in our studies of dental allometry, habilis, African Homo erectus, and early Homo specimens of especially for incisors, for which size estimates are based on uncertain taxonomic affinity from Sterkfontein Member 5 samples as small as one or two individuals per species. And and Swartkrans Member 1 had average microwear pit-scratch for cheek teeth, because the relationship between occlusal area ratios intermediate between those of living hard-object feeders and diet in extant catarrhines is not consistent among higher- and folivores. Early Homo pit widths also fell near the middle level taxa, our interpretations would be limited even if our of the extant primate range, suggesting that fossil individuals data were reliable. In addition, studies of some functionally sampled did not specialize on extremely hard, stiff, or tough relevant aspects of tooth form (i.e., enamel distribution across 1 foods, at least not in the days or weeks before death. These the crown and microstructure) have not yet been published results have been confirmed by microwear-texture analysis, a for early Homo, and those that have (i.e., occlusal topography 3-D automated approach to whole-surface characterization and enamel thickness) must await larger samples for com- that combines white-light confocal profilometry and scale- parisons among Homo habilis, Homo rudolfensis,andHomo sensitive fractal analysis (Scott et al. 2006; Ungar et al. 2003). erectus. These things do not bode well for testing hypotheses The early Homo sample as a whole shows moderate microw- concerning dietary shifts from the australopiths to early ear-texture complexity (complex surfaces tend to be more Homo, the tempo of presumed shifts, or in which species they pitted) and fill volume (an indication of feature size) both in first occurred. terms of central tendencies and dispersion. Early Homo av- While we can say little with confidence, speculation based erage values are intermediate between extant hard-object feed- on some data is likely better than speculation based on none. ers and folivores (Ungar and Scott 2009). If incisor allometry results hold, H. habilis and H. rudolfensis A more recent study on an expanded sample of African (as identified by Wood 1991, 1992) had larger front teeth than early Homo specimens by Ungar et al. (2012) suggests dif- either the australopiths or African H. erectus. One possible ferences between H. habilis and H. erectus (see table 1 for interpretation is a shift toward foods requiring more incisal taxonomic attributions of specimens included in this analysis preparation in H. habilis and H. rudolfensis followed by a and fig. 4 for illustration of results). Homo habilis has a higher decrease in front tooth size due to either a change in diet in average scale of maximum complexity and textural fill volume H. erectus or a change in selective pressures related to in- (both indicative of fewer small features; see Scott et al. 2006 creased extraoral food processing. for details) and less variance in texture complexity than H. As far as the back teeth are concerned, there is a tendency erectus. In fact, H. erectus has remarkably high variance in toward increasing occlusal area through time in the austra- texture complexity, matched only by Paranthropus robustus lopiths then a decrease through time in Homo. That said, H. among the early hominins. The average complexity of H. habilis and H. rudolfensis appear to have retained large cheek erectus is lower than that of the P. robustus, however, sug- teeth, in the size range of Australopithecus, with fossils com- gesting that while the two may have had similar ranges of monly referred to H. rudolfensis having an occlusal area av- food hardness, the latter ate more hard-brittle foods on av- erage comparable to that of Paranthropus robustus. Homo erage. These results indicate that early Homo as a group prob- erectus, on the other hand, shows a substantive decrease in ably did not regularly consume foods that were either espe- cheek-tooth size, with values approaching those of modern cially hard or tough but that H. erectus may have had a humans. Some have suggested that smaller cheek teeth might reflect selection to slow down the process of digestion or to somewhat broader diet, at least in terms of food fracture reduce dental crowding given a shorter jaw. Interpretations properties, than did H. habilis. Microwear-texture data for of variation among hominins in occlusal surface area will two H. erectus specimens from Dmanisi are consistent with remain uncertain, however, until we better understand rela- these results, as both Georgian specimens have complexity tionships between diet and cheek-tooth area in living pri- values within the interquartile range of African H. erectus but mates. above that for H. habilis (Pontzer et al. 2011). We may be on firmer ground regarding interpretations of 1. Small pits can form with the consumption of tough foods as prisms topographic relief, though small samples prevent comparisons are “plucked” from their surrounding matrix because of friction (Teaford of early Homo species to one another. Early Homo as a group and Runestad 1992). has more occlusal topographic relief than the australopiths, Figure 4. Dental microwear-texture data. Box-and-whiskers plots of microwear data for area-scale fractal complexity (A), scale of maximum complexity (B), and textural fill volume (C). The hinges mark the first and third quantiles, the horizontal lines between them are medians, each whisker represents a value 1.5 times the interquartile range, asterisks are outliers, and circles are far outliers. The data illustrated are from Ungar et al. (2012), with early Homo specimen attributions as indicated in table 1. Ungar Diet in Early Homo S327 though these teeth are much more bunodont than those of References Cited gorillas or tough-food specialist monkeys. Aiello, Leslie C., and Peter Wheeler. 1995. The expensive-tissue hypothesis: And early Homo molars tend to have unremarkable mi- the brain and the digestive system in human and primate evolution. Current crowear texture complexity and anisotropy, suggesting that Anthropology 36:199–221. Anto´n, Susan C. 2008. 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Body Size, Body Shape, and the Circumscription of the Genus Homo

by Trenton W. Holliday

Since the 1984 discovery of the Nariokotome Homo erectus/Homo ergaster skeleton, it has been almost axiomatic that the emergence of Homo (sensu stricto) was characterized by an increase in body size to the modern human condition and an autapomorphic shift in body proportions to those found today. This was linked to a behavioral shift toward more intensive carnivory and wider ranging in the genus Homo. Recent fossil discoveries and reanalysis of the Nariokotome skeleton suggest a more complex evolutionary pattern. While early Homo tend to be larger than Australopithecus/Paranthropus, they were shorter on average than people today. Reanalysis of the Nariokotome pelvis along with the discovery of additional early and middle Pleistocene pelves indicate that a narrow bi-iliac (pelvic) breadth is an autapomorphy specific to Homo sapiens. Likewise, it appears that at least some early Homo (even those referred to H. ergaster/H. erectus) were characterized by higher humero-femoral indices than the H. sapiens average. All these data suggest a pattern of mosaic postcranial evolution in Homo with implications for the increased ranging/carnivory model of the origin of Homo as well as for which species are included within the Homo hypodigm.

Introduction lutionarily the only successful taxon, because the other African apes appear poised for extinction in the wild, and importantly, The oldest and most persistent questions in paleoanthropol- their decline is not likely merely the result of recent habitat ogy are those that pertain directly to us. Specifically, the two destruction due to an ever-expanding human population but longest-lived questions in our discipline are (1) the origin of rather may have more to do with their overreliance on a highly our own species, Homo sapiens, which occurred sometime K-selected reproductive “strategy” coupled with a decreased around the end of the middle Pleistocene; and (2) the origin population growth rate associated with larger brains (Isler of our own genus, Homo, which most likely occurred in the and van Schaik 2012; Lovejoy 1981, 2009). late Pliocene. The questions surrounding the origins of these This paper studies early (ca. 2.0–1.5 million years ago taxa are not merely of phylogenetic bookkeeping interest. Be- [mya]) Homo specifically with regard to its postcranial skel- cause they involve our direct ancestors, we tend to imbue eton, body size, and limb and body proportions. The study these questions with a suite of functional/adaptive explana- of limb and body proportions of early Homo in particular tions (e.g., intelligence and/or spoken language in the case of has led to extensive debate as to whether the earliest members modern human origins and increased encephalization, larger of the genus had limb and body proportions similar to those body and home-range size, more efficient bipedality, and in- of Australopithecus (who are presumed to have included more creased carnivory in the case of the origins of the genus of an arboreal component in their locomotor behavior) or, Homo). In light of humanity’s global distribution, invoking in contrast, whether their limb and body proportions were adaptation when our own species/genus’s evolution is con- more similar to those of modern humans, which could be cerned is certainly warranted. Our widespread geographic dis- taken as indicative of fully committed terrestrial bipedality tribution is even more impressive when one considers that (Bramble and Lieberman 2004; Haeusler and McHenry 2004, among the African hominids (sensu lato), humans are evo- 2007; Hartwig-Scherer and Martin 1991; Holliday and Fran- ciscus 2009; McHenry and Berger 1998a, 1998b; Pontzer 2012; Pontzer et al. 2010; Reno et al. 2005; Richmond, Aiello, and Trenton W. Holliday is Professor of Anthropology at Tulane University (101 Dinwiddie Hall, 6823 St. Charles Avenue, New Wood 2002). Observed (or presumed) differences in body Orleans, Louisiana 70118, U.S.A. [[email protected]]). This paper size and proportions between Homo sapiens and some early was submitted 12 XII 11, accepted 11 VI 12, and electronically Pleistocene hominins referred to Homo have even played a published 14 IX 12. role in some researchers’ call to remove key specimens (and

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0006$10.00. DOI: 10.1086/667360 Holliday Body Size and Shape in Early Homo S331 even presumed species-level taxa) from the genus Homo al- Wood and Collard (1999a, 1999b) used an operational defi- together (Collard and Wood 2007; Wood and Collard 1999a, nition of the genus category that combined what they viewed 1999b). as the stronger aspects of both Mayr’s (1942) and Hennig’s (1966) approaches. They recognized that a strict “Hennigian” Circumscribing the Genus Homo approach to defining genera gave no real guidance as to how to circumscribe genera versus other higher Linnaean cate- In order to discuss body size and shape in the genus Homo, gories and that Mayr’s (1942) approach was faulty in that it it is critical to determine the composition of that genus. In could lead to the recognition of paraphyletic genera—taxa zoology, there are generally four nonmutually exclusive sets that are biologically “unreal” in that they do not reflect the of criteria by which species taxa are considered congeneric: true evolutionary relationships of the taxa in question. In- (1) recency of common ancestry, (2) ecological/adaptive sim- stead, Wood and Collard (1999b:66) define a genus as “a ilarity, (3) genetic divergence, or (4) morphological similar- species, or monophylum, whose members occupy a single ities. However, there is little agreement among zoologists as adaptive zone.” Importantly, their definition of a genus does to how exactly this is done, and, as recently pointed out by not restrict any particular “adaptive zone” to a single genus, Collard and Wood (2007), relatively little attention has been instead allowing “for the possibility that species assigned to paid by taxonomists as to how the genus category is opera- different genera will occupy the same adaptive zone,” but it tionally defined. Ernst Mayr (1942:283), one of the founders does prevent “species in the same genus from occupying dif- of the school of evolutionary taxonomy, defined a genus as ferent adaptive zones” (Collard and Wood 2007:1584). An “one species or a group of species of presumably common “adaptive zone” is characterized by Wood and Collard (1999a: phylogenetic origin, separated by a decided gap from other 202) as being related to an organism’s phenotype and its similar groups.” Mayr’s definition therefore allows for “grade” ability to “maintain homeostasis, acquire food, and produce characters (or at a minimum, perceived “gaps” between them) offspring.” While recognizing that not all of these aspects of to be involved in circumscribing taxa, making it unacceptable the phenotype are easily recognizable in the fossil record, to strict practitioners of phylogenetic systematics (cladistics) Wood and Collard (1999a, 1999b) maintain that certain fea- as developed by Willi Hennig. tures, such as the size of the masticatory apparatus, relative Hennig (1966) argued that all biological taxa be strictly brain size, ontogenetic pattern, body size and shape, and lo- monophyletic (what Mayr [2000] suggests should instead be comotor behavior all leave phenotypic traces observable in referred to as “holophyletic”); that is, taxa at all levels should hominin fossils. be made up of all the descendents of an ancestral taxon re- In circumscribing the genus Homo, then, Wood and Collard gardless of their plesiomorphic versus apomorphic (i.e., (1999a, 1999b) argued that two main criteria must be met: “grade”) status. Of course, the criterion of monophyly alone (1) that the genus Homo be monophyletic (holophyletic) and does not help one distinguish a monophyletic genus from a (2) that all its members share a common adaptive strategy or monophyletic tribe, subfamily, or family. Hennig (1966) zone. To test the first criterion, Wood and Collard (1999a, therefore suggested that time since divergence be the second 1999b) reported the results of multiple cladistic analyses, some major criterion for circumscribing genera, but he also argued of which failed to consistently link Homo habilis and Homo that rather than using a universal “one size fits all” time frame rudolfensis as sister taxa to Homo sapiens to the exclusion of (i.e., all genera everywhere should be 8–10 million years old), the australopiths. temporal criteria should be specific to each particular bio- For the second (i.e., the adaptive-zone) criterion, Wood logical group studied. While admittedly subjective, this would and Collard evaluated whether a presumed member species seem appropriate given vast differences in divergence times of the genus Homo was more similar to the type species of among long-recognized “good” zoological higher taxa. For the genus Homo (H. sapiens)orAustralopithecus (Australo- example, molecular data suggest that the two genera of Asiatic pithecus africanus) for the following adaptive complexes: (1) horseshoe crabs (Tachypleus and Carcinoscorpius) diverged body size, (2) body shape, (3) locomotion, (4) mastication, from their North American cousins (genus Limulus) ca. 45– (5) growth and development, and (6) relative brain size.1 They 60 mya (Avise, Nelson, and Sugita 1994), which may be earlier found that Homo ergaster, Homo erectus, Homo heidelbergensis, than the divergence of the Old World anthropoids (infraorder and Homo neanderthalensis were more similar to H. sapiens Catarrhini) from the New World monkeys (infraorder Pla- than A. africanus for all, or at least the vast majority, of these tyrrhini) and certainly millions of years earlier than diver- adaptive complexes (the clade including these five species will gence of the family Hominidae (apes and humans) from the Cercopithecidae (Old World monkeys). 1. Anto´n (2012) points out that comparing 2.0–1.5-million-year-old Thus, it is evident that neither the phylogenetic systematic fossil hominins to modern humans (Homo sapiens) in order to refer them description of genera nor the definition of genera employed to Homo (or not) is problematic in that it will tend to disregard similarities shared between Homo habilis/Homo rudolfensis and Homo ergaster/Homo by evolutionary taxonomists is without its flaws, but it should erectus, instead emphasizing differences between earliest Homo and the be possible to combine the strengths of both into a better most derived taxon in the clade (H. sapiens), a taxon that also happens means by which to define generic taxa. Applying this logic, to be far removed from early Homo in time. S332 Current Anthropology Volume 53, Supplement 6, December 2012 here be referred to as Homo [sensu stricto]). In contrast, problem with this line of evidence is that lower limb length according to their analyses, H. rudolfensis and H. habilis were shows positive allometry in humans (Auerbach and Sylvester decidedly more Australopithecus-like. Wood and Collard 2011; Holliday and Franciscus 2009; and see Pontzer 2012) therefore came to the conclusion that these two species failed such that the expectation is for small-bodied hominins such both the phylogenetic and the adaptive-zone criteria for in- as “Lucy,” including members of the genus Homo, to have clusion in the genus Homo and suggested that they instead shorter lower limbs (Franciscus and Holliday 1992; Holliday be referred to the genus Australopithecus. and Franciscus 2009; but see Haeusler and McHenry 2004). More recently, Collard and Wood (2007) redid their 1999 The discovery of diminutive late Pleistocene (but clearly genus analyses taking into account new fossil data as well as more Homo) fossils at the site of Liang Bua on Flores (referred to recently published cladistic analyses. As before, the cladistic the species Homo floresiensis; Brown et al. 2004), which are analyses remained somewhat inconsistent in clustering H. ha- characterized by relatively short lower limbs (Jungers et al. bilis and H. rudolfensis with later Homo to the exclusion of 2009), provides further support for this idea no matter what other taxa. Based on new data, they did find some changes those specimens’ ultimate taxonomic status within our genus in adaptive-zone patterning from their 1999 results (partic- (Holliday and Franciscus 2009). ularly with regard to the pattern of growth and development Likewise, there have been numerous recent discoveries and/ of H. ergaster; and see Schwartz 2012); however, their ultimate or reanalyses of larger-bodied members of the genus Aus- conclusion remained that neither H. habilis nor H. rudolfensis tralopithecus who (unlike “Lucy”) are characterized by rela- should be included in the Homo hypodigm (Collard and tively elongated lower limbs. These include the A. afarensis Wood 2007). specimens A.L. 333-3, A.L. 827-1 (Harmon 2005; Kimbel and This paper evaluates five reflections of body size and shape Delezene 2009), and KSD-VP-1/1 (Haile-Selassie et al. 2010) in early Homo (sensu lato) that figure into the adaptive-zone and the (presumed) Australopithecus africanus specimen StW half of the circumscription of the genus Homo. The features 99 (T. W. Holliday, unpublished data). The overall pattern of evaluated here allow the examination of three of the six adap- lower limb length relative to size in hominins is illustrated tive “complexes” as defined by Wood and Collard (1999a, by the scatterplot in figure 1, which shows femoral length 1999b): (1) body size, (2) body shape, and (3) locomotion. regressed on femoral head diameter. The former measurement The current analyses also include recently published data not reflects lower limb length, while the latter reflects overall body available to Wood and Collard (1999a, 1999b) or Collard and mass. Note that Homo sapiens is largely separated from Pan Wood (2007). This paper will attempt to assess whether (1) and Gorilla in bivariate space in that for any given femoral the emergence of the genus Homo is associated with an in- head size, our species is expected to have a much longer femur. crease in locomotor efficiency specifically as related to ter- With two exceptions, all of the fossil hominins fall within the restrial bipedality and its relationship to ranging behavior, 95% confidence limits about the H. sapiens individuals for and (2) H. habilis and H. rudolfensis should be removed from this relationship and fall outside the 95% confidence limits the genus Homo based on Wood and Collard’s adaptive-zone about Pan and Gorilla. The exceptions, notably, are the di- criteria for body size and shape and locomotion. The five minutive A.L. 288-1 (“Lucy”) and Liang Bua 1 (holotype of specific postcranial features to be examined are (1) relative H. floresiensis) specimens, which fall among the chimpanzees. lower limb length, (2) humero-femoral proportions, (3) rel- The slightly larger (but still diminutive by modern human ative forearm length, (4) relative pelvic breadth, and (5) body standards) A.L. 152-2 A. afarensis individual falls at the limits size as reflected in predicted body mass and a proxy for stat- of the H. sapiens sample and just beyond the 95% confidence ure. limits about the chimpanzee individuals. Note, however, that this individual falls almost directly on a modern human Relative Lower Limb Length “Pygmy” individual’s values for both measurements. In con- trast, the larger-bodied australopiths (A.L. 333-3, A.L. 827-1, Longer limbs are known to increase the efficiency of animal KSD-VP-1/1, and StW 99), while characterized by smaller locomotion by reducing the number of strides necessary to femoral heads than most members of the genus Homo (long cover any given distance (Jungers 1982; Pontzer 2007, 2012; known to be an australopith characteristic; Galik et al. 2004; Steudel-Numbers 2006; Steudel-Numbers and Tilkens 2004). Harmon 2009; Jungers 1988, 1991a; Kennedy 1983; Lovejoy, In this light, it has long been argued that Australopithecus had Heiple, and Burstein 1973; Napier 1964; Richmond and Jung- relatively short lower limbs while Homo (sensu stricto) was ers 2008; Robinson 1972; Ruff 1988; Walker 1973), nonethe- characterized by longer lower limbs (Bramble and Lieberman less fall among the H. sapiens sample for this relationship and 2004; Jungers 1982, 1991a; Jungers and Stern 1983; Pontzer beyond the confidence limits about the African ape samples, et al. 2010; Richmond, Aiello, and Wood 2002). However, as do the early Homo specimens KNM-ER 1472 and 1481, there are many recent data that challenge this assumption. KNM-WT 15000 (the “Nariokotome Boy”), and Dmanisi First, this view, while prevalent, has been largely based on the 4507. diminutive A.L. 288-1 Australopithecus afarensis (“Lucy”) A scaling difference in femoral head size between Homo specimen (Jungers 1982, 1991a; Jungers and Stern 1983). The and the australopiths has also been documented (Jungers Holliday Body Size and Shape in Early Homo S333

Figure 1. Scatterplot of femoral length regressed on femoral head diameter for Pleistocene/Holocene Homo sapiens, Pan, Gorilla, and Pliocene/Pleistocene early hominins (and Liang Bua 1). Australopiths are indicated by open squares, fossil Homo by filled squares. The ordinary least squares regression lines for the comparative samples are represented by solid lines with the 95% confidence limits for the individuals indicated about them. The reduced major axis (RMA) regression lines for the comparative samples are the dashed lines. Homo sapiens RMA formula:y p 8.074x ϩ 77.175 ; Pan RMA formula:y p 7.159x ϩ 56.2 ; Gorilla RMA formula: y p 6.439x ϩ 53.28.

1988; Ruff 1990). It is probable that this difference is in some lowed were years of intense debate as to whether the humero- way related to a shift in locomotor repertoire between Homo femoral proportions of “Lucy” were due to a long humerus, and the australopiths, but the exact nature of such a shift is a short femur, or a combination of both (Franciscus and uncertain, especially when one considers that there are ap- Holliday 1992; Jungers 1982, 1991a; Jungers and Stern 1983; parent differences in upper versus lower limb articular and Wolpoff 1983). It now seems probable that the last of these length proportions even within the genus Australopithecus (see alternative explanations best accounts for the data (Holliday below). Despite this caveat, the pattern of relative lower limb and Franciscus 2012). length revealed in figure 1 is mirrored in plots for which body It has also been argued that the humero-femoral propor- mass and not femoral head diameter is plotted along the X- tions of Australopithecus africanus and/or Homo habilis were axis (Franciscus and Holliday 1992; Holliday and Franciscus as different, or more different, from modern humans than 2009; Pontzer 2012; Pontzer et al. 2010). those of A. afarensis (Hartwig-Scherer and Martin 1991; Mc- Henry and Berger 1998a). Unfortunately, in the case of H. Humero-Femoral Proportions habilis, at least, this supposition is based on faulty data— The discovery of the A.L. 288-1 specimen, with its nearly specifically the femoral length of the OH 62 specimen, which intact humerus and femur, led to the confirmation that Aus- cannot be reliably reconstructed with any degree of confidence tralopithecus afarensis was characterized by very different (see below). Another presumed H. habilis partial skeleton, humero-femoral proportions than the genus Homo (or, for KNM-ER 3735, is even less complete (Haeusler and McHenry that matter, the genus Pan), with longer humeri relative to 2007). Similarly, there is a relative dearth of associated A. their femora than Homo and much shorter humeri relative africanus skeletons, and those that are available (e.g., Sts 14 to their femora than Pan (Johanson et al. 1982). What fol- and StW 431) lack complete limb bones. S334 Current Anthropology Volume 53, Supplement 6, December 2012

Patterning in humero-femoral proportions among African oral proportions lies with its femur. As noted by Reno et al. hominids (sensu lato) is shown in figure 2, which is a scat- (2005), it is likely that less than half of the femur’s length is terplot of humeral length regressed on femoral length. As has preserved, and among hominids (sensu lato) there is no pre- long been appreciated, gorillas have the longest humeri rel- dictable relationship between proximal femoral length and ative to their femora, followed by chimpanzees, while humans maximum (or bicondylar) femoral length. Because Johanson have the shortest humeri relative to the length of their femora et al. (1987) argued that the OH 62 shaft was smaller and (or the longest femora relative to their humeri). The first less robust than that of A.L. 288-1, some researchers (e.g., pattern evident in the graph is that the humero-femoral pro- Haeusler and McHenry 2004; Richmond, Aiello, and Wood portions of OH 62 are impossible to assess (as was argued 2002) have taken to using Lucy’s femoral length of 280 mm by Haeusler and McHenry 2004, 2007; Korey 1990; Reno et as the minimum length for the OH 62 femur, a convention al. 2005; Richmond, Aiello, and Wood 2002). The primary followed here. Haeusler and McHenry (2004) argue, however, problem in the assessment of OH 62’s humero-femoral pro- that the longer (albeit damaged; see Green, Gordon, and Rich- portions is unlikely to be its humerus; Haeusler and McHenry mond 2007) OH 34 femur is a better analog for the OH 62 (2004:446) point out that the OH 62 humerus is “relatively femur than is A.L. 288-1. They therefore used their estimated well preserved, lacking only the proximal and distal extrem- OH 34 femoral length of 374 mm as the maximum (potential) ities. Its length can be estimated with only minor error.” They femoral length for OH 62; the same is done here. This equates estimate humeral length of the specimen at 270 mm. Here with nearly 100 mm of difference between the minimum and an estimate of 264 mm from Johanson et al. (1987) is used maximum estimates of the OH 62 femoral length. Thus, even (these two estimates differ from each other by only 2%). in the absence of error in humeral length, we can say nothing Despite the fact that Korey (1990) argues there is a high about OH 62’s humero-femoral proportions because, as is degree of variability in humeral length estimation for OH 62, evident in figure 2, they could range from somewhat more the more intractable problem with assessing its humero-fem- chimpanzee-like than “Lucy” (as was maintained by Hartwig-

Figure 2. Scatterplot of humeral length regressed on femoral length for Pleistocene/Holocene Homo sapiens, Pan, Gorilla,and Pliocene/Pleistocene early hominins (and Liang Bua 1). Australopiths are indicated by open squares, fossil Homo by filled squares. The ordinary least squares regression lines for the comparative samples are represented by solid lines with the 95% confidence limits for the individuals indicated about them. The reduced major axis (RMA) regression lines for the comparative samples are the dashed lines. Homo sapiens RMA formula:y p 0.748x Ϫ 14.432 ; Pan RMA formula:y p 1.01x ϩ 4.15 ; Gorilla RMA formula: y p 1.092x ϩ 26.715. Holliday Body Size and Shape in Early Homo S335

Scherer and Martin 1991) to falling almost directly on the respectively) above the Homo sapiens mean. While falling Homo sapiens reduced major axis (RMA) and ordinary least within the anatomically modern human range, Dmanisi 4507 squares (OLS) regression lines. and KNM-WT 15000 still have high index values because they Note, too, that as was the case for the previous relationship, lie at the modern human 97th and 84th percentiles, respec- the only fossil hominins to fall squarely outside of the H. tively. In fact, a special case of Student’s t-test for comparing sapiens sample in figure 2 are the diminutive A.L. 288-1 and a single individual to a sample (Sokal and Rohlf 1981) finds LB1 specimens. The limb-segment lengths of the 2.5-million- that Dmanisi 4507 is statistically significantly different (at ! p p year-old taxonomically unassigned remains from Bouri P .05) from modern humans (ts 2.134 ,P .033 ), p p (BOU-VP-12/1) were estimated anatomically by Asfaw et al. whereas KNM-WT 15000 is not (ts 1.014 ,P .311 ). Given (1999) at 226–236 mm for the humerus and 335–348 mm that Dmanisi dates to ca. 1.77 mya (Gabunia, Vekua, and for the femur, which places them squarely among H. sapiens Lordkipanidze 2000) and KNM-WT 15000 dates to ca. 1.53 in bivariate space (although there is likely a problem with mya (Brown and McDougall 1993), if each is reflective of its these estimates; see below). The early Pleistocene Homo re- population, and assuming that these skeletons represent a mains from Dmanisi and KNM-WT 15000 also fall among lineage in the broadest sense, then it may be that humero- the more recent humans, although Dmanisi 4167/4507 falls femoral indices decreased through time in early Homo. on the 95% confidence limits about the recent human in- In light of the above patterning, the extremely low humero- dividuals. This graphic result is, however, somewhat different femoral index values (ranging from below the first to the 32nd from that depicted in figure 3b of Lordkipanidze et al. (2007), percentiles of H. sapiens) of the 2.5-million-year-old BOU- where Dmanisi 4167/4507 appears to fall in the middle of the VP-12/1 specimen appear particularly incongruous. This recent human scatter for the humerus length to femoral length could be due to the humerus and femur coming from different bivariate relationship. On closer inspection of Lordkipanidze individuals or (more likely) one or both of the estimated long- et al. (2007), however, it becomes evident that the 295-mm bone lengths being erroneously reconstructed. If the latter is maximum humeral length of Dmanisi 4507 is erroneously the case, the most probable scenario, given the preservation represented as ca. 275 mm in their figure 3b. of the remains shown in figure 4 of Asfaw et al. (1999), is A histogram of humero-femoral indices of the H. sapiens that the humeral length of the specimen has been underpre- sample is presented in figure 3 with the positions of the fossils dicted, because the femur preserves the diaphysis from the that preserve both a humerus and a femur indicated by ar- inferior margin of the neck to an area just proximal to the rows. As has been noted multiple times (e.g., Brown et al. lateral epicondyles, and therefore its length should be accu- 2004; Johanson et al. 1982; Jungers 1982; McHenry 1978), rately reconstructed. In contrast, while on the humerus a A.L. 288-1 and LB1 lie far (5.6 and 6.6 standard deviations, proximal portion of the medial epicondyle is preserved (giving

Figure 3. Histogram of humero-femoral indices, Pleistocene/Holocene Homo sapiens sample with the values (or in the case of BOU- VP-12/1, the range of potential values) of fossil hominins indicated by arrows. Homo sapiens mean p 71.5; SD p 2.3. S336 Current Anthropology Volume 53, Supplement 6, December 2012 one a solid idea of where the distal end of the bone should with each other. Ha¨usler (2001) believes the bony contact be), it is impossible to ascertain from the figure alone how between these two pieces to be good, and when they are much of the proximal diaphysis is present. joined, the ulnar length of 191 mm suggests to him a radius length of ca. 181 mm. However, Richmond, Aiello, and Wood (2002) published a “humanlike” radius length of 174 mm for Relative Forearm Length “Lucy” based on Schmid’s (1983) reconstruction (this value closely corresponds to the radius length [175 mm] estimated One of the key features long thought to distinguish the aus- from a 191-mm ulnar length for a sample of recent humans; tralopiths from the genus Homo is that the former are said T. W. Holliday, unpublished data). Kimbel, Johanson, and to have had longer (and therefore more “apelike”) forearms Rak (1994) generate a radius length of 206 mm for the spec- than the latter (Asfaw et al. 1999; Haeusler and McHenry imen, and Asfaw et al. (1999) generated a “chimpanzee-like” 2004; Howell and Wood 1974; Kimbel, Johanson, and Rak 1994; McHenry 1978; but see Drapeau and Ward 2007; Haeus- A.L. 288-1 radius length of 215 mm. Here I use this last ler and McHenry 2007). A scatterplot of radius length re- estimate as the specimen’s maximum length and 174 mm as gressed on femoral length is shown in figure 4. As expected, its minimum. As seen in figure 4, the result is a radius that for any given femoral length, humans have much shorter radii perhaps falls just outside the modern human sample’s 95% than the African apes. Note, too, that for this relationship, confidence limits but is almost certainly longer than would gorilla radii appear to lie along a continuation of the chim- be expected for a modern human of its diminutive size. Yet panzee trajectory, something that was not the case for the even the longest length estimate for the specimen does not humerus. fall near the Pan 95% confidence limits, a result consistent With regard to the fossils, the left ulna of A.L. 288-1 is with the findings of Haeusler and McHenry (2007) and preserved in two pieces that make only ambiguous contact Drapeau and Ward (2007), who found no evidence of chim-

Figure 4. Scatterplot of radius length regressed on femoral length for Pleistocene/Holocene Homo sapiens, Pan, Gorilla, and Pliocene/ Pleistocene early hominins (and Liang Bua 1). Australopiths are indicated by open squares, fossil Homo by filled squares. The ordinary least squares regression lines for the comparative samples are represented by solid lines with the 95% confidence limits for the individuals indicated about them. The reduced major axis (RMA) regression lines for the comparative samples are the dashed lines. Homo sapiens RMA formula:y p 0.623x–33.815 ; Pan RMA formula:y p 1.175x–70.195 ; Gorilla RMA formula: y p 0.93x ϩ 3.713. Holliday Body Size and Shape in Early Homo S337 panzee-like antebrachial elongation in Australopithecus afa- expected to have a wider bi-iliac breadth. Irrespective of their rensis. generic classification, the fossil hominins tend to fall into two As was done for A.L. 288-1, the radius length of LB1 was clusters: a small-bodied cluster and a large-bodied cluster. The estimated from its nearly complete right ulna at 190 mm three Australopithecus specimens for which bi-iliac breadth (Morwood et al. 2005), placing it near the middle of the can be reconstructed (A.L. 288-1 [Australopithecus afarensis], predicted range of A.L. 288-1 and well beyond the 95% con- Sts 14 [Australopithecus africanus], and MH2 [Australopithecus fidence limits for both Homo and Pan, albeit closer to the sediba]) fall among the wide-trunked chimpanzees in bivariate former than to the latter. The taxonomically unassigned BOU- space for this relationship, although Sts 14 and MH2 also fall VP-12/1 specimen falls beyond the range of both Pan and just within the 95% confidence limits about the H. sapiens Homo for this bivariate relationship, which might be expected, individuals. The recently described 1.0-million-year-old given its early date. However, recall that at least some of the BSN49/P27 pelvis from Ethiopia, referred to Homo by Simp- estimated limb-segment lengths for this specimen are suspect. son et al. (2008), has a wider pelvis than expected for even The radius length (255 mm, predicted from ulnar length by a Pan individual of its body size. The Gona pelvis lies closest Walker and Leakey [1993]) of KNM-WT 15000 falls just be- in bivariate space to the female Levantine Neanderthal spec- yond the 95% confidence limits about the Homo sapiens in- imen Tabun C1, the bi-iliac breadth of which was acquired dividuals while lying within the scatter of the H. sapiens sam- from the virtual reconstruction of that pelvis by Weaver and ple. The radio-femoral (RL/FL # 100) index for KNM-WT Hublin (2009). This specimen also falls well beyond the 95% 15000 (59.0) falls at the 98th percentile of the H. sapiens confidence limits of the H. sapiens individuals. sample (n p 1,060 ) and is statistically significantly different The larger-sized fossil hominins on the right side of the ! p p from that sample atP .05 (ts 2.000 ;P .0457 ). While plot include KNM-WT 15000, two middle Pleistocene hom- this result is based on a juvenile (who is potentially patho- inins (Jinnuishan and Atapuerca Pelvis 1), and two Nean- logical; Ohman et al. 2002), it does suggest that relative fore- derthals (La Chapelle-aux-Saints 1 and Kebara 2). The Na- arm length may have decreased over time in Homo. riokotome specimen falls at the margins of the H. sapiens sample, but its position in bivariate space is less reliable than the other fossils because of two factors. The first is that its Relative Pelvic Breadth acetabular height was estimated from femoral head diameter. The second is that its predicted adult bi-iliac breadth is es- Narrow pelves have long been known to be a human autap- timated by Ruff (2010), and there is considerable debate as omorphy. They have been hypothesized to be related to ob- to how much further growth would be expected for the spec- stetrical selection (Lovejoy 1988; Simpson et al. 2008), re- imen (Graves et al. 2010) and even as to how wide the Na- duced gut size (Aiello and Wheeler 1995), or thermal adap- riokotome pelvis was in its juvenile state (Ruff 1995, 2010; tation to hot climates (Weaver and Hublin 2009). This last Simpson et al. 2010). The two middle Pleistocene Homo spec- explanation seems unlikely in light of the discovery of the imens, Atapuerca Pelvis 1 and the Jinnuishan pelvis, have tropical yet wide Gona BSN49/P27 pelvis, which has been extremely wide bi-iliac breadths such that they fall well beyond attributed to Homo (Simpson et al. 2008; but see Ruff 2010). the 95% confidence limits about the H. sapiens individuals. It is, however, possible that a narrower pelvis in humans is The La Chapelle-aux-Saints 1 bi-iliac breadth used here related to increasing locomotor efficiency, given that a broad (292 mm) is taken from Trinkaus’s (2011) recent reconstruc- pelvis is less biomechanically stable and less efficient in bipedal tion. While Neanderthals are known for their wide bi-iliac locomotion (Bramble and Lieberman 2004; Langdon 2005; breadths (Churchill 1998; Holliday 1997; Ruff 2002; Steeg- Rosenberg and Trevathan 2007), and in light of the fact that mann, Cerny, and Holliday 2002), among the large Nean- more cursorial members of the Canidae, including dog breeds derthals included in the plot, La Chapelle-aux-Saints 1 falls such as greyhounds, tend to have narrower pelves than less within the H. sapiens’s scatter and in fact falls below the H. cursorial canids (Carrier, Chase, and Lark 2005; Schutz et al. sapiens RMA line. This indicates that La Chapelle has a re- 2009). This hypothesis enjoys little experimental support, markably narrow pelvis for nonmodern Homo. This is in part however, because in laboratory settings pelvic breadth is not due to the specimen’s remarkably narrow sacrum (falling at associated with locomotor efficiency in humans (Pontzer the 15th percentile of the H. sapiens [n p 726 ] sample). The 2012) and given the fact that effective limb length alone ex- specimen also lacks the marked iliac flare seen in Kebara 2. plains 98% of the variance in locomotor efficiency across a In contrast, Kebara 2, with a bi-iliac breadth of 313 mm, falls wide range of terrestrial animals (Pontzer 2007). just beyond the 95% confidence limits of the H. sapiens sam- A scatterplot of bi-iliac (pelvic) breadth regressed on ace- ple. tabular height is presented in figure 5. The former is a measure of body breadth while the latter is a pelvic reflection of body Body Size (Mass and Stature) mass. Note that Homo sapiens and Pan troglodytes have nearly parallel regression lines, with the chimpanzees differing from It has long been posited that body size increased with the modern humans in that for any given acetabular size they are emergence of the genus Homo. Body size is an important S338 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 5. Scatterplot of bi-iliac breadth regressed on acetabular height for Pleistocene/Holocene Homo sapiens, Pan, and Pliocene/ Pleistocene early hominins. Australopiths are indicated by open squares, fossil Homo by filled squares. The ordinary least squares regression lines for the comparative samples are represented by solid lines with the 95% confidence limits for the individuals indicated about them. The reduced major axis (RMA) regression lines for the comparative samples are the dashed lines. Homo sapiens RMA formula:y p 4.833x ϩ 3.279 ; Pan RMA formula:y p 5.429x ϩ 33.197 . variable because of its behavioral, biological, and ecological tion; see Hens, Konigsberg, and Jungers 2000; Jungers 1982; correlates (Calder 1984; Damuth and MacFadden 1990; Jung- Martin, Genoud, and Hemelrijk 2005; Smith 2009) from Mc- ers 1985; Millien and Bovy 2010; Schmidt-Nielsen 1984). Henry (1992) is used here to predict body mass from femoral Across taxa, body mass is generally considered to be the most head diameter. appropriate measure of an animal’s overall size (Darveau et From this, the mean body mass of Australopithecus afarensis al. 2002; Garcia and da Silva 2006; West, Brown, and Enquist is estimated at ca. 41 kg, while those of Australopithecus af- 1997), but predicting body mass from skeletons involves the ricanus, Australopithecus (P.) robustus,andAustralopithecus introduction of a level of error that some find problematic (P.) boisei are slightly smaller, at ca. 37.3, 37.0, and 38.5 kg, (Smith 1996). It has been shown that among primates, limb respectively. In contrast, early (ca. 1.8–1.5 mya) Homo is articular dimensions, especially articular breadths, are among found to be considerably (ca. ϩ33%) heavier, at ca. 54.5 kg. the best predictors of body mass (Jungers 1990; McHenry This is close to the mean of the recent low-latitude human 1992; Ruff 2003; Ruff, Walker, and Teaford 1989). In esti- sample (55.1 kg) although less heavy than that of recent high- mating body mass for A.L. 288-1 using an all-hominoid re- latitude humans (59.9 kg) and considerably lighter than Homo gression, Jungers (1990) found that femoral head diameter neanderthalensis (ca. 73.6 kg) or late Pleistocene Homo sapiens showed the lowest standard error (SE) of the estimate and (64.1 kg). These and other differences are best visualized in lowest percentage predicted error of six lower limb articular the box plots in figure 6. There is a clear dichotomy in es- measurements, and importantly, McHenry (1992) found that timated body mass between the members of the genera Aus- human regression formulas likely outperformed cross hom- tralopithecus and Paranthropus (on the left side of the graph) inoid predictive formulas in estimating fossil hominin body and Homo on the right, a result similar to that obtained by mass. For this reason, a recent human least squares regression Pontzer (2012). Note, however, that while the earliest undis- formula (arguably the most appropriate formula for predic- puted members of the genus Homo (at least those that pre- Holliday Body Size and Shape in Early Homo S339

Figure 6. Box plots of estimated body mass for fossil hominin and recent human samples. serve a femoral head) are larger than almost all of the indi- for the small A.L. 288-1 specimen, based on the all-hominoid vidual australopiths, overall size in early Homo remains versus human regressions, are both 27.9 kg according to Mc- smaller than that of Holocene or late Pleistocene H. sapiens Henry (1992). Likewise, Jungers (1990) arrives at a similar with the exception of modern-day “Pygmoid” groups, who estimate of 29.6 kg (only 6% higher) using a nonhuman- themselves show a reduction in body size likely due to selec- hominoid formula. In contrast, McHenry’s (1992) least tion related to climate, diet, high mortality rates, and/or island squares femoral head estimate of body mass for the larger biogeography (Bailey 1991; Cavalli-Sforza 1986; Hiernaux and A.L. 333-3 specimen is 50 kg (based on a human formula), Froment 1976; Kuzawa and Bragg 2012; Lomolino 2005; Mig- and 37% higher, at 68.6 kg, for an all-hominoid formula. liano and Guillon 2012; Migliano, Vinicius, and Mirazo´n Lahr Worse still, the nonhuman-hominoid least squares formula 2007). reported in Jungers (1991b) produces an estimated body mass Because of the importance of body mass in biology, there of 81.9 kg for the specimen, 64% higher than McHenry’s is a rich literature on the estimation of body mass in fossil (1992) human estimate. The body mass estimates reported hominins (Hartwig-Scherer 1993; Jungers 1990; Kappelman here must therefore be approached with caution. Despite this 1996; McHenry 1992; Ruff 1990; Ruff, Trinkaus, and Holliday caveat, other researchers, using different means of body mass 1997). As mentioned before, some (e.g., Smith 1996) feel that estimation, have found a similar dichotomy in body mass because of the introduction of prediction error, body mass between australopiths and Homo erectus (Kappelman 1996; in fossils should not be estimated but rather comparable mea- McHenry 1988; and see Pontzer 2012). surements that are known to be highly correlated with body For recent humans, in addition to body mass, stature (or mass should be compared (although this alternative method standing height) is also frequently used as a proxy for body is not without its own problems; see Smith 1980). It should size (Auerbach and Sylvester 2011; Malina et al. 2004; Ruff therefore be noted that while body mass estimation formulas 2007; Zakrewski 2003). The problem with stature as a mea- based on femoral head size show low SEs of the estimate, surement is that with skeletal data it is always estimated with they are subject to error and interpretation. error. Given potential differences in limb : trunk proportions One potential problem with body mass estimation from between living humans and at least some australopiths (Fel- femoral head size lies in the apparent difference in relative desman, Kleckner, and Lundy 1990; Franciscus and Holliday femoral head size between Australopithecus (smaller femoral 1992; Jungers and Stern 1983; but see Wolpoff 1983), and heads) and Homo (larger femoral heads). Given this differ- given the fact that cranial height for most fossil hominins is ence, should body mass in Australopithecus be estimated from shorter than that of modern humans (Graves et al. 2010; Ruff the femoral head using a nonhuman-hominoid formula or and Walker 1993), it is probably better to avoid estimating rather a human and/or an all-hominoid one? In the smaller- stature in fossil hominins and instead analyze one of its major body size range, this question is largely academic, but it be- constituents. In this study, femoral length is used as a proxy comes problematic for larger-sized australopiths. For exam- for stature. While an imperfect reflection of stature, it is the ple, two estimates of body mass from femoral head diameter longest limb bone making up a portion of stature, and among S340 Current Anthropology Volume 53, Supplement 6, December 2012 the long bones, it tends to show the lowest SE of the estimate A.L. 288-1 or LB1) appear to be primarily a function of their in stature prediction (Trotter 1970). diminutive body size (Franciscus and Holliday 1992; Holliday The distribution of femoral lengths of fossil and recent and Franciscus 2009; Pontzer 2012). Likewise, while the hominins is shown in the box plot presented in figure 7. As humero-femoral indices of early Homo are not as elevated as was the case with body mass, there is a dichotomy between those observed in Australopithecus afarensis (or likely those Australopithecus on the one hand (here represented solely by of Australopithecus africanus; see McHenry and Berger 1998a, the species A. afarensis) and Homo on the other. All of the 1998b), it is evident that at least some specimens referred to undisputed early Homo specimens fall well within the size early Homo (e.g., Dmanisi 4167/4507) have longer humeri range of recent humans, and most have femora that are longer relative to their femora than do later members of the genus. than those of modern-day “Pygmoid” peoples (the early This suggests that contra Asfaw et al. (1999), modern hu- Homo mean and median lie just below a single large “Pyg- manlike humero-femoral indices were likely not characteristic moid” outlier). In contrast, two of the five A. afarensis spec- of hominins 2.5 mya but rather the low index values calculated imens fall well below the modern human range of variation, for the taxonomically unassigned BOU-VP-12/1 specimen are and for the three who fall within the modern human range the result of erroneous reconstruction of at least one of the of variation, none falls outside the “Pygmoid” range of var- specimen’s limb bone lengths (most likely its humerus). iation. It is more difficult to evaluate relative forearm length in Homo given a dearth of individuals who preserve antebrachial elements. In general the genus Australopithecus, including the Summary late species Australopithecus sediba (Berger et al. 2010), ap- With regard to the emergence of our genus, the postcranial pears to have had relatively longer forearms than modern morphology of early Homo appears to have been mosaic in humans. At the same time, however, these forearms were nature. Of the features examined here, the most significant considerably shorter than those of Pan. While one must re- difference between Australopithecus and early Homo is an in- main mindful that KNM-WT 15000 is a juvenile, its predicted crease in body size as reflected in both body mass and stature radius length relative to the length of its femur falls near the (importantly, this finding excludes OH 62, the femoral length upper margins of the combined late Pleistocene/Holocene of which remains unknown). In contrast, differences in limb Homo sapiens sample, which may suggest that early members proportions and body shape between the two genera are more of the genus Homo, including Homo ergaster/Homo erectus, nuanced. For example, the differences in lower limb length were characterized by longer forearms than later members of relative to overall size between Australopithecus and early the genus. Homo are not as great as was once thought but rather the In terms of relative pelvic breadth, early Homo is similar relatively short femora of some specimens of both genera (e.g., to Australopithecus in that it is characterized by wide bi-iliac

Figure 7. Box plots of femoral length for fossil hominin and recent human samples. Holliday Body Size and Shape in Early Homo S341 breadths. This plesiomorphic character is also observed in indicative of a shift toward consistent early access to carcasses middle Pleistocene Homo and Homo neanderthalensis,sug- by hominins (Cachel and Harris 1998). gesting that the relatively narrow bi-iliac breadth seen in peo- Despite the important adaptive implications surrounding ple today is an autapomorphy of H. sapiens. increased ranging activity in early Homo, aside from a few What emerges from these analyses, then, is that the origin anatomical features of the foot (DeSilva et al. 2012; Pontzer of the genus Homo is not a marked postcranial shift from an et al. 2010; Zipfel et al. 2011), pelvis (Berger et al. 2010; Kibii australopith-like morphological pattern to an H. sapiens–like et al. 2011), and some features related to head carriage (Bram- one, but as has been noted by others (e.g., Berger et al. 2010; ble and Lieberman 2004), there is little evidence of a major Kivell et al. 2011; Lordkipanidze et al. 2007; Pontzer 2012; locomotor shift between Australopithecus and Homo. Instead Pontzer et al. 2010), it is more complex. For example, lower it appears that Homo augmented an existing australopith pat- limb length appears to be as long in Australopithecus as it is tern almost exclusively via an increase in body size (and see in early Homo once one corrects for differences in body size. Pontzer 2012). This brings up the fact that one long-recognized difference Following these observations, at least from a postcranial between the australopiths and Homo that remains borne out adaptive-zone perspective, there are insufficient data to war- by the current analyses is that Homo tends to be much larger rant the removal of Homo habilis and Homo rudolfensis from in body size than Australopithecus or Paranthropus. This pat- the genus Homo as recommended by Wood and Collard (Col- tern holds despite recent work (Graves et al. 2010; Ohman lard and Wood 2007; Wood and Collard 1999a,1999b). Of et al. 2002) finding that the original projection of the adult the cranial remains assigned to these two species, only two stature of KNM-WT 15000 (Ruff and Walker 1993) was far (OH 62 and KNM-ER 3735) have associated postcrania, and too tall, or the revelation that many of the 1.77-million-year- in both cases, the postcranial remains are extremely frag- old Homo specimens from Dmanisi were of relatively dimin- mentary and therefore relatively uninformative (Haeusler and utive size (Lordkipanidze et al. 2007), or even the discovery McHenry 2007). In this light, if any of the long (but isolated) of relatively long-legged australopiths such as KSD-VP-1/1 femora dating to ca. 1.8 mya in Africa is referred to either of (Haile-Selassie et al. 2010). It is a robust pattern: while on these species, then we have probably underestimated both average smaller than many people today, early Homo was body size and lower limb length in these two taxa. Addition- significantly larger than the australopiths in both body mass ally, because H. ergaster/H. erectus may have retained a some- and stature. And because among mammals, home-range size what elongated upper limb and an equally broad pelvis, it is to a great extent a function of body size (Eisenberg 1990; appears that many of the perceived proportional differences Harestad and Bunnell 1979; Kelt and Van Vuren 2001; McNab between H. habilis and/or H. rudolfensis on the one hand and 1963; Vieira and Cunha 2008), it is almost certain that Homo specimens assigned to H. ergaster or H. erectus on the other ranged more widely than Australopithecus, a notion under- are diminished.2 scored by the presence of Homo (and apparent lack of Aus- As for the monophyletic nature of the genus Homo, while tralopithecus or Paranthropus) outside of Africa. some recent cladistic analyses (e.g., Cameron and Groves Increased ranging in early Homo is most likely tied to an 2004) fail to cluster H. habilis and H. rudolfensis with H. increase in carnivory (Aiello and Key 2002; Martin 1981; sapiens to the exclusion of any australopith taxon, it is im- McHenry 1994; O’Connell, Hawkes, and Blurton Jones 1999). portant to note that Cameron and Groves’s (2004) result is First, mammalian carnivores need larger home ranges than entirely due to the inclusion of Kenyanthropus platyops in the comparably sized herbivores or omnivores (Gittleman and analyses, a paleospecies whose taxonomic validity has been Harvey 1982; Harestad and Bunnell 1979; Lindstedt, Miller, questioned (White 2003). Simply removing this species from and Buskirk 1986) and tend to exploit much greater day Cameron and Groves’s (2004) analysis makes Homo (sensu ranges than noncarnivores as well (Carbone et al. 2005). Sec- lato) a monophylum. More importantly, the most rigorous ond, larger bodies (and bigger brains; Aiello and Wheeler cladistic analyses of fossil hominins done to date, including 1995) would likely only be made possible via an increase in some analyses that include K. platyops (Strait and Grine 2004) nutritional quality of the diet, and animal muscle and fat are show Homo (sensu lato) to be a monophylum. In any case, very high-caloric food sources known to have been exploited the close phylogenetic relationship of Homo and the austral- by early Homo. Evidence in favor of increased carnivory in opiths (it seems unlikely that they split much before 2.5 mya) early Homo include the 1.7-million-year-old partial H. erg- probably lent itself to some (albeit low) level of interbreeding aster/H. erectus skeleton KNM-ER 1808, argued by Walker, between these taxa, which in turn could produce confusing Zimmerman, and Leakey (1982) to show pathological bone patterns of synapomorphy (Holliday 2003, 2006; Jolly 2001). suggestive of hypervitaminosis A, which can be caused via In conclusion, then, while the emergence of Homo (sensu ingestion of carnivore livers. Likewise, from an archaeological 2. There are also numerous craniodental characters that support the perspective, the Acheulean Industry, which is now known to inclusion of Homo habilis and Homo rudolfensis in the genus Homo date as early as 1.76 mya (Lepre et al. 2011), is temporally (Anto´n 2012; Bromage, Schrenk, and Zonneveld 1995; Kimbel, Johanson, correlated with zooarchaeological evidence from multiple sites and Rak 1997; Rightmire and Lordkipanidze 2009). S342 Current Anthropology Volume 53, Supplement 6, December 2012 lato) is an important chapter in human evolution—one likely Cachel, Susan, and John W. K. Harris. 1998. The lifeways of Homo erectus inferred from archaeology and evolutionary ecology: a perspective from involving increased ranging, carnivory, and encephalization— East Africa. In Early human behaviour in global context: the rise and diversity it is also the case that we now have the resolution in the fossil of the lower Palaeolithic record. Michael D. Petraglia and Ravi Korisettar, record to actually capture the gradual mosaic nature of that eds. Pp. 108–132. New York: Routledge. Calder, William A. 1984. Size, function and life history. Cambridge, MA: Har- emergence. The long-standing idea of the origin of Homo vard University Press. (sensu stricto) as a punctuated event involving the geologically Cameron, David W., and Colin P. Groves. 2004. Bones, stones and molecules: rapid emergence of hominins who (at least from the neck “Out of Africa” and human origins. Amsterdam: Elsevier. Carbone, Chris, Guy Cowlishaw, Nick J. B. Isaac, and J. Marcus Rowcliffe. down) were H. sapiens–like seems less applicable now than 2005. How far do animals go? determinants of day range in mammals. it did a decade ago. American Naturalist 165:290–297. Carrier, David R., Kevin Chase, and Karl G. Lark. 2005. Genetics of canid skeletal variation: size and shape of the pelvis. Genome Research 15:1825– 1830. Acknowledgments Cavalli-Sforza, Luigi L. 1986. African Pygmies. New York: Academic Press. Churchill, Steven E. 1998. Cold adaptation, heterochrony, and the Neandertals. I would like to thank Leslie Aiello and Susan Anto´n for in- Evolutionary Anthropology 7:46–61. Collard, Mark, and Bernard Wood. 2007. Defining the genus Homo.InHand- viting me to participate in the Wenner-Gren symposium, and book of paleoanthropology, vol. 3 of Phylogeny of hominids. Winfried Henke to them and all the other participants, my thanks for making and Ian Tattersall, eds. Pp. 1575–1611. Berlin: Springer. the symposium such a phenomenal and unforgettable expe- Damuth, John, and Bruce J. MacFadden, eds. 1990. Body size in mammalian paleobiology: estimation and biological implications. Cambridge: Cambridge rience. Thanks also to Tim Weaver for supplying a bi-iliac University Press. breadth estimate for Tabun C1 and to Erik Trinkaus for insight Darveau, Charles-A., Raul K. Suarez, Russel D. Andrews, and Peter W. 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Ecological Energetics in Early Homo

by Herman Pontzer

CAϩ Online-Only Material: Supplement A

Models for the origin of the genus Homo propose that increased quality of diet led to changes in ranging ecology and selection for greater locomotor economy, speed, and endurance. Here, I examine the fossil evidence for postcranial change in early Homo and draw on comparative data from living mammals to assess whether increased diet quality has led to selection for improved locomotor performance in other lineages. Body mass estimates indicate early Homo, both males and females, were approximately 33% larger than australopiths, consistent with archeological evidence indicating an ecological change with the origins of our genus. However, many of the postcranial features thought to be derived in Homo, including longer hind limbs, are present in Australopithecus, challenging the hypothesis that early Homo is marked by significant change in walking and running performance. Analysis of energy budgets across mammals suggests that the larger body mass and increased diet quality in early Homo may reflect an increase in the hominin energy budget. Expanding the energy budget would enable greater investment in reproduction without decreasing energy available for larger brains or increased activity. Food sharing and increased adiposity, which decrease variance in food energy availability, may have been integral to this metabolic strategy.

Introduction data from living mammals and the fossil evidence of post- cranial anatomy and locomotor performance in Plio-Pleis- In describing the first specimens of Homo habilis 5 decades tocene hominins. ago, Leakey, Tobias, and Napier (1964) argued for two distinct Researchers have long focused on foraging behavior in re- grades within the hominin lineage. Australopithecus species of constructing hominin ecology and evolution (Bramble and south and east Africa—with their large molars and ape-size Lieberman 2004; Dart 1949, 1957; Darwin 1871; Hawkes et brains—were viewed as more primitive in their cognitive abil- al. 1998; Lee and Devore 1968; Lovejoy 1981). Unlike the ities and behavior, while H. habilis—with its larger brain, other great apes, which travel modest distances each day in smaller molars, and dexterous hands capable of making the search of plant foods and must fend for themselves, human earliest stone tools—marked the beginnings of modern hu- foragers range widely, hunt regularly, and share religiously man ability and behavior (Leakey, Tobias, and Napier 1964). (Marlowe 2005). Early models of hominin evolution proposed While Leakey, Tobias, and Napier (1964:9) viewed Australo- that these defining aspects of modern human foraging be- pithecus and Homo as “two branches of Hominidae evolving havior arose early in the hominin lineage. Darwin (1871:40) side by side,” subsequent work has suggested that the origin offered that our species’ “preeminent success in the battle of of our genus marks an ecological shift in foraging behavior life” was in large part due to our progenitors’ bipedal posture, and diet from an earlier australopith strategy that persisted which freed their hands and allowed them “to defend them- throughout much of the Pliocene (Aiello and Wheeler 1995; selves with stones or clubs, to attack prey, or otherwise obtain Bramble and Lieberman 2004; Conroy and Pontzer 2012; food.” Dart’s (1949, 1957) osteodontokeratic interpretations Leonard and Robertson 1997; O’Connell, Hawkes, and of Australopithecus behavior followed, with the Man the Hun- Blurton Jones 1999; Shipman and Walker 1989). In this re- ter paradigm emerging in the 1960s (Lee and Devore 1968). view, I briefly outline current ecological models for the evo- As late as the 1980s, models of early hominin evolution lution of the genus Homo and examine whether the proposed suggested that Australopithecus, then the oldest hominin genus changes in foraging behavior are consistent with comparative known, engaged in hunting and food sharing (Carrier 1984; Lovejoy 1981). However, over the past 3 decades, analyses of australopith dental and postcranial anatomy have typically Herman Pontzer is Assistant Professor in the Department of Anthropology, Hunter College (728 North Building, 695 Park portrayed them as semiarboreal and vegetarian (Conroy and Avenue, New York, New York 10065, U.S.A. [herman.pontzer@ Pontzer 2012). Analyses of australopith locomotor anatomy, hunter.cuny.edu]). This paper was submitted 12 XII 11, accepted 15 based largely on the A.L. 288 Australopithecus afarensis skel- VI 12, and electronically published 3 X 12. eton (e.g., Stern and Susman 1983; see Ward 2002), have

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0007$10.00. DOI: 10.1086/667402 Pontzer Ecological Energetics in Early Homo S347 suggested that they were too arboreal and too inefficient on life spans and increased body size (O’Connell, Hawkes, and the ground—in essence, too apelike—to be plausible hunter- Blurton Jones 1999). In a variant of this model, the adoption gatherers (but see Latimer 1991). Instead, recent models of of cooking plays a key role by unlocking otherwise indigestible hominin evolution have proposed that the roots of modern carbohydrates in USOs and alters the social dynamics of early human foraging ecology lie in the origin of the genus Homo, Homo by creating a home base where males and females would recalling the distinction made by Leakey and colleagues nearly cook and share food (Wrangham 2009; Wrangham et al. 50 years ago (Aiello and Wheeler 1995; Bramble and Lieber- 1999). man 2004; Leakey, Tobias, and Napier 1964; O’Connell, Several studies have modeled the energetic consequences Hawkes, and Blurton Jones 1999; Shipman and Walker 1989). of improved diet quality and larger body size of Pleistocene Homo (Aiello and Key 2002; Aiello and Wheeler 1995; Leon- Ecological Models for the Origin of Homo ard and Robertson 1997; Steudel-Numbers 2006). Perhaps the most influential has been the expensive tissue hypothesis Because of the inclusion of meat, underground storage organs of Aiello and Wheeler (1995), which proposes that the ad- (USOs), and cooking, the diet quality (i.e., kcal/g of food; see dition of readily digestible and energy-rich meat into the diet Leonard and Robertson 1997) of modern human foragers is of early Homo decreased their required gut size, freeing met- greater than that of living apes, and most ecological models abolic energy to fuel a larger brain. Other studies have focused for the origin of Homo suggest that a shift toward modern primarily on differences in daily energy expenditure (DEE; human diet quality was instrumental in shaping the evolution kcal/day) between Australopithecus and Homo, suggesting that of our genus (Aiello and Wheeler 1995; Bramble and Lie- the larger body size in H. erectus and an increase in ranging berman 2004; Leonard and Robertson 1997; O’Connell, activity associated with a higher-quality diet would have sub- Hawkes, and Blurton Jones 1999; Shipman and Walker 1989). stantially increased daily energy requirements for Pleistocene However, current models differ in which aspects of modern Homo (Aiello and Key 2002; Leonard and Robertson 1997; human foraging behavior they view as seminal. Steudel-Numbers 2006). This increase in DEE is generally Many ecological models for the evolution of the genus viewed as increasing the challenge of meeting food require- Homo emphasize the adoption of hunting and scavenging ments in Pleistocene Homo, although one analysis by Steudel- (Aiello and Wheeler 1995; Bramble and Lieberman 2004; Numbers (2006) has suggested that this increase in DEE Shipman and Walker 1989). In these hunting and scavenging would be partially offset by an improvement in locomotor models, meat and marrow provided valuable energetic and economy due to increased hind-limb length in Homo. nutritional rewards for early Homo while simultaneously cre- ating selection pressure for locomotor and cognitive adap- tations to pursue prey or monopolize fresh carcasses. These Testing Ecological Models for the models often envision the pursuit of prey and carcasses oc- Origin of Homo curring under the midday sun of equatorial Africa, producing additional selection pressure for effective thermoregulation The models briefly outlined above each provide a compelling (Bramble and Lieberman 2004; Ruff and Walker 1993; Walker reconstruction of the origin and evolution of our genus. De- 1993). Proponents of these hunting and scavenging models spite their differences, these models share a common logical view the tall, long-limbed proportions of Homo erectus (epit- framework and set of assumptions that can be tested using omized by the KNM-WT 15000 skeleton) as evidence for comparative data from living mammals as well as evidence improved running and thermoregulatory ability and the in- from the hominin fossil record. Recent work in the hominin crease in brain size and reduction in tooth size as evidence fossil record, locomotor energetics, ranging ecology, and the for the inclusion of energy-rich meat/marrow into the diet evolution of mammalian metabolic strategies provide the op- (Aiello and Wheeler 1995; Bramble and Lieberman 2004; portunity to reexamine these ecological models with new data. Shipman and Walker 1989). In discussing the transition from Australopithecus to Homo, Others have suggested that hunting and scavenging were it is necessary to address the taxonomic placement of the of negligible importance in the evolution of our genus and oldest taxon in the genus Homo, Homo habilis.Woodand have instead focused on the gathering of USOs, food sharing, Collard (1999) have suggested that the primitive morphology and cooking (O’Connell, Hawkes, and Blurton Jones 1999; of H. habilis more accurately places it within Australopithecus. O’Connell et al. 2002; Wrangham et al. 1999). In these USO Similarly, many of the ecological models discussed above view models for the origin of Homo, climatic changes leading to Homo erectus as the earliest species to exhibit the morpho- increased aridity in the early Pliocene led to an increased logical and behavioral traits they view as critical and definitive reliance on USOs, which are rich in calories and nutrients of the genus. The ecological reconstruction and taxonomic and available even in dry seasons (O’Connell, Hawkes, and placement of H. habilis affect the timing but not the nature Blurton Jones 1999). The difficulty in locating and harvesting of the proposed transition from Australopithecus to Homo; these underground foods led to selection favoring the pro- instead, the assessment of H. habilis affects whether it is visioning of children, which in turn resulted in longer female viewed as a latest exemplar of the Australopithecus grade or S348 Current Anthropology Volume 53, Supplement 6, December 2012 the earliest exemplar of the Homo grade. This timing is dis- aptations for walking long distances to gather plant foods cussed below. (Isbell et al. 1998; O’Connell, Hawkes, and Blurton Jones For the purposes of this analysis, I use a simplified taxo- 1999). nomic scheme that combines specimens assigned to H. habilis 4. Evolutionary increases in diet quality result in increased and Homo rudolfensis into a single taxon, Homo habilis sensu ranging activity. Ecological reconstructions of Plio-Pleistocene lato, and similarly places specimens previously assigned to hominins suggest an increase in ranging activity as a conse- Homo ergaster into H. erectus. Given the difficulty in assigning quence of changing foraging behavior in Homo (Anto´n, Leon- postcranial elements to species and the grade-level focus of ard, and Robertson 2002; Leonard and Robertson 1997; Steu- these analyses, further distinction seems unwarranted. Fur- del-Numbers 2006). In hunting and scavenging models, the ther, I focus only on gracile Australopithecus taxa (Australo- pursuit of prey or fresh carcasses requires increased running pithecus afarensis, Australopithecus africanus, Australopithecus speed (Shipman and Walker 1989) or endurance (Bramble garhi, and Australopithecus sediba) because the postcranial evidence for robust forms is poor and because current hy- and Lieberman 2004). The USO models do not explicitly link potheses (both phylogenetic and ecological) view robust the change in diet quality to an increase in ranging but suggest forms as an evolutionary side branch rather than ancestral to that increased ranging would be a consequence of the drier Homo (Conroy and Pontzer 2012). climate and decreased food availability (O’Connell, Hawkes, Ecological models of past evolutionary events are inherently and Blurton Jones 1999). complex. In order to organize and facilitate discussion, I have 5. Evolutionary increases in ranging activity lead to corre- outlined five broad points on which current ecological models sponding increases in locomotor performance (speed, economy, for the origin of Homo rest. Some points are more vital to endurance) in mammals. Ecological models for the evolution some models than to others, but all draw on these five points of our genus view changes in foraging behavior (point 4) as to some degree. Points 1–3 concern the evolution of hominin resulting in a new set of selection pressures on locomotor postcranial anatomy and the biomechanical effects of these performance (point 2). Hunting and scavenging models are changes on locomotor performance. Points 4–5 concern pro- typically very explicit in outlining the aspects of performance posed links between ecological change and evolutionary pres- most affected. In discussing the evolutionary consequences of sures on locomotor performance. I use this broad distinction a transition to hunting and scavenging, Shipman and Walker to organize the analyses and discussion below. (1989) emphasized the importance of running speed. More 1. The postcranial anatomy of early Homo (at least by early recently, Bramble and Lieberman (2004) argued that the crit- Homo erectus) shows significant departures from the postcranial anatomy of earlier hominins. All of the ecological models out- ical aspect of performance for early Homo was running en- lined above draw on fossil analyses indicating that the post- durance, the ability to run at a moderate speed for long pe- cranial anatomy of early Homo differs from that of Austral- riods in order to exhaust prey or outpace other scavengers to opithecus. Derived aspects of modern human postcranial distant carcasses. The USO models for the evolution of Homo anatomy thought to be evident in early Homo include larger suggest increased ranging would lead to improved economy body size (especially females), longer hind limbs, shorter fore- and endurance as well, although these models typically em- limbs, a narrow pelvis, shorter phalanges, and a stiff springlike phasize walking performance (Isbell et al. 1998; O’Connell, plantar arch. A long list of derived postcranial changes in Hawkes, and Blurton Jones 1999). early Homo was given by Bramble and Lieberman (2004), who viewed these traits as critical for long-distance running. As mentioned above, the earliest evidence for larger female Postcranial Change in Homo (Points 1–3) body size and some derived postcranial morphology is often noted in early Homo erectus rather than Homo habilis. Ecological models for the evolution of our genus draw on 2. Postcranial changes evident in early Homo are products postcranial differences between Homo and Australopithecus. of natural selection, not neutral processes such as drift.The Dozens of morphological features have been cited by previous ecological models discussed above view the ecological tran- studies as distinguishing the locomotor anatomy of austral- sition from Australopithecus to Homo as a selection event. The opiths from modern humans (see Bramble and Lieberman behavioral and morphological traits adopted by early Homo 2004; Stern 2000; Ward 2002). Here, I focus primarily on are viewed as a response to changing climatic conditions and morphological features that have been shown through ex- the transition to a new foraging regime. 3. The derived postcranial characters evident in early Homo perimental testing to significantly affect locomotor perfor- improve locomotor performance (speed, economy, endurance). mance. The discussion below is organized by the demon- Hunting and scavenging models typically emphasize the im- strated contribution of each trait to locomotor performance portance of derived postcranial traits in early Homo for run- or foraging ecology beginning with traits known to have the ning performance (Bramble and Lieberman 2004; Shipman greatest effect. The evolutionary forces shaping these changes and Walker 1989). Others have suggested these traits are ad- (point 2) are briefly discussed afterward. Pontzer Ecological Energetics in Early Homo S349

Body Size The USO models for the evolution of Homo draw on the evidence for increasing body size—particularly female body size—reported for Homo erectus (McHenry 1994). Increased female body size is taken as evidence for delayed female life history schedules (i.e., later age at maturity and longer life span) associated with the advent of provisioning by postre- productive females (O’Connell, Hawkes, and Blurton Jones 1999). The cooking hypothesis also views increased female body size as evidence for increased diet quality and a changing social landscape that favored a decrease in sexual dimorphism (Wrangham et al. 1999). Figure 1 shows estimated body masses for Plio-Pleistocene hominins. Body mass estimates were taken from the literature or calculated from reported femoral head diameters (or, for the MH-1 Australopithecus sediba tibia, from the tibiotalar surface dimensions) using the intra-Homo least squares re- Figure 1. Estimated body mass for fossil hominins: Australopi- gression in McHenry (1992). Data and sources are shown in thecus (triangles), Homo (filled circles), and modern humans and Neanderthals (open circles; from Ruff, Trinkaus, and Holliday table 1 and in the extended version of this table (table A1 in 1997; see table 1). Recent finds are labeled KSD-VP-1/1 Aus- ϩ CA online supplement A). tralopithecus afarensis specimen (K), Australopithecus sediba (S), As reported previously (McHenry 1992, 1994), there is three Dmanisi specimens (D), and the Gona pelvis (N). Estimated good evidence for an increase in body mass from Australo- ages for individual australopith specimens have been adjusted pithecus to Homo. Mean body mass for the pooled sample of slightly to improve symbol clarity. n p 15 ) was 32%, 11.3 ע Homo specimens (48.8 kg,SD n p 24 ). Body Limb Length, 7.4 ע greater than in Australopithecus (36.8 masses for specimens identified as male in the Homo sample Increased relative hind-limb length in Homo has been cited p ע (56.4 7. 8 ,n 9 ) were 34% larger than those in Australo- as evidence for increased cursoriality, improving both walking p ע pithecus (42.2 4.9 ,n 13 ), and masses for purported fe- and (especially) running performance in our genus (Bramble p ע males in the Homo sample (40.7 9.3 ,n 7 ) were 32% and Lieberman 2004; Isbell et al. 1998; Jungers 1982; Ruff p ע larger than those of Australopithecus (,).30.5 3.7 n 11 and Walker 1993). Indeed, limb length is one of four primary Given the inherent error in estimating mass and the small determinants of locomotor cost (kcal/m) in terrestrial ani- samples available, further parsing into individual species is mals, the others being body mass, the effective mechanical statistically unpalatable. Indeed, sample sizes become so min- advantage (EMA) of the limb joints, and the fascicle lengths iscule that the confidence intervals for mean male and mean of limb muscles (Pontzer, Raichlen, and Sockol 2009). The female body mass overlap (see McHenry 1994). Recent finds, metabolic cost of walking and running derives from the vol- while consistent with the general conclusion of increasing ume of muscle activated in each step to support body weight; body size in Homo, advise caution in estimating the degree consequently, larger animals spend more energy to walk and of dimorphism in Homo habilis or early H. erectus. Small run (Kram and Taylor 1990; see Pontzer, Raichlen, and Sockol specimens from Gona and Dmanisi indicate that the range 2009). Limb length, EMA, and muscle length largely deter- of body mass in early Pleistocene Homo may not have been mine the volume of muscle activated to support each gram substantially less than that of Australopithecus (fig. 1; see also of body mass. Animals with longer limbs, greater EMA (i.e., Anto´n 2012; Anto´n and Snodgrass 2012). more straight-legged postures), and shorter muscle fascicles As discussed in USO models for the origin of Homo, adult use less energy per gram of body mass to walk and run body size is correlated with life history schedules (Charnov (Pontzer 2007; Pontzer, Raichlen, and Sockol 2009; Roberts, and Berrigan 1993; O’Connell, Hawkes, and Blurton Jones Chen, and Taylor 1998). The effects of limb length and EMA 1999), and sexual dimorphism is correlated with mating and are evident within our own species. Humans with longer hind reproductive strategies in primates (Plavcan 2012; Wrangham limbs use less energy to walk and run (DeJaeger, Willems, et al. 1999). The DEE (kcal/day) also increases with body size and Heglund 2001; Steudel-Numbers and Tilkens 2004; Steu- (Leonard and Robertson 1997; Nagy, Girard, and Brown 1999; del-Numbers, Weaver, and Wall-Scheffler 2007), and our use see also Anto´n and Snodgrass 2012). Body mass also has a of more flexed hind limbs while running decreases the EMA direct effect on locomotor cost, discussed below, but notably of our knee and hip joints such that the energy cost (kcal/ has no apparent effect on running speed. Maximum running m) of running is greater than the cost of walking (Biewener speed in mammals is independent of body mass for species et al. 2004; Pontzer, Raichlen, and Sockol 2009). Notably, the greater than 10 kg (Garland 1983b). number of limbs used in locomotion (e.g., whether a species S350 Current Anthropology Volume 53, Supplement 6, December 2012

Table 1. Estimated body masses and femur and tibia lengths for Plio-Pleistocene hominins

Species and specimen Mass (kg) Sex Femur (mm) Tibia (mm) Source Ardipithecus ramidus: ARA-VP-6/500 51.0a F . . . 262.0 Lovejoy et al. 2009 Australopithecus anamensis: KNM KP 29285 51.0a M ...... Leakeyetal.1995 Australopithecus afarensis: KSD-VP-1/1 45.4 M . . . 355.0 Haile-Selassie et al. 2010 AL 827-1 45.6 M 368–382 . . . T. Holliday, personal communication AL 333-3 50.1 M 373–391 . . . McHenry 1992; T. Holliday, personal communication AL 333-4 41.3 M ...... McHenry 1992 AL 333-7 42.6 M ...... McHenry 1992 AL 333-w-56 40.2 M ...... McHenry 1992 AL 333x-26 48.2 M ...... McHenry 1992 AL 129a 27.1 F ...... McHenry 1992 AL 333-6 33.5 F ...... McHenry 1992 AL 288-1 28.0 F 281.0 241.0 McHenry 1992; Pontzer et al. 2010b Australopithecus africanus: Sts 34 38.4 M ...... McHenry 1992 Stw 99 45.4 M 433.5 . . . McHenry 1992; T. Holliday, personal communication Stw 311 40.7 M ...... McHenry 1992 Stw 389 37.9 M ...... McHenry 1992 Stw 443 41.3 M ...... McHenry 1992 Sts 14, 34 30.3 F 276.0 . . . Steudel-Numbers and Tilkens 2004 Stw 392 32.7 F ...... McHenry 1992 TM 1513 32.5 F ...... McHenry 1992 Stw 25 34.2 F ...... McHenry 1992 Stw 102 30.5 F ...... McHenry 1992 Stw 347 27.5 F ...... McHenry 1992 Stw 358 23.3 F ...... McHenry 1992 Australopithecus sediba: MH 1 31.5 M . . . 262–269 T. Holliday, personal communication MH 2 35.7 F ...... Berger et al. 2010 Australopithecus garhi: BOU-VP-12/1 30–43a . . . 335.0 . . . Steudel-Numbers and Tilkens 2004 Homo habilis: KNM ER 3228 63.5 M ...... Ruff, Trinkaus, and Holliday 1997 KNM ER 1472 49.6 M 401.0 . . . Steudel-Numbers and Tilkens 2004 KNM ER 1481 57.0 M 396.0 . . . Steudel-Numbers and Tilkens 2004 OH-35 31.8 F ...... McHenry 1992 OH-8 31.0 F ...... McHenry 1992 OH-62 33.0a . . . 315.0 . . . McHenry 1991, 1992 Homo erectus: KNM WT 15000 51.0 M 429.0 380.0 Pontzer et al. 2010b Dmanisi large adult 48.8 M 382.0 306.0 Pontzer et al. 2010b KNM ER 736 68.3 M ...... Ruff, Trinkaus, and Holliday 1997 KNM ER 1808 63.4 M 485.0 . . . Ruff, Trinkaus, and Holliday 1997 Dmanisi subadult 49.4b M ...... Pontzer et al. 2010b BSN49/P27 39.7 F ...... Simpson et al. 2008 Dmanisi small adult 40.2 F ...... Pontzer et al. 2010b OH 34 51.0 F 432.0 . . . Steudel-Numbers and Tilkens 2004 OH 28 54.0 F 456.0 . . . Steudel-Numbers and Tilkens 2004 a Not included in body mass comparisons of Australopithecus and Homo. b Estimated adult mass. is bipedal or quadrupedal) has no effect on locomotor cost of surface area to body mass (see Tilkens et al. 2007 and (Pontzer 2007; Pontzer, Raichlen, and Sockol 2009; Sockol, references therein). Small increases in core body temperature Raichlen, and Pontzer 2007; Taylor, Heglund, and Maloiy can have catastrophic effects on the brain and other organs, 1982). making adaptations for heat dissipation critical in hot envi- Longer limbs—both forelimb and hind limb—are also ronments (Schmidt-Nielsen 1999). Overheating also curtails known to improve an individual’s ability to dissipate heat and ranging activity, as animals must stop walking and running thermoregulate in hot environments by increasing the ratio if the heat produced from muscle activity threatens to raise Pontzer Ecological Energetics in Early Homo S351

(range 0.81–0.89 , 0.02 ע the body temperature. Thus, in addition to improving lo- index for the Pygmy sample (0.85 comotor economy, longer hind limbs in early Homo would was similar to the “black” sample (P p 0.83 , t-test). likely improve endurance by preventing overheating (Bramble Fossil dimensions were taken from the literature (except and Lieberman 2004; Ruff and Walker 1993). A.L. 333-3, A.L. 827-1, StW 99, and MH-1, which were gen- In assessing the evidence for increased hind-limb length in erously provided by T. Holliday). Data and sources are given Homo, one must account for its correlation with body mass. in table 1. Where only tibia or femur lengths are known (the Figure 2 shows estimated hind-limb lengths (femur ϩ tibia) case for most early hominins including early Homo), hind- plotted against estimated body mass for Plio-Pleistocene hom- limb length was estimated using a crural index (tibia/femur inins. A sample of modern humans (n p 110 , including mea- length) 0.85. This value (0.85) is equal to the mean crural , 0.03 ע surements ofn p 24 Pygmy skeletons generously provided index for fossil Homo sapiens in the sample (0.85 by W. Jungers), chimpanzees (n p 60 ), and gorillas (n p n p 12) and near the means for the modern H. sapiens sample n p 110 ) and combined Pan and Gorilla sample, 0.03 ע is shown for comparison (data from Pontzer et al. 2010a). (0.84 (22 n p 82 ). To account for potential variation in, 0.02 ע The non-Pygmy human sample is from the Hamman-Todd (0.84 25ע collection at the Cleveland Museum of Natural History and crural index among early hominins, an error range of consists of adults who died in the Cleveland area in the 1900s. mm was plotted with the estimated hind-limb length, equiv- While detailed genealogical data are not available for the alent to a range of crural indexes from 0.80 to 0.90 for these Hamman-Todd sample, 60% (n p 52 ) of the individuals in fossils; this range is equivalent to that of the “black” and this data set are identified as “black,” while 40% (n p 34 ) are Pygmy samples, which is appropriate because the specimens identified as “white.” Individuals identified as “black” had a for which femur or tibia length was estimated are all African table 1). For incomplete specimens, when a maximum and) ( 0.03 ע greater crural index (tibia/femur length: mean0.85 suggesting the “black” minimum estimated length were available, the error range ,( 0.03 ע than “white” individuals (0.82 and “white” populations represent more equatorial (presum- plotted in figure 2 was further expanded to reflect this range ably African) and more northerly (presumably European) of uncertainty. populations, respectively. However, while the difference in Figure 2 includes the Ardipithecus ramidus skeleton (ARA- mean crural index was significant (P ! 0.001 , t-test) it was VP-6/500; Lovejoy et al. 2009), the recent Australopithecus relatively small, and the ranges for these populations (“black”: afarensis skeleton from Ethiopia (KSD-VP-1/1; Haile-Selassie 0.79–0.91, “white”: 0.76–0.90) largely overlap. Mean crural et al. 2010), Australopithecus garhi (BOU-VP-12/1; Asfaw et

SDs of residuals 2ע Figure 2. Estimated hind-limb length versus estimated body mass for fossil hominins. Shaded areas indicate mm estimated 25ע from the human and African ape ordinary least squares regression trend lines. Error ranges (gray) represent estimated body mass; see text for details. A color version of this figure is available in the online edition 5%ע hind-limb length and of Current Anthropology. S352 Current Anthropology Volume 53, Supplement 6, December 2012 al. 1999), A. sediba (MH-1; Berger et al. 2010), and the larger Plantar Arch and Achilles Tendon adult H. erectus specimen from Dmanisi (Lordkipanidze et During running, the limbs of terrestrial animals act like al. 2007). The range of body mass estimates for the A. garhi springs. With each step the ligaments, tendons, and muscles specimen (30–43 kg) was based on the male and female means store energy as the limb flexes under body weight and then for Australopithecus (see above). As with hind-limb length release this strain energy to help propel the body into the of estimated body mass was plotted 5%ע estimates, a range of next step (Biewener et al. 2004). In modern humans, much for early hominin specimens in figure 2 to reflect some degree of this springlike work is performed by the plantar arch and of uncertainty in mass. the Achilles tendon (Alexander 1991). Together, the plantar Recent finds strongly challenge previous reconstructions of arch and Achilles tendon convert over 50% of the energy Australopithecus as having short hind limbs. Previous assess- stored as strain into kinetic energy, reducing the amount of ments of australopith hind-limb length focused on A.L. 288 muscular work and metabolic energy needed to power our and Sts 14, the only Australopithecus specimens for which stride (Alexander 1991). A rigid midfoot also appears to im- reliable estimates of limb length and body mass were obtain- prove walking economy by increasing the efficiency with able (Jungers 1982; McHenry 1991, 1992; Pontzer et al. 2010a; which the foot pushes off the ground at toe off: when the Steudel-Numbers 2006). These specimens have shorter hind rigidity of the foot is effectively compromised by walking over limbs than expected for a human of similar mass (fig. 2; see a soft surface, the energy cost of walking increases (Lejeune, Jungers 1982). However, hind-limb lengths for these speci- Willems, and Heglund 1998). Bramble and Lieberman (2004) mens are ambiguous because the range of limb lengths seen have argued that a springlike Achilles tendon and plantar arch in modern humans overlaps considerably with that of African evolved early in the genus Homo as adaptations for endurance apes at body sizes below 30 kg (fig. 2). Inclusion of new running. specimens suggests hind-limb length in Australopithecus is in The evolutionary history of these traits is difficult to assess. fact similar to modern humans. Hind-limb lengths for the The presence of an elongated, humanlike Achilles tendon can- large-bodied A. afarensis specimen (KSD-VP-1/1), A. sediba, not be discerned from fossil remains using current techniques. and A. garhi all fall within modern human range, with KSD- However, it is notable that gibbons have an elongate Achilles VP-1/1 clearly distinguished from the African apes (fig. 2). tendon (Payne et al. 2006), indicating that its presence need These results are robust to error in hind-limb length and body not coincide with habitual endurance running. The plantar mass estimation; australopith hind-limb lengths relative to arch is more amenable to measurement in the fossil record, body mass remain in the modern human range even when although associated foot bones are rare. Previous analyses of hind-limb length and body mass estimates are varied sub- A. afarensis and A. africanus foot morphology have suggested stantially (fig. 2). that these species lacked the derived tarsal morphology, par- Hind-limb length within the genus Homo warrants dis- ticularly of the navicular and cuboid, associated with the cussion. Contrary to reconstructions of H. habilis as having springlike modern human plantar arch, and some have even short hind limbs, specimens of H. habilis—including OH argued that these species retained an opposable hallux (Har- 62—fall clearly within the range of modern humans. The court-Smith and Aiello 2004). However, more recent work hind-limb proportions (relative to body mass) of H. habilis has provided evidence that australopiths may have had a plan- combined with evidence for a springlike plantar arch in this tar arch. The hominin footprints at Laetoli, usually attributed species (see Harcourt-Smith and Aiello 2004; and below) sug- to A. afarensis, suggest a foot that is functionally similar in gest the bipedal capabilities of H. habilis would have been many ways to that of modern humans, with a stiff midfoot, similar to those of H. erectus. Late Pleistocene hominins ex- adducted hallux, and at least some arching (Tuttle, Webb, and hibit a substantial degree of variation in relative hind-limb Baksh 1991). Ward, Kimbel, and Johanson (2011) have re- length (fig. 2). Several Neanderthal specimens, including all cently described a fourth metatarsal from Hadar, attributed of the European specimens and two Middle Eastern speci- to A. afarensis, that has a humanlike degree of torsion that mens, are more than 2 SDs below the range for modern along with its proximal articular morphology suggests the human hind-limb length. While their relatively short tibiae presence of an arch. Evidence of an arch appears less ambig- contribute to a shorter hind limb, it is their total hind-limb uous in early Homo. Specimens of H. habilis (OH-8) and H. length, not their crural index, that places Neanderthals outside erectus (Dmanisi) show strong evidence for the presence of a the modern human range: the range of crural indexes among plantar arch in these taxa (Harcourt-Smith and Aiello 2004; the Neanderthal sample (0.76–0.81) falls within the observed Pontzer, Raichlen, and Sockol 2009). Thus, while it remains range in the modern human sample, but their relative hind- plausible that the springlike plantar arch typical of modern limb lengths do not. As discussed by Weaver and Steudel- humans arose with the genus Homo, recent morphological Numbers (2005), the short hind limbs of Neanderthals may evidence as well as mechanical analyses of the Laetoli trackway have increased their daily foraging costs. suggest this morphology may extend back to Australopithecus. Pontzer Ecological Energetics in Early Homo S353

Stabilization and Stress Reduction straight-legged walking gait similar to modern humans (Pontzer, Raichlen, and Sockol 2009; Raichlen et al. 2010; Numerous changes in the size and morphology of the limb Sockol, Raichlen, and Pontzer 2007; Wang et al. 2004). Thus, joints and inferred changes in the size of the muscles that with the possible exception of the plantar arch, the locomotor stabilize the trunk have been argued to reflect an increase in anatomy of Australopithecus,atleastasitpertainstowalking terrestrial locomotion, particularly running, in Homo (see and running performance, appears to have been functionally Bramble and Lieberman 2004; Stern 2000; Ward 2002). For equivalent to that of early Homo. example, Bramble and Lieberman (2004) have suggested that Perhaps the clearest signal for postcranial change in early the larger hind-limb joints and inferred increases in the size Homo is an increase in body mass of roughly 33% compared of the erector spinae and gluteus maximus muscles in early with australopiths (fig. 1). However, while an increase in body Homo serve to improve trunk stability and reduce mechanical mass may signal an ecological change (see below), experi- stress on the joints during long-distance running. While these mental and comparative evidence suggest increased size would traits may in fact distinguish Australopithecus from Homo, not have improved walking and running performance. Larger their effects on locomotor performance are difficult to assess; animals use more energy to walk and run (Taylor, Heglund, none have been tested experimentally. Further, in light of the and Maloiy 1982), and the proportion of DEE spent on travel evidence for larger body size in early Homo (fig. 1), it is also tends to increase with body size (Garland 1983a). As possible that some of these changes are allometric effects of noted above, maximum running speed among mammals is increased mass. independent of body mass above 10 kg (Garland 1983b), al- Bramble and Lieberman (2004) suggest that these traits though it should be noted that among modern human ath- improve endurance, implicitly defined as the ability to run at letes, sprinters are generally taller and heavier than distance a moderate to high speed for a long period of time (up to 1 runners (Weyand and Davis 2005). Indeed, larger body size hour or more), by improving stability of the trunk and re- in early Homo, absent an increase in relative hind-limb length, ducing mechanical stress and fatigue in the hind-limb joints. may be particularly difficult to reconcile with endurance run- However, the only morphological traits known to affect run- ning models. Among modern human athletes, endurance run- ning endurance across mammals are the mass and mito- ning appears to favor shorter, lighter individuals, while sprint- chondrial density of the limb muscles (Weibel et al. 2004); ers are heavier and taller (Weyand and Davis 2005). Further, the capacity of the liver and limb muscles to store glycogen because larger body size tends to reduce the ratio of surface may also constrain endurance ability (see Rapoport 2010). area to body mass (Ruff 1994), increased body size in early Hind-limb muscle mass is greater in modern humans than Homo would likely diminish its ability to shed heat, contra in living apes (Payne et al. 2006), as expected given our bipedal behavioral reconstructions suggesting intense activity in the posture, but it is unclear whether australopiths, which were heat of the day. similarly dependent on their hind limbs for weight support, Evidence for increased body mass does provide some sup- had similar hind-limb muscle mass. Current techniques are port for hypotheses suggesting a change in ecology in early not capable of assessing mitochondrial density in extinct hom- Homo, but this support is tempered by three observations inins. More work is needed to assess hind-limb muscle prop- from the fossil and comparative record. First, with the inclu- erties in Plio-Pleistocene hominins and to determine the effect sion of newer specimens of early Homo (fig. 1), there is no of other implicated anatomical variables on locomotor per- evidence that female size increases more than male size, which formance. indicates that an emphasis on increasing female size in Homo may be unwarranted. Second, while larger species tend to Interpreting Postcranial Anatomy in Early Homo have slower life histories (Charnov and Berrigan 1993), there is a considerable degree of variation in this relationship, and The evidence outlined above challenges the hypothesis that analyses of hominin tooth formation suggest that growth rates walking and running performance improved substantially and thus life history schedules in early Pleistocene Homo were with the origin of the genus Homo. The similarity in hind- similar to those of Australopithecus (Dean and Smith 2009; limb length between Australopithecus and Homo suggests that Dean et al. 2001), though perhaps somewhat slower in H. the derived longer hind limb typical of modern humans was erectus (see Schwartz 2012). Third, while larger species tend already present in australopiths nearly 4 million years ago. to have larger energy budgets, there is also a considerable Similarly, while australopith foot anatomy remains a subject degree of variation in this relationship. Measurements of DEE of debate, there is evidence of a rigid, possibly springlike, across a broad range of taxa indicate a sixfold range of var- plantar arch in both the skeletal anatomy of the A. afarensis iation in DEE even after accounting for the effects of body foot (Ward, Kimbel, and Johanson 2011) and the Laetoli mass and phylogeny (Nagy, Girard, and Brown 1999). This trackway (Tuttle, Webb, and Baksh 1991). Analyses of the last point is discussed below. Australopithecus pelvis and the footprints at Laetoli as well as These analyses have omitted discussion of forelimb length computer simulations of australopith gait have previously in- in Australopithecus and Homo because arm length has no dicated that Australopithecus most likely used a relatively known effect on walking or running performance (other than S354 Current Anthropology Volume 53, Supplement 6, December 2012 its effect on body mass). However, it may be that the primary (Bramble and Lieberman 2004; Leonard and Robertson 1997; change in limb length with the genus Homo is shorter arms O’Connell, Hawkes, and Blurton Jones 1999; Shipman and rather than longer legs (Holliday 2012). Analyses of the in- Walker 1989; Wrangham et al. 1999). In these models, par- termembral index of Australopithecus suggest substantially ticularly those emphasizing hunting and scavenging, higher- longer arms than in Homo, although whether this is a prim- quality diet in early Homo provided the benefit of increased itive retention or an adaptation to climbing remains a matter energy availability but required a substantial increase in rang- of debate (Ward 2002). Homo habilis has also been argued to ing activity. The USO models generally frame this increase in have long arms, based primarily on the OH 62 specimen, ranging activity as an increase in the daily distance traveled although this reconstruction is debated (Haeusler and Mc- (O’Connell, Hawkes, and Blurton Jones 1999; see also Isbell Henry 2004). Thus, rather than an increase in walking and et al. 1998), while hunting and scavenging models emphasize running performance, the origin of Homo, or perhaps H. not only increased travel distance but also the need to travel erectus, may mark a decrease in arboreal ability. This scenario is consistent with shorter, straighter phalanges evident in quickly to run down prey or monopolize carcasses (Bramble Homo (Aiello and Dean 1990); with the pattern of limb ro- and Lieberman 2004; Shipman and Walker 1989). Increased busticity in African H. erectus (but not OH-62; Ruff 2009); ranging activity is in turn thought to increase DEE and to and perhaps with the larger body size evident in early Homo, impose a new set of selection pressures on hominin locomotor but it warrants further scrutiny of the hominin forelimb. Here performance (Bramble and Lieberman 2004; Leonard and again the small body size of A.L. 288, the primary specimen Robertson 1997; Steudel-Numbers 2006). used to calculate australopith intermembral index, may con- Comparative studies of living mammals suggest that in- flate the difference in proportions with a difference in size. creased diet quality leads to increased daily travel distance. Analysis of the large-bodied KSD-VP-1/1 specimen suggests Carbone et al. (2005), in a phylogenetically controlled mul- that forelimb and hind-limb proportions of A. afarensis may tivariate analysis of daily travel distance in 200 mammal spe- be more similar to modern humans than previously thought cies, showed that daily travel distance increases significantly (Haile-Selassie et al. 2010). with diet quality. While variation in ranging distance is con- Given the evidence for postcranial change, or lack thereof, siderable, faunivores travel farther, on average, than similarly in the origin of Homo, it is important to address whether sized frugivores, which in turn travel farther than herbivores reported changes in locomotor anatomy may reflect neutral (Carbone et al. 2005); on average, carnivores travel four times evolutionary processes rather than selection (point 2). Recent farther each day than similarly sized herbivores (Garland comparisons of the human and Neanderthal cranium provide 1983b). An analysis by Anto´n and colleagues showed that an important reminder that differences in hominin skeletal anatomy often thought to reflect natural selection may in fact home range size among primates increases with both body reflect neutral processes (Weaver 2009). With this in mind, mass and diet quality (Anto´n, Leonard, and Robertson 2002). it is notable that the majority of postcranial traits distinguish- Applying results from extant primates to fossil hominins, they ing Australopithecus from Homo have not been tested with estimated that home ranges for Homo erectus would have been regard to their effect on locomotor performance. Traits with 10 times larger than those of Australopithecus (Anto´n, Leon- known effects on walking and running performance, namely ard, and Robertson 2002). hind-limb length, appear to have remained stable over the Yet increased travel distance does not appear to result in past 4 million years of hominin evolution, perhaps changing improved locomotor economy, speed, or endurance. Com- in the transition from Ardipithecus to Australopithecus (fig. parative studies of locomotor cost indicate that the economy 2). Similarly, the reorganization of the hominin pelvis for of carnivores is no different than that of artiodactyls or other bipedalism, a likely product of natural selection (Grabowski, herbivores (Taylor, Heglund, and Maloiy 1982). Further, limb Polk, and Roseman 2011), appears to predate the genus Aus- length in “cursorial” species is no different than that of other tralopithecus and the transition to Homo. Thus, it is difficult mammals and is unrelated to daily travel distance (Harris and to reject the hypothesis that the hominin postcranial skeleton Steudel 1997; Steudel and Beattie 1993). Similarly, maximum has largely been under stabilizing selection since the middle running speed does not differ between carnivores and ar- Pliocene, with neutral evolutionary forces leading to small tiodactyls, even among predator-prey pairs (Garland 1983a; changes in joint morphology over time. The strongest can- Shipman and Walker 1989). Maximum aerobic power, a re- didate for postcranial change under natural selection in the evolution of Homo may be body mass (fig. 1). liable measure of endurance, has not been investigated to determine whether it correlates with diet quality or ranging ecology in mammals, but several herbivores, including An- Foraging Ecology and the Evolution of tilocapra and Equus, have relatively high maximum aerobic Locomotor Performance (Points 4 and 5) power for their body size (Weibel et al. 2004), suggesting that As discussed above, current ecological models for the evo- diet quality and aerobic performance are not strongly posi- lution of the genus Homo envision an increase in diet quality tively correlated. Pontzer Ecological Energetics in Early Homo S355

Limitations of Current Ecological Models doubt on the applicability of this approach to hominin evo- lution. Despite having the largest, most metabolically expen- The lack of correspondence between ranging activity and lo- sive brains and longest daily travel distances of any primate comotor performance, particularly locomotor economy, runs species, human foragers outpace all other hominoids in terms counter to the expectations of most ecological models for the of reproductive output and maximum life span (Hawkes et evolution of Homo. However, these ecological models rest on al. 1998; Isler and van Schaik 2012). two critical assumptions that are not well supported by the Recent work on mammalian metabolic strategies offers an available comparative evidence. The first is that selection for alternative to zero-sum game approaches. Nagy, Girard, and improved locomotor economy is a relatively strong force Brown (1999), in reviewing measurements of DEE in wild shaping locomotor anatomy, particularly in cursorial species. populations of 79 mammal species, noted that there is a six- In fact, analysis of foraging efficiencies among modern mam- fold range of variation in DEE among species even after con- mals suggests that selection pressure for improved locomotor trolling for body mass and phylogeny. This variation in DEE economy is probably quite low relative to other selection pres- appears to reflect evolved strategies for energy throughput sures in most species because they already obtain a high rate (McNab 1986; Pontzer and Kamilar 2009; Sibly and Brown of energy return while foraging (Pontzer 2012). In an analysis 2007). In habitats where food is abundant, species may adopt of foraging return rates for 228 mammal species, the median high-throughput (i.e., high DEE) strategies that increase food estimated foraging efficiency was56:1 , or 56 calories of food requirements but also provide more energy for reproduction. energy obtained for every 1 calorie spent on locomotion Alternatively, in habitats where food availability is highly var- (Pontzer 2012). With such high foraging efficiencies, even iable or where foraging increases the risk of predation, species large reductions in locomotor cost have relatively small effects may evolve a low-throughput strategy that reduces the energy on net energy intake (i.e., gross energy intake minus travel requirements even at the cost of lower reproductive output. cost). For an organism obtaining a foraging efficiency of In a test of this hypothesis, Pontzer and Kamilar (2009) con- 40:1, a 20% reduction in locomotor cost, requiring sub- ducted a phylogenetically controlled multivariate study of stantial anatomical change, would improve net energy intake daily travel distance and reproductive output in a sample of by only 0.5% (Pontzer 2012). Even when foraging efficiency 110 mammal species. While there was considerable variation is halved, to20:1 , a 20% reduction in locomotor cost would among species, daily travel distance was found to be positively yield only a 1% gain in net intake (Pontzer 2012). Thus, given associated with lifetime reproductive output among mam- the myriad selection pressures acting on the hominin post- mals, suggesting that species that travel farther generally do cranial skeleton, it is likely that selection for improved econ- so as part of a high-throughput strategy of increased DEE omy remained relatively weak throughout the Plio-Pleistocene and reproductive investment (Pontzer and Kamilar 2009). regardless of any changes in foraging ecology. Rather than a zero-sum game framework in which DEE is A second problematic assumption of many ecological mod- relatively constant, these results suggest that species’ metabolic els is that they generally view DEE in hominins and other strategies are labile over evolutionary time, with DEE shrink- lineages in a “zero-sum game” framework in which any in- ing or expanding in response to environmental pressures. crease in the energy spent on one activity must be matched by a corresponding decrease in the energy spent on another (e.g., Aiello and Wheeler 1995; Charnov and Berrigan 1993; Ecological Implications of Increasing Diet Quality and DEE Isler and van Schaik 2009). Zero-sum frameworks have had A dynamic view of mammalian metabolic strategies focusing success in explaining large-scale trends in life history (e.g., on throughput rather than efficiency and trade-offs changes Charnov and Berrigan 1993) and brain size among primates the way one interprets the evidence for increased diet quality and other animals (Fish and Lockwood 2003; Isler and van and ranging activity in Homo. Rather than presenting an eco- Schaik 2006, 2009), although some studies have found little logical or energetic cost, increased travel distance and body evidence for energetic trade-offs (Barrickman and Lin 2010; mass in early Homo may reflect an improved ability to procure Bordes, Morand, and Krasnov 2011; Jones and MacLarnon food energy and a subsequent expansion of the energy budget. 2004). In the context of foraging ecology, zero-sum game Indeed, comparisons with the limited data available for ape models predict that longer daily travel distances increase the DEE suggests humans may have evolved larger energy budgets portion of the daily energy budget spent on travel, which at some point in our lineage (Pontzer et al. 2010b), and as detracts from the energy spent on other activities and in turn discussed above, modeling studies suggest this may have oc- leads to selection to improve locomotor economy and restore curred with Homo (Aiello and Key 2002; Leonard and Rob- energy expenditure to those activities. ertson 1997; Steudel-Numbers 2006). Expansion of the daily While this logic is compelling, it is not supported by data energy budget would make more energy available for brain on locomotor cost or anatomy; as noted above, daily travel growth, reproduction, and other investments without nec- distance is not correlated with locomotor efficiency among essarily resulting in increased selection for locomotor per- mammals. In fact, humans themselves do not appear to fit formance. the predictions of a zero-sum game framework, casting some Greater DEE in early Homo would suggest an increase in S356 Current Anthropology Volume 53, Supplement 6, December 2012 food availability either through an increase in abundance or which decrease variance in food availability. A cooperative a decrease in variability (McNab 1986; Pontzer and Kamilar foraging strategy would have pervasive effects on the social 2009; Sibly and Brown 2007). Given the evidence for im- and nutritional ecology of early Homo (O’Connell, Hawkes, proved diet quality, particularly the inclusion of meat, an and Blurton Jones 1999; Wrangham et al. 1999). Food sharing increase in abundance is unlikely because higher-quality foods could also mitigate the ecological risk of seeking high-value, are generally less abundant (Carbone et al. 2005), requiring high-risk foods such as meat, and indeed the earliest con- larger home ranges (Anto´n, Leonard, and Robertson 2002). firmed evidence of butchery is associated with Homo habilis. Instead, the combination of increased DEE and higher diet Future efforts to reconstruct the evolution of our genus quality suggests that early Homo evolved strategies for de- should seek to examine evidence for food sharing in the early creasing variance in food intake. Decreased variability might Pleistocene. be achieved in a number of ways, but one intriguing possibility is the advent of food sharing, which would reduce day-to- day variance in food availability. The USO and cooking mod- els (O’Connell, Hawkes, and Blurton Jones 1999; Wrangham Acknowledgments et al. 1999) and hunting and scavenging models proposing I thank Leslie Aiello and Susan Anto´n for inviting me to exploitation of large game (e.g., Bramble and Lieberman 2004; participate in this symposium, and I thank them and the other Bunn and Pickering 2010; Shipman and Walker 1989) all symposium attendees as well as anonymous reviewers for implicate food sharing as a key derived ecological feature of comments, conversations, and insights that improved this early Homo. Increasing adiposity, which is evident in modern study considerably. William Jungers generously shared mea- humans, would also serve to buffer variability in food avail- surements of Pygmy femoral dimensions, and Trent Holliday ability by providing energy reserves during periods of food generously shared measurements of hominin fossils. shortage (see Wells and Stock 2007). If the increase in body size and diet quality in early Homo is read as evidence for increased energy throughput, it may indicate that provisioning References Cited and food sharing, and perhaps increased body fat, were critical Aiello, Leslie, and Christopher Dean. 1990. An introduction to human evolu- early adaptations in the evolution of our genus. tionary anatomy. London: Academic Press. Aiello, Leslie C., and Catherine Key. 2002. Energetic consequences of being a Homo erectus female. American Journal of Human Biology 14:551–565. Aiello, Leslie C., and Peter Wheeler. 1995. 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The Effects of Mortality, Subsistence, and Ecology on Human Adult Height and Implications for Homo Evolution

by Andrea Bamberg Migliano and Myrtille Guillon

CAϩ Online-Only Material: Supplement A

The increase in body size observed with the appearance and evolution of Homo is most often attributed to ther- moregulatory and locomotor adaptations to environment; increased reliance on animal protein and fat; or increased behavioral flexibility, provisioning, and cooperation leading to decreased mortality rates and slow life histories. It is not easy to test these hypotheses in the fossil record. Therefore, understanding selective pressures shaping height variability in living humans might help to construct models for the interpretation of body size variation in the hominins. Among human populations, average male height varies extensively (145 cm–183 cm); a similar range of variation is found in Homo erectus (including African and Georgian samples). Previous research shows that height in human populations covaries with life history traits and variations in mortality rates and that different environments affect adult height through adaptations related to thermoregulation and nutrition. We investigate the interactions between life history traits, mortality rates, environmental setting, and subsistence for 89 small-scale societies. We show that mortality rates are the primary factor shaping adult height variation and that people in savanna are consistently taller than people in forests. We focus on relevant results for interpreting the evolution of Homo body size variability.

Body size is one of the major features that distinguishes aus- sociated with reduced mortality rates (associated with in- tralopiths from early Homo and early Homo from Homo creased alloparenting) in comparison with earlier members erectus (Anto´n 2012; Holliday 2012; Pontzer 2012). Some of of Homo and australopithecines. the most important questions about the evolution of Homo These hypotheses are largely mutually exclusive, and the concern the reasons behind the observed size increase between explanation for size variation in the hominins undoubtedly these taxa and the variation within them. involves a complex interaction between such factors as cli- Paleoanthropologists have offered a number of hypotheses mate, mortality rates, and nutrition. By building a detailed for body size increase in hominins. For example, Wheeler understanding of the causes of body size differences in mod- (1992) proposed that body size and body proportions were ern human populations, we believe that we will be in a much specific thermoregulatory adaptations to the environments stronger position to generate testable hypotheses for body size encountered by the hominins, as have Vrba (1996), Passey et changes during hominin evolution. al. (2010), and Trauth et al. (2010). A number of authors also In modern humans there is good evidence of the relation- have related diet to increased body size (e.g., Aiello and ship between body size and climate. For example, Roberts Wheeler 1995; Carmody and Wrangham 2009). And (1973) demonstrated body size increase with distance from O’Connell, Hawkes, and Blurton Jones (1999) argue that the the equator. Size variation has also been linked directly to evolution of larger body size in H. erectus was originally as- thermoregulatory adaptations. Specifically, smaller body size (both in height and weight) may help to reduce heat pro- duction in hot and humid environments (Cavalli-Sforza 1986) Andrea Bamberg Migliano is Lecturer in Evolutionary Anthropology while larger bodies may help to conserve heat in cold envi- in the Department of Anthropology at University College London ronments (Bergmann 1847), a pattern that is generally found (14 Taviton Street, London WC1H 0BW, U.K. [[email protected] .uk]). Myrtille Guillon is a graduate student in the Department of among other mammals (Ashton, Tracy, and de Queiroz 2000). Anthropology at University College London (Gower Street, London With the publication of Charnov’s (1992) general life his- WC1E 6BT, U.K). This paper was submitted 12 XII 11, accepted 9 tory model, growing attention has been directed to mortality VII 12, and electronically published 27 XI 12. risk as a factor potentially shaping body size evolution. As

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0008$10.00. DOI: 10.1086/667694 S360 Current Anthropology Volume 53, Supplement 6, December 2012 death restricts the amount of time available to an organism, Material and Methods time and energy invested into one process (growth, reproduc- tion, and maintenance) cannot be invested in another. In other We use a compiled database that includes information on the words, not all processes can be simultaneously maximized life histories of 89 small-scale human populations. Part of the (Charnov 1992; Stearns 1992). Because larger individuals tend data was obtained from the Comparative Human Life History to have a higher energy capture rate during growth and thus Spreadsheet,1 with part of the data previously published in a higher production rate at adulthood and a higher energy Migliano, Vinicius, and Lahr (2007) and Walker et al. (2006). budget to be invested into reproduction (Stearns 1992), more We supplement this database with data from other ethno- time allotted to growth (i.e., late maturation) will tend to be graphic sources that provide information about average stat- favored. However, there are potential costs to delaying matu- ure, age at menarche, and survival to age 15 in traditional ration as it increases the likelihood of death before reproduc- small-scale societies. All populations are classified according tion. For this reason, low mortality rates favor delayed matu- to their primary environment using relevant ethnographic ration and large body size, and high mortality favors earlier literature (supplement A). reproduction and growth termination and hence small body Most mortality data were obtained from Walker et al. size. For this reason, mortality rates are likely to determine the (2006), which describes data quality. Populations were se- pace of life histories, the balance of investment in growth versus lected for inclusion on the basis of two specific criteria; only reproduction, and variation in adult body size (Harvey and traditional small-scale societies were sampled, and popula- Clutton-Brock 1985; Harvey and Purvis 1999; Harvey and tions that had experienced recent significant changes in life- style were excluded. Zammuto 1985; Promislow and Harvey 1990). Dietary variables were taken from Binford (2001), who This general relationship between mortality and growth described the diet of hunter-gatherer populations in terms of should influence body size variability not only across taxa but percentage of food coming from hunting (percentage of re- also among human populations (Adair 2007; Kuzawa and liance on hunting), from fishing (percentage of reliance on Bragg 2012; Migliano, Vinicius, and Lahr 2007; Walker et al. fishing), and from gathering (percentage of reliance on gath- 2006). One example of this relationship in humans is the ering). We use these data to estimate the effects of reliance short stature of Pygmies, which we found to be best explained on animal protein (increased meat and fish in the diet) on as a consequence of an accelerated life history (early growth hunter-gatherers’ size variation. cessation) caused by high mortality rates in a nutritionally There are several limitations to this cross-cultural approach. stressful environment (Migliano 2005; Migliano, Vinicius, and First, the fact that different measurements have been taken by Lahr 2007, 2010; Stock and Migliano 2009). different people at different times with variable sample sizes Diet and nutrition are also important factors affecting potentially introduces a number of sources of error. Second, growth and consequently adult height in modern humans the demographic indicators of mortality (survival to age 15, (Bailey 1991; Golden 1991). For example, malnourished chil- life expectancy at birth, and life expectancy at age 15) are de- dren suffering from protein or calorie deficiency grow slowly, rived primarily from retrospective interviews but in some cases delay maturation, and achieve shorter stature (Akachi and are inferred from stable population models. Third, dietary per- Canning 2007; Cameron 1991; Danubio and Sanna 2008; centages rely on the quality of the data obtained for each pop- Lampl, Johnston, and Malcolm 1978; Silventoinen 2003). In- ulation (see Binford 2001 for a description of the subsistence terestingly, these factors affect adult body size through dif- data). Nonetheless, if we are to understand how different eco- ferent mechanisms; while malnourishment will lead to slower logical and demographic variables affect variation in human growth rates and delayed maturation (Lampl, Johnston, and body size worldwide, it is necessary to rely on cross-cultural Malcolm 1978), increased adult mortality rates should lead samples. Here, we have done our best to ensure compatibility to the acceleration of growth rates and earlier maturation of the data and present the results of this analysis as hypotheses (Migliano, Vinicius, and Lahr 2007; Walker et al. 2006). to stimulate further work in this area. To test data quality, we analyzed subsets of the data as well What is the effect of adult mortality rates, rates of growth as the entire data set. The results were very similar in all and maturation, subsistence strategies, and variation in en- analyses. For example, we regressed adult body size on prob- vironmental settings on current human height diversity? We ability of survival to age 15 controlling for continent, sex, and analyze a cross-cultural database that includes 89 living hu- environment for the total data set (n p 42 ) and only for the man populations of foragers, small-scale farmers, horticul- hunter-gatherer sample (n p 29 ). In both samples survival at turalists, and pastoralists living in varying environments from age 15 had a significant positive effect on adult height, and ϩ forests to deserts (see CA online supplement A). We then people in the savanna were significantly taller than people in discuss the applications of our findings to the hominin fossil the forest (comparisons not shown). record and propose testable hypotheses for explaining the variation in body size observed in the genus Homo. 1. http://dice.missouri.edu. Migliano and Guillon Mortality and Height Variability S361

Table 1. Linear regression models using life expectancy at birth, life expectancy at age 15, and probability of survival to age 15 to predict adult height

Last block (change) Whole model (including sex, continent, when including Partial correlation and standardized and one of the three mortality one of the three b coefficient (controlling for predictors) mortality predictors sex and continent)

2 2 Predictor RR(SE) ANOVA (P) R change Fchange (P) Partial correlation Standardized b (P) Life expectancy at birth (n p 19) .787 .620 (.017) F p 4.24 (.001) .253 8.66 (.011) .632 .593 (.011) Life expectancy at age 15 (n p 19) .843 .711 (.015) F p 6.38 (.003) .336 15.06 (.002) .733 .649 (.002) Probability of survival to age 15 (n p 42) .755 .570 (.017) F p 6.43 (!.001) .299 23.6 (!.001) .640 .592 (!.001)

Least squares multiple regression models are employed to to adult height variation and to growth and development. The assess the extent to which estimates of mortality (life expec- second two focus on environmental setting and its relation- tancy at birth, life expectancy at age 15, and survival to age ship to adult height variation and to both mortality rate and 15) and diet predict human height. In order to include the adult height variation. The last analysis looks at the relation- effect of the primary environment in the analysis, dummy ship between subsistence strategy and adult height and life variables were created for each environment type and sub- history diversity. The major result emerging from these anal- sistence strategy. The primary environments are categorized yses is that measures of mortality (or survivorship) are the as forest, savanna, desert, and tundra. When dummy variables prime determinate in adult height in the sample of small- are included in a regression model, stepwise methods become scale human populations, although environmental setting also inappropriate, and so the enter method was used. To control has a significant influence. for the nonindependence of human societies as statistical points that can arise because of phylogenetic history, popu- Analysis I: Relationship between Mortality lations were classified according to their continents, and this Rate and Adult Height Variation variable was used as a control in the regression analyses. This was considered appropriate because our sample involves iso- In separate multiple regression analyses including sex and lated populations that have a long tradition of life in their continent, three different measures of mortality/survivorship current geographical settings. Bivariate correlation analyses each show a significant correlation with adult height, popu- p 2 p are used to investigate relationships between life history var- lation average life expectancy at birth (n 19 ,R 0.620 , ! p 2 p iables and body size. We control for sex when males and P .001), life expectancy at age 15 (n 19 ,R 0.711 , ! p females from different populations were entered in the same P .001), and the probability of survival to age 15 (n 42 , 2 p ! analyses and when the analyses included populations for R 0.570,P .001 ; table 1). The fact that life expectancy which male and female variables had been calculated together at age 15 is strongly correlated with adult height suggests that in the original publications. We used log transformation when mortality rates in adulthood affect adult stature. normality transformations were required. All regression, cor- Controlling for sex and continent, life expectancy at birth p p relation, and variance analyses were produced using PASW is a strong predictor of adult height (b 0.593 ,P .011 ), 18 (SPSS, Chicago). explaining an extra 25.3% of the variance in height in relation to what is explained only by continent and sex. When the Results probability of survival to age 15 is used to predict adult height, the relationship is very similar to that with life expectancy at Five separate sets of multiple regression analysis are carried birth (b p 0.592 ,P ! .001 ), with an extra 29.9% of the variance out. The first two focus on mortality rate and its relationship explained in relation to the basal model (which includes sex

Table 2. Linear regression model using probability of survival to age 15 to predict relative height at age 10

Last block (change) when including Partial correlation and standardized Whole model (including sex, continent, probability of b coefficient (controlling for and probability of survival to age 15) survival to age 15 sex and continent) Predictor RR2 (SE) ANOVA (P) R2 F (P) Partial correlation Standardized b (P) Probability of survival to age 15 (n p 16) .878 .771 (.015) F p 9.24 (.002) .357 17.14 (.002) Ϫ.780 Ϫ.766 (.002) S362 Current Anthropology Volume 53, Supplement 6, December 2012

Table 3. Linear regression model using survival to age 15 and life expectancy at age 15 to predict age at menarche

Last block (change) when including probability of Whole model (including continent and survival to age 15 Partial correlation and standardized probability of survival to age 15 or or life expectancy b coefficient (controlling life expectancy at age 15) at age 15 for continent)

2 2 Predictor RR(SE) ANOVA (P) R change Fchange (P) Partial correlation Standardized b (P) Probability of survival to age 15 (n p 16) .832 .693 (.033) F p 6.196 (.007) .073 2.62 (.134) .439 .324 (.134) Life expectancy at age 15 (n p 13) .864 .747 (.032) F p 5.915 (.016) .191 6.05 (.039) .656 .456 (.039) and continent). Using life expectancy at age 15 as a predictor arche was analyzed. When probability of survival to age 15 of adult height slightly increases correlations (b p 0.642 , P ! is used as the predictor variable to assess the effect of mortality .001), and an extra 33.6% of the variance is explained in relation on age at menarche, the relationship is not significant because to the basal model. This brings the total variance explained by the inclusion of survival to age 15 as a predictor to the basal the whole model (including continent, sex, and life expectancy model (including continent) does not improve the model p 2 p p p at age 15) to 71% (table 1). Survival to age 15 and life expec- (n 16 ,R change0.073 ,F change 2.62 ,P .134 ; table 3). tancy at age 15 are highly correlated (n p 18 ,R p 558 , P p However, when life expectancy at age 15 is used as the in- .016); however, the first expresses prereproductive survival, dependent variable, there is a significant correlation with age while the second expresses adult survival. at menarche when continent is controlled for (b p 0.456 , P p .039; table 3). Including life expectancy at age 15 as a p Analysis 2: Relationship between Mortality predictor significantly improves the basal model (n 16 , p p Rates, Growth, and Development Fchange 6.05,P .039 ), explaining an extra 19.1% of the variability in age at menarche in our samples and bringing This analysis investigates the relationship between probability the total variability explained by the whole model to 74.7%. of survival to age 15 and relative height at age 10 (percentage This is a positive relationship, meaning that populations who of adult height achieved by age 10), which is used as a proxy live for longer have a later age at menarche (table 3). for growth rate (the more growth completed by age 10, the faster the growth rate). Probability of survival to age 15 is Analysis 3: Relationship between Environmental used here rather than life expectancy at age 15 because of Settings and Adult Height Variation sample size constraints. The multiple linear regression model controlling for sex and continent shows a negative association To test whether environmental setting has an effect on body between probability of survival to age 15 and percentage of size, we ran a multiple regression analysis controlling for sex adult height achieved by age 10 (n p 16 ,b p Ϫ0.766 , P p and continent, with adult height as the dependent variable .002), which implies that children exposed to higher mortality and environmental settings (savanna, forest, tundra, and des- environments grow at faster rates than children in lower mor- ert) as predictor variables. Dummy variables are used to enter tality environments (table 2). the environmental settings as predictors, as environmental In addition, the influence of mortality rate on age at men- settings are discrete. The inclusion of environmental settings

Table 4. Linear regression model using environmental settings (forest, savanna [S], tundra [T], and desert [D]) to predict adult height

Partial correlation and standardized Last block (change) b coefficient, foresta as Whole model (including sex, continent, when including reference (controlling for and environment) environment sex and continent)

2 2 Predictor RR(SE) ANOVA (P) R change Fchange (P) Partial correlation Standardized b (P) Environmental settings (n p 150) .789 .622 (.016) F p 22.8 (!.001) .167 20.5 (!.001) S, .539; D, .270; S, .442 (!.001); D, T, .06 .181 (.001); T, .089 (!.476) a Environmental settings were entered as dummy variables because “environmental settings” is a categorical variable. As such, one of the categories has to be a reference (all other categories are measured against the reference). Migliano and Guillon Mortality and Height Variability S363

Table 5. Total frequency of cases in each continent and each environmental setting

Ecology Africa Asia Australia Europe North America South America Desert 5 0 4 0 1 1 Forest 17 53 3 2 2 18 Savanna 14 8 1 0 2 6 Tundra 0 0 0 2 10 1 in the last block significantly improves the basal model significant (n p 42 ,b p 0.115 ,P 1 .05 ). Probability of sur- p ! (Fchange 22.8 ,P .001 ), explaining an additional 16.7% of vival to age 15 is the strongest predictor of height in the model the height variability. The complete model including sex, con- (n p 42 ,b p 0.569 ,P ! .001 ; table 6). The reduction of the tinent, and environment is highly significant and explains explanatory power of the environmental factors when the 62.2% of the variance in height (n p 150 ,R 2 p 0.622 , P ! probability of survival to age 15 is introduced as a predictor .001). Controlling for sex and continent, the savanna envi- has to be interpreted with caution because the sample size ronment has a significantly positive effect on adult height (and therefore the representation of all environmental settings compared with the forest environment (n p 150 ,b p 0.442 , in each continent) is reduced when all variables are included P ! .001) and the desert environment (n p 150 ,b p 0.181 , (table 7). P p .001; table 4). Populations are represented from all con- Unfortunately, sample sizes and sample distributions are tinents, and therefore phylogenetic relationships are unlikely insufficient to allow height, environmental variables, and to explain why living in the savanna or desert is associated other mortality indicator variables (life expectancy at birth with greater stature than living in the forest (table 5). and life expectancy at age 15 in the same analyses) to be analyzed together. However, the results do show that the prob- Analysis 4: Relationship between Environmental Setting, ability of survival to age 15 is a strong predictor of adult Mortality Rates, and Adult Height Variation height and that living in the savanna has a more positive influence on height than living in the forest independent of When probability of survival to age 15 is included as a pre- the effect of mortality. dictor variable together with the environmental settings, the general model improves (n p 42 ,R 2 p 0.700 ,P ! .001 ) in Analysis 5: Relationship between Subsistence Strategies, spite of the much smaller sample sizes (n p 42 vs.n p 150 ). Adult Height, and Life History Diversity The inclusion of probability of survival to age 15 together with environmental settings in the last block of the regression In order to assess the effect of subsistence strategy on adult explains an additional 26.9% of the height variability in our body size variation, we used data on diet composition in sample. Living in the savanna remains positively associated hunter-gatherer groups assembled by Binford (2001, table with height compared with living in the forest even when the 5.01). The percentages of reliance on fishing and hunting were effect of survival to age 15 is taken into account (n p 42 , combined to calculate reliance on animal protein. b p 0.387,P ! .001 ), but the contrast between living in the We use a multiple linear regression analysis with height as desert and living in the forest found previously is no longer the dependent variable to understand the role of the per-

Table 6. Linear regression model using environmental settings (forest, savanna [S], tundra [T], and desert [D]) and prob- ability of survival to age 15 to predict adult height

Last block (change) Partial correlation and standardized b Whole model (including sex, continent, when including coefficient, foresta as reference environment, and probability of survival to (controlling for sex, continent, survival to age 15) age 15 and environment)

2 2 Predictor RR(SE) ANOVA (P) R change Fchange (P) Partial correlation Standardized b (P) Environmental settings and survival to age 15 (n p 42) .836 .700 (.015) F p 7.22 (!.001) .269 27.7 (!.001) S, .543; D, .187; T, S, .387 (.001); D, Ϫ.065; probability .115 (.296); T, of survival, .687 Ϫ.106 (.717); probability of survival 15, .569 (!.001) a Environmental settings were entered as dummy variables because “environmental settings” is a categorical variable. As such, one of the categories has to be a reference (all other categories are measured against the reference). S364 Current Anthropology Volume 53, Supplement 6, December 2012

Table 7. Frequency of cases in each continent and each en- faster, achieving adult body sizes sooner, and should also ma- vironmental setting when only individuals with data on ture earlier in order to start reproducing sooner. This is what survival to age 15 are considered we find in our analyses: populations living in higher mortality environments have earlier menarche and grow at a faster rate Ecology Africa Asia North America South America (as proxied by the proportion of adult body size achieved at Desert 3 0 1 1 age 10) than populations living in lower mortality environ- Forest 9 10 2 18 ments (see tables 2, 3). This is the opposite effect observed Savanna 4 0 2 6 Tundra 0 0 10 1 when short stature is determined by malnourishment, where populations should achieve short stature as a result of delayed sexual and growth maturation (Migliano, Vinicius, and Lahr centage of reliance on animal protein in shaping adult height 2007). variability among hunter-gatherers, controlling for sex, con- As Kuzawa and Bragg (2012) have shown, developmental tinent, and environmental variables. Although the total model plasticity exerts a strong influence on age at menarche and including sex, continent, environment, and percent reliance body size (both weight and height). Populations experiencing on animal protein is highly significant (n p 52 ,R 2 p 0.811 , overnutrition in the West or individuals recently adopted into P ! .05), percent reliance on animal protein is not a significant Western culture have earlier menarche and earlier growth factor in predicting height when the other variables are con- cessation and achieve larger body sizes as a consequence of trolled (n p 52 ,b p 0.196 ,P 1 .05 ; table 8). decreasing nutritional constraints. The expression of this phe- notype should, therefore, be interpreted as a response to an Discussion unconstrained environment (where time and resources are virtually unlimited, releasing trade-offs; fig. 1). However, this These results show that variation in adult height is highly situation is virtually nonexistent in tribal populations, where influenced by mortality patterns in our worldwide sample of both time (survivorship) and resources (calories) are limited small-scale human populations. Preadult mortality (proba- to varying extents. Our results suggest that mortality rates bility of survival to age 15) alone (when controlled by sex have a strong influence on adult height and maturation var- and continent) explains 29.9% of the variation in adult height, iability in natural environment populations; although the im- while adult survival (life expectancy at age 15) explains 33.6%. The model combining life expectancy at age 15 with sex and portance of nutrition should also be considered (fig. 1; see continent explains a great proportion of the variance (71.1%). Kuzawa and Bragg 2012, fig. 3). Our analysis of the effects These results are in accordance with the predictions of life of diet on height variation in a subset of the sample (the history theory (Charnov 1992). Life history theory predicts hunter-gatherers) for which data on reliance on gathering, that high mortality rates should lead to relatively fast-paced fishing, and hunting were available did not reach significance. life history strategies (Charnov 1992). Correspondingly, we There was a positive correlation between a diet high in animal should expect that those human populations that face higher protein and adult stature; however, a larger sample size and rates of adult mortality will have individuals who, on average, better data are needed. develop earlier. They will achieve full growth relatively early, Finally, our results indicate that living in the savanna has reproduce at an earlier age than those with relatively low a positive correlation with height compared with living in the mortality rates, and thereby reduce the chances of death be- forest irrespective of the differences observed in mortality fore reproduction (Migliano 2005; Migliano, Vinicius, and rates. This result is found even when controlling for continent Lahr 2007; Walker et al. 2006). (as a way to control for phylogenetic and statistical nonin- Our results also provide clues to the mechanisms through dependence between populations). Other effects, such as dif- which mortality rates affect adult body size. According to the ferences in temperature, humidity, or diet undoubtedly play theory, populations under high risk of death should develop a role in explaining interpopulation differences in stature. Tall

Table 8. Linear regression model using environmental settings (forest, savanna, tundra, and desert) and percentage of de- pendence on animal protein to predict adult height

Last block (change) Whole model (including sex, continent, when including Partial correlation and standardized environment, and percent reliance percent reliance on b coefficient (controlling for on animal protein) animal protein sex and continent)

2 2 Predictor RR(SE) ANOVA (P) R change Fchange (P) Partial correlation Standardized b (P) Percent reliance on animal protein (n p 52) .901 .811 (.0137) F p 15.6 (!.001) .008 1.73 (.196) .204 .196 (.196) Migliano and Guillon Mortality and Height Variability S365

stature and narrow elongated bodies have long been explained as a thermoregulatory mechanism in hot savanna environ- ments (e.g., Ruff 1993). The association between tropical for- ests and short human stature has also been identified, and different adaptive hypotheses have been suggested to explain it, from thermoregulatory adaptations proposing that shorter humans produce less heat in a tropical humid environment, being more efficient at cooling down (Cavalli-Sforza 1986), to easier locomotion in closed forests (Turnbull 1986) and adaptation to poor carbohydrate availability in tropical forests (Bailey and Peacock 1988). Small body size in forested en- vironments is also seen in other mammals. For example, forest elephants have been estimated to be 35%–40% smaller in stature than their savanna counterparts (Morgan and Lee 2003), and the pygmy hippopotamus is found mainly in Li- beria and only in thick forests (Eltringham 1999). More data are necessary to test whether these other variables explain part of the variance not captured by differences in mortality rates and to understand how mortality rates interact (or are influ- enced) by these other pressures.

Applications to Hominin Evolutionary History

Body size increase is one of the main features distinguishing the australopiths from early Homo and early Homo from Homo erectus (Anto´n 2012; Holliday 2012; Pontzer 2012). For early Homo, height and weight can be approximately esti- mated for KNM-ER 3735, OH 62, KNM-ER 1472, and 1481. The height range is 118–149 cm (Anto´n 2012), and average weight is 50–54 kg (Holliday 2012). This represents a 30% increase over the condition in Australopithecus (Anto´n 2012; Holliday 2012; Pontzer 2012). With the appearance of H. erectus there was an additional increase in body size of com- parable magnitude (Anto´n 2012). When comparing the variability in body size in modern humans to early Homo and H. erectus, it is clear that H. erectus height overlaps with the recent human range, while the early Figure 1. Interaction between nutrition and mortality rates in- Homo variation falls below recent human variation (fig. 2A). fluencing adult height. In populations with no caloric restrictions In contrast, inferred weight variation falls well within the and low mortality rates, growth cessation happens relatively early human range for early and late Homo (fig. 2B). This pattern (maximizing reproductive span) at larger body sizes (maximizing indicates important stature/weight differences between early energy budget to be invested into reproduction), such as in the Homo and living humans, implying differences in body pro- populations of the United States (National Center for Health portions (see Holliday 2012). Statistics [NCHS] data; white squares, dashed lines, NCHS 2002). In H. erectus the range of body size variation (40–68 kg, A, In populations where nutritional stress is high and life ex- pectancy is relatively high, such as the Turkana pastoralists (data 146–185 cm) falls well within the interpopulation variation from Little, Galvin, and Mugambi 1983; black squares), growth observed in modern humans (fig. 2; Anto´n 2012). Moreover, cessation is delayed (maximizing body size); that is, Turkana Georgian specimens have ranges of size overlapping the in- pastoralists achieve the same adult height as the well-nourished trapopulation variation observed in Philippine Pygmies (fig. Americans—however, much later. B, When high mortality rates 2). Although there is great variation in body size within H. are combined with relatively poor nutrition, growth cessation erectus, the similarities with modern human ranges indicate cannot be delayed because reproductive life span is already im- that perhaps the same patterns of diversification apply to the paired; thus, populations in these conditions, such as the Aeta from the Philippines (data from Migliano, Vinicius, and Lahr two groups. Therefore, we suggest that understanding the 2007; gray squares), have an early growth cessation (as early as causes of body size variation in living human populations is the Americans) at much smaller sizes (2 SD below the American relevant to interpreting the variation observed within Homo average). and in particular within H. erectus. S366 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 2. A, Distribution of height across 3,263 small-scale world population averages (gray) and within Aeta Pygmies from the Philippines (black;n p 348 ). The thick black line is the range of height variation in early Homo, while the thick dark gray line is the range of height variation in Homo erectus (Georgian specimens), and the thick light gray line is the range of height variation in H. erectus (African specimens). B, Distribution of weight across 249 small-scale world population averages (gray) and within Aeta Pygmies from the Philippines (black;n p 348 ). The thick black line is the range of weight variation in early Homo, while the thick dark gray line is the range of weight variation in H. erectus (Georgian specimens), and the thick light gray line is the range of weight variation in H. erectus (African specimens). Human variation from Kings Diversity Project (M. M. Lahr and R. Foley, unpublished data); Aeta Pygmy data (Philippines) from Migliano (2005); and hominin data from Anto´n (2012).

Our results indicate that two factors could have been as- we would expect lower rates of growth and development in sociated with the stature variation observed both between and relation to larger H. erectus specimens. On the other hand, if within hominin taxa. The first is variation in preadult and differences were due to differing mortality environments, we adult mortality rates, and the second is occupation of different would expect the smaller specimens to have a more rapid life environments. Although diet was not significant in our anal- history pace (as proxied by their patterns of tooth develop- yses, we know from studies of modern human populations ment). that it also could be a relevant factor (e.g., Kuzawa and Bragg Although the data are not yet available to test the rela- 2012). tionship of nutrition and mortality rate on hominin stature Testing the distinct influences of at least mortality rate and and the relationship of these variables to the third compli- nutrition on observed body size in the fossil record may be cating factor, environment, it is interesting to speculate on possible to achieve. The results of this study and of others the implications of these factors to the evolution of Homo.If (Kuzawa and Bragg 2012; Migliano, Vinicius, and Lahr 2007; mortality rate does prove to be a significant factor associated Walker et al. 2006) indicate that poor nutrition and high with hominin stature as our analyses suggest, it would imply mortality rates both lead to short stature but through different that early Homo had a reduced mortality rate in relation to mechanisms: poor nutrition should lead to delayed growth the australopiths and that H. erectus had further reduced its and maturation (due to the lack of resources), while high mortality rate in relation to early Homo. The question then mortality rates should lead to early development and matu- is how the hominins achieved reduced mortality rates in the ration (due to selection for early reproduction). Understand- context of an increasingly variable environment and expan- ing how closely the pace of tooth development and the se- sion into a broader range of niches (Potts 2012). Potts argues quence and timing of dental eruption match the pace of life that greater behavioral flexibility associated with a larger brain history in current and extinct populations (Dean 2006; size together with the capacity to extract more effectively pro- Schwartz 2012) would help immensely with understanding tein and fat resources and an increased capacity for avoiding the causes behind body size variation in Homo. For example, predation might have contributed to the reduction of mor- if the short stature of Homo floresiensis (Brown et al. 2004) tality rates (see also Anto´n and Snodgrass 2012; Kaplan et al. and H. erectus in Georgia (aka Homo georgicus; Lordkipanidze 2000). et al. 2007) were a consequence of nutritional insufficiency, Important factors undoubtedly include subsistence shifts Migliano and Guillon Mortality and Height Variability S367 and predator avoidance but would also include other cultural Aiello, Leslie C., and Catherine Key. 2002. Energetic consequences of being a Homo erectus female. American Journal of Human Biology 14(5):551–565. adaptations as well as opportunities for cooperation, allo- Aiello, Leslie C., and Peter Wheeler. 1995. The expensive-tissue hypothesis: parenting, parental investment, and increased child provi- the brain and the digestive system in human and primate evolution. 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How our ancestors broke through symposium in Sintra, Portugal, and to all participants in the the gray ceiling: comparative evidence for cooperative breeding in early symposium for insightful comments. We thank Lucio Vini- Homo. Current Anthropology 53(suppl. 6):S453–S465. cius, Rodolph Schlaepfer, Ruth Mace, Tom Currie, and the Kaplan, Hillard, Kim Hill, Jane Lancaster, and A. Magdalena Hurtado. 2000. A theory of human life history evolution: diet, intelligence, and longevity. Human Evolutionary Ecology Research Group at University Evolutionary Anthropology 9(4):156–185. College London for useful comments. Kuzawa, Christopher W., and Jared M. Bragg. 2012. Plasticity in human life history strategy: implications for contemporary human variation and the evolution of genus Homo. Current Anthropology 53(suppl. 6):S369–S382. References Cited Lampl, Michelle, Francis E. Johnston, and Laurence A. Malcolm. 1978. 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Plasticity in Human Life History Strategy Implications for Contemporary Human Variation and the Evolution of Genus Homo

by Christopher W. Kuzawa and Jared M. Bragg

The life history of Homo sapiens is characterized by a lengthy period of juvenile dependence that requires extensive allocare, short interbirth intervals with concomitantly high fertility rates, and a life span much longer than that of other extant great apes. Although recognized as species-defining, the traits that make up human life history are also notable for their extensive within- and between-population variation, which appears to trace largely to phenotypic and developmental plasticity. In this review, we first discuss the adaptive origins of plasticity in life history strategy and its influence on traits such as growth rate, maturational tempo, reproductive scheduling, and life span in modern human populations. Second, we consider the likely contributions of this plasticity to evolutionary diversification and speciation within genus Homo. Contrary to traditional assumptions that plasticity slows the pace of genetic adaptation, current empirical work and theory point to the potential for plasticity-induced phenotypes to “lead the way” and accelerate subsequent genetic adaptation. Building from this work, we propose a “phenotype-first” model of the evolution of human life history in which novel phenotypes were first generated by behaviorally or environ- mentally driven plasticity and were later gradually stabilized into species-defining traits through genetic accom- modation.

Introduction in the fossil signatures of life history variation in Homo erectus, calling into question previous assumptions regarding the evo- Modern humans are characterized by a life history strategy lution of size and shape in Homo and bringing variation per with features that are distinct from other nonhuman primates, se to the fore as an important focus of analysis (e.g., Anto´n including slow childhood growth, early weaning followed by 2003; Anto´n et al. 2007). These findings raise questions about a long period of dependence, a shortened interbirth interval, the evolutionary origins of this diversity, which might reflect and lengthy life spans (Hawkes et al. 1998; Hill 1993; Hill distinct species or locally adapted variants of the same species and Kaplan 1999; Robson, van Schaik, and Hawkes 2006). (Anto´n 2003). While the magnitude of this regional variation Extensive provisioning of dependents by kin and potentially may complicate taxonomic distinctions, it is also notable for unrelated individuals allows humans to “stack” offspring and its similarities to the variation observed across contemporary spread the burden of provisioning across alloparents, thus human populations, among which there is extensive variation facilitating relatively high fertility despite the intensity of in- in life history traits such as growth rate, body size, repro- vestment and high survival of each offspring (Bogin 1999; ductive scheduling, and even life span. Biological anthropol- Hawkes et al. 1998; Hill and Hurtado 1996; Kaplan et al. ogists and others who study the life histories of contemporary 2000). Current interest in reconstructing the evolutionary humans have shown that much of this variation can be ex- emergence of these characteristics in modern humans and the plained as the outcome of phenotypic or developmental plas- life histories, behaviors, and biology of fossil hominins rep- ticity triggered in response to social, nutritional, demographic, resents a key intersection between human biology and paleo- and other environmental conditions (Chisholm 1993; Ellis et anthropology. al. 2009; Kuzawa and Pike 2005; Walker et al. 2006a). If Recent fossil discoveries have revealed extensive variation plasticity is an important contributor to contemporary human variation, it follows that it has likely also been important as an influence on the life histories of human ancestors. As such, Christopher W. Kuzawa is Associate Professor and Jared M. Bragg considering the mechanisms and adaptive significance of phe- is a Doctoral Student in Biological Anthropology in the Department of Anthropology, Northwestern University (1810 Hinman Avenue, notypic plasticity in modern human life histories provides Evanston, Illinois 60208, U.S.A. [[email protected]]). This insights into the origin and function of similar variation in paper was submitted 12 XII 11, accepted 18 VI 12, and electronically early Homo. published 27 VIII 12. We have several interrelated goals in this review. We first

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0009$10.00. DOI: 10.1086/667410 S370 Current Anthropology Volume 53, Supplement 6, December 2012 discuss the role of phenotypic and developmental plasticity duction—or have long life spans, but not both (Stearns 1989; as a primary means of population adjustment to environ- Williams 1966). mental changes occurring on generational or multigenera- As the reproductive benefits from investing in a durable, tional timescales. This background discussion culminates in long-lived body may only be realized in the future, the utility a review of evidence for environmental influences on human of allocating scarce resources to maintenance activities is life history variation, which highlights the effects that nutri- linked to the risk of unavoidable extrinsic mortality (e.g., tion and cues of mortality risk have on growth rate, matu- predation) that members of a population or species face, rational tempo, and adult size. A review of the literature on which is viewed as a primary driver of life history diversifi- modern humans confirms that developmental plasticity is the cation and evolution (Charnov 1993; Promislow and Harvey primary source of much human life history variation across 1990). Species living in ecological contexts characterized by contemporary populations and points to the likely impor- high mortality risk are less likely to live into the future and tance of similar processes as contributors to regional and thus are predicted to allocate a larger fraction of their energy temporal variation in the fossil record. budget to current reproduction with comparably little devoted Because only those genotypes that are expressed pheno- to maintenance (Kirkwood and Rose 1991). As a result, these typically are subjected to selection, environment-driven phe- “fast” life history species typically have shorter life spans and notypic variation in human populations may also influence give birth to many lower-quality offspring with relatively low the process, pace, and direction of evolutionary change (West- survival prospects. Conversely, when mortality risk is low, Eberhard 2003). From the perspective of the emerging syn- theory predicts a “slow” life history characterized by reduced thesis of developmental and evolutionary biology, the gen- expenditure on growth or reproduction and greater invest- eration of regional variation through plasticity likely provided ment in life span–extending maintenance. Slow life history the raw phenotypic variation that was then selectively retained species tend to give birth to fewer offspring, but they invest or pruned, leading the way for more gradual adaptation via more intensively in each, enhancing survival (Charnov and natural selection. We conclude by speculating that environ- Berrigan 1993). ment-driven developmental plasticity may not only provide The human life history strategy is unusual in that it is clearly insights into the origins of variation in contemporary and a slow and investment-oriented strategy in most respects while fossil hominin populations but also may have played a fun- also characterized by some of the demographic benefits typ- damental role in the evolution of our species by facilitating ically associated with fast life histories. Low mortality rates phenotypic adaptation that preceded more durable genetic enable slow childhood growth and delayed onset of physical change and speciation. maturity, nutritional independence, and reproduction well be- yond what is seen in other great apes (Hawkes et al. 1998; The Unusual Human Life History Kaplan et al. 2000; Walker et al. 2006b). Also consistent with a slow strategy, humans invest extensive amounts of time and Organisms vary remarkably in the size and pace of life, which energy in offspring during this protracted period of depen- is reflected in body size, growth rate, fertility rate, and life dence (Gurven and Walker 2006). Yet despite this, contem- span. These traits help define a species’ life history, which porary foraging populations manage to reproduce nearly twice may be viewed as a life-cycle strategy that optimizes expen- as fast as other great apes and have higher completed fertility ditures in service of reproductive success (Stearns 1992). Clas- (Walker et al. 2008). sically, organisms are viewed as being constrained by finite This unusual life history capacity to invest heavily in more energetic resources that must be partitioned to growth, re- offspring has been traced to the distinctively human practice production, and maintenance functions (Gadgil and Bossert of weaning offspring early and the consequent shortening of 1970). Growth builds a larger body that is less prone to pre- the interbirth interval relative to other great apes (Galdikas dation and has an absolutely greater capacity to invest in and Wood 1990; Humphrey 2010; Knott 2001; Sellen 2006, reproduction. After growth ceases at maturity, energy previ- 2007). Early weaning is accompanied by a long transitional ously allocated to growth is then shunted into reproduction. period of providing weanlings specially prepared foods that In females this involves support of offspring growth in utero may be acquired and provisioned flexibly within human social and via breast milk, and in males the building and mainte- units (Bogin 1999; Bogin and Smith 1996; Hawkes et al. 1998; nance of sexually dimorphic, energetically costly traits and Kaplan et al. 2000; Lee 1996). This allows alloparents, such behaviors (Charnov 1993; Kuzawa 2007). Consequently, or- as grandmothers or older siblings, to provide a substantial ganisms face a fundamental trade-off in deciding how much fraction of the energetic needs of each offspring, thus freeing of their time and energy budget to invest in growth or re- maternal metabolism to initiate new pregnancies. It is in- production in the present or to processes that minimize or creasingly recognized that the remarkable demographic suc- repair cellular or tissue damage to extend life span. For in- cess and geographic range of our species hinges on the flex- stance, because resources are finite, it is assumed that organ- ibility of these alloparental transfers, which allow us to “have isms may invest heavily in productivity—growth and repro- our cake and eat it too,” producing many high-quality and Kuzawa and Bragg Plasticity and Human Life History Evolution S371 low-mortality offspring (Kramer 2010; Lee 2003; Wells and Stock 2007).

The Timescales of Human Adaptation and the Role of Developmental Plasticity

While this strategy is characteristic of the human life history generally, nutritional and mortality conditions can vary widely across environments and through time. Although genetic ad- aptation by natural selection helps explain the durability of species-level characteristics that differentiate us from other Figure 1. Timescales of human adaptability (modified after Ku- great apes, the transience of many of the ecological challenges zawa 2005, 2008). Light gray p more rapidly responsive/less that populations confront may not be dealt with effectively durable; black p slowest to respond/most durable. Black arrows by changes in gene frequencies, which require many gener- indicate the order with which novel phenotypes appear. Under most circumstances, novel environments or behaviors first induce ations and hundreds if not thousands of years to accrue in novel phenotypes via reversible homeostatic processes that may the gene pool. As such, population variation in life history be replaced by more durably accommodated phenotypes via de- parameters is largely traceable to developmental plasticity. velopmental and intergenerational plasticity. If the changed con- West-Eberhard (2003:33) defines “phenotypic plasticity” as ditions are stable for sufficient generations, natural selection may “the ability of an organism to react to an internal or external gradually fix the phenotype or reduce the costs associated with environmental input with a change in form, state, movement producing it. In this way, highly plastic traits can “lead the way” or rate of activity.” “Developmental plasticity” refers to that and accelerate the pace of genetic change. subset of plastic phenotypic responses that involve irreversible modifications to growth and development. Plasticity is un- derstood as being undergirded by a genetic architecture that crease in heart rate, such as running from a predator. Ho- allows context-dependent trait expression in response to vary- meostatic changes may work as short-term solutions, but they ing environmental experiences and behaviors (McIntyre and are a poor means of coping with a condition such as high- Kacerosky 2011; Stearns 1992; Stearns and Koella 1986). altitude hypoxia if this is the new baseline environmental state. Biological anthropologists have long emphasized nonge- This is where the value of developmental plasticity becomes netic means of adapting to environmental challenges, and this clear. Individuals raised at high altitude have a more efficient work has highlighted the importance of developmental plas- strategy for coping with low oxygen availability, for they sim- ticity as a key mode of human adaptation (fig. 1; Frisancho ply grow larger lungs during childhood (Frisancho 1977). This 1977; Kuzawa 2005, 2008; Lasker 1969). The body copes with is an example of how developmental plasticity allows organ- the most rapid ecological fluctuations using rapid, self-cor- isms to adjust biological structure on timescales too rapid to recting, and reversible homeostatic systems that respond to be dealt with through genetic change but too chronic to be changes or perturbations in a way that offsets, minimizes, or efficiently buffered by homeostasis. Other classic examples of corrects deviations from an initial state. Homeostatic systems experience-driven plasticity include the development of the can be viewed as buffering the effects of environmental fluc- skeletal system (Pearson and Lieberman 2004), the central tuations to maintain approximate internal stability. A subset nervous system (Edelman 1993), and the immune system of homeostatic processes (Sterling 2004) also have an antic- (McDade 2003). ipatory component and a capacity for gradual resetting of target state and regulatory set points described as “allostasis.” Intergenerational Phenotypic Inertia When environmental trends are too chronic to be efficiently buffered by homeostasis or allostasis and yet not chronic There is a growing list of biological systems that are not enough for substantial genetic change to consolidate around, modified in response to the environment itself but to hor- the flexible capacities of such systems may be overrun. It is monal or nutrient signals or cues of past environments as easy to see how a sustained environmental change might over- experienced by ancestors, most typically the mother (Bateson load a homeostatic system. As an example, consider an in- 2001; Gluckman and Hanson 2004; Kuzawa 2001, 2005; Wells dividual who moves to high altitude where oxygen saturation 2007; Worthman 1999). Brief “critical” or “sensitive” periods is low. Initial physiologic responses will include an elevated in early development often overlap with ages of direct nu- heart rate, which increases the volume of blood and thus the trient, hormone, or behavioral dependence on the mother number of oxygen-binding red blood cells that pass through (e.g., via placenta, breast milk, or emotional attachment), the lungs. By engaging a homeostatic system—heart rate— which facilitate the transfer of integrated cues of past maternal the body has found a temporary fix. However, if heart rate or matrilineal experience (Kuzawa and Quinn 2009). These is already high under resting conditions, there is less leeway newer examples of early life developmental plasticity are thus to deal with new challenges that might require a further in- distinct from conventional plasticity in the time depth and S372 Current Anthropology Volume 53, Supplement 6, December 2012 stability of information to which the developing body re- sponds. The tendency for plasticity to respond to parental nutrient, hormonal, or behavioral cues that integrate past environ- mental experience has been defined as “phenotypic inertia” (Kuzawa 2005, 2008). One possible explanation for the utility of such effects is that offspring are calibrating growth and nutrient expenditure to the mother’s capacity and willingness to invest in the present offspring, which reflect her own phe- notypically embodied nutritional history (Wells 2003, 2007). From an alternative perspective, these intergenerational effects could calibrate offspring growth, metabolism, and physiolog- ical settings to a stable “running average” index of conditions experienced by recent matrilineal ancestors that serve as a “best guess” of conditions likely to be experienced in the Figure 2. Value of intergenerational averaging as a way to identify future (fig. 2; Kuzawa 2005). By this reasoning, intergener- a trend in a noisy signal, in this case representing availability of ational effects of matrilineal experience (and possibly also a hypothetical ecological resource. The two lines are running averages calculated across 10 time units (thin line) and 100 time patrilineal experience via germ-line epigenetic inheritance; see units (dark line). As the window of averaging increases, an un- Eisenberg, Hayes, and Kuzawa 2012; Pembrey 2010) could derlying long-term trend is uncovered. Transgenerational influ- extend the utility of developmental plasticity as a mode of ences of maternal and grandmaternal experience on fetal and adaptation by allowing organisms to track more integrated infant biology (inertia) may help achieve a similar feat. (From and stable trends occurring across a multigenerational time- Kuzawa and Quinn 2009, with permission.) scale (for more, see Kuzawa 2005, 2008; Kuzawa and Quinn 2009; Kuzawa and Thayer 2011). tions. Consistent with this expectation, most human life his- Thus, the type of organismal response to ecological chal- tory traits exhibit extensive sensitivity to ecological context lenge or novelty depends not only on the type of stressor or (see table 1). Here we summarize the role of nutrition and experience but also its stability and duration. Selection has cues of environmental risk as influences on the key life history shaped biology to respond to such experiences in a myriad parameters of growth trajectory, adult size, and reproductive of ways; as such, adaptation does not simply occur through strategy. evolution by natural selection and alteration of gene fre- quencies but also through homeostasis, allostasis, phenotypic/ Somatic Growth and Adult Body Size developmental plasticity, and phenotypic inertia across gen- erations (fig. 1). As life history characteristics take many Growth during the postnatal period can be divided into sev- forms, from behavioral to physiological to molecular (Hill eral periods of distinct hormonal regulation that vary in sen- and Hurtado 1996), we should expect a similar breadth of sitivity to environmental influence and that ultimately deter- mechanisms and timescales underlying life history evolution mine age-specific contributions to adult size and sexual and adaptation. As one example, mounting evidence suggests dimorphism (Karlberg 1989). Roughly the first two postnatal that many key life history traits are among those most strongly years reflect a continuation of a growth regime begun in utero. shaped by early life experiences and that they may respond At this age, production of insulin-like growth factors that to signals conveyed by the mother across the placenta or via stimulate skeletal and somatic growth is insulin dependent, breast milk (Kuzawa 2007; Kuzawa and Pike 2005; Kuzawa tying growth rate directly to nutritional intake and nutritional and Quinn 2009; Wells 2003). Continuing in this vein, we sufficiency. Prenatal evidence for this effect comes from a argue that adaptive phenotypic plasticity has a central place recent large study showing that the level of a woman’s fasting in explaining variation in life history traits among contem- glucose during pregnancy is a robust predictor of the size of porary human populations. her offspring at birth, illustrating that fetal glucose supply drives fetal growth (Metzger et al. 2009). After birth, exclusive Variation in Modern Human Life Histories breast-feeding sustains the infant’s nutritional requirements Traces Primarily to Environment- for about the first 6 months of life, after which complementary Driven Plasticity foods must be introduced to avoid growth faltering (Sellen 2006). While breast-fed, infants obtain balanced nutritional We have reviewed the key derived characteristics of the human resources to support growth and passive maternal immune life history strategy. We have also considered the need for a protection, which minimizes the burden of energetically costly capacity to modify priorities “on the fly” as an important infections. The weaning transition often introduces nutri- dimension of life history strategy for most organisms in light tional stress as these resources are replaced with less balanced of changing nutritional and demographic/mortality condi- and less sterile complementary foods. As such, infancy is often Table 1. Range of variation for key life history characteristics in modern human populations

Males Females Characteristic Range Degree of plasticity Range Degree of plasticity Environmental influences Height (cm): Birth (length) 49.0a–51.9b ϩ 48.1a–52.2b ϩ Mother’s nutrition before pregnancy increases; stress, infection decrease Weaning (3 years) 82.0a–99.0b ϩϩ 81.0a–98.6b ϩϩ Exclusive breast-feeding until 6 months protects; introduction of complementary foods, and infection lead to faltering Midchildhood (6 years) 97.0b–120.8b ϩϩ 96.8a–120.2b ϩϩ Deficits from early growth and poor environmental or nutritional milieu reduce stature Adult 144.4b–181.6a ϩϩ 135.8a–168.2b ϩ Low birth weight and poor nutrition/growth before 3 years of age reduce stature Weight (kg): Birth 2.4a–3.57a ϩϩ 2.50b–3.5a ϩϩ Weaning (3 years) 10.3a–16.1b ϩϩ 10.1a–16.1a ϩϩ Midchildhood (6 years) 14.5b–23.3b ϩϩ 13.8b–23.4b ϩϩ Adult 40.0a–88.1b ϩϩ 37.0a–87.4b ϩϩ Age at maturity (years): Menarcheal age 12.1b–18.4a ϩϩϩ Poor growth/nutrition delay; prenatal stress/childhood psychosocial stress and abun- dant nutrition accelerate Age at peak height velocityc 12.0–17.0 ϩϩ Fast postnatal/infancy growth accelerates Age at first birthc 20.9–37.0 16.2–25.0 Stress or cues of extrinsic mortality accelerates Age at menopaused 48.2–52.6 ϩϩ Higher parity, longer cycles delay menopause; some evidence that smoking, small size at birth, poor early growth lead to earlier menopause Life span:e

e0 21–37 21–37 Higher infant mortality and rates of infection and violence/accidents decrease

e15 28.6–42.5 28.6–42.5 Reduced exposure to environmental and health stressors increases

e45 13.7–24.2 13.7–24.2 a Eveleth and Tanner 1976. b Eveleth and Tanner 1990. c Walker et al. 2006a. d Leidy Sievert 2006. e Gurven and Kaplan 2007; ex is life expectancy at age x. S374 Current Anthropology Volume 53, Supplement 6, December 2012 an age of nutritional stress with a high-mortality burden. This, partial genetic explanation (Gray, Wiebusch, and Akol 2004). combined with the need to buffer an unusually large and However, these extremes aside, environmental factors, espe- inflexible cerebral energy need, may help explain the heavy cially differences in nutrition and pathogen burden during human investment in deposition of protective fat stores before the first 2–3 years of life, are recognized as the primary driver birth and during the first 6 months of postnatal life (Kuzawa of variation in mean adult size across populations (Eveleth 1998). and Tanner 1976, 1990). Because this difficult transition coincides with the age of insulin-dependent, nutrition-driven growth, weaning-related Nutrition as an Influence on Age at Reproductive Maturity growth deficits can carry into adulthood to influence final stature and body weight. Indeed, the magnitude of adult Age at maturity represents an important life history transition height deficits relative to healthy reference data has been because it marks the age at which the body shunts energy shown to trace largely to growth faltering already present at previously allocated to somatic growth into reproduction 2 or 3 years of age (Billewicz and McGregor 1981; Martorell (Charnov 1993; Kuzawa 2007). Although large adult size car- 1995), and much of the contemporary population variation ries reproductive benefits, the ability to sustain the nutritional in adult standing height is believed to reflect the effect of requirements of fast growth and the risk of preadult mortality nutrition and hygiene during infancy and early childhood that determines how long it is prudent to delay maturing are (Eveleth and Tanner 1976, 1990; Habicht et al. 1974; Victora both variable. Thus, it is expected that maturational tempo et al. 2008). will follow a gradient of developmental plasticity (i.e., a re- Although growth rate remains sensitive to nutrition during action norm) that is sensitive to availability of nutritional the entire period of growth and development, long-term ef- resources and also to cues reflecting the level of mortality risk fects of nutrition on adult size diminish after infancy and (Coall and Chisholm 2003; Ellis et al. 2009; Stearns and Koella early childhood as insulin-dependent growth is gradually re- 1986; Walker et al. 2006a). Consistent with this expectation, placed by a growth-hormone-regulated growth regime (Karl- maturational tempo is among the most variable of human berg 1989). During childhood and puberty, nutritional deficits life history characteristics and exhibits sensitivity to both nu- primarily slow the pace of maturity without affecting final tritional and psychosocial stressors. stature or body size. During the pubertal growth spurt (see The role of nutrition as a driver of childhood and adoles- below), onset of gonadal production of sex steroids increases cent growth helps explain the extreme environmental sensi- growth rate, especially in males. However, as with childhood tivity of pubertal timing. Population means for menarcheal growth, there is little evidence for lasting effects of nutrition age range from about 12 to 18 years (table 1). Rapid multi- during adolescence on final adult size. Generally, individuals generational secular trends clearly show that this variability who are better nourished or have more abundant fat stores largely reflects environmentally driven plasticity in matura- during childhood enter puberty earlier, experience a more tional tempo. As noted above, in some Western European and intense but briefer period of heightened pubertal growth, and Scandinavian countries, menarcheal age declined from around attain maturity at a younger age (Tanner 1962). As nutritional 17 to 18 years in the mid-nineteenth century to present pop- conditions deteriorate, onset of pubertal growth is delayed, ulation means of 12 or 13 years (Eveleth and Tanner 1976, and the spurt is also protracted such that growth velocities 1990). More recent studies in non-European populations also are slower but spread across a longer period. Collectively, these demonstrate rapid declines in menarcheal age. For instance, findings show that nutrition primarily influences adult size in South Korea, age at menarche declined from 17 years in by influencing growth attainment during fetal life, infancy, 1920 to 12–14 years in 1985, representing a rate of decline and early childhood, when nutritional resources are derived of 0.68 years/decade (Cho et al. 2009), while age at menarche primarily from the mother’s body, thus linking adult size in declined at a similar rate of 0.65 years/decade from 1989 to the present generation with matrilineal nutritional history 2008 in a rural Gambian population (Prentice et al. 2010). (Kuzawa 2005, 2007; Kuzawa and Quinn 2009; Wells 2007). Striking evidence for the sensitivity of menarcheal timing Although nutrition is clearly a powerful influence on hu- to environmental influence is illustrated in growth studies of man variation in growth rate and adult size, it is worth noting girls adopted from orphanages in India or Bangladesh into that important genetic contributions to population variation high-income Scandinavian households. These studies docu- in stature are especially likely at the extremes. For instance, ment relatively high rates of precocious puberty with adoptees the shortest populations in the world are “Pygmy” popula- entering puberty as early as 7 years of age (Proos, Hofvander, tions such as the Efe or Mbuti, whose atypically short stature and Tuvemo 1991; Teilmann et al. 2006). Intriguingly, the likely has at least a partial genetic component that reflects degree to which maturation was sped up in these girls de- convergent genetic selection in response to ecological or mor- pended on their age of adoption: girls adopted at older ages, tality conditions common in rainforest environments (Perry who therefore spent more time in less favorable conditions, and Dominy 2009; Pickrell et al. 2009; Walker et al. 2006a). entered puberty earliest upon environmental improvement Similarly, the tall mean stature of the tallest human groups, (Proos, Hofvander, and Tuvemo 1991). Such findings suggest such as the Rift Valley pastoralist populations, may have a that an individual’s developmental response to environmental Kuzawa and Bragg Plasticity and Human Life History Evolution S375 factors such as nutrition may itself be contingent upon prior organizational effects as potential sources of plasticity in the developmental conditions experienced during early life. Ad- pattern and degree of biological and behavioral difference ditional evidence for such “programming” effects of early between males and females. In a well-characterized birth co- experiences comes from the finding that being born small— hort in the Philippines, males who grew rapidly during the often a result of fetal nutritional deficit or maternal stress age of high postnatal testosterone but not at other early ages during or before pregnancy—predicts earlier maturity espe- gained weight and height faster, matured earlier, and were cially when small birth size is followed by rapid catch-up taller and more muscular as adults (Kuzawa et al. 2010). These growth after birth (Adair 2001; Iba´n˜ez et al. 2000; Karaolis- relationships were greatly reduced or not present for most Danckert et al. 2009; Ong et al. 2009). outcomes among same-aged females. Men who grew rapidly The lack of an easily measured maturational marker in after birth also reported an earlier age at first sex, more life- males comparable to the onset of menses has constrained time sex partners, and more recent sexual activity. Because understanding of both the extent of variability in male pu- these men also showed evidence for greater adult testicular bertal timing and sensitivities of male maturational tempo to sensitivity to luteinizing hormone and higher testosterone lev- environmental change. In the populations for which data are els, the authors speculated that nutritional experiences during available from Walker et al.’s (2006a) tabulation of growth the early postnatal critical period might have lasting effects rates in small-scale societies, age at peak height velocity (a on the magnitude of physical and behavioral differences be- proxy for pubertal timing) ranges from 12 to 17 years (table tween males and females. It is notable that male body size 1). However, few studies have investigated the environmental and related energetic costs were reduced in response to early or nutritional factors that predict variability in male matu- life cues reflecting reduced nutrition, perhaps indicating a rational tempo. A recent study conducted in Germany found capacity to calibrate life history and energetic expenditure as that in accordance with the effect of birth weight and early prevailing nutritional conditions change. Sex-specific sensi- growth among females, males who were born small and gained tivities of growth rate and developmental processes suggest weight rapidly from birth to 2 years experienced peak height that any environmental changes that influence food avail- velocity earlier (Karaolis-Danckert et al. 2009). Similarly, a ability could have differential effects on males and females recent study in a longitudinal birth cohort in the Philippines that could thereby influence the pattern of sexual dimorphism reported that males who experienced rapid weight gain im- within and between populations. mediately after birth reached puberty earlier (Kuzawa et al. 2010). Psychosocial Stress, Maturational Tempo, and Reproductive Scheduling Nutrition, Developmental Plasticity, and the Origins Although the public health and growth and development lit- of Sexual Dimorphism eratures have traditionally focused on the role of nutrition In species marked by sexual size dimorphism, the greater size and hygiene as influences on growth and adult size, more of males leads to correspondingly higher nutritional require- recent work is showing that psychosocial stress can also in- ments. This is believed to help explain why males tend to fluence growth rate and maturational tempo. One link be- exhibit greater responses, both positive and negative, to tween stress and growth stems from the energy burden of the changes in nutritional conditions (Stinson 1985). As a result stress response itself, which may compete with growth, leading of this differential sensitivity, the magnitude of sexual di- to a reduced growth rate (Nyberg et al., forthcoming). morphism in traits such as body size will tend to shift as In addition to such direct resource trade-offs, stress may prevailing nutritional conditions change. For instance, ba- also serve as a barometer of nonnutritional risks, such as boons that self-provisioned off of trash dumps were found unavoidable mortality, which is recognized as shaping the to weigh 50% more than wild-fed baboons (Altmann et al. optimal timing of maturity and reproductive scheduling in 1993). The magnitude of the weight gain was much greater models of mammalian life history evolution (Charnov 1993; in the males than in the females, leading to an increase in Promislow and Harvey 1990). Building from this premise, a adult size dimorphism (Altmann and Alberts 2005). In human long-standing research tradition in developmental psychology populations, adult size in males has similarly been shown to and anthropology has developed evolutionary explanations be more sensitive to changes in socioeconomic condition or for the sensitivity of maturational tempo to parental or other nutritional abundance (Stinson 1985). social cues (Belsky, Steinberg, and Draper 1991; Chisholm Environmental experiences early in the life cycle may be 1993; Draper and Harpending 1982). In these studies, the key to the establishment of these differences. Before birth and observation that girls from harsh or unstable family environ- during the first 6 months of postnatal life, testosterone pro- ments tend to mature earlier is interpreted as evidence that duction is temporarily high in males, which has long-term human maturational tempo is responsive to cues of extrinsic “organizational” effects on male reproductive biology, behav- mortality risk as reflected in attachment quality and parental ior, and body growth (Jost 1961; Phoenix et al. 1959). Recent investment (Chisholm 1993; Ellis 2004; Ellis et al. 2009). Nu- evidence points to these early periods of hormonally driven merous studies have tested this and related predictions (Ellis S376 Current Anthropology Volume 53, Supplement 6, December 2012 and Garber 2000; Hulanicka, Gronkiewicz, and Koniarek mans can be described as a cooperatively breeding species in 2001; Pesonen et al. 2008; Tither and Ellis 2008). For instance, which reproducing females rely on flexible patterns of allo- Chisholm et al. (2005) found that retrospectively reported parental care as a fundamental component of their repro- total life stress explained about 11% of the variance in me- ductive strategy (Hill and Hurtado 2009; Hrdy 2005, 2009; narcheal age in a sample of college-aged women, with higher Kramer and Ellison 2010). Moreover, complicating the tra- stress levels predicting earlier maturity. Quinlan (2003) sim- ditional emphasis on the presumed primary role of men as ilarly found that women whose parents separated before they hunters and providers of calories, recent work highlights evi- were 6 years old matured earlier than girls whose parents did dence for derived neuroendocrine adaptations specific to the not separate. The effect size in these studies is often on the human lineage that encourage direct male care of offspring order of 1–2 months (e.g., Belsky et al. 2010), which is quite (Gettler et al. 2011). In light of these revelations, it seems small, especially when compared with the large multigener- likely that the developmental capacities for facultative ad- ational trends in menarcheal age documented in association justment of life history have been shaped to be sensitive to with nutritional improvements. a much broader range of social cues than previously theorized. Cues of extrinsic mortality may better explain variation in For instance, while transplacental nutrients or maternal breast reproductive scheduling and the intensity of parental invest- milk are important sources of maternal ecological information ment. Age at first reproduction varies widely in the data com- before birth and during infancy (Kuzawa and Quinn 2009), piled by Walker et al. (2006a; table 1), and there is a large after 6 months of age, an increasing proportion of energetic and growing literature showing that children exposed to high needs are met by complementary feeding of specially prepared extrinsic mortality or low parental investment during early foods that may be provided by various relatives or group life not only mature earlier but also start reproducing at a members (Bogin and Smith 1996; Sellen 2006, 2007). To the younger age (Burton 1990; Chisholm et al. 2005; Low et al. extent that nutrition during infancy helps calibrate growth 2008; Nettle, Coall, and Dickins 2010). Nettle (2010) found and reproductive expenditure, in humans these trajectories that across neighborhoods in England, women in the most may be as much reflective of availability of alloparental care socioeconomically deprived communities gave birth for the as any direct maternal metabolic investment. This example first time an average of 8 years earlier than women in the illustrates how theories concerning the role of stress and social most affluent communities, paralleling Wilson and Daly’s cues in life history scheduling and resource allocation need (1997) finding of earlier and more intensive reproductive to address the fact that human children are often highly reliant scheduling in Chicago neighborhoods with the highest ho- on investment from individuals other than biological parents. micide rates. In another study, Nettle, Coall, and Dickins (2011) found that prolonged maternal absence, low paternal Summary: Phenotypic Responses to Changing investment, and many residential moves during childhood Ecological Conditions were independent predictors of earlier age at first birth. Each of these stressors lowered the age at first reproduction by In figure 3, we summarize the pattern of life history traits about half a year, and their effects were additive. that theory predicts in environments with different combi- There is also evidence that individuals who experience nations of nutritional sufficiency and unavoidable mortality stressful environments during childhood invest less in their risk. At one extreme are the most-favorable environments in own offspring (Ellis et al. 2009; Hurtado et al. 2006). For which nutritional sufficiency is high, allowing fast growth and instance, parental investment is reduced under conditions of the attainment of a large adult size despite relatively early harsh, unavoidable stressors such as pathogen loads, famine, maturity (fig. 3A). In this example, early maturity is secondary or warfare (Quinlan 2007). Such reduced investment need to favorable nutrition and a consequent fast growth rate. not be solely behavioral: associations between low socioeco- When populations experience energy sufficiency but cues of nomic status and birth weight have been documented and high extrinsic risk, they are expected to grow quickly but also interpreted in terms of reduced investment in offspring (Coall mature early and thus are predicted to be slightly smaller as and Chisholm 2003, 2010; Nettle 2010). Conversely, in high- adults (fig. 3B). In contrast, low-nutrition and low-risk en- opportunity/low-mortality populations, age at first reproduc- vironments are expected to lead to growth that is sufficiently tion is typically delayed as a response to lowered mortality slow that despite a compensatory delay in maturity, individ- rates and higher costs and future payoffs of investing in off- uals still attain a shorter adult size (fig. 3C). Finally, another spring (Low et al. 2008). Indeed, in many European countries, theoretical extreme is represented by a combination of low age at first birth now routinely occurs in the 30s (ESHRE nutritional resources and high extrinsic risk, which should Capri Workshop Group 2010) even as age at biological ma- lead to relatively early maturation at a small size (fig. 3D). turity has declined because of nutritional and energetic im- Mortality risk influences optimism about surviving into the provements. future to reproduce, and as such there are predicted to be Anthropologists have criticized the focus on the nuclear tandem shifts in relative allocation between maintenance and family as the presumed unit of human child rearing in much reproduction and also in the level of investment in each off- of this work (Chisholm et al. 2005; Hrdy 2009). Instead, hu- spring. Theory predicts that as unavoidable mortality in- Kuzawa and Bragg Plasticity and Human Life History Evolution S377

Figure 3. Summary of developmentally plastic life history changes predicted by different combinations of nutritional sufficiency and cues of threat or extrinsic mortality risk. Comparison group for depiction of birth weight, maturational tempo, and adult stature p high nutrition/low extrinsic mortality risk group (see text for discussion). Not drawn to scale. creases, not only is maturity sped up but also age at first birth, ulations, developmental plasticity has likely been an important which is accompanied by an increase in fertility rate related influence on the phenotypes of earlier members of the hom- in part to a reduction in the interbirth interval and reductions inin lineage. As the ancestors of contemporary human pop- in offspring investment, size, and survival (Belsky, Steinberg, ulations spread across Africa and eventually Eurasia, the local and Draper 1991; Chisholm 1993; Ellis et al. 2009; Nettle, conditions that they faced would have varied in energetic and Coall, and Dickins 2011). This plasticity in both the rate of demographic conditions. Regional or population differences metabolic expenditure and in the scheduling of developmental in such parameters as growth rate, maturational tempo, body and reproductive events helps explain much of the variation size, and sexual dimorphism would have likely arisen via plas- in growth rate, body size, and reproduction across contem- ticity as local or regional populations were confronted by these porary human populations. ecological differences. While at present it is impossible to know whether the same range of plasticity in life history re- sponses was present in ancestral hominins, it is likely that Discussion: Summary and Implications plastic responses were at least similar in kind if not degree. of Life History Plasticity For instance, it is probable that hominin populations that experienced nutritional abundance grew faster and matured Organisms must manage the costs of building a body and the bodies of offspring while calibrating the scheduling of de- earlier at larger body sizes. Similarly, populations in contexts velopmental and reproductive events in response to nutri- with relatively easy-to-exploit transitional foods may have tional resources, the risk of mortality, and other changing or weaned earlier than other groups, leading to the achievement unpredictable ecological conditions (Charnov 1993; Prom- of higher fertility rates. It is also interesting to consider that islow and Harvey 1990; Stearns 1992). It is this environmental males were likely more strongly influenced by improvements variability that necessitates plasticity in growth, development, in energetic conditions than were females, which could in- reproduction, and other components of a species’ life history crease sexual size dimorphism in such environments. Con- strategy. Consistent with this perspective, our review high- versely, in energetically marginal circumstances, maturation lights the overwhelming importance of environmentally was likely delayed, dimorphism reduced, and body size and driven developmental plasticity as a source of contemporary growth rates diminished. Building on this theme, we conclude human life history variation. by considering a final question with central importance to Extrapolating from these findings in modern human pop- attempts to reconstruct hominin evolution and to interpret S378 Current Anthropology Volume 53, Supplement 6, December 2012 the fossil record: what is the relationship between a trait’s plasticity was replaced by trait fixation after many generations plasticity and its genetic evolution via natural selection? of consistent selection for larger jaws. Other studies illustrate how developmental mechanisms underlying such adaptively Did Plasticity Lead the Way in plastic phenotypes can provide the substrate for later species Human Evolution? divergence following longer periods of niche specialization. Among species of spadefoot toads, between-species diversity While biological anthropologists have long considered the role largely traces to ancestral larval plasticity in response to cli- of phenotypic and developmental plasticity as a means of mactic conditions (Gomez-Mestre and Buchholz 2006). Sim- adaptation and a source of within-species variation, recent ilarly, a study of developmental morphology among three- theoretical and empirical work in evolutionary biology has spined sticklebacks found that the phenotypes of divergent emphasized the role of plasticity as an influence on the pace freshwater species mirrored patterns of environmentally in- of evolutionary change and speciation (Kuzawa 2012; West- duced developmental variation in the marine species, an ex- Eberhard 2003). Classically, it was often assumed that plas- tant representative of the ancestor to the freshwater species, ticity decouples genotypes from the specifics of phenotypes, suggesting that plasticity provided the developmental alter- which could reduce the strength of selection on underlying natives from which the various freshwater species diverged as genetic variants (see Ghalambor et al. 2007). Contrary to this they moved into novel environments with different prey types perspective, studies have shown that at least in some instances, (Wund et al. 2008). the most phenotypically and developmentally plastic traits can Each of these examples illustrates how species diversity can evolve most rapidly (Stearns 1983; Wund et al. 2008). For originate from ancestrally shared patterns of plasticity among example, after it was introduced to Hawaii, evolution of the populations exposed to distinct environmental conditions. mosquito fish has been most rapid for traits that exhibited This likely reflects gradual genetic improvement of the in- the greatest plasticity (Stearns 1983). There is similar evidence duced phenotype via natural selection, which can take the that the diversification of fish species in the Canadian lakes form of fixation (loss of plasticity), as a shift in the underlying created after the retreat of the Laurentide Ice Sheet was fa- genetic architecture of the reaction norm (Ghalambor et al. cilitated by plasticity (Robinson and Parsons 2002). Recent 2007; Price, Qvarnstro¨m, and Irwin 2003), or as a compen- evolutionary theory is providing insights into how plasticity sation for some of the physiologic or other costs associated can accelerate rather than dampen the pace of genetic ad- with the induced phenotype (Storz, Scott, and Cheviron aptation (West-Eberhard 2003): when novel environments 2010). first induce phenotypes via developmental plasticity, plasticity By this reasoning, the various modes of adaptation (fig. 1) serves as the source of raw phenotypic variability on which do not simply cover different timescales of variability but may natural selection then acts to shape subsequent genetic ad- also represent a sequence of evolutionary change with less aptation. durable nongenomic modes of biological adaptation allowing For phenotypic plasticity to “lead the way” and facilitate appropriate phenotypic adjustments to novel conditions genetic evolution, several steps must occur, with a typical which are eventually superseded by more durable and efficient scenario involving the following: (1) an organism or popu- genetic accommodation (arrows, fig. 1; West-Eberhard 2003). lation moves into a novel environment or experiences a Indeed, this idea that plasticity-induced phenotypic variants change in an existing environment, (2) plasticity facilitates allow organisms to cope with environmental and behavioral accommodation to the novel conditions by improving the novelty and that more durable genetic change might only later “fit” between phenotype and environment, (3) the genetic and more gradually follow has a long history (Baldwin 1896; architecture of this newly expressed phenotypic variation is Waddington 1953) and has recently been the focus of rekin- then modified by natural selection to improve on the initially dled attention among evolutionary biologists (Sarkar 1999; plastic phenotype or to increase the efficiency with which the West-Eberhard 2003). phenotype is produced. Some examples of plasticity “leading the way” are intuitive. A growing list of studies provides evidence that plasticity For instance, the biomechanical sensitivity of skeletal devel- can serve as an important source of phenotypic alternatives opment shows that behavioral change is accompanied by that are then filtered by natural selection and stabilized changes in trabecular alignment and diaphyseal robustness through genetic change. In an experiment designed to assess (Pearson and Lieberman 2004). The capacity for more dra- the degree of developmental plasticity of jaw morphology matic plasticity-induced realignment of musculoskeletal ele- (Aubret and Shine 2009), tiger snakes from populations re- ments is illustrated by examples of quadrupedal animals born cently introduced to island environments (where larger jaw without forelegs that facultatively adopt bipedal locomotion sizes are favored because of larger prey) showed a greater (West-Eberhard 2003:51–54). Similarly, Japanese macaques capacity for plasticity to match head growth to prey size. Snake trained to perform by walking upright exhibit a humanlike populations with longer histories on the island grew larger gait (Hirasaki et al. 2004), which is facilitated in part by similar head sizes regardless of the size of prey consumed during changes in bone morphology (Nakatsukasa and Hayama 1991, growth and development, showing that the initial capacity for cited in Hirasaki et al. 2004). In light of this work, it seems Kuzawa and Bragg Plasticity and Human Life History Evolution S379 likely that the gradual adoption of locomotor changes among cision. Early weaning facilitated by complementary feeding early hominins was first a behavioral innovation that led to likely “freed up” energy for increased maintenance expen- plasticity-based developmental changes in skeletal morphol- ditures, allowing investment in more durable and long-lived ogy (Hirasaki et al. 2004) that were gradually and incremen- somas. Consistent with this perspective, the longest human tally fixed by genetic evolution (West-Eberhard 2005). life spans tend to accompany reduced reproductive expen- We noted that developmental adaptation in lung volume diture as reflected in lower fertility rate or completed family allows populations raised at high altitude to cope with hypoxia size (e.g., Doblhammer and Oeppen 2003; Gagnon et al. 2009; without having to mobilize homeostatic responses. While de- Jasienska 2009; but see Le Bourg 2007). By analogy, we spec- velopmental adaptation of this type is well documented (Fri- ulate that behaviorally driven decreases in reproductive effort sancho 1977; Moore, Niermeyer, and Zamudio 1998), pop- facilitated the initial expression of longer-lived phenotypes, ulations with long histories living at high altitude show made possible through increased maintenance effort, that evidence for genetic adaptation to hypoxia (Beall 2007). Some were later genetically accommodated by natural selection as of these adjustments appear to compensate for some of the a species-defining trait over a longer, evolutionary time frame. costs associated with plasticity-induced phenotypes (Storz, This sequence of changes contrasts from scenarios posited Scott, and Cheviron 2010), demonstrating how developmental previously in discussions of the adaptive evolution of human adaptation is not only engaged before genetic change but may longevity, which often implicitly or explicitly assume that ge- lead the way for gradual fixation of more durable genetic netic changes that favor increased longevity would have ini- adaptations. tiated this life history pattern (e.g., Hawkes et al. 1998). Extrapolating from these cases, we speculate that similar The extensive developmental plasticity in human life his- principles may apply to the evolution of human life history tory traits reviewed here gains new importance in light of traits. As one example, take the human Pygmy phenotype evidence that plasticity can influence the direction and pace found in populations inhabiting environments characterized of evolutionary change. Many of the traits that differentiate by low nutritional sufficiency (Shea and Bailey 1996) and high the human life history from that of other primates and great unavoidable mortality (Migliano and Guillon 2012; Migliano, apes—including slow growth rate, early weaning, delayed ma- Vinicius, and Lahr 2007; Walker et al. 2006a). Because a slow turity, high fertility, and perhaps even long life span—dem- growth rate is a well-described response to low nutritional onstrate phenotypic variation that traces to developmentally availability (Eveleth and Tanner 1990) while early maturity or behaviorally mediated plasticity in response to environ- may be driven by cues signaling high unavoidable mortality mental factors such as nutrition and cues of unavoidable mor- risk (Ellis et al. 2009), features of this phenotype were likely tality. We have sketched some of the observations that lead induced first by developmental plasticity within individuals us to hypothesize that this environmentally induced pheno- who moved into these ecologies. Evidence for genetic con- typic variation likely preceded and ultimately facilitated ge- tributions to short stature in these populations (Pickrell et al. netic adaptations that gradually stabilized the life history char- 2009) suggests that phenotypes induced by plasticity were acteristics that help define our species. We hope that this eventually accommodated by selection operating on novel review helps stimulate interest in the broader insights that growth-regulating mutations. developmental plasticity may provide into the diversification If some plastic traits have the potential to evolve most and evolution of genus Homo, including the lineage that led rapidly under selection pressure (Stearns 1983; West-Eberhard eventually to modern Homo sapiens. 2003), it is interesting to consider the role of development in the evolution of the derived plastic features of the human life history. Take, for instance, human longevity (Gurven and Acknowledgments Kaplan 2007; Hawkes et al. 1998; Kaplan et al. 2000). The We thank Leslie Aiello and Susan Anto´n for the invitation to delay in senescent processes that extend the human life span participate in this stimulating conference and the Wenner- by several decades beyond that of other extant great apes likely Gren Foundation for sponsoring it. J. M. Bragg was supported required increasing maintenance expenditures (Hawkes 2003; by a National Science Foundation Graduate Research Fellow- Kaplan, Lancaster, and Robson 2003; Kaplan et al. 2000) that ship. almost certainly required reduced expenditure in other do- mains, such as reproduction (Hawkes et al. 1998; Kirkwood and Rose 1991). In humans, any reduction in maternal re- References Cited productive effort is likely facilitated by early weaning of de- Adair, Linda S. 2001. Size at birth predicts age at menarche. 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Conditions for Evolution of Small Adult Body Size in Southern Africa

by Susan Pfeiffer

Discoveries from diverse locales indicate that early Homo was sometimes petite. Small body size among fossil forms is difficult to explain because its existence in modern human populations is not fully understood. The history, ethnography, genetics, and bioarchaeology of KhoeSan peoples of southern Africa are reviewed in the context of their small adult body size. Since the Middle Stone Age, at least some southern African foragers were petite. Throughout the Later Stone Age (LSA; the Holocene), most groups followed a mobile, coastally oriented foraging strategy that relied on small package size foodstuffs. Distinctive skeletal shape and allometry of LSA adult skeletons provide clues about selective factors. Neither dietary insufficiency nor heat dissipation models of selection apply in the LSA context. Energetics and avoidance of serious accidents may be relevant factors. An aspect of life history— the timing of cessation of growth—has been assessed by comparing dental and skeletal development within juvenile skeletons. After a slow start, LSA child growth shows a tempo like that of modern children and no evidence of early maturation. Among fossil or recent forms, small body size should be assessed not only as possible evidence of selection for smallness but also as evidence of the absence of selection for large body size.

Recent discoveries have drawn attention to the importance lineage. The small, lightly built foragers of Holocene South of variability in human body size. The discovery of exceed- Africa are ancestral to the contemporary KhoeSan-speaking ingly small people of late Pleistocene Indonesia (Brown et al. peoples of southern Africa. The ancestors’ skeletons provide 2004; Jungers et al. 2009; Larson et al. 2009; Morwood and a basis for a focused examination of one context of small Jungers 2009) is the best known example, but fossil elements body size. Genetic studies provide corroboration of the tem- at the lower range of modern human size occur among new poral and spatial framework of KhoeSan people, reinforcing discoveries of putative Homo from east Africa and Georgia archaeological evidence of their antiquity and distinctiveness. (Anto´n et al. 2007; Graves et al. 2010; Rightmire 2008; Ruff From this base, information from bioarchaeology can be used 2010; Spoor et al. 2007). Unresolved topics include how much to test hypotheses that are important to evolutionary an- of the size diversity should be attributed to sexual dimor- thropology. phism, how this diversity arose, and whether smallness was a response to environmental variables (McHenry and Brown The Southern African Context 2008; Reno et al. 2010). These discoveries have drawn atten- tion to the need for more focused study of the ecological and behavioral conditions under which isolated human popula- The adult body size of KhoeSan speakers of southern Africa tions may develop small, gracile adult body size. (often referred to as “Bushmen”) is quite small relative to Theories about the selective value of small body size are that of most human groups. With average adult statures doc- numerous, and opportunities to test competing hypotheses umented in historic times at 160.9 cm (men,N p 79 ) and are rare. The population history of a more recent human 150.1 cm (women,N p 74 ; Truswell and Hanson 1976), the lineage can provide a case study, exploring possible selective hunter-gatherers of the Kalahari region may not reach the processes. As well, the morphological characteristics of the pygmoid category (defined as 155 cm; Cavalli-Sforza 1986), recent group may help shape expectations about the mor- but male and female averages approximate the third percentile phology of small-bodied forms from earlier in the human values of Centers for Disease Control 2000 adult statures (www.cdc.gov/growthcharts). As with many other small-bod- ied groups, there is a history of debate regarding whether Susan Pfeiffer is Professor in the Department of Anthropology at the University of Toronto (19 Russell Street, Toronto, Ontario M5S their body size represents adaptation or pathology (cf. Lee 2S2, Canada [[email protected]]) and Research Associate 1979; Wilmsen 1989). Their demographic and anthropomet- in the Department of Archaeology at the University of Cape Town, ric features, including the growth of KhoeSan children, figure South Africa. This paper was submitted 12 XII 11, accepted 21 VI into the modeling of possible selection for smallness. Groups 12, and electronically published 18 IX 12. such as the !Kung (or Ju/’hoansi) and the G/wi have been

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0010$10.00. DOI: 10.1086/667521 S384 Current Anthropology Volume 53, Supplement 6, December 2012 documented in their Kalahari home ranges at latitudes of 20Њ near-coastal South African Cape comes from primary inhu- to 23ЊS. They are typically portrayed as representing a desert- mations of adults and juveniles found in rock shelters, shell or semidesert-adapted population (e.g., Walker et al. 2006). middens, and sand dunes. Single bodies are normally hori- Archaeological evidence (Deacon and Deacon 1999; Mitch- zontally positioned in a flexed posture with no clear preference ell 2002) and genetic studies (Scheinfeldt, Soi, and Tishkoff for side of the body or direction of the head (Inskeep 1986). 2010; Schuster et al. 2010; Tishkoff et al. 2009) indicate that The Cape (including the Cape Fold Mountains) is distinct contemporary KhoeSan speakers are descendants of an an- from the karoo, the eastern savannah and grasslands, in the cestral population that probably extended north at least to frequency of discovered burials. Whether because of cultural the Kalahari and the Zambezi and south to the shores of the differences or because of substantial differences in population South Atlantic and Indian oceans. Physical evidence of the density throughout the Holocene, very few burials of foragers ancestors includes not only sites and artifacts but also exten- are known from beyond the western and southern coasts and sive rock art and open-air engraving sites, their creation span- coastal forelands regions (Morris 1992). All burials are con- ning the Holocene (Barham and Mitchell 2008). Naturalistic sistent with the observation that Holocene Bushman ancestors representations of human figures in the rock art show were consistently petite in stature (fig. 2; Kurki et al. 2008, KhoeSan morphological traits, and the hand prints are of 2010; Sealy and Pfeiffer 2000). Adult body size fluctuates small hands of adult proportions (Manhire 1998; Parkington through time and space as communities dealt with stressors 2003). not yet fully defined (Pfeiffer and Sealy 2006), but no group The greatest concentration of Later Stone Age (LSA) ar- from any time or place exceeded historic Bushman statures. chaeological material has been documented in southernmost A coefficient of variation of 6% for the plotted sample of 172 coastal and near-coastal regions of South Africa, with the maximum femoral lengths (mean p 407.8 mm, SD p 25.3 highest Holocene population numbers found around latitude mm) illustrates the temporal and spatial homogeneity of the 34ЊS (fig. 1). While there are variations in rainfall, topography, population. and food resources throughout the region, the consistency of Skeletal features can be used to extrapolate habitual be- the Mediterranean climate, fynbos, and Afromontane forest haviors, which in turn can reflect morphology. The common plants (Cowling and Hilton-Taylor 1997; Schulze 1997) and occurrence of articular facet modification (Dewar and Pfeiffer marine and terrestrial animals supported a broadly identifi- 2004) and acetabular beveling (Pfeiffer 2011) suggests that able cultural adaptation (Deacon and Deacon 1999; Mitchell LSA people habitually assumed deep squatting postures. This 2002; Pfeiffer and Sealy 2009). Modeling based on contem- would be possible only if subcutaneous fat deposits on the porary genomic diversity indicates that LSA hunter-gatherer lower limbs were minimal. Hence, LSA people were both small populations expanded substantially during the past ca. 41,000 and lean. Skeletal dimensions confirm that at birth, infants years (Cox et al. 2009). Therefore, when trying to understand were not notably small (Harrington and Pfeiffer 2007). Fol- what factors might have acted on adult body size in this lowing a slight lag during the first year, the linear growth of population, evidence from South African LSA archaeology is LSA children followed a normally shaped growth curve lead- more pertinent than evidence from the Kalahari environment ing to petite adult stature (Harrington and Pfeiffer 2008; Pfeif- in which relict populations live today. fer and Harrington 2010). While some regional and temporal Bioarchaeological evidence of the LSA in the coastal and variations in morphology have been documented (Ginter

Figure 1. Map of southernmost Africa, modified from Morris (1992). The area in which most burials are recovered is bounded by a curved line paralleling 34ЊS between the Cape Fold Mountains and the sea. KRM p Klasies River main site; Fy p fynbos biome; Fo p forest biome; Sa p savannah biome. Immediately north of these biomes are types of karoo. Pfeiffer Small Body Size S385

Figure 2. Maximum femur length versus uncalibrated radiocarbon dates for 172 Later Stone Age adult skeletons: west (squares, N p 76), south (circles,N p 50 ), east (triangles,N p 43 ), north coast and interior (stars,N p 3 ). A femur length of 460 mm is roughly equivalent to a stature of 170 cm, or 5 feet 7 inches. Pygmy femur length is ca. 380 mm.

2009; Pfeiffer and Sealy 2009; Stock and Pfeiffer 2004; Stynder, et al. 2007), and a humerus shaft from Border Cave (Pfeiffer Ackermann, and Sealy 2007a, 2007b), there is also evidence and Zehr 1996). There is also some scant evidence of large for a genetically modulated morphology with considerable body size in the early Holocene. One first metatarsal from a antiquity. Genetic studies of descendant populations suggest southern Cape rock shelter (SAM-AP 4208B) is substantially that the KhoeSan lineage is one of Africa’s oldest (Tishkoff larger than other LSA first metatarsals (Pfeiffer and Sealy et al. 1996, 2009). Craniometric research of archaeologically 2006). Dating to about 9,500 years ago, this bone is a reminder derived material indicates a homogeneous population until that pre-Holocene and early Holocene skeletal remains are at least 2000 BP (Stynder, Ackermann, and Sealy 2007a, extremely rare, and we know very little about the population 2007b). Even dental dimensions are distinctively small (Black, at that time (fig. 3). Ackermann, and Sealy 2009). Thus, the factors required for Early literature on southern African prehistory posited a natural selection—namely time and isolation—were available. large, robust ancestral population known as the Boskop It is not clear when adult small body size became established “race.” Before the era of radiocarbon dating, the size of a in southern Africa. Small adult bones are found among the skeleton was treated as an indication of its relative antiquity human remains from some Middle Stone Age sites. Cranial (Drennan 1938; FitzSimons 1926). The Boskop idea was and postcranial specimens from Klasies River main site, dating soundly refuted on cranial grounds (Brau¨er and Ro¨sing 1989; to about 115,000 years ago, have been observed to have ex- Rightmire 1978, 1984; Singer 1958), but the temporal and ternal dimensions comparable to LSA skeletons (Rightmire spatial extent of the small-bodied population across the Af- and Deacon 1991, 2001). This has been corroborated in anal- rican landscape is open to interpretation (Morris 2002, 2003). yses of individual skeletal elements (Churchill et al. 1996; Lam, There may have been morphological variability in the late Pearson, and Smith 1996; Pearson and Grine 1996, 1997; Pleistocene and the early Holocene for which evidence is not Pearson et al. 1998). However, there are other putatively Mid- yet available. Marine-oriented adaptations along lowered dle Stone Age skeletal elements that are not particularly small, coastlines (relative to modern levels; Marean 2010) may ex- such as a fifth metatarsal from Klasies River main site (Right- plain why late Pleistocene archaeological evidence is rare. mire et al. 2006), the late Pleistocene Hofmeyr skull (Grine Based on current evidence, it appears that adult smallness S386 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 3. Adult first metatarsals, plantar view, demonstrating size differences. In the upper left-hand corner is the Middle Stone Age metatarsal from Klasies River main site, estimated maximum length 56 mm, similar to the Later Stone Age (LSA) average. All other metacarpals are LSA. In the upper right-hand corner is an LSA metatarsal (SAM-AP 4208B), radiocarbon dated to about 9500 BP, maximum length 70 mm, well outside the LSA range. Photo by Susan Pfeiffer. existed at the southern coast from 115,000 years ago, and it these distinctive aspects of pelvic shape, accommodating an was typical of the population by about 10,000 years ago, at adequate birth canal despite small external hip dimensions. least in the coastal and near-coastal regions. A recently described case study illustrates the narrow mar- gin of error within which this population operated. The sa- crum of a middle-aged LSA woman shows slight develop- Some Morphological Correlates of Smallness mental asymmetry, with one wing (ala) about 5 mm narrower than the other. Probably subsequent to the strains of child- Pelvic Shape birth, this slightly asymmetrical and narrowed pelvis shows Among modern KhoeSan people, ethnographic evidence in- skeletal indications of joint instability to the point of ebur- dicates that newborns are not smaller than global standards. nation on all pubic and auricular joint surfaces (Pfeiffer 2011). Howell recorded a mean birth weight of 3.08 kg (SD p 0.458) Had the obstetric canal been any further constrained, the birth in 10 newborns, with just one infant falling below the World event might have been fatal to mother and child. Health Organization low birth weight criterion of 2,500 g (Howell 2000). To explore perinatal size in earlier millennia, Physique and Proportions the skeletons of 18 perinates from the LSA were measured. They show dimensions that are well within modern norms Studies comparing skeletal variation in response to ecogeo- (Harrington and Pfeiffer 2008). To explore the relationship graphic factors often inappropriately categorize KhoeSan ma- between pelvic capacity and perinatal size, Kurki (2007) com- terial as derived from 20Њ to 25ЊS, thereby positioning the pared adult body size and pelvic dimensions in small-bodied population as heat adapted. These comparative samples often southern African Holocene foragers (women,N p 28 ; men, rely on small collections of “Bushman/Kaffir/Hottentot” skel- N p 31) with those from historic Portuguese of intermediate etons that are held in Northern Hemisphere museums, ob- size (Coimbra) and larger-bodied adults (Hamann-Todd). tained through purchase or exchange from South African cu- Both males and females in the LSA sample show distinctive rators. Interest in the physical “type” fueled an active trade pelvic shapes. Despite narrow bi-iliac breadths, the small- for decades, with some exploitation of marked graves for bodied forager females have the relatively largest midplane material (Legassick and Rassool 2000). Such selective practices and outlet canal planes, suggesting adaptive allometric re- could lead to morphological biases in those collections. modeling in this small-bodied population. The LSA males Kurki et al. (2008) used a well-characterized archaeologi- also follow this pattern, although with smaller pelvic dimen- cally derived sample (N p 124 , ca. 34ЊS) to demonstrate that sions. The distinctive pelvic shape stays stable during the mid- limb and limb-trunk proportions of that set are the same as Holocene period of body size variation, when some adults those from samples used by earlier researchers. Small values were exceptionally small (Kurki, Stynder, and Pfeiffer 2012). for dispersion around mean values reinforce the consistency The antiquity of KhoeSan skeletal morphology is reflected in of proportionality within the sample. Comparative study Pfeiffer Small Body Size S387 shows that both brachial and limb-to-trunk indices for the and types of food available coupled with the thermoregulatory LSA sample are consistent not with low-latitude but with mid- advantage of a high surface-to-volume ratio. Looking beyond latitude populations, such as those from North Africa. In this Pygmy groups, food limitations may occur in a variety of respect, the presumption of heat adaptation is not supported. habitats. Small size can enhance mobility by reducing the On the other hand, the LSA sample shows some features that metabolic costs of activity so that small bodies can be efficient are normally linked to heat adaptation, including distinctly if the necessary work does not require bursts of intense power. narrow bi-iliac breadth (BIB), low ratio of BIB to femur A hypothesis of recent interest, potentially applicable to all length, and small stature. The authors demonstrate that small- habitats, places body size in a life history framework (Charnov bodied human groups show considerable diversity in skeletal 1993, 2001). It predicts a relationship between the pattern of shape and proportions. They conclude that in zones that are adult mortality risk and body size in which populations with not subject to climatic extremes, climatic factors may play a consistently high risk of young adult mortality will show early less important selective role and that life history or other onset of reproduction, truncating growth to initiate repro- factors may have affected body size and proportions. Sub- duction. Recent work by Migliano and colleagues has ex- sequent research has demonstrated that when various stature panded the focus to include preadult mortality and evidence and mass estimation methods are applied to the LSA sample, for cessation of linear growth at around 13 years for Pygmy results can be quite anomalous (Kurki et al. 2010). Taken women as additional evidence for selection in very small- together, the numerous well-preserved skeletons of the LSA bodied humans (Migliano 2005; Migliano and Guillon 2012; provide opportunities to explore morphological variation at Migliano, Vinicius, and Lahr 2007). Methodological aspects a level of detail that is not possible with less well-provenienced of the Migliano group’s approach have been debated (Becker samples of small-bodied modern humans. et al. 2010; Migliano, Vinicius, and Lahr 2010), but there continues to be interest in the idea that adult small size may result from indirect selection, and there is no question that Allometry of Head and Body Size adaptive features of childhood can be crucial to a group’s The scope of the LSA sample allows exploration of how dif- survival. ferent skeletal components respond to transient stressors. Comparison of cranial centroid data (Stynder 2006) with pel- Evolution of KhoeSan Small Body Size vic and femoral dimensions in a sample of 65 dated adult skeletons demonstrates the relationship between cranial and In the context of the evolutionary pathways toward small body postcranial components. During the mid-Holocene period, size that have been postulated, the LSA skeletal material can when variance increases through the presence of some even be assessed. Given the absence of climatic extremes, the ther- smaller adults, reduced major axis regression of body size on moregulatory rationale is set aside. cranial size indicates negative allometry between head and body size. Femoral length, and to a lesser degree femoral head Dietary Insufficiency diameter, decline more abruptly than cranial size; cranial size is more conserved when growth falters (Kurki, Stynder, and The earliest evidence of small adult body size comes from Pfeiffer 2012). Klasies River main site, where there is evidence for dietary activities that included roasting geophytes (corms and bulbs), Evolution of Small Body Size hunting large game, and collecting shellfish (Barham and Mitchell 2008). Evidence of harvesting of aquatic foods, es- With new evidence of size variability in fossil Homo, attention pecially shellfish, is strongly associated with Middle Stone Age has been given to possible mechanisms of evolution of small sites and continues to be important to coastal and near-coastal human body size (Becker et al. 2010; Bernstein 2010; Froment subsistence throughout the LSA. Access to freshwater, in- 2001; Migliano, Vinicius, and Lahr 2007, 2010; Perry and cluding storage of freshwater in containers, is another theme Dominy 2008; Walker and Hamilton 2008; Walker et al. 2006). from the Middle Stone Age onward. Terrestrial game hunting The adaptive value of larger size is thought to reflect higher remains important, with regional and temporal changes in fecundity among larger females and greater access to mates the species exploited and a general trend toward smaller among larger males as a result of male-male competition. “package size” as human population density increased during These positive features are then balanced against the fitness the LSA. Evidence of light-draw bows (and presumably poi- costs of growing and maintaining large body size (Blancken- son-tipped arrows) is found around the end of the Pleistocene horn 2000). Hypotheses about selection for smallness or the (Parkington 1998; Wadley 1998), although earlier invention absence of selection for largeness have been characterized as has been proposed (Lombard and Phillipson 2010; Wadley, taking four approaches (Perry and Dominy 2008): thermo- Hidgskiss, and Grant 2009). This technology continued regulation, food limitation, mobility, and life history. Pygmy throughout the LSA to the historic era. populations from humid, closed habitats such as tropical rain- If population density was focused along the coast, the ma- forests may be adapted to long-term limitations on amount rine diet may be especially relevant if we assume that relatively S388 Current Anthropology Volume 53, Supplement 6, December 2012 few people were foraging throughout the interior. While the the LSA diet was always nutrient dense, thereby being low in idea of the “aquatic diet” being necessary for encephalization food energy, the evidence is not in place to test this idea with has been laid to rest (Carlson and Kingston 2007; Snodgrass, much rigor. Leonard, and Robertson 2009), a diet high in marine protein does have unique features that could influence selective path- Energetics and Accident Avoidance ways. Thanks to the research into dietary stable isotopes of carbon and nitrogen, chiefly from human bone collagen, re- Much of the coastal and near-coastal terrain of southern Af- gional dietary protein patterns are well characterized (Sealy rica is characterized by hills and mountains of moderate to 2010; Sealy and van der Merwe 1988; Sealy et al. 1987). High high relief (Kruger 1983; Schulze 1997). Foragers needed to in nutrient density (the ratio of nutrient content to total traverse loose, sometimes wet rocky slopes daily. The LSA energy content), marine foods and geophytes are easily gath- subsistence strategy—relying on accessing freshwater, corms, ered, if available. Shellfish and geophytes are relatively broadly and small protein packages—required persistent landscape distributed and could be readily harvested by almost all group scans, persistence hunting (Liebenberg 2006), and transport members, and so it is difficult to restrict access to them. Ready of parcels of variable size to camp sites that were frequently access to reliable beds of shellfish could have sustained the moved. Being mobile was probably more important than be- nutrition of mothers during prolonged lactation (Clayton, ing particularly strong. In similarly rugged landscapes else- Sealy, and Pfeiffer 2006) and formed part of an egalitarian where, skeletons of foraging groups show relatively high prev- subsistence framework. However, stable isotope evidence alence of healed bone fractures (Kilgore, Jurmain, and van from the region of highest marine exploitation, the south Gerven 1997). Breaks of arm bones and clavicles are associated coast, indicates a time in the mid-Holocene when the land- with accidents rather than interpersonal violence and are often scape was divided between foragers who had access to Cape quantified to study trauma in past populations (Roberts and fur seals and other high trophic-level foods and neighboring Manchester 1995). Accidental fractures tend to be more com- groups who lacked that access (Sealy 2006). This is a reminder mon among hunter-gatherers than among more sedentary that access to coastal resources could be restricted, thereby groups. An assessment of 1,353 major long bones from 152 shifting interpersonal competition from a scramble to a con- LSA adult skeletons showed 13 healed fractures, all of arm test. Another example of apparently stressful dietary condi- bones except for one clavicle and one distal tibia (at the medial tions comes from the western coast during the “megamidden malleolus). This is a comparable pattern of distribution to period,” ca. 3000–2000 BP (Jerardino 2010). Evidence of large that seen in other hunter-gatherers but a lower prevalence open sites plus intensification of harvesting of terrestrial and (Pfeiffer 2007; fig. 4). It is possible that a lighter, smaller body marine foods is combined with a peak in numbers of human is less likely to sustain serious injury from slips and falls. burials and some evidence of interpersonal violence (Pfeiffer Adult mortality has an effect on healed-fracture data because 2013). It appears that increased human numbers outstripped it is a cumulative measure. That is, a longer-lived group may local resource availability, although it is difficult to identify show a higher prevalence of healed fractures. It can also be what dietary elements were the limiting factors. Protein argued that hazards such as a broken ulna or clavicle are not sources do not appear to have been completely depleted, but likely to affect fitness. Nevertheless, this evidence suggests that perhaps the supply of carbohydrates (geophytes) was inade- the sequelae of serious injury—including shock, blood loss, quate. and immobility—may have been less common than would In brief, there is no evidence for prolonged periods of be the case among groups with higher average adult body significant shortages either to specific dietary components or mass. to food energy more generally. The topic of climate stability is also pertinent. Current reconstructions of late Pleistocene Life History and Holocene climate across southern Africa identify no par- ticularly rapid or dramatic changes. Southern African deep- There are several aspects to this theoretical approach. One sea cores document temperature fluctuations on a scale of 2Њ aspect has been explored within the LSA context, that of a to 4ЊC (Farmer, deMenocal, and Marchitto 2005) and a rel- shorter childhood period to allow earlier onset of reproduc- atively humid period in the late Pleistocene followed by a tion. While cross-sectional growth data from skeletons cannot period of gradually increasing aridity from 3800 cal BP to be used to track the adolescent growth spurt (Sinclair and very recent times (Chase et al. 2010; Quick et al. 2011; Scott Dangerfield 1998), cross-sectional plots of achieved linear et al. 2012). growth coupled with the timing of epiphysis closure, can be Given the absence of pervasive skeletal indications of di- useful. Child growth during the South African LSA has been etary insufficiencies and no strong correlations between adult studied from various perspectives using a substantial sample body size and stable isotope values (Pfeiffer and Sealy 2006), of immature skeletons with documented archaeological con- it appears that nutrient levels were generally adequate. text, age at death, and (often) radiocarbon date. Juvenile re- Whether food energy was adequate is a more difficult ques- mains have been described and analyzed in bioarchaeological tion. While there may be some merit to an argument that descriptions and analyses (Harrington 2010; Pfeiffer and van Pfeiffer Small Body Size S389

Figure 4. Prevalence (%) of healed fractures for the most common accidentally broken bones, the radius and ulna. The first three comparators are hunter-gatherer groups: Kulubnarti, Nubia (Kilgore, Jurmain, and van Gerven 1997); Atacama, Chile (Neves, Barros, and Costa 1999); and central California (Jurmain 1991). Numbers 1–6 are medieval British sites (Roberts and Manchester 1995). Number 5, Chichester, was a hospital site. der Merwe 2004; Sealy et al. 2000). No instances of periostitis the proportion of adult growth that would be expected for or other infectious processes have been found (Pfeiffer 2007). living healthy children (Harrington and Pfeiffer 2008). The The rock shelter burial of one infant who had been suffering absence of growth lag before death suggests that causes of from a metabolic disorder for a prolonged period before death death were typically acute conditions rather than chronic con- indicates that poor health before death did not preclude nor- ditions where death would be preceded by a slowing or ces- mal burial practices (Pfeiffer and Crowder 2004). These ob- sation of growth. Assessment of long bone growth arrest lines servations enhance confidence in the sample’s validity for (present in 25 of 53) and cribra orbitalia on juvenile frontal health-related studies. bones (present in 15 of 38) indicates that these signs of non- The growth of immature LSA skeletons has been ap- specific stress occur, but they are neither ubiquitous nor severe proached as a cross-sectional sample (Harrington and Pfeiffer (Pfeiffer 2007). 2008). From initial scrutiny of 25 juvenile mandibular den- Femur lengths of juveniles show that adult lengths are not titions (15 of which were radiographed), we determined that achieved until dental ages of about 16 years (fig. 5), at which the order and relative timing of deciduous and permanent time skeletal maturation remains incomplete. Maturation and tooth development were fully congruent with developmental attainment of femur lengths representing probable adult stat- standards (Matzke 2000). This congruence supports reliance ure occur at ages that are compatible with a mean age at first on age estimates based on dental development (Smith 1991). reproduction of 19.5 years, as noted among the !Kung by While the teeth of southern Africans have been shown to Howell (Howell 2000), because menarche occurs after the complete crown formation at slightly earlier ages than teeth peak in height velocity, and full sexual maturation occurs a of North Europeans (Reid and Dean 2006), that collection of year or two after menarche (Sinclair and Dangerfield 1998). diverse black African tribes is genetically distinct from the Among LSA populations, this suggests that child growth pro- LSA population. Hence, if there is bias in the age estimates, ceeded at a normal tempo (assuming progress toward a small its direction and magnitude remains unknown. It has been adult end point) and that growth did not cease prematurely. reported that the error associated with dental age estimation methods is about 1 year and that the tendency of these meth- Discussion and Conclusions ods is to slightly overage the younger children and underage older children (Liversidge, Smith, and Maber 2010). Many societies tend to favor tallness as an indicator of ma- Focusing on juveniles for whom dental maturation can be turity, strength, and even leadership potential (Ekwo et al. used to estimate age at death, LSA data show that the linear 2005). Groups of small people or small individuals have been growth of juveniles who failed to survive falls within 1 SD of alternately portrayed as anomalies of growth perturbation or S390 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 5. Percentage of adult linear growth (femur length measurements) attained among Later Stone Age juveniles with age estimates (years) based on dental maturation. Shaded boxes summarize diaphysis measurements; the open box summarizes mea- surements of complete femora (diaphyses and epiphyses) of the oldest juveniles. Midlines indicate medians; boxes indicate first to third quartiles; whiskers indicate the range excluding outliers, which are shown as circles. Figure prepared by L. Harrington. the result of evolutionary adaptation (Schell and Magnus ideas could be explored further, especially if new information 2007). In the case of KhoeSan-speaking people, bioarchaeo- and approaches arise. logical evidence provides a framework for understanding the The exploration of life history factors as the basis of a group’s origins. The locus of population density appears to selective framework could be taken further. Adult propor- have been substantially south of the location where relict com- tionality is not temporally or spatially variable, suggesting munities live today. This genetically unique population consistent canalization during development. Assessment of evolved outside the range of climatic extremes, so their mor- juvenile growth, comparing the completion of long bone phology is not likely to reflect a strong influence of extreme growth against dental development, indicates no early trun- temperature or humidity. The long period of consistently cation of growth. Assuming that puberty and long bone small adult stature, documented through study of archaeo- growth were linked in past peoples as they are today, this logically derived skeletons, is inconsistent with the idea that suggests that onset of reproduction was not early. However, smallness reflects stressors within each individual’s lifetime. another perspective would be to argue that through slowed It is very improbable that for thousands of years, each in- growth, LSA children were demanding less food energy, dividual failed to achieve her/his body size potential in vir- thereby leaving it for the reproducing adults. Future work to tually the same way. The consistency of growth tempo and accurately determine the adult ages at death is needed to the low coefficients of variation associated with linear mea- explore the possibility of early adult mortality. Questions re- sures suggest canalization (Waddington 1957). The smallness main about the evolutionary value of postreproductive group of LSA people and their KhoeSan descendants appears to members (Hawkes 2010) and the adaptive value of equitable represent adaptation, but to what? gendered roles (Gurven and Hill 2010). Given the strong roles The LSA people had access to a wide range of food resources identified for older, postreproductive members of KhoeSan over thousands of years, although there may have been locales societies (Howell 2010), it seems unlikely that this class was and periods in which shortages occurred. The framework for rare in past generations. postulating small stature as a response to pervasive food short- An alternate approach to the question of KhoeSan smallness age—either specific nutrients or collective food energy—is would be to look at it as the product of the removal of not apparent. Although much of the landscape is potentially selection for large size coupled with isolation and stabilizing treacherous to wide-ranging foragers, it seems improbable selective pressures favoring smallness. Sexual selection for that avoidance of serious injury would have been a strong large males can be mitigated by cultural practices, thereby factor influencing survival and reproduction, although these removing that directional pressure. Selection for larger females Pfeiffer Small Body Size S391 through fecundity can be mitigated through shape adjust- Based on parallels with the LSA example, we can identify ments that optimize obstetric canal volume. Assuming that ecological factors that may have supported small body size the KhoeSan ancestors were the only human inhabitants of in some early Homo populations. Geographic isolation for a a large region for at least 10,000 years, perhaps substantially prolonged period is an important permissive variable. The longer, and assuming a small founding population at some dynamics that are understood within island biogeography point, smallness may have arisen by chance or in response to (Brown 1995) may apply to contiguous regions if there are selective pressures at that earlier time. Those pressures may significant physical barriers, such as mountains, and if pop- have related to energetics or diet or some other factor. There ulation density is well within the area’s carrying capacity. is some evidence to support this hypothesis. A distinctive Dmanisi may be an example of this among known early Homo pelvic shape accommodates relatively large infants, thereby sites. Possible selective variables include food resources with reducing the selection for larger women through fecundity. small package size dispersed so that interpersonal competition A lightweight tool kit that relies on poison-tipped arrows and is a scramble rather than a contest. Small body size could be the practice of persistence tracking may reduce or reverse the linked to a social system with little emphasis on strength selection for larger men through muscular strength. Rock art competition among males so that larger males have little or portrays men as lean, muscular, and small relative to animals. no reproductive advantage. Uneven, irregular, or challenging Ethnographically, R. B. Lee documented that smaller hunters topography could also be a relevant variable insofar as serious were more successful than larger men (Lee 1979). George personal injury can reduce fitness. A subsistence system based Silberbauer, when asked about sexual selection among the on small package resources can be fashioned within many G/wi, said that tall men were viewed as “geeks,” that is, po- ecological contexts and could be relatively flexible when en- tentially less desirable mates (G. Silberbauer, personal com- vironmental conditions shift. As we learn more about the munication, 1994). natural history of small-bodied humans, we can weigh the Directional selective factors appear to have elicited small relative importance of an array of conditions possibly asso- body size among some humans in this region during the ciated with natural selection for that bauplan. Pleistocene before ca. 110 ka. The evidence regarding what such forces might have been is unavailable. Changes in sea level (Carr et al. 2010) and some climatic shifts may be im- Acknowledgments plicated. During the Holocene, the low variance in skeletal I thank the organizers of the Wenner-Gren 2011 spring sym- measures indicates the operation of stabilizing natural selec- posium for including me in this very stimulating dialogue. I tion in an environment where climate and food availability am indebted to colleagues and to curators of South African do not appear to impose particular constraints on survival. institutions; they have guided me through study applications A biocultural mix of dietary constraints and behavioral ad- and details of archaeological context. They include Judith aptations may be the most plausible explanation for the Ho- Sealy, Chopi Jerardino, Helen Kurki, Lesley Harrington, Alan locene adaptive pattern. In the most recent millennium, con- Morris, Johan Binneman, and James Brink. Jaime Ginter tact with black Africans and subsequently with Europeans kindly provided unpublished data for figure 2. The Social altered the picture dramatically. From that point onward, Sciences and Humanities Research Council of Canada has small body size was one of several disadvantages borne by the supported much of my work. Bushmen. 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Growth, Development, and Life History throughout the Evolution of Homo

by Gary T. Schwartz

For over a century, paleoanthropologists have listed the presence of prolonged periods of gestation, growth, and maturation, extremely short interbirth intervals, and early weaning among the key features that distinguish modern humans from our extant ape cousins. Exactly when and how this particular scheduling of important developmental milestones—termed a “life history profile”—came to characterize Homo sapiens is not entirely clear. Researchers have suggested that the modern human life history profile appeared either at the base of the hominin radiation (ca. 6 Ma), with the origins of the genus Homo (ca. 2.5 Ma), or much later in time, perhaps only with H. sapiens (ca. 200–100 Ka). In this short review, evidence of the pace of growth and maturation in fossil australopiths and early members of Homo is detailed to evaluate the merits of each of these scenarios. New data on the relationship between dental development and life history in extant apes are synthesized within the context of life history theory and developmental variation across modern human groups. Future directions, including new analytical tools for extracting more refined life history parameters as well as integrative biomechanical and developmental models of facial growth are also discussed.

Introduction this transition occurred and thus determine whether the hu- man life history package appeared as part of a suite of fun- damental adaptations at the base of the hominin clade; Compared with our closest living relatives—the extant great whether it evolved somewhat later, perhaps tied to the re- apes—the sole surviving member of the genus Homo possesses organization of the cranium and postcranium that charac- a suite of features that make us quite distinct, including un- terized the earliest members of the genus Homo; or whether usually large brains, obligate bipedality, a reliance on the pro- it appeared even later still, perhaps in the last hundred thou- duction and use of tools, and a strikingly different life history. sand years or so. Generally, patterns of mammalian growth, development, and The last decade has been marked by a tremendous amount life history are thought of as lying along a spectrum some- of research into reconstructing the pattern of growth, devel- where between two end points that are colloquially referred opment, and life history of extant great apes, australopiths, to as “live fast, die young” and “live slow, die old.” Modern and early to later members of the genus Homo. Novel ana- human life history incorporates elements of both schedules: lytical techniques, imaging modalities, and hard-fought ob- long gestation periods, altricial offspring, enlarged brains, servational data from naturalistic studies of great apes can slow maturation rates, increased life span, and protracted pe- now be synthesized to paint a broad view of the evolution of riods of offspring dependence are suggestive of a “live slow” life history throughout the course of the human story. The strategy, whereas relatively early weaning, short interbirth in- goal of this paper is to review the current state of knowledge tervals, and the ability to overlap births (resulting in the pres- of the evolution of human life history within the comparative ence of multiple offspring) are suggestive of a “live fast” sched- context of what we know about these attributes in populations ule. Of interest to paleoanthropologists is whether this of extant hominoids and fossil hominins. These data will be “modern human life history package” evolved as a single de- evaluated within the light of what is known about primate velopmental module or accumulated in a mosaic fashion life history, ecology, diet, and so forth, and will be used to (with different attributes appearing at different points in help suggest future avenues of inquiry into studies of hominin time). Furthermore, it is of great interest to understand when life history.

Gary T. Schwartz is Associate Professor of Anthropology at the What Is Life History? Institute of Human Origins at Arizona State University (900 South Cady Mall, Tempe, Arizona 85287-2402, U.S.A. [[email protected]]). By marrying the principles of organic evolution with those This paper was submitted 12 XII 11, accepted 28 VI 12, and of theoretical population ecology, life history theory seeks to electronically published 20 XI 12. understand the general rules that account for the tremendous

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0011$10.00. DOI: 10.1086/667591 S396 Current Anthropology Volume 53, Supplement 6, December 2012 variation in life cycles across all organisms (Stearns 1992). In 2012). For instance, in a survey of 22 small-scale societies, short, life history theory views variation in the pattern, se- Walker et al. (2006) found that populations experiencing low quence, and pace of growth as the outcome of how natural survivorship (i.e., high mortality) during the subadult years selection operates on a series of trade-offs in the allocation were characterized by an overall pattern of accelerated de- of an organism’s energetic budget. Smith and Tompkins velopment and thus reached the important developmental (1995:257) emphasized the importance of these trade-offs in milestones of puberty, menarche, and first reproduction at defining life history as the allotment of an organism’s energy relatively earlier ages. Interestingly, new evidence suggests that “towards, growth, maintenance, reproduction, raising off- adverse early life conditions in humans, ranging from the spring to independence, and avoiding death.” Bogin (1988: biological (low birth weight for gestational age, breast-feeding 154) suggested that the life history of a species can be viewed duration) to the psychosocial (separation anxiety, family res- as a strategy that determines “when to be born, when to be idential relocation, degree of parental involvement) mediate weaned, how many and what type of prereproductive stages reproductive scheduling by accelerating the age at first preg- of development to pass through, when to reproduce, and nancy (Nettle, Coall, and Dickins 2010 and references when to die.” Central to these and other definitions is the therein). A more detailed understanding of exactly how such notion that energy is a limiting commodity that is distributed environmental constraints, broadly speaking, shape life his- toward growth, maintenance (of tissues), and/or reproduction tory variation across human populations would be extremely throughout the lives of individuals (Bogin and Smith 2000; informative. Similarly, uncovering the role developmental Roff 2002; Stearns 1992). In a strict Darwinian sense, selection plasticity (the capacity of an individual to modify its ontogeny should favor an apportionment of energy in ways that reduce in response to shifting environmental conditions on a fairly mortality and maximize fecundity. Thus, the application of rapid timescale—days, months, or a few years) plays in gen- life history theory to ontogenetic studies seeks to understand erating novel phenotypes that enhance the evolutionary po- how the scheduling of key events in an organism’s life cycle tential, or “evolvability,” of developmental systems may help (including but not limited to gestation length, age at weaning, illuminate the process(es) whereby selection assembled the interbirth interval, timing of maturation, age at first repro- total package of modern human life history attributes over a duction, frequency of reproduction, fecundity, and life span) period of several hundred thousand years (e.g., see Kuzawa better enable some individuals of a species to minimize mor- and Bragg 2012; West-Eberhard 2003). tality risks more effectively and thus increase overall fitness. This scheduling or sequence of events can be thought of as Reconstructing Hominin Life History Profiles a “life history profile” and is, effectively, the product of how developmental variables (e.g., growth rates, age at skeletal When viewed in the light of life history theory, it might seem maturation) interact with demographic variables (e.g., sur- impossible to infer such reproductive, physiological, demo- vival, reproduction, population growth) to influence individ- graphic, environmental, and behavioral parameters from fos- ual survival (Godfrey, Petto, and Sutherland 2002; Ross 1998). silized remains. However, the vast majority of the hominin Aside from being viewed as an energetic trade-off, a species’ fossil record comprises isolated teeth and dentognathic re- life history profile is directly linked to rates of extrinsic mor- mains, and many of the important life history variables dis- tality, which is defined as the risk of death as a result of cussed above are tightly linked with aspects of developing environmental conditions such as predation, disease, acci- dentitions. As a result, studies on the timing of particular dents, and so forth (Stearns 1992). High extrinsic mortality dental developmental events figure prominently in paleoan- should favor shorter life spans, while lower extrinsic mortality thropological investigations that aim to reconstruct the life results in a larger proportion of the population surviving to history profiles of fossil primates and hominins (e.g., Beynon older ages. Compared with great apes, human populations et al. 1998; Bromage and Dean 1985; Conroy and Kuykendall are able to ramp up reproductive success because our life 1995; Conroy and Vannier 1991a, 1991b; Dean et al. 1993, history profile is characterized by lower mortality rates, which 2001; Godfrey et al. 2001; Mann 1975; Robson and Wood has the effect of slowing down rates of maturation, delaying 2008; Schwartz et al. 2005; Smith 1989, 1993; Smith, Crum- reproduction, and thus spreading it out across later years. For mett, and Brandt 1994; Smith, Gannon, and Smith 1995; a large primate, a strategy including a prolongation of growth Smith et al. 2010a, 2010b; Zihlman, Bolter, and Boesch 2004). and development comes with some risk, as evidenced by re- Ever since the pioneering studies on primate growth by cent data on the inability of orangutan populations (with late Schultz (1935, 1940, 1960) and Sacher (1959, 1975, 1978; ages of reproductive maturity and interbirth intervals of ∼7 Sacher and Staffeldt 1974), evolutionary biologists and paleo- years) to recover from even slight reductions in population anthropologists have linked aspects of somatic and neural density (Knott, Thompson, and Wich 2009). At a finer scale growth rates to reproduction, metabolism, and life span in of comparison (i.e., across populations of modern Homo sap- an attempt to reconstruct aspects of early hominin matura- iens), differences in subsistence strategies, environments, and tion. The first study to flesh out the relationship between the mortality rates comingle to produce tremendous variation in sequence and pace of dental development and aspects of life patterns of human ontogeny (e.g., Migliano and Guillon history was by Schultz (1949), who observed that the per- Schwartz Life History Evolution in Homo S397 manent replacement molars emerge into the oral cavity before striations and Retzius lines in the enamel and the correspond- the shedding of deciduous teeth in faster-growing primates. ing von Ebner and Andresen lines in dentine (Dean 1987, This phenomenon has since been dubbed “Schultz’s rule” 2006; Schwartz and Dean 2000; Smith 2006, 2008). Careful (Smith 2000) and accurately relates dental emergence se- counts of these lines reveal the time taken to form a tooth, quences to maturation rates across primates as a whole, es- including the tooth crown and however much root had pecially anthropoids (see Godfrey et al. 2005). It also allowed formed at the time of death, thereby providing a detailed paleoanthropologists an opportunity to evaluate when the chronology of dental development that can, under the right modern human developmental pattern (i.e., tooth crown de- circumstances, also yield precise ages for key events such as velopment and emergence sequence) first appeared during molar emergence (e.g., Beynon, Dean, and Reid 1991; Dean the course of human evolution as it could be used to assess et al. 2001; Dirks 1998; Kelley and Schwartz 2010; Smith, the relative developmental status of juvenile hominins (Smith Reid, and Sirianni 2006; Smith et al. 2010a, 2010b). 1986). Along with other studies examining the sequence of Data on molar emergence ages in hominins, while rare, are dental development and emergence in hominins (e.g., Conroy becoming more accessible, especially with the application of and Kuykendall 1995; Conroy and Vannier 1991a,1991b), it new, noninvasive imaging modalities that allow access to the became increasingly clear that the earliest hominins, and in- internal dental growth record (e.g., Smith et al. 2007b, 2007c, deed even fossil species of the genus Homo, were characterized 2010b). While it is critically important to establish a growing by dental developmental patterns, and thus maturational pro- database on molar emergence ages in key hominin taxa, it is files, more similar to extant apes (at the time, meaning pre- also necessary to chart more fully dental developmental var- dominantly Pan troglodytes). This work was extremely im- iation in extant hominoids and to interpret that variation in portant because the prevailing paradigm held that all light of a particular species’ population ecology, demography, hominins, including the earliest australopiths, possessed a and life history. For now, good population data on molar modern humanlike maturation profile with the attendant pro- emergence ages exist only for P. troglodytes (Anemone, Moo- longed infant and childhood dependency that was so fun- ney, and Siegel 1996; Conroy and Mahoney 1991; Kuykendall, damental to producing the social, cognitive, and cultural com- Mahoney, and Conroy 1992; Nissen and Reisen 1945, 1964; plexity that serves as the hallmark of our species (Mann 1975). Reid et al. 1998; Schultz 1940; Smith et al. 2007a, 2010a; Given the intimate relationship between brain size, life Zihlman, Bolter, and Boesch 2004; though see Dirks 2003 and span, and rates of maturation and the plasticity of certain Dirks and Bowman 2007 for individual hylobatids; and Bey- reproductive parameters, Smith (1989) reasoned that the den- non, Dean, and Reid 1991; Winkler, Schwartz, and Swindler tition should be one of the more stable markers of growth 1991; and Kelley and Schwartz 2010; and Willoughby 1978 given its high heritability and resistance to environmental for individual gorillas and orangutans). There is also a grow- perturbations. She conducted a broad, interspecific compar- ing awareness that emergence ages for captive primate pop- ison of dental maturation with various life history variables ulations may be slightly advanced compared with wild pop- and revealed the extremely high correlation between brain ulations (e.g., Kelley and Schwartz 2010; Smith and Boesch size and the age at first molar (M1) emergence on the one 2011; Zihlman, Bolter, and Boesch 2004), suggesting at the hand and between M1 emergence age and various life history very least some caution in relying on databases derived ex- variables related to reproduction (gestation length, ages at clusively from captive colonies. Expanding our knowledge of weaning and first breeding, life span) on the other. This sem- dental developmental variation across natural fertility pop- inal study laid the groundwork for linking aspects of the ulations of modern humans is another key element (e.g., Liv- timing or pace of dental development to critical components ersidge 2003) and will ultimately allow more fine-scale tests of a species’ life history and, equally importantly, provided a of how population-level variation in aspects of dental devel- chronological marker for probing the maturation rates of fos- opment (e.g., M1 emergence age) relates to that for various sils if information on the timing of key dental development life history attributes. events (i.e., M1 emergence) could somehow be retrieved from the fossil record. Early Homo At around the same time, a group of paleoanthropologists began to mine the rich vein of growth data contained within It has generally been viewed that the origin of the genus Homo teeth. Based on some foundational work in dental hard tissue was characterized by a trend away from bipedal apelike forms biology (Boyde 1963, 1964), a series of investigations began to obligate terrestrial bipeds who were endowed with much to appear that documented how to retrieve information on larger brains and the capacity to manufacture and use stone the absolute timing of dental development utilizing the tool technology and who also exhibited a shift in dietary and growth record contained within enamel and dentine. The cells foraging adaptations. Fossil representatives of the genus Homo that secrete the dental tissues enamel and dentine (for reasons were first described by Leakey, Tobias, and Napier (1964) from of brevity, cementum is not discussed here) leave a record of material derived from Bed I, Olduvai Gorge, Tanzania, and their activity in the form of short- and long-period incre- were dated to 1.8–1.7 Ma. These authors viewed the material mental growth lines. These include, respectively, daily cross as distinct from australopith material given its possession of S398 Current Anthropology Volume 53, Supplement 6, December 2012 a larger, more globular and gracile cranium with a cranial What Do We Know about Life History in Early Homo? capacity 1600 cm3 and a concomitant reliance on the habitual In short, not as much as we would like to know. This is in production and use of lithic technology. Fossil evidence for part because an organism’s “strategy” for parsing out energy even earlier representatives of Homo includes mostly isolated for purposes of growth, maintenance, and/or reproduction specimens from South Africa (Sterkfontein, ca. 2.6 Ma), (i.e., their gestation length, age at weaning, interbirth interval, Kenya (Chemeron, 2.4 Ma), and Malawi (Uraha, ∼2.5–1.9 timing of maturation, frequency of reproduction, fecundity, Ma), with a maxilla from Hadar, Ethiopia (A.L. 666-1, 2.3 and life span) is not a durable part of the fossil record. Im- Ma) being the best candidate for the earliest Homo (Kimbel, portantly, there are now some good attempts at deriving ges- Johanson, and Rak 1997; see recent review in Kimbel 2009), tation length, interbirth intervals, and weaning age from hard thereby extending the origin of Homo further back in time tissue remains for certain primate taxa (see Dirks et al. 2010; to at least 2.5 Ma, to a time when Africa was undergoing a Humphrey et al. 2008a, 2008b; Schwartz et al. 2002), though transition toward cooler, drier conditions with an increase in how fruitful they will be if applied to fossil human taxa is more open habitats (see also Potts 2012). Regardless of the currently unknown. precise time and location of the origins of our own genus— For several decades, paleoanthropologists have viewed the though it is generally held to be within the critical interval evolution of modern human growth, development, and life of 3–2.0 Ma—many paleoanthropologists support the usage history through the lens of a comparative dichotomy between of Leakey, Tobias, and Napier’s morphological-behavioral modern Pan on the one hand and modern humans on the complex (increased brain size, stone tool production) as the other. This is not unreasonable given that recent DNA analyses sole criterion for inclusion within the genus and would there- support a Pan-Homo clade to the exclusion of all other hom- fore recognize three securely attributed representative species inoids (e.g., Bradley 2008; Ruvolo 1994). It is interesting, of premodern early Homo in Africa: Homo habilis (1.9–1.4 however, that several early hominin specimens exhibit striking Ma), Homo rudolfensis (1.9–1.8 Ma), and Homo ergaster and anatomical similarities with extant gorillas (Dean 2010). For Homo erectus (1.9–0.9 Ma; see Anto´n 2012; Kimbel 2009; and instance, certain aspects of scapular morphology in the re- Wood and Lonergan 2008 for recent reviews of the fossil cently discovered Dikika skeleton and the mandibular mor- evidence of Homo). phology of other Australopithecus afarensis specimens bear a Not everyone would include the “transitional” species of close resemblance to the condition in extant Gorilla (Alem- H. habilis and H. rudolfensis within the genus Homo.Wood seged et al. 2006; Rak, Ginzburg, and Geffen 2007). Unfor- and Collard (1999) maintained that all members of a genus tunately, not enough is currently known about development should occupy the same adaptive zone (and thus possess a in Gorilla, or developmental variation among Gorilla spp., to similar adaptive strategy) and proposed a set of criteria for speculate on the importance of this for understanding how the inclusion of any species into the genus Homo. Based on best to model the mosaic pattern of great ape morphology/ its large body size, body proportions, reduced dentition, and dental development evident within australopiths and perhaps commitment to long-range bipedality, they recommend that early Homo (Dean 2010). H. ergaster be the earliest hominin to satisfy their adaptive What we have been able to reconstruct about life history criteria, thereby relegating both of the earlier “Homo” species in early Homo, and indeed for several earlier and later hom- to the genus Australopithecus. Recent metric analyses, how- inins, is based on estimates of the pattern and pace of dental ever, demonstrate similarities in some of these anatomical development or on the tight association between brain size complexes (limb lengths and proportions) and suggest that and life history (or some skeletal correlate of life history). reassigning these species may be unwarranted (Holliday Thus, a series of key questions related to understanding the 2012). ontogeny of early Homo can now be asked. Is there evidence Regardless of generic assignations, many of the hominins that the earliest hominins (including the earliest members of before 2.5 Ma can be broadly characterized as relatively small- the genus Homo) matured in a way—had a chronology of brained, large-toothed, non–stone tool producing human an- dental development—that was similar to extant chimpanzees cestors (though recent work suggests that some australopith (and moreover, do all extant apes mature, dentally, in an taxa may have been using stone tools; McPherron et al. 2010). identical manner)? Do the early hominins differ in the chro- As such, it may seem reasonable to postulate some sort of nology of tooth emergence in ways that might suggest de- grade shift in life history during this critical interval. Alter- velopmental heterogeneity in their reconstructed life history natively, species of early Homo (and Australopithecus for that profiles? Do the earliest representatives of the genus Homo matter) might each possess slightly different life histories, as exhibit dental developmental chronologies that align them more closely with the penecontemporaneous australopiths or these profiles are closely calibrated to local environment and with geologically younger Neanderthals and archaic Homo ecologies, and the critical time interval for the evolution of sapiens populations? Homo (3–2.0 Ma) is characterized by magnified climate var- iability and thus variable adaptive settings (deMenocal 1995; Inferences from extant ape development. We know more about Potts 1996, 2012). chimpanzee growth, development, diet, and ecology than we Schwartz Life History Evolution in Homo S399

Table 1. Comparative life history and M1 emergence age (years) in extant great apes and hu- mans

Variable Gorilla Pan Pongo Homo Age at first reproduction 10.1a (51.3) 14.3b (72.6) 15.7c (79.7) 19.7 Interbirth interval 4.3 5.8b 6.9c 3.4d Survivorshipe 20.6f (38.1) 29.7 (54.9) 43.0 (79.5) 54.1 Age at M1 emergence 3.8 (65.5) 4.0b (69.0) 4.6c (79.3) 5.8 Cranial capacity (cm3) 484 383 379 1,293 Note. Numbers in parentheses indicate the percentage relative to the values in modern humans. References for life history, survivorship, and M1 emergence data are reported in Kelley and Schwartz (2010). a Value for mountain gorilla Gorilla gorilla beringei, which is likely to be earlier than in Gorilla gorilla gorilla. b Values for Pan troglodytes verus only (Taı¨ Forest, Ivory Coast). c Values for Pongo pygmaeus pygmaeus (i.e., orangutans from Borneo) only. d Interbirth interval is anomalously low in modern humans compared with other anthropoid species. This life history variable is included for between-ape comparisons only, and percentages of human values were not calculated. e Expected age at death at age 15 years based on empirically derived survivorship curves. f Average of female (24.8 years, or 45.8%) and male (16.4 years, or 30.3%) values. Courtesy of Anne Bronikowski and the Dian Fossey Gorilla Fund International. do for any other ape, and with the exception of baboons, great ape species other than the common chimpanzee. This perhaps for any other primate. Dean (2010) recently synthe- deficiency may limit the accuracy and reliability of life history sized all that is known about dental development in Pan, reconstructions for fossil hominins, and so it is critical to revealing some interesting similarities with and differences obtain M1 emergence data for both African and Asian apes from modern humans. Overall, chimpanzee dental develop- and to obtain these data from noncaptive animals. Recently, ment occurs along an accelerated schedule, taking ∼12 years reliable ages at M1 emergence were reported for orangutan compared with 18 years in modern humans. This acceleration (Pongo pygmaeus pygmaeus, 4.6 years) and gorilla (Gorilla is reflected in advanced median molar emergence ages that gorilla gorilla, 3.8 years) obtained from wild-shot individuals occur well before those of humans. The first mean gingival in museum osteology collections (Kelley and Schwartz 2010). emergence ages for chimp M1s were reported to be 3.3 years These data offer support for the likelihood of a later average (range of 2.6–3.8 years; Nissen and Reisen 1964). After three age at M1 emergence in free-living chimpanzees than in cap- more decades of studies on captive chimps, median emergence tive animals. Although limited, they also suggest that the av- ages for M1s are reconstructed as quite close to that original erage age at M1 emergence in noncaptive extant great apes 1 estimate, at 3.2 years (M range, 2.26–4.38 years; M1 range, ranges from just younger than 4 years to just older than 4.5 2.14–3.99 years; Kuykendal, Mahoney, and Conroy 1992). years, or approximately 1 year later than the conventional Thus, for several decades, it was generally taken that M1 range reported as ∼3.0–3.5 years. emergence in Pan, and thus for African apes as a whole, These new comparative data allow an evaluation of just occurred somewhere in the range of 3.0–3.5 years. By com- how consistent M1 emergence data are with the comparative parison, the range for modern humans calculated across life histories of extant Asian and African apes and modern global populations averages 4.7–7.0 years (Liversidge 2003). humans. As can be seen from table 1, the new ape emergence Given the presence of the so-called “wild effect” (sensu data fit well with expectations based on the comparative life Smith and Boesch 2011; see also Hamada et al. 1996; Kimura histories of living hominoids both in relation to one another and Hamada 1996), it became critical to evaluate gingival and in comparison with that of modern humans. Ages at M1 emergence ages in wild populations. To date, the only reliable emergence between 3.8 and 4.6 years for great apes represent estimate for age at M1 emergence in noncaptive apes is a ∼65%–80% of modern human emergence at ∼6 years SD), signaling a close fit between 1 ע years, mean 0.8 ע single individual of Pan troglodytes verus at approximately 4.1 (6.2 years for the maxillary M1. The likely age of emergence for ages at attainment (or duration) of some key life history events the mandibular M1 in this individual was approximately 3.8– in great apes, as these life history attributes are also ∼60%– 3.9 years, resulting in a combined age of M1 emergence of 80% of the modern human value. As a side note, and by approximately 4.0 years (Smith et al. 2010a; Zihlman, Bolter, comparison, gingival emergence ages of 3.0–3.5 in extant apes and Boesch 2004). Interestingly, a recent analysis by Dean would represent only ∼50%–60% of the average modern hu- (2010) using data from the histological growth record of man value. These new data reinforce earlier studies (Smith crowns and roots found that the predicted mean age of at- 1989) that identified dental eruption as a reliable means by tainment for molar emergence in Pan M1 is 4.1 years, nearly which to reconstruct life history profiles in extinct hominins. coincident with that reported in the wild P. troglodytes verus Unfortunately, reliable ages at M1 emergence are available individual. for a very small number of fossils. It is difficult to extract To date, no reliable gingival emergence data exist for any these data given the relatively few specimens that died during S400 Current Anthropology Volume 53, Supplement 6, December 2012 the eruptive process of M1 and the difficulty in arranging for molars would be delayed perhaps beyond ages that are fully these specimens to be subjected to the latest in noninvasive compatible with weaning and the food-processing require- imaging technology. Rather, utilizing the incremental growth ments of adolescent growth. All of the australopith and early record contained within dental hard tissues, estimates of the Homo specimens (and thus, perhaps, species) also fall below age at death for juveniles with mixed dentitions (both decid- the regression line, indicating that these species were also uous and permanent teeth present) near or subsequent to M1 characterized by a relatively advanced age at M1 emergence gingival emergence do exist for a handful of australopiths and for their brain size. early and later species of the genus Homo. These age-at-death The total range of variation in modern human M1 emer- estimates can thus be used as the basis for estimating ages at gence age is quite large, spanning almost 2.5 years (reviewed M1 emergence (table 2; Kelley and Schwartz 2012). All of the in Liversidge 2003). Despite that, reconstructed emergence australopith emergence age estimates resemble extant African ages for some of the early Homo species do not extend into apes more than they do modern humans, and this also holds the range for modern humans. Importantly, we do not yet for the earliest members of the genus Homo (H. erectus, H. know exactly how, if at all, certain life history attributes covary ergaster) for which there are reliable data. with dental development within and among modern human An important way to evaluate these calculated ages at M1 peoples or how to integrate these sorts of important intra- emergence is in the context of its relationship with cranial specific data with the interspecific trends discussed here. capacity. As mentioned earlier, cranial capacity and age at M1 emergence are strongly correlated in extant anthropoids (Godfrey et al. 2001; Smith 1989), and both exhibit a high The earliest species of Homo: the “transitional” hominins H. correlation with aspects of life history. As is evident in figure habilis and H. rudolfensis. Based on detailed reconstructions 1, all of the great apes fall on or above the regression line, of dental chronologies, it seems that australopiths fall well with Gorilla having the relatively earliest age at M1 emergence, within the range of emergence ages known for captive and as might be expected given its more folivorous diet (see God- wild chimps, and none falls within the ranges known for frey et al. 2001). Humans fall well below the regression line, modern humans. Thus, it is reasonable to conclude that early but it is most reasonable to attribute this to the tremendous hominins possessed a life history profile more similar to mod- increase in cranial capacity in human populations during the ern African apes than to modern humans. Dental maturation later Pleistocene, which has seemingly forced a partial dis- data for the earliest members of Homo, however, are much sociation between cranial capacity and age at M1 emergence. more limited. To date, dental maturational data for H. habilis Without this dissociation, M1 emergence (with a predicted and H. rudolfensis consist of either reconstructed root for- mean age of 7.1 years using the regression model versus the mation times (OH 16, H. habilis) or crown formation times actual modern human interpopulation mean of ∼5.8 years) (KNM-ER 1805E, H. habilis; KNM-ER 1590, KNM-ER 1802, as well as the subsequent emergence of the more posterior KNM-ER 1482B, H. rudolfensis; but see Anto´n 2012 as to

Table 2. Estimated ages (years) at death and M1 emergence in great apes, australopiths, and Homo

Species (specimen) Estimated age at death Age at M1 emergence Great apes: Pongo pygmaeus pygmaeus 4.6 Gorilla gorilla beringei 3.8 Pan troglodytes verus 4.0 Australopiths: Australopithecus afarensis (LH 2) 3.25 2.9* Australopithecus africanus (Sts 24) 3.30 2.9* A. africanus (Taung 1) 3.73–3.93 3.3–3.5* Paranthropus robustus (SK 62) 3.35–3.48 3.8–3.9* P. robustus (SK 63) 3.15–4.23 2.9–3.2* Paranthropus boisei (KNM-ER 1820) 2.5–3.1 2.7–3.3* Homo: Homo erectus (Sangiran S7-37) 4.4* Homo ergaster (KNM-WT 15000) 8.3–8.8 4.5* Homo neanderthalensis (La Chaise) 6.7* Homo sapiens (Global) 5.8 (4.7–7.1) Note. An asterisk indicates estimated values. Sources. Data for australopiths compiled from Dean et al. (1993); Bromage and Dean (1985); Dean (1987); Beynon and Dean (1988); Conroy and Vannier (1991a, 1991b); Lacruz, Ramirez Rozzi, and Bromage (2005); and Kelley and Schwartz (2012). Data for species of Homo are combined from Dean et al. (2001); Liversidge (2003); and Macchierelli et al. (2006). Schwartz Life History Evolution in Homo S401

of somatic development suggests an age at death of 7–7.5 years, while the state of dental development suggests an age estimate of 7 years (Smith 1993). Each scenario carries vastly different implications for the life history profile of H. erectus, and dental developmental data hold the potential to resolve the discrepancy. Data on the pace of development derived from the histology of enamel and dentine originally yielded an age-at-death es- timate of closer to 8 than to 12 years of age (Dean et al. 2001). A more extensive analysis, informed by several more years of data on crown and root development in larger samples of humans and fossil hominins and thus based on clearer esti- mates of certain dental growth parameters, has confirmed this by suggesting that an age-at-death interval of 7.6–8.8 years is most appropriate (Dean and Smith 2009). Furthermore, the reconstructed age at M1 emergence based on inferences from incremental growth data is 4.5 years, just slightly outside the Figure 1. Bivariate plot of ln M1 emergence age in months (y) known ranges for extant captive (2.1–4.0 years) and wild (3.8– versus ln cranial capacity in cubic centimeters (x) for a sample 3.9 years) Pan and slightly earlier than that for modern hu- of anthropoids (taxa include Callithrix jacchus, Saguinas fusci- mans (4.7–7.0 years). Given the relationship between brain collis, Saguinas nigricollis, Cebus albifrons, Cebus apella, Saimiri sciureus, Aotus trivirgatus, Trachypithecus cristata, Chlorocebus ae- size and dental development (see fig. 1), a brain size estimate 3 thiops, Macaca fascicularis, Macaca mulatta, Macaca nemestrina, for KNM-WT 15000 (810 cm ) generates a point prediction Macaca fuscata, Papio cynocephalus, Papio anubis, Pan troglodytes, for M1 emergence age of 5.2 years (95% prediction interval: Pongo pygmaeus, Gorilla gorilla, and Homo sapiens and are derived 3.2–8.7 years), suggesting that H. erectus likely possessed rapid primarily from Smith [1989] with supplemental data from recent maturation and was more modern apelike in overall growth analyses, especially on great ape molar emergence; see references). and development and “certainly closer to the expectation for Summary statistics for the ordinary least squares regression are an ape of comparable dental and skeletal maturity (ca. 7.5) as follows:y p 0.630x Ϫ 0.072 , 95% confidence interval (CI; slope): 0.555–0.704,R2 p 0.949 (P ! .001 ), and the 95% predic- than for a human (ca. 10–15)” (Dean and Smith 2009:114). tion intervals are indicated by the shaded region. Reduced major Taken together, these data make it unlikely that all or even axis regression:y p 0.646x Ϫ 0.144 , 95% CI (slope): 0.572–0.721. some of the distinctive features of modern human life history Ceboids are indicated by x, cercopithecoids are filled circles, great were present ca. 2.0–1.5 Ma. apes are filled squares, and H. sapiens is the open diamond. Slower maturation translates into later ages for achieving Australopith species are represented by triangles (from top left, certain developmental milestones, such as the onset of pu- clockwise: SK 48, DIK-1-1, Taung 1, OH 5) and Homo erectus berty, adolescence, and so forth, and is intricately linked to (KNM-WT 15000 and Sangiran S7-37) by open squares. the ability of mothers to wean offspring earlier and shorten interbirth intervals, thereby increasing fertility by having mul- species groups). Taken together, they suggest a dental devel- tiple, overlapping offspring. This “stacking” phenomenon is opmental profile that was more modern apelike than modern only possible because of the lower energetic requirements for humanlike, providing some tantalizing evidence that neither fueling growth in slower maturing organisms compared with species likely possessed an extended period of childhood de- the tremendous energetic burden mothers would face having pendence (Dean 1995; Dean et al. 2001). to subsidize the growth of fast-growing, multiple offspring Later species of Homo. Given the extraordinarily complete and (Dean and Smith 2009; Gurven and Walker 2006). Available well-preserved juvenile specimen KNM-WT 15000, we per- data from modern hunter-gatherers suggest that humans fol- haps know more about overall growth and development, and low the ecological risk aversion model (Janson and van Schaik thus life history, in African H. erectus than any other early 1993) that posits slow growth and the maintenance of small hominin taxon. Based on the lack of fusion of the distal elbow sizes for longer periods of time, reduces feeding competition, joint and the acetabulum in particular, KNM-WT 15000 was and translates into significant energetic savings. This energetic given an age of death at ca. 13 years, or the early part of the savings is offset by a period of accelerated growth, known as adolescent stage of growth (i.e., postpubertal; Ruff and Walker the adolescent growth spurt, which could be subsidized by 1993). Interestingly, the mostly completed dentition (26 per- older individuals, highlighting the importance of older in- manent teeth had emerged, all but the M3s and maxillary dividuals in contributing to the care and feeding of children canines) suggested an age at death of ∼10.2 years. This discord (i.e., paternal care, “grandmothering,” etc.; e.g., Hawkes 2003; of almost 3 years suggests a somewhat unique developmental Hawkes et al. 1998; Kaplan et al. 2000). Thus, the human trajectory for H. erectus (Smith 2004). Equally interesting is strategy can be seen as one where higher fertility is achieved that based on a chimpanzee developmental standard, the state by emphasizing more slow-growing children with a later S402 Current Anthropology Volume 53, Supplement 6, December 2012 growth spurt than few faster-growing ones (e.g., Bogin 1988, many hominin taxa, it is clear that members of early Homo 1997; Gurven and Walker 2006; Leigh 2001; Leigh and Park were committed terrestrial bipeds. Across primates, highly 1998). The combined lack of evidence for protracted growth terrestrial species possess more accelerated life history sched- and for an adolescent growth spurt (Anto´n and Leigh 2003; ules than nonterrestrial species (Deaner, Barton, and van Smith 1993; Smith and Tompkins 1995) in H. erectus and H. Schaik 2003; Ross 1992, 1998), likely as a result of increased ergaster supports the assertion that fully modern human life extrinsic mortality in the form of predation. Early hominins histories had yet to evolve by 1.5 Ma. clearly succumbed to predation with some regularity, and the Recently, several investigations have been launched to as- signal of relatively rapid life history profiles in australopiths certain whether the modern human pattern of growth, de- and early Homo may be a direct outcome of selection oper- velopment, and life history characterized Neanderthal (Homo ating on low survivorship by accelerating overall development sapiens neanderthalensis) populations (e.g., Bayle et al. 2009a, to reach sexual maturity at an earlier age. In that context, 2009b, 2010; Coqueugniot and Hublin 2007; Guatelli-Stein- dental development may be linked, perhaps through a mech- berg 2009; Guatelli-Steinberg et al. 2005; Macchiarelli et al. anism such as pleiotropy, to overall somatic development and 2006; Ponce de Leo´n et al. 2008; Ramirez-Rozzi and Bermu´dez is therefore similarly accelerated. de Castro 2004; Smith et al. 2007b, 2007c, 2010b). A con- Scenarios to explain early Homo life history need not rely vincing argument is mounting that dentally, Neanderthals on inferences based on diet or inferred mortality profiles may have experienced accelerated growth, which would in alone. The combination of low nutritive value of ingested turn suggest that a growth profile that included prolonged food with high rates of extrinsic mortality would have the dental development, and one that may have included most result of selecting for individuals within populations that or all of the other human life history attributes, did not evolve would grow at a slow rate and mature early, producing adults until the appearance of H. sapiens. Unfortunately, very little of small stature such as those found within contemporary is known about dental development in taxa postdating H. hunter-gatherers of the rainforests (Kuzawa and Bragg 2012). erectus and predating Neanderthals, but it would seem par- High mortality on its own would also select for faster growth simonious to reconstruct dental development as being at least and early maturation, though at “normal” adult sizes. In this as accelerated in middle Pleistocene taxa such as Homo an- context, it is interesting to speculate that populations expe- tecessor and Homo heidelbergensis. Limited data are not in- riencing increases in nutritional quality along with high ex- consistent with this hypothesis: certain growth parameters of trinsic mortality should grow faster to reach maturation ear- anterior teeth in these species seem more similar to Nean- lier at larger adult sizes compared with ancestral populations derthals than to modern humans (Ramirez-Rozzi and Ber- with low nutritional quality and high mortality. As shown by mu´dez de Castro 2004). McHenry (1992, 1994), Holliday (2012), and Pontzer (2012), there is good evidence for a general trend of an increase in Reconstructing life history in early Homo. Given the available body mass from Australopithecus to Homo (also see Ruff 2002 data, the full suite of modern human life history character- and references therein). If rates of extrinsic mortality were istics was most certainly not present at the base of the hominin held constant, this could imply a transition from hominin lineage, nor was it present at the emergence of the genus populations with low nutritional quality to those with higher Homo, but it likely occurred at some time during the middle nutritional quality. This is not inconsistent with recent dietary to late Pleistocene. That does not mean, however, that all reconstructions of early Homo, wherein H. erectus diets were hominins before the appearance of H. sapiens possessed a life reconstructed as far more varied than in preceding H. habilis history that was completely modern apelike despite the fact (Ungar 2012; Ungar et al. 2011), perhaps suggesting that a that all of the included species of early Homo seem quite broadening of the resource base was an important contrib- accelerated dentally. There are several possible interpretations uting factor to the evolution of larger body sizes and perhaps of the relatively early M1 emergence ages of the hominins ultimately to shifts in life history. Interestingly, researchers (reviewed in detail in Kelley and Schwartz 2012). Aside from have speculated on whether similar conditions may have led scenarios regarding the manner in which these age estimates to selection for accelerated growth in Neanderthals and in- were generated or how incremental growth is charted, there clude scenarios where they experienced serious nutritional are several ways to interpret these data. stress linked with elevated rates of young adult mortality (Og- Perhaps the ages at M1 emergence indicate the presence of livie, Curran, and Trinkaus 1989; Pettitt 2000; Trinkaus 1995; relatively rapid life histories in australopiths and early Homo Trinkaus and Tompkins 1990). According to life history the- and thus are more similar to Gorilla than to Pan. This could ory, both of these factors in combination would have the be related to dietary differences: lower-quality food such as effect of selecting for rapid and early maturation. that preferred by primary folivores such as Gorilla gorilla ber- A second possible interpretation is that reconstructions of ingei display more accelerated life history schedules and rel- the pace of life history are indeed more accurately reflected atively precocious dental development than similar-size fru- by brain size, and so the scheduling of at least some life history givores (Breuer et al. 2009; McFarlin et al. 2009). attributes occurred at a slower pace than would be inferred While diet type and nutritional quality are still debated for from simply evaluating M1 emergence ages alone. In other Schwartz Life History Evolution in Homo S403 words, different life history parameters could be dissociated span, for example, may be a more recent acquisition. New from one another so that selection could act on them indi- data on adult mortality patterns suggest similar population vidually or as smaller developmental subsets. It is critical to demographics for late archaic (Neanderthals) and early mod- bear in mind that dissociations among developmental sys- ern (Middle and earlier Upper Paleolithic) humans, an ob- tems—the scheduling of dental events versus that of repro- servation that weakens support for some sort of demographic ductive events, for instance—may not be as tightly linked advantage related to enhanced longevity for early modern across closely related species as they appear to be across hom- humans (Trinkaus 2011). inoid genera. In fact, the clear associations between dental development and life history variables as well as among life history variables that exist when examined across primates as Future Directions a whole are known to break down when examined across Discoveries of new infant and subadult fossils along with closely related species. The general trend for primates holds advances in noninvasive imaging and analytical methods are that larger species take longer to grow and reach sexual ma- providing opportunities to probe further the fossil record of turity; however, data on hylobatids suggest that it is the human growth and development. For instance, it is likely that smaller-bodied Hylobates, not the larger Syndactylus that pos- the age at which important life history events, such as wean- sesses a later age at sexual maturity and a longer life span ing, will be assessable directly from the fossil record. The (Dirks and Bowman 2007). That same study also demon- timing of weaning is a key life event for both mother and strated that the age at molar emergence is not correlated with offspring, and analyses of life history variation as it relates to age at menarche or the age at first reproduction in exactly weaning across Primates provide one example of the selective the same way in both cercopithecoids and hylobatids. On an basis of these sorts of developmental dissociations. Within even broader scale, certain strepsirrhines “buck” the primate Malagasy prosimians, selection has acted to accelerate weaning trend as a means of solving the problem of how to cope with and dental development but has delayed the age at first re- highly seasonal and unpredictable environments. Compared production (Godfrey et al. 2001; Richard et al. 2002; Schwartz with lemurids, large-bodied indriids exhibit extreme dental et al. 2002). It has been suggested that some australopiths precocity while maintaining slower rates of somatic growth, show rapid deciduous tooth wear, which was taken as evidence thus allowing for relatively earlier weaning as a strategy to suggestive of relatively early weaning (Aiello, Montgomery, help reduce the metabolic burden on mothers (e.g., Godfrey and Dean 1991; Dean 2006, 2010). It may now be possible et al. 2001). These are just a few examples of how an un- to retrieve direct evidence for reconstructing weaning age and derstanding of developmental dissociations, or “modularity” shifts in energy provisioning for offspring through the evo- (sensu Leigh and Blomquist 2007), urges some caution in lution of Homo. Across Primates, weaning is closely tied in directly linking dental development and the scheduling of life history. An exciting avenue of future study would be to doc- time to the emergence of M1. However, human life history ument the extent to which dental developmental profiles are is characterized by relatively early weaning followed by a pro- correlated with life history attributes within populations of longed period of postweaning dependency. The advancement modern humans, an endeavor made easier these days by the of weaning age throughout human evolution coupled with ever-expanding data on the chronology of developing teeth rapid and early brain growth implies a shift in how the rising in worldwide populations (see Liversidge 2003). This may energetic demands of offspring are met: initially, energetic ultimately yield clearer and more refined insights into the costs are subsidized completely by the mother but then by finer details of life history evolution across hominin species members of the social group through the provisioning of and especially within more closely related and even conspecific weanlings (Humphrey 2010). This pattern of high maternal hominin populations. At the same time, these analyses may investment and alloparenting behavior is important because unveil the extent to which the human life history package is it is a clear determinant of birth spacing. Such a stratagem dissociable and allow us to begin to develop models of how has also been suggested to characterize the earliest members shifting patterns of ecology, subsistence, demography, diet, of Homo (Aiello and Wells 2002). Recently, models have been and so forth, throughout the Homo lineage may have resulted proposed to establish the precise age at which organisms were in a more piecemeal acquisition of the fully modern human weaned by accessing the isotopic record, in particular, stron- life history profile. Some new data suggest that this may be tium : calcium ratios (Sr/Ca) preserved within dental hard an interesting way forward. Very recently, DeSilva (2011) pos- tissues (e.g., Humphrey et al. 2008a, 2008b). Charting shifts ited that infant : mother mass ratios of ∼5% (generally ∼6% in this ratio throughout the developmental period associated in modern humans; cf. 3% in extant chimpanzees) were al- with early tooth tissue formation is one exciting way of re- ready present in early australopiths. That author suggests that constructing infant diet as well as tracking dietary transitions more modern humanlike birthing strategies, the adoption of throughout early life. If early Homo and later-occurring ar- alloparenting behavior, and so forth, may have been present chaic Homo populations were indeed characterized by rela- 13 Ma, well before the origin of Homo. On the other hand, tively early weaning, then analyses of the isotopic chemistry other aspects of the human life history package such as life throughout enamel development hold the potential to verify S404 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 2. Bivariate plot of bite point positions for all teeth and masticatory muscle positions relative to the temporomandibular joint (TMJ; y-axis) versus age (x-axis) in a cross-sectional ontogenetic series of modern humans (Nubian archaeological sample housed at University of Colorado, Boulder). Bite points are measured as the distance of each tooth from the TMJ, measured in the occlusal plane, and are illustrated by the two vertical arrows (left) indicating bite points for the dm1 and dm2. Masticatory muscle position (for the superficial and deep masseters, temporalis, and medial pterygoid muscles) is defined as the point where each muscle’s resultant force crosses the occlusal plane relative to the position of the TMJ. Primary masticatory adductor position and orientation are based on a series of 2-D and 3-D linear and angular measurements and, taken together, capture what has been termed “masticatory system configuration” (see Spencer 1995, 1999). Note the consistent position of the dm2 (small white sphere) and the permanent M1,M2, and M3 (large white spheres) anterior to the masticatory muscles (i.e., above the white dotted line) at the time of emergence. Also note the differing rates of anterior growth of the dental arcade and masticatory muscles (as indicated by the slopes of second-order polynomials); space for emerging molars is a product of these different growth rates. A color version of this figure appears in the online edition of Current Anthropology. this with direct evidence for the age at weaning from the fossil molar emergence events are predominantly a function of rates record itself. of facial growth such that successive molars (deciduous and While continued probing of the fossil record to establish permanent) emerge at a consistent position relative to the more precise demographic and maturational profiles holds masticatory musculature (fig. 2). Moreover, there appears to the potential to yield key details in the evolution of human be a consistent position of newly erupted molars (deciduous life history, another interesting way forward is to attempt to and permanent) relative to the temporomandibular joint understand the processes that lie behind the slightly dissimilar (TMJ) that in an archaeological sample of modern humans patterns in dental development, and thus inferred life history is ∼40 mm (fig. 3). This ontogenetic arrangement ensures profiles, among hominins. A host of studies have advanced that there is a biomechanically optimal location for molar our understanding of how dental developmental variation eruption anterior to the net vector of masticatory muscle intersects with primate life history variation, but surprisingly effort (note position of white dots relative to dotted white little is known about the precise mechanism that governs, line, fig. 2) and that each successive molar erupts into this modulates, regulates, constrains, and so forth, the timing of optimal position only at a point during ontogeny when it is molar eruption and as such the underlying processes that vacated as a result of facial growth. This all suggests covari- regulate these temporal events are largely unknown. ation in rates of facial growth (indicated by the slope of the Recently, it was postulated that a set of biomechanical con- first part of the curve for each molar, fig. 2), the position of straints regulates masticatory system configuration through- the masticatory musculature, the spatial position of an erupt- out ontogeny and therefore modulates the position and ul- ing molar, and the timing of molar emergence. timately the timing of emerging molars within developing The validity of this biomechanical model for modulating faces (Spencer and Schwartz 2008). Based on an ontogenetic the timing of molar emergence has not been fully established. sample of modern human crania, it seems that successive Indeed, whether this constraint operates across hominoids is Schwartz Life History Evolution in Homo S405

ages in modern humans may therefore result from reduced rates of facial growth and extreme orthognathy, perhaps in combination with a developmental delay in facial growth. A later initiation of facial growth would result in a delay in clearance of a “biomechanically appropriate” space available for molar emergence. In the absence of good ontogenetic data on craniofacial growth in early Homo, it is useful to evaluate how well this biomechanical model integrates craniofacial morphology with data on developmental rates within other members of the Homo lineage. This model predicts the advanced molar emer- gence schedules of Neanderthals to be related to a combi- nation of their higher degree of midfacial prognathism and accelerated cranial growth trajectories. Some evidence in sup- port of faster rates of craniofacial growth (Ponce de Leo´nand Zollikofer 2001; Ponce de Leo´n et al. 2008) and dental de- velopment (Smith et al. 2007c, 2010b) exist. Thus, selection may have accelerated age at weaning and thus ecological in- dependence by advancing rates of cranial growth in a manner that permitted a more accelerated molar development/erup- tion schedule, which would represent an effective life history strategy under conditions of high extrinsic mortality. More thorough explorations of how the timing of molar develop- ment and emergence may result from the complex spatial interplay between growing faces and expanding neurocrania hold tremendous potential for illuminating the underlying mechanism that regulates molar emergence and, ultimately, Figure 3. Consistent position of newly erupted molars relative to the temporomandibular joint (TMJ) as indicated by the length for unlocking the linkages between dental development and of the horizontal white line. The dot on the left of the line marks life history events. the position of the TMJ in lateral view, while the dot on the right Finally, it is generally agreed that the earliest species of marks the position of the newly emerged molar. Note that the Homo evolved from Australopithecus, either in East or South line is the same length for individual human crania at the time Africa. The cranium from Bouri, Ethiopia, at 2.5 Ma attrib- of M1 emergence (top), M2 emergence (middle), and M3 emer- uted to Australopithecus garhi (Asfaw et al. 1999) and the gence (bottom). This is illustrated graphically by the consistent associated cranial and postcranial material for the newly an- width of the shaded rectangle. While the absolute distance is different, the same pattern of spatial consistency in molar po- nounced Australopithecus sediba from Malapa, South Africa, sition holds for an ontogenetic sample of wild-living Pan (see at 1.9 Ma (Berger et al. 2010) may therefore provide important text). A color version of this figure appears in the online edition. clues for helping to better understand the complex interplay among morphological, ecological, reproductive, and behav- ioral adaptations that underlies the transition to and ultimate not yet clear, but preliminary data on an ontogenetic series success of the genus Homo. of western African chimpanzees (Pan troglodytes verus; n p 37) are striking: like the modern human sample, no significant differences are present between the position of each succes- sively emerging molar and the TMJ (Kruskal-Wallis,df p 2 , Acknowledgments P p .6215) despite the fact that, unsurprisingly, the absolute distance is slightly greater in this sample (∼48 mm). I would like to thank Leslie Aiello and Susan Anto´n for their A fuller mapping of the influence of these biomechanical invitation to participate in the Wenner-Gren workshop, all of constraints onto variation in the ontogeny of masticatory the conference participants for their stimulating and thought- muscle position and explicitly testing hypotheses that inte- ful discussions throughout the conference, and the two anon- grate craniofacial architecture, muscle function, facial growth, ymous reviewers for their input and constructive comments and molar emergence across hominoids is currently under- on this manuscript. The ideas and work laid out here are the way. These are critical comparative data because selection for results of many discussions and ongoing collaborations, es- accelerated molar eruption, as seems to characterize early pecially with Chris Dean, Jay Kelley, Tanya Smith, Debbie Homo relative to modern humans, should require a similar Guatelli-Steinberg, Laurie Godfrey, Wendy Dirks, Bill Kimbel, acceleration in facial growth. The delay in molar emergence Mark Spencer, Terry Ritzman, Kierstin Catlett, and Halszka S406 Current Anthropology Volume 53, Supplement 6, December 2012

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Journal of Human Evolution 29:155–168. taxa, grades and clades. Journal of Anatomy 212:354–376. Smith, Shelley. 2004. Skeletal age, dental age, and the maturation of KNM- Zihlman, Adrienne, Debra Bolter, and Christophe Boesch. 2004. Wild chim- WT 15000. American Journal of Physical Anthropology 125:105–120. panzee dentition and its implications for assessing life history in immature Smith, Tanya M. 2006. Experimental determination of the periodicity of in- hominin fossils. Proceedings of the National Academy of Sciences of the USA cremental features in enamel. Journal of Anatomy 208:99–114. 101:10541–10543. Current Anthropology Volume 53, Supplement 6, December 2012 S409

Body Size, Size Variation, and Sexual Size Dimorphism in Early Homo

by J. Michael Plavcan

Size variation provides important clues about the taxonomy, morphology, behavior, and life history of extinct species. Body size variation in living species is commonly attributed to Bergmann’s rule, resource availability, nutrition, local selection pressures, and sexual size dimorphism. While our understanding of the mechanisms producing size variation in living species has grown more sophisticated in recent years, our ability to apply this knowledge to the fossil record is limited by the quality of the available fossil and extant comparative samples. New discoveries of fossil Homo have expanded the known range of size variation and provide hints of geographic and temporal variation in size within and between named taxa and possible strong sexual size dimorphism. Even so, the range of size variation in Homo habilis/rudolfensis and Homo erectus matches or even is less than that seen in geographically restricted samples of living anthropoid primates. These observations dictate caution in interpreting the meaning of variation in early Homo but also underscore the critical necessity of improving comparisons of size among fossils and establishing an adequate comparative database of living species that allows us to discriminate between the effects of epigenetic and selective factors on the expression of variation.

The meaning of size variation has long been a topic of debate ena such as Allen’s and Bergmann’s rules, secular trends in concerning the origins and evolution of Homo, playing a key diet and nutrition, selection for smaller or larger size in as- role in discussions about species recognition, sexual dimor- sociation with environmental or behavioral factors, and sexual phism, life history, and behavior (Aiello and Key 2002; Anto´n dimorphism (Ruff 2002). The role of developmental plasticity 2003; Kappelman 1996; McHenry 1992, 1994; Wood 1993). in response to environmental and nutritional variation as a Discoveries of new specimens of early Homo and Homo erectus cause of size variation is also receiving greater attention (An- have expanded the apparent range of size variation, raised to´n 2012; Kuzawa and Bragg 2012). awareness of the biological implications of geographic and At the same time, great apes, and particularly Pongo and temporal variation in early Homo, and altered our perception Gorilla, are among the most sexually dimorphic primates (Smith and Jungers 1997). Australopithecus too shows evi- of potential size dimorphism in early Homo and H. erectus dence of strong sexual size dimorphism (Gordon, Green, and (Aiello and Key 2002; Anto´n 2012; Anto´n and Snodgrass 2012; Richmond 2008; Lockwood et al. 1996), raising the question Kuzawa and Bragg 2012; Rightmire, Van Arsdale, and Lord- of whether size variation in early Homo could reflect strong kipanidze 2008; Ruff 2002; Spoor et al. 2007). To understand sexual dimorphism as opposed to either taxonomic variation the implications of this variation, it is critical to parse out or intraspecific variation due to other factors. This issue is the sources and causes of size variation in living animals and critical, because strong size dimorphism has been linked to look for ways to identify the causes of variation in the fossil sexual selection, and changes in size dimorphism imply sig- record. nificant changes in behavior and life history (Gordon 2006a, Discussions of variation in fossil Homo naturally turn to 2006b; Leigh 1992; Lindenfors 2002; Lovejoy 2009; Martin, modern humans as a model of patterns of intra- and inter- Willner, and Dettling 1994; Plavcan 2001; Plavcan and van specific size variation and sexual dimorphism (e.g., Anto´n Schaik 1997a,1997b; Reno et al. 2003, 2010). 2003; Kramer et al. 1995; Lieberman, Pilbeam, and Wood Most analyses of size variation in the fossil record focus 1988; Miller 2000; Rightmire, Van Arsdale, and Lordkipanidze on adult variation. Ontogenetic variation is informative about 2008; Skinner, Gordon, and Collard 2006). Modern Homo life history adaptations during growth and development shows substantial size variation that is attributed to phenom- (Leigh 1992, 1995) and about species life history and adap- tations in general (Leigh and Blomquist 2007). Ontogenetic J. Michael Plavcan is Professor in the Department of Anthropology, variation is relatively easy to recognize as a separate source University of Arkansas (Fayetteville, Arkansas 72701, U.S.A. of variation because juvenile mammals leave indications of [[email protected]]). This paper was submitted 12 XII 11, immaturity, including unfused epiphyses and cranial sutures accepted 3 VII 12, and electronically published 15 X 12. and unerupted teeth. Variation in patterns of growth and

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0012$10.00. DOI: 10.1086/667605 S410 Current Anthropology Volume 53, Supplement 6, December 2012 development themselves constitute important evidence about Plavcan 1998; Kramer et al. 1995; Lockwood et al. 1996; Plav- a species biology, morphology, and life history (e.g., studies can and Cope 2002). of KNM-WT 15000; Schwartz 2012) and so are outside the Critically, variation itself is size dependent, but in a regular, scope of this review. But it is also important to recognize that mathematically predictable way. In absolute terms, gorilla adult variation is the product of ontogenetic variation. Hence, body size (average female mass 71,500 g in western lowland factors that may affect growth and development—such as gorillas; Smith and Jungers 1997) is more variable than that nutrition, disease, or other intrinsic factors—may ultimately of pygmy marmosets (average female body mass 122 g; Smith generate adult size variation (Kuzawa and Bragg 2012). Pat- and Jungers 1997). A 5% weight difference from the average terns of adult morphological variation also are altered by gorilla female is 3,575 g, more than 29 times the average mass variation rates of growth and maturation of organ systems of the pygmy marmosets. Thus the standard deviation (SD) and skeletal components (e.g., Isler et al. 2007; Leutenegger of any trait in a gorilla will be enormously larger than that and Masterson 1989a, 1989b; Lockwood 1999; Plavcan 2003), of the same trait in a marmoset. leading to natural interspecific variation in the patterns of Consequently, any study of size variation in living or fossil trait variation. species must compare measures of relative size (Plavcan and Outside of ontogenetic variation, we can think of variation Cope 2002; Sokal and Braumann 1980; Yablokov 1974). There within species as falling into three classes (simplifying the are two simple methods: the coefficient of variation (CV) and scheme of Albrecht and Miller 1993): intrinsic character var- the simple log transformation of raw data (one should not, iation within an interbreeding population, intersexual varia- however, compare CVs of log-transformed data, as this will tion indicative of separate selective forces acting on males and reintroduce a correlation of size with variation). CVs are com- females or sexual differences in response to environmental monly used, being simply the SD divided by the mean of a factors (Altmann and Alberts 2005; Fernandez-Duque 2011; trait multiplied by 100 to represent the value as a percentage (Sokal and Braumann 1980). A correction factor is usually Kuzawa and Bragg 2012; Wells 2007, 2012), and interpopu- added for small sample sizes. Log transformation is more lational variation due to variable local adaptations or temporal convenient, however, for statistical comparison of the data shifts in selective or environmental factors. A final source of (Plavcan and Cope 2002), though nonparametric tools such variation in fossil samples is the mixing of multiple taxa. This as the Fligner-Killeen test (Kramer et al. 1995) are also pow- can be thought of as confounding variation because it both erful. interferes with the recognition of taxonomic diversity and Traits differ in the magnitude of variation, but most, ad- obscures levels of intraspecific variation. The rest of this article justing for the correlation between size and variation, fall will first review what is known about the pattern and causes within a modest range (Yablakov 1974). As a rule of thumb, of these sources of variation in living species as it might apply molar teeth are the least variable dental traits, with within- to the fossil record generally and then briefly consider vari- sex CVs ranging from about 1.5% to 8% across primates for ation in fossil Homo in the light of variation in living primates. relatively geographically restricted samples (Gingerich and Schoeninger 1979; Plavcan 1993). Osteological traits likewise Intrinsic Population Variation tend to show low within-sex variation. Among 40 craniofacial dimensions for 135 species of primates, within-sex CVs for most average less than 10% (fig. 1). Postcranial variation is Variation is a natural feature of any morphological character similarly low (Gordon 2004). Within-sex CVs for body mass and is classically separated into genetic and environmental itself range from about 12% to 15% (Smith and Jungers 1997) components (Lande 1980). Identifying the separate genetic for a sample of 19 primates, which, when accounting for and nongenetic components of variation in living species is dimensionality, is comparable to values for dental, cranial, difficult and requires information on pedigrees and, ideally, and skeletal characters. Thus, within-sex variation is generally all of the environmental variables that might influence the limited across primates. It should be emphasized that these expression of a trait from growth in the womb to diet and assessments of variation refer to living species sampled from disease process in an adult. In practice, this sort of analysis restricted geographic ranges or at least subspecies of living of the causes of normal interindividual population variation species. cannot be carried out for fossil samples. However, if there are Most anthropoid primates, including humans, are sexually limits to what might be thought of as “normal” variation dimorphic to some degree. This means that variation needs within populations, then at least a rough baseline of com- to be considered within the sexes separately to control for the parison can be established to help recognize variation due to effect of dimorphism on population variation. It has been environmental, geographic, temporal, or sexual differences. suggested that males are more variable than females in pri- This logic forms the foundation of most comparative studies mates (Leutenegger and Cheverud 1982, 1985) and that such of variation in fossils that employ living species as a baseline variability is causally related to the evolution of sexual di- of comparison for the fossils (Albrecht and Miller 1993; Cope morphism. Controlling for the correlation between size and and Lacy 1992; Fleagle, Kay, and Simons 1980; Kelley and variation, males and females on average do not differ from Plavcan Variation in Early Homo S411

Figure 1. Profile of average coefficients of variation (CVs) for 40 linear craniometric dimensions from females in 135 primate taxa. Male profiles are nearly identical. For most characters, CVs do not exceed a value of 8. one another across species (Plavcan 2000b; Plavcan and Kay less population variation. Wood and Lieberman (2001) pro- 1988; Smith and Jungers 1997). However, males of strongly vide evidence that while heritability is not systematically as- dimorphic species do tend to be more variable than females sociated with greater or lesser variability, craniofacial traits in raw data space. Interestingly, males of Pongo may show subjected to low strains (e.g., from the basicranium and neu- unusual size variation in association with a “waiting room” rocranium) tend to show less variation than those subjected mating strategy (Utami Atmoko and van Hooff 2004). Adult to higher strains and therefore are preferable for assessing male orangutans are dimorphic in that only resident domi- whether populations show unusual variation. nant males achieve full body size with the development of strong secondary sexual features, including cresting and ro- Sexual Dimorphism busticity of the skull. Other males retain a subadult body form even though the dentition has completely erupted and these Sexual dimorphism has played a key role in debates about males are capable of reproduction (Utami Atmoko and van the biological and taxonomic meaning of variation in early Hooff 2004). The result is that while male teeth are not nec- Homo, especially Homo habilis, Homo rudolfensis, and Homo essarily more variable than those of females, skeletal and cra- erectus (e.g., Anto´n 2003; Miller 2000; Rightmire, Van Arsdale, nial features are (Leutenegger and Masterson 1989a, 1989b). and Lordkipanidze 2008; Skinner, Gordon, and Collard 2006; This pattern of variation is exceptional among primates, but Wood 1993). In most anthropoid primates, males are larger a similar pattern has been associated with variation in Par- than females. Females can be larger than males in callitrichids, anthropus robustus (Lockwood et al. 2007). while strepsirrhines show minimal dimorphism (Kappeler Although in general, trait variation tends to be limited in 1991; Smith and Jungers 1997). Gorillas show the greatest populations, some traits show intrinsically higher or lower degree of body mass dimorphism among hominoid primates, degrees of variation (fig. 1). Those interested in assessing the though Mandrillus sphinx appears to be the most size- cause of variation in fossils intentionally focus on characters dimorphic anthropoid (Gordon 2004). Modern humans show that show inherently low degrees of variation. For example, an unusual pattern of relatively modest body mass dimor- the first molar teeth tend to be the least variable and show phism (about 15%; Smith and Jungers 1997) but moderate the lowest degrees of sexual dimorphism in the dentition “lean” body mass dimorphism (about 44%; Wang et al. 2001). regardless of size dimorphism (Gingerich and Schoeninger This latter value reflects a proportionally greater amount of 1979). Therefore, tests of whether fossil dental samples show fat in human females (Plavcan 2012; Wang et al. 2001; Wells inflated variation usually focus on the molar teeth. Articular 2007, 2012). Skeletal dimorphism in modern humans is mod- surfaces of joints are strongly correlated with body size and erate and slightly greater than that of chimpanzees (Gordon, tend to show less variation than, for example, diaphyseal Green, and Richmond 2008), but when corrected for dimen- breadths (Lieberman, Delvin, and Pearson 2001; Ruff 2002; sionality it is proportional to lean body mass dimorphism in Trinkaus, Churchill, and Ruff 1994). Wood and Lieberman magnitude (Plavcan 2012). Cranial dimorphism in modern (2001) evaluated whether craniodental traits that might be humans tends to be modest, being intermediate between body under greater or lesser mechanical loads or that show different mass dimorphism and lean body mass dimorphism (Plavcan degrees of heritability might be expected to show more or 2012). S412 Current Anthropology Volume 53, Supplement 6, December 2012

Because most cranial, dental, and postcranial traits are nor- of dimorphism in the fossil record, we need to understand mally or at least unimodally distributed in males and females, the factors that affect both male and female size. the effect of dimorphism is to simultaneously increase the Body size dimorphism should represent a balance of the total sample variance and generate bimodality (Godfrey, Lyon, costs and benefits of altering body size from a theoretical and Sutherland 1993; Plavcan 1994, 2000b; Plavcan and Kay optimum (Fairbairn 1997; Gordon 2006a; Lande 1980; Leigh 1988). For fossils, dimorphism is commonly estimated using and Blomquist 2007). In all nonhuman primates, males and one of several techniques that correlate sample variation with females occupy similar niches, living together, eating the same dimorphism (Gordon, Green, and Richmond 2008; Joseph- foods, occupying the same substrates and territories, and sus- son, Juell, and Rogers 1996; Plavcan 1994; Plavcan and Cope ceptible to the same forces of ecological variation and pre- 2002) largely because the sex of individual specimens cannot dation. While the phenomenon of niche dimorphism is com- be reliably determined. It is common practice to assume that mon in, for example, monogamous birds (Emlen and Oring large specimens are male and small specimens are female (e.g., 1977; Selander 1972), it has never been demonstrated in pri- Lockwood 1999; McHenry 1992). However, this practice will mates (Plavcan 2001). Rather, those differences in diet, lo- tend to overestimate the magnitude of sexual dimorphism (as comotion, and substrate use that do occur in primates are will all methods) by ignoring overlap in male and female more likely a consequence of dimorphism than a cause of it distributions, especially when true dimorphism is slight. (Clutton-Brock, Harvey, and Rudder 1977). The result is that Importantly, while dimorphism in some skeletal features in the absence of selective factors uniquely targeting size in such as pelvic size and shape can reflect functional or devel- one sex, both sexes should achieve approximately the same opmental differences between males and females, dimorphism body size. Corroborating this is the observation that mono- in most skeletal features is often assumed to reflect overall morphism has evolved independently in association with an body size dimorphism. However, patterns of dimorphism dif- absence of agonistic male competition and sexual selection fer throughout the dentition, skull, mandible, and skeleton, for male size (Lindenfors and Tullberg 1998). and such patterns differ between species (Gordon, Green, and The male contribution to dimorphism in primates is gen- Richmond 2008; Plavcan 2001, 2002, 2003). For example, erally thought to be straightforward: agonistic male-male within M. sphinx, possibly the most size-dimorphic primate competition for mates as predicted by sexual selection theory alive (ratio of male to female body mass 2.69; Gordon 2004), (Clutton-Brock, Harvey, and Rudder 1977; Ely and Kurland dimorphism in skull dimensions ranges from a low of 1.06 1989; Ford 1994; Gaulin and Sailer 1984; Gordon 2006b;Kay (male mean divided by female mean) for postorbital breadth et al. 1988; Lindenfors 2002; Lindenfors and Tullberg 1998; to a high of 2.5 for zygomatic arch thickness (Plavcan 2002). Martin, Willner, and Dettling 1994; Mitani, Gros-Louis, and Orbital dimensions differ dramatically in dimorphism in this Richards 1996; Plavcan 2001, 2004b; Plavcan and van Schaik species (as in most other primates), with orbital height di- 1992, 1997b). Where males can monopolize access to receptive morphism of 1.07 and biorbital breadth dimorphism of 1.73. females to the exclusion of other males, competition resulting The implication is that one cannot simply compare variation in male reproductive skew will ensue. Because body size helps across traits and assume that they will yield similar signals of males win contests and is heritable, selection should favor size dimorphism for any particular species (Plavcan 2002, large male size. Multiple comparative studies have corrobo- 2003). rated the sexual selection hypothesis using surrogate measures The issue of estimating the magnitude of dimorphism is of sexual selection and male competition, including compe- important because dimorphism constitutes critical evidence tition levels (the potential frequency and intensity of male of behavior and life history in extinct species and thus has competition), breeding system (monogamous/polyandrous, weighed heavily in discussions of the evolution of hominin multimale, single male), socionomic sex ratio (the number behavior (e.g., DeSilva 2011; Gordon 2006a; Lovejoy 1981, of adult males to adult females per group), and operational 2009; Martin, Willner, and Dettling 1994; McHenry 1994; sex ratio (the number of adult males to the number of re- Moore 1996; Plavcan and van Schaik 1997a). Dimorphism is ceptive adult females in a group; Cheverud, Dow, and Leu- one of the only anatomical traits that is directly causally re- tenegger 1985; Ely and Kurland 1989; Ford 1994; Gaulin and lated to social behavior that is preserved in the fossil record Sailer 1984; Gordon 2006a, 2006b; Greenfield 1992; Leuten- (Plavcan 2004a). But dimorphism is a complex phenomenon, egger and Kelly 1977; Lindenfors and Tullberg 1998; Mitani, and a simple one-to-one correspondence between behavior Gros-Louis, and Richards 1996; Plavcan 2004b; Plavcan and and the magnitude of dimorphism does not exist (Plavcan van Schaik 1992; Plavcan, van Schaik, and Kappeler 1995). 2000a). Dimorphism reflects separate causal factors influenc- The above analyses have been used to support inferences ing male and female traits whose expression is potentially of polygyny or specific mating systems in hominins and other limited by the genetic correlation between males and females extinct taxa (e.g., Gordon, Green, and Richmond 2008; Kap- (Gordon 2006a, 2006b; Greenfield 1992; Lande 1980; Leigh pelman 1996; Lockwood 1999; McHenry 1994). However, in 1992; Lindenfors 2002; Martin, Willner, and Dettling 1994; no study is the magnitude of size dimorphism uniquely as- Plavcan 2011; Plavcan, van Schaik, and Kappeler 1995). sociated with one or the other breeding system, competition Therefore, in order to understand the biological implications level, sex ratio, or operational sex ratio (OSR; Plavcan 2000a). Plavcan Variation in Early Homo S413

While very strong dimorphism is invariably associated with sources (Gordon 2006a; Leigh 1995; Leigh and Shea 1996; polygyny, skewed OSRs, and intense male competition, mono- Lindenfors 2002; Martin, Willner, and Dettling 1994). morphism is not uniquely associated with any particular mat- Within humans, some evidence suggests that small female ing system. This means that a lack of dimorphism alone in body size is favored where resources are scarce during lac- a fossil sample cannot be used as evidence for monogamy, a tation (Gordon 2006b; Ralls 1976). Kuzawa and Bragg (2012) humanlike mating system, polyandry, or any other mating note that larger female body size may be an epiphenomenal system (Plavcan 2004a). response associated with better maternal nutrition. At the Apart from sexual selection acting on males, no other factor same time, human males appear to respond more rapidly to (predation, diet, life history variables, etc.) has been shown changes in nutrition than human females (Anto´n and Snod- in comparative analysis to be consistently associated with di- grass 2012; Bribiescas, Ellison, and Gray 2012). morphism, at least as far as the male contribution to dimor- Each of the above hypotheses has some data to support it. phism (Ford 1994; Gordon 2006a; Plavcan 2001). This does Still open to question is how much dimorphism can be at- not mean that male size is only affected by sexual selection tributed uniquely to changes in female size in any given spe- in every species. Rather, across species this is the only factor cies. There is no species of primate that shows strong size to have a consistently detectable association with dimorphism. dimorphism without male competition and polygyny. Two Recent years have seen greater attention to the female con- cercopithecoid taxa were thought to show a combination of tribution to body size dimorphism (Bribiescas, Ellison, and strong size dimorphism and monogamy (Cercopithecus ne- Gray 2012; Clutton-Brock, Harvey, and Rudder 1977; Gordon glectus and Simias concolor; Leutennegger and Lubach 1987). 2006a, 2006b; Kuzawa and Bragg 2012; Lindenfors 2002; Mar- Further study of both of these species demonstrated that po- tin, Willner, and Dettling 1994; Plavcan 2004b; Wells 2007, lygyny is present in other parts of the species range and that 2012). Several models posit the importance of changes in hunting pressure explained the presence of monogamous female body size in the evolution of hominin dimorphism pairs at least in S. concolor (Brennan 1985; Watanabe 1981). (Cartmill and Smith 2009; Gordon 2006a; Lovejoy 2009; Mar- On the other hand, there are no monogamous or polyandrous tin, Willner, and Dettling 1994). There is clear evidence that anthropoids that show strong size dimorphism, though sev- eral monogamous species do show modest levels of size di- dimorphism changes through changes in female size within morphism (Plavcan 2000a, 2001). If selection to alter female species, even in monogamous species. For example, Fenandez- size—either larger or smaller—is common independent of Duquez (2011) demonstrates that dimorphism in Aotus varies changes in male size and contributes significantly to inter- as a result of changes in female size correlated with longitude. specific variation in size dimorphism, then we should expect Similarly, intraspecific variation in dimorphism associated to see greater variation in dimorphism among monogamous with changes in female trait size has been documented for and polyandrous species. That this is not the case suggests howler monkeys (Jones et al. 2000), vervet monkeys (Turner, that large male size in dimorphic species is maintained in Anapol, and Jolly 1997), baboons (Dunbar 1990), macaques spite of pressure to reduce male size to that of females and (Macaca fascicularis [Fooden 1995]; Macaca nemestrina [Al- that most substantial dimorphism in primates is a function brecht 1980]), and guerezas (Hayes, Freedman, and Oxnard of changes in male and not female size. 1995). On the other hand, that variation in dimorphism within Females of most primates compete for resources rather than species has been documented and tied to changes in both access to mates (Sterck, Watts, and van Schaik 1997). Selection male and female size (Albrecht 1980; Altmann and Alberts for larger or smaller female size centers on the balance be- 2005; Fernandez-Duque 2011; Gordon 2006b; Plavcan, van tween resource abundance and reliability, risks to infant and Schaik, and McGraw 2005; Turner, Anapol, and Jolly 1997) maternal mortality, and maximizing reproductive success raises the question of how to reconcile broadly based inter- (Gordon 2006a; Kuzawa and Bragg 2012; Leigh 1995; Lin- specific comparative analyses with studies of changes within denfors 2002; Ralls 1976; Turner, Anapol, and Jolly 1997; Wells species. The answer probably lies partly in the scale of com- 2012). Factors hypothesized to favor larger females are re- parison. Broadly based comparative analyses offer statistical source competition (Gordon 2006a; Leigh and Shea 1996; tests of factors that should have a general effect on dimor- Lindenfors 2002; Plavcan 2011) and the fact that larger fe- phism, but they mask considerable variation. Even the stron- males can produce larger offspring that suffer lower mortality gest behavioral correlate of dimorphism in anthropoid pri- risk, can produce more or better milk (thereby allowing off- mates explains less than half of the interspecific variation in spring to grow faster), or may be better at defending and dimorphism among species. Beyond this, there are few data carrying offspring (Gordon 2006a; Kuzawa and Bragg 2012; allowing a systematic, broadly based comparative analysis that Ralls 1976; Smith et al. 2012; Wells 2012). Factors hypothe- can effectively quantify variation in the factors that affect sized to favor smaller females are selection for early cessation female size and hence the general contribution of changes in of growth (favoring earlier breeding and increased reproduc- female size to dimorphism. tive output) and size reduction to decrease absolute metabolic The implications of this for the fossil record and for models demand when individuals may face periods of limited re- of human evolution are important. It appears that large S414 Current Anthropology Volume 53, Supplement 6, December 2012

temporal variation have been cited as factors confounding attempts to recognize and estimate dimorphism when the sex of individuals cannot be determined, and these factors have played significant roles in debates concerning how much var- iation should be expected within fossil species especially if the fossils show a wide geographic or temporal distribution (Al- brecht and Miller 1993; Gordon, Green, and Richmond 2008; Plavcan, van Schaik, and McGraw 2005; Reno et al. 2003, 2010; Shea, Leigh, and Groves 1993). The magnitude of size differences between closely related species or subspecies can vary widely. Figure 2 shows variation in skull size in closely related species or subspecies of Pongo and Cebus olivaceus. Size differences among the groups in each set are comparatively minimal. In contrast, figure 3 shows similar plots illustrating strong geographic variation Figure 2. Box plots showing variation in skull size in Pongo and Cebus olivaceus. Skull size is represented by a geometric mean of among subspecies of Papio and Semnopithecus. nine dimensions. While numerous studies have documented geographic var- iation in primate size, comparatively few have tested hypoth- changes in dimorphism are not likely to be either gained or eses about the specific causes of size differences among pop- lost through changes in female size alone. Rather, a loss or ulations (Albrecht and Miller 1993). Those have found that gain of dimorphism accompanied by substantial shifts in fe- body size tends to follow Bergmann’s rule, with size increasing male size should signal both selection to alter female size and with increasing latitude, and that populations living in more a change in selection on male size, most likely because of productive habitats with higher rainfall and less seasonality changes in female distribution or behavior that alter the mo- tend to be bigger (Albrecht and Miller 1993; Dunbar 1990; nopolization potential of females (Plavcan, van Schaik, and Fernandez-Duque 2011; Fooden 1995; Katzmarzyk and Leon- McGraw 2005). ard 1998; Plavcan, van Schaik, and McGraw 2005; Ruff 2002; Beyond this, two points need to be emphasized. First, the Turner, Anapol, and Jolly 1997). However, Albrecht and Miller correspondence between dimorphism and categorical esti- (1993) caution that some species fail to show this relationship mates of breeding system or male competition commonly between productivity and size (toque macaques), while others used to support inferences of mating system or male com- actually reverse the trend (Sundaic pigtail macaques). Plavcan, petition in hominins (e.g., Kappelman 1996; Kimbel and De- van Schaik, and McGraw (2005) find that while intraspecific lezene 2009; Lovejoy 1981, 2009; McHenry 1994; Moore 1996; size variation is associated with variation in latitude and pro- Plavcan 2000a, 2001; Plavcan and van Schaik 1997a)istoo ductivity, interspecific size variation is not correlated with crude to provide anything but the most general information— measures of rainfall or seasonality. substantial size dimorphism is associated with male compe- Male and female size have been shown to vary among tition and polygyny (Plavcan 2000a). A single numerical es- populations independently within species but in association timate of dimorphism tells us little else. However, as our knowledge of the factors that change male and female size increases, the greatest information about changes in behavior and life history in the fossil record and in human evolution should come through the study of temporal changes in male and female size relative to each other. But before this can be done, much more study is required of the forces that influence female size independently of male size.

Temporal and Geographic Variation Geographic variation is common in primates and can be sub- stantial. Well-documented examples of strong size variation include savanna baboons, various macaques, and Hanuman langurs (Albrecht and Miller 1993; Dunbar 1990; Jolly 2001). Because geographic variation represents population-specific Figure 3. Box plots illustrating strong geographic variation size changes within a species, it can be used to model temporal among baboons and Hanuman langurs. Note that changes in variation (Albrecht and Miller 1993; Plavcan 1993; Shea, female size are consistently accompanied by parallel changes in Leigh, and Groves 1993). At the same time, geographic and male size. Plavcan Variation in Early Homo S415

ilar patterns to those seen in nonhuman primates. Humans tend to be larger in more productive habitats, and body size tends to increase with increasing distance from the equator. Human body size is also thought to vary with nutrition and disease (Ruff 2002). Local adaptation to variation in climate, resource availability, and other factors is also thought to con- tribute to variation in human body size. Kuzawa and Bragg (2012) specifically note that human body size tends to increase relatively faster in males with increasing resource abundance. With regard to the fossil record, it is of great interest to know how modern human interpopulation variation in cra- nial and skeletal size compares with that of extant primates. Figure 4 shows human skull bizygomatic breadth data from Howells’s (1973) data set compared with data for a sample of extant Gorilla gorilla gorilla. The human samples illustrated in the figure were selected to represent the greatest range of variation among the populations available in Howells’s (1973) data set, yet still, considered together, they show considerably less variation than seen between the sexes of the extant Gorilla sample. The CV for the entire Howells (1973) data set (N p 26 samples with both males and females represented) is 6.0, which is approximately half that of the Papio, Sem- nopithecus, and Gorilla samples shown in figures 3 and 4 and Figure 4. Box plots of skull bizygomatic breadth data from the is also less than that of a single subspecies of chimpanzees Howells (1973) data set for 10 populations of humans compared (table 1). Geographic variation is clearly present in the human with skull lengths for Gorilla gorilla gorilla. The dashed vertical line separates the Gorilla samples from the Homo samples. Sam- sample, but combining even the most disparate populations ples were selected from the Howells (1973) data set to represent of humans does not increase the total sample variation sub- the maximum range of variation in female skull size. Bizygomatic stantially (the average CV for individual human samples in breadth was chosen for comparability to the Gorilla sample. the Howells [1973] data set is 4.9). Note that in spite of the Other variables show a similar pattern. Note that in spite of the overall size differences among the human samples, sexual di- pattern of clear differences among human populations, overall human variation is limited. Note also that for all populations, changes in female size are accompanied by parallel changes in Table 1. Coefficients of variation (CV) of bizygomatic male size. Females are indicated by gray-shaded boxes, males by breadth for samples of humans, apes, and monkeys unshaded boxes. Sample CV N Howells data set: with different factors. For example, Turner, Anapol, and Jolly All 6.0 2,412 (1997) demonstrate that Cercopithecus aethiops female size Average 4.9 26a variation changes with resource abundance—where popula- Range 4.1–5.6 b tions have reliable and abundant resources and with increas- Papio spp.: All 12.9 162 ing rainfall females increase in size with a concomitant re- Average 9.6 4a duction in size dimorphism. In contrast to this, Altmann and Range 7.2–12.3 Alberts (2005) demonstrate that compared with baboons liv- Semnopithecus entellus: ing on an entirely wild diet, “resource enhanced” baboons All 12.4 116 a show greater size dimorphism through a differential increase Average 6.9 6 Range 6.3–8.4 in male body mass relative to that of females. Dunbar (1990) Gorilla gorilla 11.0 79 also presents evidence that Papio size and size dimorphism Pan pansicus 5.4 39 increases with increasing rainfall specifically through changes Pan troglodytes troglodytes 6.4 47 in male size. Albrecht (1980) demonstrates a similar phe- Pan troglodytes schweinfurthii 5.8 31 nomenon for Macaca nemestrina, noting that both male and Pan troglodytes combined 6.4 78 Hylobates lar 4.4 53 female skull size increase with increasing distance from the a equator but that male skull size increases relatively faster. Average CV based on 26 samples in the Howells (1973) data set, four for Papio, and six for Semnopithecus. For the two monkeys, Variation in body size is well documented for extant Homo CVs for subgroups were only calculated for groups with N of nine (Albrecht and Miller 1993; Katzmarzyk and Leonard 1998; or more and both sexes present in the sample. Kuzawa and Bragg 2012; Ruff 2002) and tends to follow sim- b Nonhuman primate data collected by the author. S416 Current Anthropology Volume 53, Supplement 6, December 2012 morphism remains relatively stable. Male versus female bi- Table 2. Coefficients of variation (CV) of femoral head zygomatic breadth is highly correlated in the Howells (1973) diameter for samples of humans, apes, and monkeys data set (r p 0.971 ,N p 26 samples,P ! .001 ). Thus, even though dimorphism might be influenced by shifts in male or Sample CV N female size, the overall magnitude of the effect is minimal by Homo sapiens: comparison with overall human variation and especially by All 9.2 1,519 a comparison with the magnitude of variation typically seen in Average 7.7 11 Range 6.4–9.1 single species and even subspecies of extant primates. Hylobates lar 4.4 113 Geographic variation in human femoral head size, which Pan paniscus 5.5 18 is often viewed as one of the best proxies for body size, shows Pan troglodytes 6.5 109 the same pattern as seen for human bizygomatic breadth (fig. Gorilla gorilla 12.0 122 5). The CV of femoral head diameter for all human samples Pongo pygmaeus 13.2 14 combined is 9.2, while that for the Gorilla sample is 12.1 Sources. Human data from Auerbach and Ruff (2004); nonhuman pri- (table 2). Within-population CVs for the human sample range mate data from Gordon (2004). a Number of samples. from a low of 6.4 to a high of 9.1 with an average of 7.7, suggesting, as for the bizygomatic breadth data, that geo- graphic variation, while clearly present, does not inflate com- comparable with that of the Gorilla sample. By contrast, the bined-population variation to a great degree. Even so, the CV for the same dimension for a single subspecies of chim- total range of femoral head size across human populations is panzees (Pan troglodytes troglodytes) is 6.5. It is notable that variation is similar for cranial and postcranial dimensions in great apes while the human postcranial variation is greater than that of the skull dimension. This reflects the fact that the magnitude of human postcranial dimorphism is similar to that of the lean body mass dimorphism while that of skull dimorphism is similar to that of the total body mass dimor- phism (Plavcan 2012). Finally, as for bizygomatic breadth, male and female changes in femoral head size change in par- allel to one another, withr p 0.934 for male versus female femoral head diameter (N p 42 ,P ! .001 for all samples of Homo in the Goldman postcranial data set). Thus, while di- morphism varies across populations (fig. 6), it is actually min- imally influenced by changes in the size of either sex by com- parison with interspecific variation in the magnitude of dimorphism. This observation is potentially important for translating inferences about epigenetic changes in modern human size and dimorphism to the fossil record (Anto´n and Snodgrass 2012; Kuzawa and Bragg 2012). While it is clear that changes in diet and resource availability can and do alter male or female growth and consequent size dimorphism in modern primates and humans (Altmann and Alberts 2005; Gordon 2006a; Turner, Anapol, and Jolly 1997), what we see in the human data is that at least for the craniometric data and Figure 5. Box plots showing variation in femoral head diameter for 11 human populations from the Goldman data set (Auerbach femoral head size available here, geographic variation in mod- and Ruff 2004) and Gorilla gorilla gorilla (from Gordon 2004). ern humans is relatively limited by comparison with intra- Samples of humans were selected on the basis of sample size; sexual variation in a single geographically restricted sample only samples with more than 12 males and 12 females were of Gorilla, and variation in the magnitude of dimorphism included. Note that as for the craniometric variable in figure 4, among regional human samples is comparatively restricted. male and female distributions tend to parallel one another. At the same time, the overall variation among the humans is more similar to that of the Gorilla sample. However, also note that in Temporal Variation, Sexual Dimorphism, humans, male and female distributions consistently overlap one and Fossil Homo another, reflecting lower degrees of dimorphism than the Gorilla sample, in which the male and female distributions do not over- Recent discoveries of early Homo highlight the importance of lap. Females are indicated by gray-shaded boxes, males by un- variation in the fossil record. Fossils from Dmanisi, Olorge- shaded boxes. salie, Gona, as well as a well-preserved skull of early Homo Plavcan Variation in Early Homo S417

is modest. Most postcranial remains identified as early Homo are not associated with cranial remains, making taxonomic attributions uncertain. Finally, small sample sizes introduce substantial error into any estimate of size variation even for living species. In spite of the bleak uncertainty of the fossil record, we can still estimate size and size variation and with those estimates provide limited assessments and establish at the very least a framework for establishing hypotheses and place limitations on what can and cannot be said with the remains that we do have available. Estimates of body size based on postcranial size, summa- rized in Pontzer (2012), are illustrated in figure 7 compared with a series of extant primates for which body mass data from wild-shot specimens are available (Isler et al. 2007). All data are ln transformed to standardize variation across the size range. For the fossils, presumed sex is indicated according to Pontzer (2012) and Anto´n (2012). Several features of this graph immediately stand out. First, sexual dimorphism in both Australopithecus, and in Homo habilis/rudolfensis appears strong with no overlap between sexes. This is because sex in these specimens is assigned on the basis of size itself. All three of these samples appear to show bimodality, which if the sex Figure 6. Sexual dimorphism (male average divided by female assignments are correct would imply strong size dimorphism. average) for samples of Homo from the Howells (1973) data set Importantly, the H. habilis/rudolfensis sample is likely com- and samples of extant great apes. Each circle represents a value posed of two species (Anto´n 2012), making any assessment of dimorphism for a single sample. The samples for Homo and of dimorphism highly uncertain and contingent on the tax- Gorilla are the same as were used in figure 5. onomic assignment of specimens. However, even with the confounding effect of taxonomic mixing in at least one sam- from Kenya (KNM-ER 42700) in particular suggest not only ple, the range of variation in all of these samples is comparable an increase in size variation across time and space (Anto´n with that of Hylobates lar, which shows only slight dimor- 2012; Anto´n and Snodgrass 2012; Rightmire, Van Arsdale, phism, suggesting caution. More interestingly, the total range and Lordkipanidze 2008) but also that sexual size dimorphism of variation of all four fossil samples falls within the range may have been substantial in early Homo (Spoor et al. 2007). of all extant species, including the gibbons. However, only It has long been suggested that there has been an increase in the H. erectus sample is not significantly more variable than body size in Homo erectus over earlier hominins and that a the gibbon sample. In fact, for H. erectus, in terms of relative reduction in size dimorphism in the human lineage occurred variation, the total range of estimated body mass falls within through a relative increase in female body size, yet recent that of a single-sex sample of Hylobates and Pongo abelli. discoveries underscore the uncertainty in these claims (Aiello Notably, the Dmanisi specimens, which as a group are indeed and Key 2002; McHenry 1992, 1994). smaller on average than other H. erectus (Anto´n and Snod- Size variation and dimorphism for early Homo and H. grass 2012), do not in fact alter the range of estimated body erectus has largely been assessed using craniometric data and masses. Assuming that the sex assignments are correct, the estimates of body mass based on postcranial variables. But Dmanisi specimens do increase the range of variation in either any assessment of size variation in Homo needs to be qualified sex beyond what is seen within geographically restricted sin- by the fact that the fossil record is sparse and yields only clues gle-sex samples of extant species. The impression left in this about size. Assessments of size in living species usually focus comparison is that variation within the entire H. erectus sam- on body mass as an estimate of size, and comparisons of the ple is unremarkable by comparison with that found in typical fossil record should understand that skeletal size variation is living primates. not uniform and isometric within or between species (Gor- McHenry (1992, 1994) suggested that H. erectus may have don, Green, and Richmond 2008), making comparisons of lost sexual size dimorphism through a disproportionate in- estimated mass in fossils to actual mass of living species prone crease in female size. Close examination of figure 7 supports to significant error (Smith 1996). As noted above, dimor- this notion, albeit very weakly. Homo habilis/rudolfensis phism among skeletal features with a single species can vary “males” are about the same size as those of H. erectus, while substantially. Our inability to accurately identify sex with H. habilis/rudolfensis “females” are visibly smaller even though available remains adds considerable uncertainty to estimating the H. erectus sample illustrated here includes the Gona and the magnitude of dimorphism, particularly when dimorphism Dmanisi specimens. As noted by Anto´n (2012) and Anto´n S418 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 7. Estimated body mass (Pontzer 2012) for hominins based on postcrania compared with body mass data for selected extant taxa (Isler et al. 2007). Sex assignations for hominins are according to Pontzer (2012). Arrows for Homo erectus indicate Dmanisi specimens. and Snodgrass (2012), the sample sizes are small, sex assig- variation in the African sample can be attributed to OH 9 nation is uncertain, and there are almost certainly two taxa and KNM-ER 42700. If the large African variation is due to in the H. habilis/rudolfensis sample, meaning that support for sexual dimorphism, than the magnitude would lie between the hypothesis must be considered weak, and could change that of chimpanzees and gorillas. However, the specimens are with the addition of a single specimen to the early Homo separated geographically and by 320,000 years in time, a mag- sample. nitude easily unappreciated in a graph. Figure 8 suggests that there is an effect of geographic var- Figure 8B shows the sample comparison using biasterionic iation on cranial size in H. erectus. Spoor et al. (2007) analyze breadth. For the ape samples, bimastoid breadth is substi- skull length in samples of Pan, Gorilla, and H. erectus,sug- tuted, which should be roughly comparable for the purposes gesting that variation within the fossil sample may indicate of this comparison. A similar pattern to that seen for skull substantial size dimorphism, especially given the diminutive length is found in terms of a correlation with age and greater size of KNM ER 42700. Figure 8A shows skull lengths of H. variation in the African versus the Javan and Chinese samples. erectus plotted against age along with a sample from the However, the Chinese sample is clearly smaller in this di- Howells (1973) data set. The combined-sex CV for samples mension than contemporaneous Javan specimens (Anto´n of Gorilla gorilla and Gorilla beringei for the same measure- 2002; Kidder and Durband 2004), and while numerically the ment is 12.1 and 10.1 respectively (Plavcan 2003), and the size-adjusted residual variation of the early African specimens combined-sex CV for the extant humans shown in figure 8A lies between that of a chimpanzee and a gorilla (table 3), OH is 3.4 (N p 110 , Norse sample, Howells [1973] data set). The 9 and KNM-ER 42700 do not stand out as extreme outliers. CV for the entire H. erectus sample is 7.9 (N p 22 ). However, p the H. erectus sample is correlated with age (r 0.683 , Discussion N p 22,P ! .001 ). Evaluating the standard error (SE) of re- siduals of the fossils and living species, variation of H. erectus While these comparisons should not be considered the de- drops when controlled for geological age as expected given finitive assessment of variation in early Homo, they do serve the significant correlation (table 3). However, breaking the the purpose of illustrating the difficulty of assigning specific sample into African, Javan, and Chinese samples shows that causes to variation in fossil samples. Ideally, we need fossils the African sample, which is older (and includes the Dmanisi from the same time and locality in order to quantify variation specimens), shows almost twice the residual variation of the and sexual dimorphism and to test hypotheses about the later samples, which themselves show variation comparable causes of such variation. Indeed, even studies of living species to modern Homo and Pan paniscus, and less than Gorilla and are strongly limited by the quality of samples available. Most Pan troglodytes. Figure 8A shows that most of the excessive museum osteological collections of humans and primates Plavcan Variation in Early Homo S419

Figure 8. Skull length (glabella-opisthocranion) and biasterionic breadth plotted by age for Homo erectus compared with a single sample of Homo sapiens (Norse) from the Howells (1973) data set. Black circles are African H. erectus, diamonds are Javan, and triangles are Chinese specimens. Gray circles are H. sapiens. Data for H. erectus from Spoor et al. (2007) and Anto´n (2003). Where ages were given as a range, the approximate midpoint was used. were not systematically collected and cannot be used to test figure 7, there is an apparent shift in female size that is not hypotheses about the influence of changes in resource abun- accompanied by a shift in male size, thereby giving the im- dance, dietary quality, disease, and other factors on intra- pression that sexual dimorphism is reduced from earliest specific variation in a controlled, comparative context. Thus, Homo to H. erectus. Within H. erectus, early African samples the baseline of comparison for testing hypotheses about the are clearly more variable in skull dimensions than later sam- causes of variation in fossils is limited by the quality of data ples, and this variation might reflect sexual dimorphism (the available for extant taxa, adding to the problems inherent to temporal trend does not appear to explain the variation in the fossil record itself. these early specimens). However, the individual sex of the H. That said, while new discoveries of Homo erectus and early habilis/rudolfensis specimens can only be inferred on size, and Homo (Homo habilis/rudolfensis) have expanded our appre- the sample itself is so small that even the introduction of a ciation of size variation in the fossil record, the current fossil few new specimens could completely change our image of record provides little information about geographic, temporal, this species. Furthermore, the impression of elevated sexual or sexual variation in any species. For example, although Aus- dimorphism in African H. erectus is essentially based on two tralopithecus afarensis appears to be strongly sexually size di- specimens separated in time and space whose size difference morphic in most analyses (Gordon, Green, and Richmond could reflect temporal or geographic variation in overall size 2008; Harmon 2006; Kimbel and Delezene 2009; Lockwood unrelated to dimorphism (see also Anto´n 2012). This leaves et al. 1996; McHenry 1992; Scott and Stroik 2006), this view us with only a tantalizing apparent signal that is suggestive is not universally accepted (Reno et al. 2010). In contrast to of changes in size and dimorphism but nothing more. Cer- this, estimated body mass for H. erectus, inclusive of Dmanisi tainly the data are suggestive that changes in female size played and Gona specimens, is not significantly different from a an important role in changes in human size dimorphism. As single sex of a single subspecies of living gibbons even though illustrated above, though, the underlying causes for shifts in the combined sample of H. erectus appears to show at least dimorphism among primates are complex, and it is difficult a temporal shift in size. Therefore, even though we know that to support any single cause directly on the basis of currently female and male body mass can change through selective and available evidence. While we can formulate reasonable models epigenetic effects associated with variation in ecology, diet, for the evolution of the modern pattern of human dimor- disease, and other factors in humans and other primates (and phism, we need much better samples of fossils in order to that such effects can potentially be substantial), any signal support or test such models with any reasonable certainty. from such effects on the current fossil sample of H. erectus These comparisons underscore several problems that need cannot be distinguished from normal intrapopulation varia- to be addressed if we are to improve our ability to interpret tion in a single living species. the causes of variation in the fossil record. First, body size Another illustration is provided by the shift in body size estimates are based on disparate parts and limited remains. between H. habilis/rudolfensis and H. erectus.Asshownin A significant portion of the fossil record is omitted from S420 Current Anthropology Volume 53, Supplement 6, December 2012

Table 3. Comparisons of variation and relative variation in analysis simply because it is difficult to estimate size from the skull length and biasterionic breadth in Homo erectus, liv- remains. As emphasized by Smith (1996), we need more sys- ing Homo, and a series of extant ape samples tematic comparative analysis of the relationship between skel- etal size and body size in living species in order to more a b Sample Skull length Biasterionic breadth effectively utilize the remains we have. Furthermore, in order Homo erectus: to understand the relevance of modern studies of life history All: and size as either responses to selection or epiphenomenal Mean (ln data) 5.246 4.770 changes to the fossil record, we need to document the changes SD .083 .084 SD age adjustedc .060 .073 in both body mass and skeletal measures of size in living CV (raw data) 7.9 8.2 species that are preserved in the fossil record. African:d Comparative studies of the selective factors that affect size Mean (ln data) 5.176 4.708 are relatively uncommon. Early Homo undoubtedly differed SD .085 .084 from modern Homo, and while studies within humans are SD age adjusted .083 .081 CV (raw) 8.3 8.2 critical for understanding human evolution, comparative Java: studies offer an understanding of the breadth of factors that Mean (ln data) 5.297 4.835 might affect variation. Thus, for example, increased resource SD .058 .036 abundance leads to larger male size in baboons and modern SD age adjusted .052 .034 humans but relatively larger female size in vervet monkeys. CV (raw) 5.5 3.5 China: It cannot automatically be assumed that patterns seen in mod- Mean (ln data) 5.266 4.716 ern humans will of necessity be found in early hominins, and SD .021 .049 the only way to understand possible variation in causes is to SD age adjusted .021 .049 increase the database of comparative studies. CV (raw) 2.0 4.6 We need much more refined studies of geographic variation Homo (Norse): Mean (ln data) 5.206 4.691 in living primates. Most of the reference samples we have SD .034 .046 from museums are not systematically collected, and many CV (raw data) 3.4 4.6 studies using museum collections not only omit information Pan paniscus: about the geographic distribution of specimens but also often Mean (ln data) 5.109 4.677 combine specimens of different subspecies and even species SD .024 .041 CV (raw data) 3.0 4.1 into a single sample. The effect of seasonality and resource Pan troglodytes troglodytes: variation cannot be assessed in such samples (Plavcan, van Mean (ln data) 5.281 4.817 Schaik, and McGraw 2005). In order to test hypotheses that SD .047 .060 variation in fossil Homo might reflect epiphenomenal varia- CV (raw data) 4.0 5.9 tion in response to variation in resource abundance or re- Pan troglodytes schweinfurthii: Mean (ln data) 5.264 4.783 sponses to selection and local adaptation, we need targeted SD .044 .060 studies that carefully measure these effects and how they CV (raw data) 4.4 6.0 might be recognized in fossil samples. Gorilla gorilla beringei: This does not mean that the study of fossils is futile, how- Mean (ln data) 5.646 5.030 ever. The samples that we do have provide us with hypotheses SD .126 .114 CV (raw data) 10.1 11.1 and directions for research in living species. For example, the Gorilla gorilla gorilla: appearance of a shift in size from early to later Homo im- Mean (ln data) 5.577 4.994 mediately raises the question of why and underscores the SD .138 .112 importance of improving samples of fossils and generating CV (raw data) 12.1 11.0 better ways of estimating size with the scattered remains that Note. SD p standard deviation; CV p coefficient of variation. we have. At the same time, our improved understanding of a Skull length from Anto´n (2012) for H. erectus. Skull length for extant the causes of variation in living species gives us a much better apes is the same measurement (glabella to inion) listed as neurocranial length in Plavcan (2002, 2003). framework for interpreting the data that we have in the fossil b Biasterionic breadth from Anto´n (2012) for H. erectus. For the apes, record. For example, we now understand and expect that size bimastoid breadth (Plavcan 2002, 2003) is used, which is based on land- changes in species may be epigenetic and reflect regional or marks that are close enough that the comparisons should not be affected. temporal variation in resource availability and not necessarily c Standard errors of residuals from a least squares regression of ln-trans- selection. Our understanding of the causes of dimorphism in formed skull length against geological age as listed in Anto´n (2012). d Divisions of H. erectus following Anto´n (2012). primates argues strongly against inferring particular mating systems associated with some degree of sexual size dimor- phism and instead suggests that we should understand long- term changes in size dimorphism as indicative of changes in the selective factors affecting males and females separately. Plavcan Variation in Early Homo S421

While on the one hand this perhaps underscores how little iation in body weight in baboons (Papio spp.). Journal of Zoology (London) 220:157–169. we actually know about the causes of variation in early Homo, Ely, John, and Jeffrey A. Kurland. 1989. Spatial autocorrelation, phylogenetic on the other hand it also gives us a clearer understanding of constraints, and the causes of sexual dimorphism in primates. International the questions we can answer and the types of data necessary Journal of Primatology 10:151–171. Emlen, Stephen T., and Lewis W. Oring. 1977. Ecology, sexual selection, and to answer them. the evolution of mating systems. Science 191:215–233. Fairbairn, Daphne J. 1997. Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics 28:659–687. Fernandez-Duque, Eduardo. 2011. Rensch’s rule, Bergmann’s effect, and adult Acknowledgments sexual dimorphism in wild monogamous owl monkeys (Aotus azarai)of Argentina. American Journal of Physical Anthropology 146:38–48. I thank Susan Anto´n and Leslie Aiello for the generous in- Fleagle, John G., Richard F. Kay, and Elwyn L. Simons. 1980. Sexual dimor- vitation to participate in this symposium as well as for their phism in early anthropoids. Nature 287:328–330. encouragement, support, and insightful comments. I am es- Fooden, Jack. 1995. Systematic review of southeast Asian longtail macaques, Macaca fascicularis (Raffles, [1821]). Fieldiana, Zoology, new series, 81. pecially indebted to all of the conference participants for their Chicago: Field Museum of Natural History. critiques, novel ideas, new perspectives, and challenges to as- Ford, Susan M. 1994. Evolution of sexual dimorphism in body weight in sumptions and cherished ideas. I thank one anonymous re- platyrrhines. 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Male Life History, Reproductive Effort, and the Evolution of the Genus Homo New Directions and Perspectives

by Richard G. Bribiescas, Peter T. Ellison, and Peter B. Gray

The evolution of male life history traits was central to the emergence of the genus Homo. Compared with earlier hominins, changes in the behavioral and physiological mechanics of growth, survivorship, reproductive effort, and senescence all likely contributed to shifts in how males contributed to the evolution of our genus. For example, the range of paternal investment in modern Homo sapiens is unusual compared with most mammals and primates, all but certainly contributing to the evolution of the suite of life history traits that define Homo, including high fertility, large bodies, altricial offspring, large brains, and long lives. Moreover, the extensive range of phenotypic and behavioral variation in somatic and behavioral reflections of male reproductive effort across modern H. sapiens is especially noteworthy. We propose that selection for a broad range of variation in traits reflective of male reproductive effort was important to the evolution of Homo. We examine factors that contribute to this variation, proposing that selection for paternal and somatic investment plasticity across the entire male life span was important for the evolution of Homo. Potential research strategies and directions for new research for exploring these issues in the fossil record are also discussed.

The evolution of the genus Homo was marked by the emer- estimates of adult size for this individual are still the subject gence of life history traits that were distinct from previous of debate (Graves et al. 2010), and considerable size variation hominins. Larger brains and bodies, more gracile and gen- is now known across the species (Anto´n and Snodgrass 2012). eralized dentition, and a general decrease in cranial robusticity Moreover, the energetic demands of a larger body size, larger indicated a novel evolutionary path that lead to our own brains, and greater investment in altricial offspring surely re- species (Wood and Collard 1999). While some early Homo sulted in the evolution of shifts in the way Homo stored, traits were not identical to modern humans, such as accel- allocated, and managed energetic resources compared with erated dental growth (Dean et al. 2001; Schwartz 2012) and earlier hominins (Aiello and Wells 2002). perhaps slower infant brain development (Coqueugniot et al. Relative changes in juvenile and adult mortality due to the 2004), neonatal brain size, as extrapolated from obstetric mea- attenuation of predation, conspecific threats, food stress, or surements of a Homo erectus female pelvis, appears similar to ecological stochasticity all likely shaped Homo life history modern Homo sapiens (Simpson et al. 2008), intimating fetal traits (Michod 1979; Stearns and Koella 1986). Greater avail- growth and maternal energetic investment that was not very ability and optimization of energy resource allocation also dissimilar from ourselves. Enhanced somatic growth through was needed to support greater female fertility (Aiello and increases in the pace of development, life span, or both com- Wells 2002; Knott 2001). What factors changed compared pared with earlier hominins were necessary to achieve the with earlier hominins that resulted in selection for these life young adult size exhibited by the most complete H. erectus history traits, ultimately leading to emergence and prolifer- specimen, KNM-WT 15000 (Brown et al. 1985), although ation of Homo? We propose that the variability and plasticity of male life histories was a potent force in the development of the defining life history traits in Homo. Richard G. Bribiescas is Professor in the Department of The high metabolic costs of female reproduction as well as Anthropology at Yale University (New Haven, Connecticut 06511, parental care requirements of Homo offspring (Aiello and Key U.S.A. [[email protected]]). Peter T. Ellison is Professor 2002) suggest that supplementary support provided a selective in the Department of Human Evolutionary Biology at Harvard University (Cambridge, Massachusetts 02138, U.S.A.). Peter B. Gray advantage to produce and raise offspring to reproductive ma- is Assistant Professor in the Department of Anthropology at the turity compared with mothers who did so independently. University of Nevada, Las Vegas (Las Vegas, Nevada 89154, U.S.A.). Aside from child self support (Kramer 2005), kin, alloparents, This paper was submitted 12 XII 11, accepted 25 VI 12, and and fathers are the sole sources of extramaternal care. Indeed, electronically published 27 IX 12. compelling arguments highlight the role of kin and nonkin

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0013$10.00. DOI: 10.1086/667538 Bribiescas, Ellison, and Gray Male Life History and the Emergence of Homo S425 support (Bentley and Mace 2009; Hill et al. 2011). Compared competing categories that maximizes fitness can be deter- with earlier hominins, Homo males had to have exerted a mined. When analyzed over the entire life span of an organ- greater positive effect on offspring and mates through the ism, such a pattern of resource allocation is often referred to accentuation of food availability and quality as well as de- as a life history or reproductive “strategy.” creasing conspecific and predation risk and immunological The key concept in life history strategies is “trade-off.” challenges, just to name a few factors. Important trade-offs occur not only between competing cat- This is not a new proposal. Gettler (2010) argues that the egories of allocation at any point in time, which might crudely evolution of male paternal investment in our genus, mostly be reduced to the trade-off between investing in offspring in the form of offspring carrying, allowed for the liberation versus investing in self, but also between reproduction now of energetic resources in females that was thereby allocated and reproduction later, or investing in offspring already born toward shorter interbirth intervals and higher female fertility. versus new offspring. Finer distinctions in reproductive ef- Key and Aiello (2000) suggest that paternal investment may fort—such as “mating effort,” “parenting effort,” “gestation have evolved in response to a “prisoner’s dilemma,” proposing effort,” “lactation effort,” and so forth—are often useful in that when male reproductive costs are less than female re- distinguishing variations in reproductive strategies (Stearns productive costs, males should cooperate with females even 1989). One can also distinguish between “behavioral effort” when females do not reciprocate. Serving to complement and “physiological effort.” The field of behavioral ecology has these perspectives, our approach is more male-centric, at- flourished by analyzing behavioral strategies in terms of their tending to the somatic and behavioral trade-offs within male effects on fitness. But the physiological modulation of energy life histories that may have primed these positive effects on allocation to all categories, including reproduction, is also offspring and mates. Because male investment in offspring fundamental. While behavioral strategies are most effective in and mates is not without cost and requires a reallocation of responding to short-term conditions and the shifting land- resources between the somatic and behavioral demands of scape of conspecific behavior, physiological strategies are usu- growth (Bribiescas 2001; Ellison 2003), the physiology central ally tuned to the longer-term features of an organism’s ecology to male life histories had to evolve as well. Here we introduce and the more predictable unfolding of its life stages. these male trade-offs, unique aspects of male reproductive investment in Homo, and discuss possible ways in which these ideas might be applied and tested within the hominin fossil Male versus Female Reproductive Effort record. Trivers (1972), drawing on Bateman (1948), noted that the asymmetry in male and female reproductive strategies in Reproductive Effort and Male Trade-Offs many animal species can be traced to the asymmetry in gamete sizes, itself a reflection of asymmetrical investment of re- Reproductive effort is defined as the allocation of limiting sources in individual gametes. Because females provide most resources, principally energy and time, to reproduction. While (in fact, all, in most cases) of the metabolic resources that elegant in its simplicity, this definition requires elaboration are required in very early embryogenesis, they produce fewer in order to be useful, because in actuality life itself can be gametes from a given supply of energy, males many more. defined as the capture of energy in the service of the pro- From this fundamental asymmetry arises a general dimor- duction of new organisms, and thus all of life’s processes are phism in reproductive strategy whereby females invest more ultimately reproductive effort. Survival only contributes to effort in the somatic growth of offspring (“parenting effort” fitness to the extent that it enhances reproduction. The con- in Trivers’s [1972] terms) and males invest more effort in cept of reproductive effort as it is deployed in life history opportunities to father those offspring (“mating effort”). theory is usually narrowed to the allocation of resources to Female parenting effort is generally considered to be heavily reproduction at the expense of other, nonoverlapping cate- weighted toward physiological investment in the offspring gories of allocation, such as survival. A conventional division soma through gestation, egg laying, lactation, and so on. Es- of allocation domains into growth, reproduction, and main- timates of female reproductive effort are therefore often made tenance was introduced by Gadgil and Bossert (1970) and from measurements of total clutch mass, birth weight, or widely adopted by others as a heuristic framework. The im- lactation performance in relation to maternal body weight portant point that all such frameworks share, however, is the (Calow 1979). Male mating effort is generally understood as premise that investment of limiting resources in one category primarily behavioral. Estimates of male reproductive effort comes at the expense of investment in other categories. This are therefore often made by measuring time or energy spent “trade-off” principle represents a constraint that allows for in territory defense, mate guarding, competitive interactions modeling optimal allocations in terms of different end points. with other males, and so forth. Alternatively, reproductive For evolutionary analysis, the most relevant end point is Dar- effort in either sex can be estimated in terms of the cost winian fitness, and based on certain sets of assumptions (e.g., imposed on other allocation categories, such as survival and stable population theory), the allocation of resources among maintenance, through measures such as body weight lost or S426 Current Anthropology Volume 53, Supplement 6, December 2012 mortality suffered during the mating season (Clutton-Brock bolic cost of sexual dimorphism in primate males is com- 1984). parable to the energetic costs of several offspring born to The dichotomization of male and female reproductive ef- females (Key and Ross 1999). fort into physiological and behavioral is not absolute, of Dimorphic somatic strategies between male and female hu- course, although it may be a useful first approximation. Fe- mans reflect differences in physiological reproductive effort. males invest considerable behavioral effort in reproduction, Human males invest a substantial amount in the production including such obvious behaviors as incubation of eggs and and maintenance of a larger overall body size and in muscle provisioning of young. Males in turn make physiological in- mass in particular, presumably a reflection of an evolutionary vestments in the somatic tissues and metabolic processes that heritage of male mating competition (Puts 2010). The degree underpin their competitive ability (Bribiescas 1996). of somatic dimorphism is not as great, however, as in other The importance of physiological investment in somatic tis- great apes or as in other hominin species. In concert with sues in males is evident, for example, in sex differences in this relative de-emphasis on somatic investment, human processes that contribute to the adolescent transition to sexual males demonstrate much more in the way of parenting effort maturity. While females must deal with the energetic and than other great apes, suggesting a legacy of relatively greater pelvic skeletal demands of passing a large-brained infant— long-term mate fidelity. The observed pattern among extant hence the relationship between skeletal growth, the produc- primates suggests that sexual dimorphism in body size in the tion of ovarian hormones, and age of menarche (Ellison fossil record can be interpreted as a reflection of the relative 1982)—male sexual maturation is less constrained by the neg- importance of mating and parenting effort in the reproductive ligible metabolic demands of spermatogenesis and instead is strategies of extinct hominin species (McHenry 1994). contingent on the need to increase testosterone levels and Reproductive effort in the form of paternal investment is grow sexually dimorphic muscle tissue as well as its sup- especially germane to the evolution of Homo. Although sexual porting skeletal structure (Bribiescas 2001). dimorphism in early Homo remains unclear, gracile mor- But neither is the dichotomization of male and female re- phology and lower sexual dimorphism in modern humans productive effort into mating and parenting effort absolute. compared with australopithecines and paranthropines suggest Females of many species compete behaviorally and physio- a greater role for paternal investment in early Homo, although logically with other females to attract the highest-quality caution is merited because of the large degree of error in males, and males of many species participate in the provi- estimating sexual dimorphism in Homo and other hominins sioning, carrying, and direct care of offspring (Gross 1996). (Anto´n and Snodgrass 2012). However, paternal investment In species that have been selected for long-term mate fidelity, is not unique among primates, with about 40% of all species male and female reproductive success become more closely exhibiting some form of paternal investment (Kleiman and aligned, and levels and patterns of reproductive effort con- Malcolm 1981). Therefore, paternal investment alone prob- verge, although phylogenetic constraints on basic patterns of ably does not account for the emergence of Homo life history reproductive physiology make it difficult to erase all asym- traits. The unique nature of paternal investment in modern metries. humans is evident not only in its presence but also in its variability, both in intensity of time and energy investment and form, in terms of offspring care, provisioning, and other Human Male Reproductive Effort social benefits (Gray and Anderson 2010; Hewlett 1992). To The aspect of male reproductive effort most often recognized understand paternal investment in early Homo,weturnto and studied is behavioral, expressed in competition with other modern humans since our species is a more appropriate com- males for reproductive access to females. The investment is parative model than are other extant apes that exhibit little not only behavioral, however. Physiological and/or somatic or no paternal investment and greater degrees of sexual di- investment is usually involved as well. Investment in body morphism. mass, particularly muscle mass, is substantial in Gorilla, Pongo, and Pan (Leonard and Robertson 1997). Pan also makes a Paternal Investment in Homo considerable metabolic investment in gamete production, pre- sumably as a consequence of sperm competition (Harcourt A meta-analysis including 22 societies found that the death et al. 1981). Males in these three genera invest little if any of a father had a measurable effect on child mortality in only parenting effort. Male siamangs, in contrast, invest less in seven societies (Sear and Mace 2008), leading some to con- mating effort, either behaviorally or physiologically, than the clude that paternal investment is of little importance. How- great apes but much more in parenting effort (Lappan 2008). ever, this ignores influences of paternal care on other aspects Although males do not incur the metabolic costs of female of maternal and child morbidity and mortality. In particular, reproduction such as pregnancy and lactation, sexually di- fathers may exert influences on their offspring’s social success morphic mass and body composition results in investment and in turn on their reproductive prospects, something that in tissue that is reflective of reproductive effort in males (Bri- is not captured in the preceding analyses. Further, a major biescas 2001). Indeed, over a lifetime, the cumulative meta- influence of paternal care appears to be in shortening human Bribiescas, Ellison, and Gray Male Life History and the Emergence of Homo S427 birth intervals, helping women have more children than they Within societies, various studies have found that biological otherwise could (Marlowe 2010). fathers provide more direct or indirect care of their offspring Forms of paternal care can be distinguished in several ways. compared with stepfathers. This has held for men’s invest- Kleiman and Malcolm (1981) distinguished between direct ments in their children’s college educational expenses (An- and indirect care. Direct care includes holding, carrying, and derson, Kaplan, and Lancaster 1999), men’s financial expen- maintaining proximity to offspring, whereas indirect care en- ditures on their high school aged children (Anderson et al. compasses more distal forms such as protection and resource 1999), the time spent by Hadza forager fathers in direct care defense. Forms of direct care may require steeper trade-offs of children (Marlowe 1999), and the time spent by rural Trin- with male mating effort than indirect care, and indeed, much idad fathers with children (Flinn 1988). Other lines of evi- of the discussion concerning whether male behavior repre- dence are consistent with differential attachment and care of sents mating or parenting effort depends on how one inter- offspring depending on paternity. Most prominently, Daly and prets resource acquisition efforts (e.g., do men hunt in order Wilson (1999) suggest that the greater risk of child abuse and to provision family members or to gain status and repro- infanticide observed among stepchildren compared with bi- ductive benefits; Hawkes 1991). ological children in Canada, the United States, and elsewhere Within contemporary hunter-gatherer societies, the most is an outcome of differential male concern over these children. salient model for early Homo socioecology, most male re- Biological fathers are less likely to inflict such costly behavior source provisioning focuses on meat and honey. Considerable on their children than are stepfathers. debate has focused on whether big game hunting by forager Mothers are situated at the intersection between male care men represents mating effort or parenting effort. Because and offspring. The nature of a man’s relationship to an off- large game are widely shared in a forager camp and successful spring’s mother thus serves as an important factor associated hunters are often rewarded with reproductive benefits such with paternal care. More affiliative husband-wife relationships as additional wives or extramarital affairs (Kaplan and Hill are associated with greater direct care across populations 1985), some scholars suggest that male hunting represents (Whiting and Whiting 1975). They are also associated with mating effort (Hawkes 1991). However, fathers often target greater paternal care within societies such as the United States resources such as smaller game and honey that are prefer- (Parke 1996). Especially in the case of caring for young chil- entially shared with their families; in some cases a larger share dren, mothers may serve as “gatekeepers,” playing an im- of big game animals may reach a successful hunter’s family; portant role determining who has access to their offspring, and by several measures biological fathers tend to provide and this may include paternal access. This concept applies to more care of their offspring than do stepfathers (Gurven and postdivorce paternal care in the United States: poorer-quality Hill 2009). Accordingly, among foragers, male care likely rep- relationships between a custodial mother and a child’s father resents a mix of mating and parenting effort and a mix that are associated with lower paternal care. However, these re- can shift depending on context (e.g., Marlowe [1999] found lationships matter less as children, especially sons, grow older, less paternal care among Hadza living in larger camps). and in societies where fathers retain child custody in the event Paternity and paternity certainty are associated with pa- of divorce. ternal care, both between and within societies. Theory sug- Mothers structure male reproductive effort in another way: gests that males seek to channel their reproductive effort in males may provide care to mothers and their offspring in ways that maximize their own fitness; accordingly, men are order to garner mating opportunities with mothers. The con- expected to preferentially bias their care toward their own cept that male care, in this context, represents mating effort offspring. Across societies, men provide more indirect care in rather than parenting effort was initially highlighted through those societies where they have higher paternity certainty field research with baboons (Smuts and Gubernick 1992). The (Hartung 1985). More specifically, societies with matrilineal same concept may apply to human male care. The direct and inheritance tend to have lower paternity certainty because indirect care that stepfathers provide to stepchildren can be fathers are often less involved in day-to-day family life, conceptualized as mating effort—care designed to maintain whether because of engagement in long-distance warfare or reproductive access to the children’s mother. Given that subsistence activities drawing them away from mothers and mothers also value traits in potential mates associated with children. Conversely, societies with patrilineal inheritance, long-term emotional stability and capacity for providing in- where fathers pass resources to their children, are character- direct care (Buss 1989), even within long-term reproductive ized by higher paternity certainty in part because a father’s relationships, men’s care devoted to mothers and their off- relatives can aid observation of his wife’s fidelity. Genetic spring can be conceived in part as mating effort. evidence of patrilineality has been reported in Neanderthals Paternal investment has primarily been addressed through as has isotopic evidence for smaller and more localized home investigations of between- and within-societal variation in ranges, which can be cautiously interpreted as patrilineality patterns of direct and indirect paternal care. Paternal care in australopiths and paranthropines (Copeland et al. 2011; varies according to a host of factors: cultural transmission, Lalueza-Fox et al. 2011). Similar molecular and isotopic meth- mode of subsistence, marital system, rates of between-societal ods could be deployed in fossil Homo specimens in the future. aggression, sexual division of labor, demographic patterns, S428 Current Anthropology Volume 53, Supplement 6, December 2012 availability of allomothers, paternity and paternity certainty, investment in association with paternity uncertainty risk. In and the nature of a man’s relationship to a child’s mother. addition to the anticuckoldry strategies deployed by other This diverse array of factors highlights the relevance of so- primates, Homo males evolved a unique suite of abilities to cioecological context to the broad expression of human pa- adjust their investment in more subtle ways in response to ternal care, suggesting that male reproductive effort can be paternity uncertainty conditions. This is evident in the di- adjusted in facultative ways likely conducive to men’s repro- versity of paternal investment behaviors under varied con- ductive success. Such facultative adjustment indicates signif- ditions of paternity certainty in modern Homo (fig. 1). icant plasticity in Homo male reproductive strategies com- Unlike other primates, even those who invest in paternal pared with other great apes. investment, modern Homo sapiens males exhibit significant population variation in direct care of offspring. Hunter-gath- Plasticity in Male Reproductive Effort erer fathers tend to spend more time in proximity and directly caring for their young offspring than men living in small- Plasticity is the range of variation and responsiveness in a scale horticultural, agricultural, and especially pastoralist so- phenotypic or behavioral trait in response to an environ- cieties (Marlowe 2000a). Several quantitative studies of for- mental challenge. The obvious advantage of plasticity is the ager paternal care suggest that fathers spend around 5% of ability to adjust appropriately to environmental stochasticity waking hours in direct care of infants and toddlers (Fouts in a manner that maintains or increases an organism’s fitness. 2008). The Aka, where fathers spend around 20% of their day An organism with infinite plasticity would be tremendously hours in camp holding children, is an outlier among foragers successful. However, plasticity has costs resulting in a range but is likely explained by husband-wife subsistence activities of phenotypic and behavioral variation that is managed by centered on net hunting together (Hewlett 1991). Across so- proximate mechanisms that are subject to natural selection. cieties including hunter-gatherers, horticulturalists, agricul- In essence, the range of trait plasticity is itself an important turalists, and pastoralists, several factors underlie this varia- adaptation (Pigliucci 2001). Compared with other great apes, tion in direct paternal care across subsistence mode. The phenotypic and behavioral plasticity are among the most im- sexual division of labor in hunter-gatherers may allow fathers portant traits in Homo as demonstrated by the geographic and mothers to spend more time near each other in relaxed expansion out of Africa into novel ecological settings (Fin- ways, fostering paternal care. Furthermore, hunter-gatherers layson 2005). The broad geographic and ecological range of tend to have lower rates of polygyny and often have lower Homo signals an extraordinary ability to adjust to environ- rates of between-group aggression, both factors that draw men mental and social variability. While some reflections of re- away from direct care in favor of investment in male-male productive effort, such as sexual dimorphism, inextricably relationships and additional mates (Gray and Anderson 2010; covary with female reproductive effort (e.g., body size), phe- Marlowe 2000a). These contexts that are similar to early Homo notypic and behavioral plasticity reflecting adjustments to re- socioecology suggest that wider socioecological factors shap- productive strategies are evident in many male mammals, including humans. Indeed, because body size sexual dimor- phism and its accompanying metabolic cost differences are likely to be smaller than initially thought in early Homo (Graves et al. 2010), more plastic aspects of male reproductive effort, such as the extent and form of paternal care, probably took on greater importance. Male plasticity provides the ability to respond to an ever- changing environmental and social landscape. However, as- sociated costs include the maintenance of detection mecha- nisms of change, possible misinformation from cues, and the need to reallocate, refurbish, and rebuild somatic resources such as muscle and fat more frequently in response to en- vironmental shifts (Relyea 2002). Arguably the most impor- tant cost of male reproductive effort plasticity is the misas- sessment of paternity certainty and cuckoldry, a hurdle that impinges on the evolution of paternal care and mate invest- ment. Accurately determining paternity is challenging because of internal fertilization, with numerous behavioral strategies evolving such as mate guarding, sperm plugs, the development of affiliations with mothers, and infanticide, just to name a few (Busse 1985). Males would either have had to decrease Figure 1. Summary of the observed diversity of male direct and the probability of cuckoldry or adjust their mate and paternal indirect reproductive investment behaviors in modern humans. Bribiescas, Ellison, and Gray Male Life History and the Emergence of Homo S429 ing subsistence, between-group aggression, and marriage pat- and ecology seems to have resulted in the potential for the terns also influence the specifics of direct paternal care. evolution of “contingency strategies” in response to the risk Men also exhibit population variation in indirect care of of nonpaternity. Partible paternity may be an example of such offspring. Highlighting a role for resource provisioning (e.g., a contingency strategy. In some societies, different men are food, money), indirect care also varies across subsistence acknowledged to be the father of the same child. Walker, Flinn, mode (Marlowe 2000a). Men in pastoralist societies tend to and Hill (2010) have discussed the role of partible paternity provide the most resource provisioning, followed by men in and the possible fitness benefits in several native South Amer- pastoralist and hunter-gatherer societies, with men in horti- ican populations. Among many of these populations, a com- cultural societies providing the least. Here, the livestock such munity consensus on paternity is determined in a number of as cattle and camels provided by a father plays important ways that involve belief systems of how children are conceived. roles in subsistence (e.g., meat or blood from animals) and The result is a partitioning of paternal investment in the face in his offspring’s—and often sons in particular—reproductive of high levels of paternity uncertainty. It is impossible to prospects. The livestock a father provides as bridewealth to determine whether such a social arrangement had any impact his male relatives may make the difference between their abil- on the evolution of our genus, but it does introduce the ity to marry or not. But what of paternal care when fatherhood possibility of paternity becoming a social currency that can is accepted by the male? Paternal care exhibits tremendous be exchanged and bartered for benefits such as greater male- variation, suggesting that it is not obligatory but rather best male affiliation and future mate access. It also illustrates the viewed as the product of adaptive male plasticity in repro- range of plasticity that can reconcile paternity uncertainty and ductive effort interacting with female (e.g., mate) and off- the care and provisioning needs of high-maintenance altricial spring (e.g., parent-offspring conflict) life history agendas in offspring (table 1). specific socioecological contexts. Across larger-scale societies, including contemporary Older Fathers: A Unique Development nation-states, direct paternal care varies considerably. Roop- in Homo? narine (cited in Gray and Anderson 2010) has summarized much of this quantitative variation, finding that fathers in The potential for significant fitness later in life is an important Japan spend about 20 minutes daily with their children, life history trait in modern humans (Bribiescas 2006, 2010). whereas fathers in India spend around 3–5 hours daily with Although spermatogenesis and the capacity to fertilize ova is their young children. Many fathers spend no time engaged somewhat compromised compared with younger men (de La in direct care. To try understanding the variation in direct Rochebrochard et al. 2006), reproductive hormone function paternal care across this larger-scale swath of societies, in- remains largely intact (Bribiescas 2005; Ellison et al. 2002), cluding the United States and European countries today, var- with cross cultural demographic assessments indicating sig- ious factors are likely at play. The sexual division of labor nificant male fertility after the age of 50 (Tuljapurkar, Pules- varies, with some cases favoring male focus on providing ton, and Gurven 2007). Fitness at later life obviously requires indirect care rather than direct care, as has been the case for an increase in longevity and the involvement of younger, pre- urban Japan (Schwalb et al. 2010). As more and more women menopausal females. The evolution of longevity in Homo has have entered the global competitive labor market in recent centered on the selection for genes that favor larger bodies decades, in the United States and elsewhere, fertility has de- and longer lives. However, what selection factors would have clined, and men have increased the time devoted to direct allowed and cultivated fertility at older ages in males? paternal care within a changing sexual division of labor (Gau- There is no evidence of early Homo cultivating or raising thier, Smeeding, and Furstenberg 2004). The availability of animals or crops or any other resource that could be accu- allomothers such as grandmothers or siblings affects direct paternal care. Where such caregivers are available, fathers may Table 1. Occurrence of significant paternal investment in provide less direct paternal care; indeed, among the Hadza, apes under various conditions of paternity certainty Bofi foragers, and Khasi of northern India, male care is neg- atively associated with grandmaternal involvement (Fouts Possible Multiple Likely 2008). Further, the availability of mates may influence direct Genus No paternity paternity paternity paternity paternal care. In demographic contexts with female-biased Homo XXXX sex ratios or high variance in male mate value, males may Pan 0 allocate their reproductive effort toward mating effort rather Gorilla 0 than direct child care. Pongo 0 Hylobates 0X Another intriguing example of the extreme malleability of paternal organization in Homo is the possibility of partitioning Note. “Significant” is defined as exhibiting enough direct offspring care and/or provisioning to be indicative of a defining trait in a species. Xs paternity between different males. The high value of paternal indicate significant occurrence of paternal investment. Zeros indicate investment, long lives, and the importance of navigating a nonhuman multiple paternity; this is culturally defined and cannot be social landscape that is shaped by complex culture, language, assessed outside of modern Homo. S430 Current Anthropology Volume 53, Supplement 6, December 2012 mulated and sequestered in the same manner that supports passed to daughters. Therefore, if older males can procure the accumulation of wealth and polygyny in modern Homo mating opportunities because of their ability to secure re- sapiens (Cronk 1991). Therefore, if males were fathering chil- sources through skill and mental capacity as opposed to phys- dren at older ages, it was the result of some other resource ical prowess, this would result in significant male fertility at or ability that benefited female fertility and/or child survi- older ages, a trait unique to Homo (fig. 2). vorship. One possibility is the leveraging of age-derived skill This also has implications for the evolution of human lon- and experience. Among modern forager groups, older men gevity, menopause, and the role of grandmothers. For ex- tend to have higher caloric returns from hunting compared ample, Eisenberg (2011) suggests that telomere length is fa- with younger men who are stronger or more physically fit, vored when older men father offspring. Offspring of older suggesting that skill and experience can supersede the physical men tend to have longer telomeres, a possible reflection of ability and strength of younger men (Walker and Hill 2003; increased investment in somatic maintenance. Marlowe ar- Walker et al. 2002). Older men can also provide child care gues further that increases in male fertility at older ages and that is especially valuable for extremely altricial offspring. selection for genes that increase longevity can be passed on Leveraging age, experience, and skill for greater fitness to daughters who then live past the viability of their ova. should result in greater mating opportunities and significant Consequently, the evolution of increased longevity via greater fertility in older men. However, the common understanding male fertility at older ages may have contributed to the emer- based on classic female-based demography is that human ag- gence of female longevity and postreproductive female re- ing outpaces reproduction in a manner that is contrary to productive effort through grandmother-based provisioning what would be expected by natural selection (Hamilton 1966). and child care (Hawkes et al. 1998; Tuljapurkar, Puleston, and But in contrast to common acceptance of low male fertility Gurven 2007). at older ages, one that basically mirrors menopause in in- dustrial societies, Marlowe (2000b) and Charlesworth (2001) 1 suggested fertility in older males ( 50 years old) to be higher Proximate Mechanisms and Male Life History in nonindustrialized populations. A comparison of male fer- tility in several populations by Tuljapurkar, Puleston, and As with most other vertebrates, reproductive effort in Homo Gurven (2007) supports their assertion, arguing that fertility is under considerable hormonal control, regulating energetic at older ages provides the selective advantage that results in resources between investment in mating effort, survivorship, greater life span, with genes associated with longevity being and paternal care (Bribiescas 2001). Understanding the role

Figure 2. Fertility distributions (in age-specific fertility [ASF] rates as a fraction of total fertility [TF] rate) for women (dashed line) and men (solid black line) for the hunter-gatherer Dobe !Kung of Botswana, the forest-living Ache, the Amazonian forager- horticulturalist Yanomamo, the Bolivian forager-horticulturalists Tsimane, agricultural Gambian villagers, and modern Canadians. The shaded area represents realized male fertility after the age of last female reproduction (Tuljapurkar, Puleston, and Gurven 2007). A color version of this figure is available in the online edition of Current Anthropology. Bribiescas, Ellison, and Gray Male Life History and the Emergence of Homo S431 of hormones in hominin evolution has potential but must be vide useful insights (Catlett et al. 2010). However, testing done cautiously because we are limited to using extant great hypotheses regarding hominin behavior using the fossil record ape models of endocrine function that may have differed in is a daunting task. Sexual dimorphism in the mammalian significant ways from other extinct hominins (Crews and Ger- fossil record is among the most salient reflections of behavior ber 2003). Nonetheless, early Homo life history and morpho- that can be discerned from extinct species; however, the fossil logical traits are more in line with modern human traits com- record of Homo is relatively sparse compared with other mam- pared with other great apes. Therefore, analyses of hormonal mals, resulting in vigorous debate around body size estimation aspects of reproductive strategies in modern human males and sexual dimorphism (Anto´n and Snodgrass 2012; Graves can be assumed to be at least a modest reflection of early et al. 2010; Plavcan 2012; Pontzer 2012). Nonetheless, the Homo. possibility of discerning cues of male reproductive effort in As in other species, human male reproductive effort is the fossil record using specific areas of morphology that are largely influenced by testosterone, which governs somatic and related to reproduction would be extremely useful. For ex- behavioral investment allocations (Bribiescas 1996, 2001). ample, baculum length relative to body size has been suggested Testosterone also has a negative effect on immune function to be associated with mating strategies, with the smallest bac- and allocation trade-offs between maintenance and repro- ulums being observed in more pair-bonded primate species ductive effort (Bribiescas and Ellison 2007; Muehlenbein and (Dixson 1987; Martin 2007). Unfortunately, only one primate Bribiescas 2005). In general, humans exhibit a 10-fold range baculum from an unidentified Eocene adapiform has been of variation in testosterone levels under daily conditions (Zitz- found in the fossil record (von Koenigswald 1979). The lack mann and Nieschlag 2001), although nonindustrial popula- of baculum in modern humans is difficult to interpret because tions exhibit lower levels and less variation, which are likely the absence of the baculum does not necessarily mean that to be more indicative of early Homo endocrine function com- as a species, we fall at the absolute lower end of the range of pared with more modern ecological settings (Bribiescas 1996, primate size variation. Nonetheless, the discovery of a hom- 2001). Age can also attenuate testosterone (Harman et al. inin baculum (if present) would be informative. 2001), although the degree and pattern change with age is The examination of other morphological characters that less in nonindustrial societies (Bribiescas and Hill 2010; El- are under the influence of sex hormones and indicators of lison et al. 2002). reproductive behaviors is a palpable possibility. For example, After controlling for energetics, age, and other extraneous sex-specific differences in the pelvis reflect variation between factors, men who traditionally spend more time with their males and females in the action and circulating levels of es- children exhibit lower testosterone levels than men who do trogens. Similar research might be deployed to explore tes- not (Muller et al. 2009). A longitudinal investigation of pair- tosterone-sensitive areas of male skeletal morphology, such as bonded Filipino men before and after becoming fathers re- craniofacial features, and cautiously testing for associations vealed a 26% and 34% decrease in median levels of morning with aspects of reproductive effort, such as behavior, attrac- and evening testosterone, respectively, compared with single tiveness, and competitiveness. Obviously there are tremen- nonfathers (Gettler et al. 2011). The selective factors involved dous hurdles to consider, not the least of which is sorting out with these testosterone differences in association with pater- sources of inter- and intraspecific variation. However, given nity are better understood and documented in other verte- the paucity of information available from the Homo fossil brates, such as lower offspring mortality due to paternal in- record and the compelling information that has been derived vestment and provisioning (Ketterson et al. 1992); however, regarding craniofacial morphology, reproductive behavior, they are less clear in Homo. and hormones in modern humans, this is certainly worthy The physiology of human reproductive behavior is also of consideration. modulated by variation in neuropeptide hormones such as Associations between fossil teeth and sex hormones would oxytocin, vasopressin, and prolactin, reflecting facultative ad- be of great value. However, sex hormones do not exhibit any justment of paternal care (Gray and Anderson 2010). These significant relationship with variation in tooth morphology, hormones commonly affect paternal investment in many such as crown size in modern humans (Guatelli-Steinberg, mammals and all but certainly affected the behavioral rep- Sciulli, and Betsinger 2008). Craniofacial sexual dimorphism ertoire of early Homo (Wynne-Edwards 2001). The ranges of is a viable alternative because it is not isometrically related testosterone within and between individuals as well as within with general body size dimorphism in primates and many and between populations illustrate the range of male Homo other organisms, with significant taxonomic differences in the plasticity. association between craniofacial and body size sexual dimor- phism (Plavcan 2003). Craniofacial sexual dimorphism seems Deriving Evidence of Reproductive Strategies to have been significantly influenced by selection factors that from the Homo Fossil Record are largely independent from those affecting sex differences in overall body size. Moreover, associations between behavior Viewing the hominin fossil record through the lens of life and sexually dimorphic features such as canine size and body history theory, energetics, and reproductive ecology can pro- size in primates are subject to significant error ranges and S432 Current Anthropology Volume 53, Supplement 6, December 2012

effects of castration, testosterone supplementation, and en- ergetic stress on skull sexual dimorphism in rats. Their find- ings showed that castration, testosterone supplementation, and energetic stress, individually and in combination, had a significant influence on skull sexual dimorphism as well as variation in androgen-sensitive craniofacial features. Estrogen supplementation of ovarectomized rats had no effect. So what testosterone-sensitive craniofacial features should be assessed in Homo or any other primate model? Such a question requires a much greater and more detailed discussion than what can be provided now. However, there are some encouraging road signs that may provide some initial guid- ance. Low-dose testosterone treatment of boys with delayed puberty revealed significant changes in craniofacial features compared with untreated boys. Significant distance-length in- creases between predefined landmarks in testosterone-treated boys were in mandibular ramus length, upper anterior face height, and total cranial base length (Verdonck et al. 1999; fig. 3). Because the focus of this study was on orthodontics, unfortunately no measurements were made on other andro- gen-sensitive sites such as the brow ridge. Using this very preliminary guidance, the following strategy might be deployed with the fossil record. (1) Determine the Figure 3. Enhanced craniofacial bone growth (arrows) between predefined points in response to low-dose testosterone treatment presence, distribution, and density of androgen receptors on in delayed-puberty boys (114 years old,n p 7 ) compared with craniofacial features in a primate model. Modern humans untreated height-matched controls (n p 7 ; Verdonck et al. 1999). would seem to be the most phylogenetically appropriate spe- cies. (2) Determine and control for allometric effects between craniofacial features and body size. (3) Conduct within-genus should be interpreted with caution (Plavcan and van Schaik 1997). While investment in larger body size and perhaps ca- (Homo) comparisons of the size, shape, landmark distances, nine size indicates metabolic investment in physical compet- and bone thickness of fossil craniofacial regions that are as- itive ability, evidence from modern humans suggests that sociated with high concentrations of testosterone receptors. craniofacial characteristics serve as cues of attractiveness, mate (4) Compare variation in testosterone-sensitive craniofacial quality, paternal investment, and competitiveness (Perrett, regions in Homo fossil specimens with modern human male May, and Yoshikawa 1994; Pound, Penton-Voak, and Surridge reproductive behaviors and associations (i.e., attractiveness). 2009; Roney et al. 2006; Waynforth, Delwadia, and Camm Drawing on modern human information, changes or dif- 2005). Many if not all of these craniofacial features are the ferences in androgen-sensitive craniofacial regions in the fossil result of testosterone variation during development (Verdonck record could then be used (cautiously) as an indication of et al. 1999). the evolution of male features that may be sensitive to female The identification of testosterone receptors in bone is well choice or indicators of intrasexual signaling. Obviously pleio- established (Colvard et al. 1989). Surprisingly, much of the tropic and other factors would need to be identified and evidence for the effects of testosterone on craniofacial features explored. is indirect, emerging from growth observations during human Beyond craniofacial and hormone associations, recent ad- male puberty or from receptor mapping in rodent models vances in sequencing the genome of Neanderthals and other (Lin et al. 2004; Pirinen 1995) with no direct mapping of prehistoric organisms raise the possibility of employing sim- craniofacial androgen receptors in any primate model. Com- ilar methods in early Homo specimens (Asara et al. 2007; parisons of orchidectomized and sham-operated newborn male mice indicate that testosterone presence does not affect Green et al. 2010), although significant hurdles remain (Aus- overall skull size but does result in differential craniofacial tin, Smith, and Thomas 1997), especially given the tropical growth patterns. Parallel comparison of ovarectomized and distribution of most early Homo specimens. If these hurdles sham-operated newborn mice indicates only modest estrogen can be overcome, exploring gene variants that regulate hor- influences, thereby supporting the dominant role of testos- mones associated with paternal behavior would be of great terone in sex differences in craniofacial morphology (Fujita utility toward understanding the evolutionary role of male et al. 2004). Dahinten and Pucciarelli (1986) examined the Homo behavior. Bribiescas, Ellison, and Gray Male Life History and the Emergence of Homo S433 Conclusion Brown, Frank, John Harris, Richard Leakey, and Alan Walker. 1985. Early Homo erectus skeleton from west Lake Turkana, Kenya. Nature 316:788– Understanding male life history and forging new and exciting 792. Buss, David M. 1989. Sex differences in human mate preferences: evolutionary methods for testing hypotheses that emerge from life history hypotheses tested in 37 cultures. Behavioural and Brain Sciences 12:1–49. theory regarding the emergence of the genus Homo should Busse, Curt D. 1985. Paternity recognition in multi-male primate groups. be a top research priority for anthropologists. As the fossil American Zoologist 25:873–881. Calow, Peter. 1979. The cost of reproduction: a physiological approach. Bi- record of early Homo grows, it would be ideal to have methods ological Reviews 54:23–40. such as those outlined at the ready to expand our under- Catlett, Kierstin K., Gary T. Schwartz, Laurie R. Godfrey, and William L. standing of the emergence and evolution of our genus. Jungers. 2010. “Life history space”: a multivariate analysis of life history variation in extant and extinct Malagasy lemurs. American Journal of Physical Anthropology 142:391–404. Charlesworth, Brian. 2001. Patterns of age-specific means and genetic vari- ances of mortality rates predicted by the mutation-accumulation theory of Acknowledgments ageing. Journal of Theoretical Biology 210:47–65. Clutton-Brock, Timothy H. 1984. Reproductive effort and terminal investment We thank Brenda Bradley, Erin Burke, Jessamy Doman, An- in iteroparous animals. American Naturalist 123:212–229. drew Hill, Marcia Inhorn, Grazyna Jasienska, Robert Walker, Colvard, Douglas S., Erik F. Eriksen, Philip E. Keeting, Elizabeth M. Wilson, and Tim Webster for their insights into genes, fossils, and all Dennis B. Lubahn, Frank S. French, B. Lawrence Riggs, and Thomas C. Spelsberg. 1989. Identification of androgen receptors in normal human things male and paternal. Susan Anto´n, Leslie Aiello, and the osteoblast-like cells. Proceedings of the National Academy of Sciences of the Wenner-Gren symposium participants made invaluable sug- USA 86:854–857. gestions that vastly improved this paper. Copeland, Sandi R., Matt Sponheimer, Darryl J. de Ruiter, Julia A. Lee-Thorp, Daryl Codron, Petrus J. le Roux, Vaughn Grimes, and Michael P. Richards. 2011. 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Evolution of Cooperation among Mammalian Carnivores and Its Relevance to Hominin Evolution

by Jennifer E. Smith, Eli M. Swanson, Daphna Reed, and Kay E. Holekamp

CAϩ Online-Only Material: Supplement A with PDF

Anthropological theory suggests direct links between the origins of cooperation in hominins and a shift toward an energy-rich diet. Although the degree to which early hominins ate meat remains controversial, here we reevaluate the notion, originally suggested by Schaller and Lowther in 1969, that mammalian carnivores can shed light on human origins. Precisely when cooperation evolved in hominins or carnivores is unknown, but species from both groups cooperatively hunt large game, defend resources, guard against predators, and rear young. We present a large-scale comparative analysis of extant carnivore species, quantifying anatomical, ecological, and behavioral cor- relates of cooperation to determine whether metabolic rate, body and relative brain size, life history traits, and social cohesion coevolved with cooperation. We focus heavily on spotted hyenas, which live in more complex societies than other carnivores. Hyenas regularly join forces with kin and nonkin to hunt large antelope and to defend resources during intergroup conflicts and disputes with lions. Our synthesis highlights reduced sexual dimorphism, increased reproductive investment, high population density, fission-fusion dynamics, endurance hunting of big game in open habitats, and large brains as important correlates of cooperation among carnivores. We discuss the relevance of our findings to understanding the origins of cooperation in hominins.

Semmann 2010; Noe¨ 2006; Nowak 2006; Queller 1985; West, The evolutionary trajectory from hominin to humanity, El Mouden, and Gardner 2011; West, Griffin, and Gardner from small-brained australopithecine to encephalised 2007). Nevertheless, solving this mystery remains central to Homo erectus, began 2.6 Ma with an interest in meat. understanding the unprecedented capacity for human range (Bunn 2006:205) expansion into an extraordinary diversity of habitats across The evolutionary origins and maintenance of cooperation the globe (Bingham 1999). pose an evolutionary puzzle for anthropologists and biologists Although there is much ongoing debate about the precise composition of the diet of early hominins (e.g., degree to (reviewed by Clutton-Brock 2009a; Dugatkin 2002; Melis and which it included nuts, tubers, and protein and fat from an- imals), most current anthropological scenarios suggest a direct Jennifer E. Smith is an Assistant Professor of Biology at Mills College link between a transition toward eating a high-quality diet (5000 MacArthur Boulevard, Oakland, California 94613, U.S.A. and the evolution of cooperation in hominins (e.g., Aiello [[email protected]]). Eli M. Swanson is a PhD candidate in the and Wheeler 1995; Bramble and Lieberman 2004; O’Connell, Zoology Department and Ecology, Evolutionary Biology, and Hawkes, and Blurton Jones 1999; O’Connell et al. 2002; Behavior (EEBB) Program (203 Natural Science Building, Michigan Pontzer 2012; Wrangham et al. 1999). Although the precise State University, East Lansing, Michigan 48824, U.S.A.). Daphna timing of events remains elusive, the suite of cooperative be- Reed is an undergraduate in the Institute for Society and Genetics, haviors that have been suggested to coevolve with a rich hom- University of California, Los Angeles (Box 957221, 1323 Rolfe Hall, inin diet includes group hunting, defense of food and space, Los Angeles, California 90095-7221, U.S.A.). Kay E. Holekamp is a Distinguished University Professor of Zoology and Director of the protection from predators, and care of young (e.g., Bunn EEBB Program (203 Natural Science Building, Michigan State 2006; Bunn and Kroll 1986; Byrne 1995; Grove 2010; Hart University, East Lansing, Michigan 48824, U.S.A.). This paper was and Sussman 2009; Milton 1999; Ungar 2012; Wrangham et submitted 12 XII 11, accepted 6 VII 12, and electronically published al. 1999). 13 XI 12. Three major ecological models proposed to explain hom-

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0014$10.00. DOI: 10.1086/667653 Smith et al. Carnivore Cooperation S437 inin evolution are currently prevalent in the literature. The Here we use the term “carnivore” to refer to those extant first two models focus on the importance of eating a calorie- species of mammals belonging to the order Carnivora re- rich diet but differ in their emphasis on the nature of the gardless of their dietary niche. The order Carnivora arose calorie-rich diet and how foraging shaped the origins of co- during the late Paleocene from a radiation of mammals whose operation (reviewed by Pontzer 2012). The “hunting-scav- diet was comprised primarily of meat (Wilson and Mitter- enging” model emphasizes the importance of energy-rich meier 2009). Importantly, however, extant carnivores occupy meat and bone marrow in the hominin diet. Some variants a vast range of habitats and many ecological niches; species of this model propose that natural selection favored coop- in this order belong to dietary classes that include herbivores, eration among individuals that hunted large game using per- insectivores, omnivores, piscivores, and carnivores (Wilson sistence running (also called “cursorial hunting”), while oth- and Mittermeier 2009). Although the extent to which early ers emphasize cooperation and food sharing with younger, hominins ate meat is the subject of ongoing debate, there is less able or less successful kin (Aiello and Wheeler 1995; growing evidence that additional aspects of hominin sociality Bramble and Lieberman 2004; Kaplan et al. 2000). The second might resemble extant mammalian carnivores. For instance, model is the “underground storage organ” (USO) model that as is the case for many mammalian carnivores (reviewed by emphasizes gathering USOs (such as tubers), food sharing, Palomares and Caro 1999), early hominins also were likely and sometimes cooking (O’Connell, Hawkes, and Blurton hunted or otherwise killed by carnivores (Hart and Sussman Jones 1999; Wrangham et al. 1999). It suggests that a shift 2009). The evolution of cooperative defense of food and space, toward an arid climate favored exploitation of these calorie- breeding, and protection from predators as well as fission- rich foods and emphasizes the role of elders in provisioning fusion dynamics (see below) in the order Carnivora suggests younger kin. Where these models posit increased energetic that this taxonomic group continues to offer underexploited benefits from intergenerational cooperation, arguments can opportunities for testing hypotheses relevant to the evolution be made for the coevolution of increases in the length of of hominins regardless of the precise diets of early hominins. lactation, gestation, and longevity as well as increases in ne- Evidence that early hominins included some meat in their onate and adult body mass and daily energy expenditure but diet from the Pleistocene onward and perhaps earlier becomes a decrease in sexual dimorphism. In contrast to these two increasingly common as we move forward in the archaeo- diet-related hypotheses, the “predator protection” hypothesis logical record. Although stone tools may have been used pri- suggests that cooperation evolved because of intense preda- marily for processing vegetative foods (Grine and Fleagle tion by large-bodied carnivores and that selection favored an 2009), discoveries of fossilized bones with butchery marks increase in relative brain size to permit complex forms of suggest early hominins might have used stones to remove cooperative defense required to outwit predators (Hart and energy-rich flesh from the carcasses of large mammals by 2.5– Sussman 2009). 3.4 Ma (McPherron et al. 2010; but see Domı´nguez-Rodrigo, Pickering, and Bunn 2010, 2011). Moreover, sharp-edged cut- Relevance of Extant Mammalian Carnivores to ting tools and cut-marked animal bones at Gona, Ethiopia Testing of Ecological Models (Semaw et al. 1997), and stone caches at Olduvai, Tanzania (Bunn and Kroll 1986; Potts and Shipman 1981), suggest Foundational inquiries about the social lives of early hominins hominin butchery and consumption of skeletal muscle and focused primarily on nonhuman primates (e.g., Reynolds tissues by 2.6 Ma (Potts 2012). By 2.5–2.0 Ma, stone tool 1966; Washburn and Devore 1961), and primate research con- transport (e.g., carrying stones hundreds of meters) for ex- tinues to be an import source of inference today (e.g., Fuentes, tractive foraging permitted access to new resources (Potts Wyczalkowski, and MacKinnon 2010). Nonetheless, Schaller 2012). Molar morphology and microwear data indicate die- and Lowther (1969) provided the transformative insight that tary expansion to include items with mechanical properties the ecologies of modern hunter-gathers—and by inference consistent with those of animal fat and protein around 2.0–1.8 those of early hominins—might closely resemble those of Ma (Ungar 2012). Fauna in archeological contexts suggest extant carnivores. Schaller and Lowther (1969:308) proposed persistent foraging on game by 2.0–1.5 Ma (Potts 2012). that “it might be more productive to compare hominids [now Nonetheless, the debate continues regarding how early hominins] with animals which are ecologically but not nec- hominins acquired prey animals (Bunn and Kroll 1986; Potts essarily phylogenetically similar, such as the social carnivores.” and Shipman 1981). Were prey run to exhaustion, ambushed This landmark paper was followed by several pioneering stud- at short range, or passively scavenged from carcasses aban- ies on wild carnivores (e.g., Kruuk 1972; Mech 1970; Schaller doned by mammalian carnivores (Bramble and Lieberman 1972). Ongoing research continues to reveal new complexities 2004; Bunn and Pickering 2010; Domı´nguez-Rodrigo and about the social lives of carnivores. Because the behavioral Pickering 2003; Shipman 1986)? Which physical, ecological, traits proposed to be important for hominin evolution are and social factors facilitated the evolutionary leap from Aus- also salient features in the lives of social carnivores, study of tralopithecus to early Homo? To answer these questions, we this taxonomic group might indeed offer important insights. search here for convergences between early hominin foragers S438 Current Anthropology Volume 53, Supplement 6, December 2012 and extant carnivores (e.g., Finarelli 2010; Finarelli and Flynn among carnivores, and access to food is critical to individual 2009). fitness (e.g., Carbone et al. 2005; Courchamp, Rasmussen, Our overarching goal is to provide an updated assessment and Macdonald 2002; Holekamp, Smale, and Szykman 1996). regarding whether the behavior of extant mammalian car- Even within the most stable groups of carnivores, intense nivores is indeed relevant to understanding early hominins competition disrupts grouping behavior (reviewed by Aureli irrespective of the degree to which the hominins may have et al. 2008; Holekamp, Boydston, and Smale 2000; Smith et been carnivorous. We draw on a unique combination of new al. 2008). Whereas individual African wild dogs living in co- knowledge and new computational tools unavailable to hesive groups maximize per capita energy gain when hunting Schaler and Lowther in the 1960s to reevaluate this notion. in large packs (Creel and Creel 1995), individual spotted hy- We first review the current literature on cooperation in mam- enas, especially low-ranking ones, accrue the greatest energetic malian carnivores, focusing primarily on new data on one benefits when they hunt alone (fig. 1; Smith et al. 2008). highly cooperative species, the spotted hyena Crocuta crocuta, Hunting in groups larger than an optimal size is also costly to update the original framework presented by Schaller and to lions (Packer, Scheel, and Pusey 1990). Lowther (1969). Then we perform a large-scale comparative Intense competition leads most social carnivores to live in analysis on extant species from Carnivora to identify variables groups structured by fission-fusion dynamics in which in- permitting and constraining cooperation. Finally, we consider dividuals regularly break up into small foraging parties when these findings in light of current ecological models proposed food is scarce and gather again when food is abundant (re- to explain the evolutionary origins for cooperation in the viewed by Smith et al. 2008). For example, dholes (Cuon genus Homo. alpinus; Venkataraman, Arumugam, and Sukumar 1995), white-nosed coatis (Nasua narica; Gompper 1996), European Feeding Competition and Fission-Fusion badgers (Meles meles; Kruuk and Parish 1982), and kinkajous Dynamics in Extant Social Carnivores (Potos flavus; Kays and Gittleman 2001), as well as spotted, brown (Hyaena brunnea), and striped (Hyaena hyaena; Kruuk Most (85%–90%) terrestrial mammalian carnivores are sol- 1976; Mills 1990; Smith et al. 2008; Wagner 2006) hyenas itary, interacting exclusively with their mates and offspring or temporarily leave (fission from) their companions to avoid alien conspecifics at territorial boundaries (reviewed by Hole- competitors when feeding. Members of each of these species kamp, Boydston, and Smale 2000). Sociality appears to have also regularly meet up again and spend time with (fusion arisen as a derived trait because the ancestral condition within with) conspecifics when the benefits of group living are high most carnivore families is to live solitarily (Dalerum 2007). (reviewed by Aureli et al. 2008; Creel and Macdonald 1995). Group life permits individuals to detect or evade predators or to improve their ability to acquire or defend resources (Johnson et al. 2002). In some species of carnivores, gregar- Maternal Capital, Tolerance, and Coalitions in iousness itself may have been favored by improved energy Hyenas and Other Carnivores intake (Creel and Macdonald 1995; Dalerum 2007). Some of Social Complexity of Spotted Hyenas the best-studied cooperative hunters include spotted hyenas (Holekamp et al. 1997; Kruuk 1972; Smith et al. 2008), lions Spotted hyenas represent a well-studied species; these hyenas (Panthera leo; Packer and Ruttan 1988; Packer, Scheel, and live in societies that are considerably more complex than those Pusey 1990; Scheel and Packer 1991), African wild dogs (Ly- of other gregarious carnivores (Drea and Frank 2003; Hole- caon pictus; Creel 1997; Creel and Creel 1995), and wolves kamp, Sakai, and Lundrigan 2007). In fact, their social lives (Canis spp.; Mech 1970). For these species, prey animals rep- are strikingly similar to those of many species of Old World resent large, ephemeral packets of energy-rich food that occur monkeys. Spotted hyenas are an interesting species in which unpredictably in space and time. Often several hunters may to investigate the evolution and mechanisms promoting co- be required to secure a single prey animal, each of which may operation in carnivores. Most social carnivores—including weigh hundreds of kilograms. Although lions assume specific wolves, social mongooses such as meerkats (Suricata suri- roles when hunting in groups (Heinsohn and Packer 1995; catta), lions, and wild dogs—live in small groups in which Stander 1992), there is no evidence that lions or other car- adult members of each sex are closely related to one another nivores rely on advanced planning to capture prey (Hole- (Clutton-Brock 2002; Creel and Creel 1991). In contrast, spot- kamp, Boydston, and Smale 2000). For example, even though ted hyenas reside in large permanent social groups called spotted hyenas are efficient hunters and directly kill 60%– “clans” (Kruuk 1972), consisting of up to 90 or more indi- 95% of the food they eat, these carnivores appear to follow viduals with low mean relatedness (Holekamp et al. 2012). simple rules when hunting together, such as “move wherever Hyena clans are strikingly similar in their size, composition, you need to in order to keep the selected prey animal between and hierarchical organization to troops of Old World mon- you and another hunter.” keys. Like troops of macaques, baboons, and vervet monkeys, Given the nature and distribution of their food resources, hyena clans contain multiple adult males and multiple ma- contest competition at ungulate carcasses is often intense trilines of adult female kin and their offspring (Frank 1986). Smith et al. Carnivore Cooperation S439

During an early stage of ontogeny, each hyena comes to understand its own position in its clan’s dominance hierarchy (Holekamp and Smale 1993; Smale, Frank, and Holekamp 1993). This process requires a type of associative learning called “maternal rank inheritance” in which the mediating mechanisms are virtually identical to those operating in cer- copithecine primates (Engh et al. 2000; Holekamp and Smale 1991). In fact, because of their aptitude for social learning, spotted hyenas are capable of solving cooperation problems in captivity (Drea and Carter 2009).

Maternal Capital Influences Reproductive Success of Spotted Hyenas Recent data suggest that maternal capital, in terms of both social allies and energy reserves, has important life history consequences for mammals (Bribiescas, Ellison, and Gray 2012; Isler and van Schaik 2012; Wells 2012). Social capital of mothers clearly is important for nonhuman primates such as in baboons Papio spp. (Silk, Alberts, and Altmann 2003; Silk et al. 2009). Similarly, data from spotted hyenas living in “baboon-like” societies suggest that maternal phenotype and maternal rank in particular have profound effects on female reproductive success (Holekamp et al. 2012). Support net- works, especially among maternal kin, endure across the life span despite ecological constraints imposed on them by fluc- tuating availability of resources (Holekamp et al. 2012). Be- cause social status determines priority of access to kills, high rank has enormous effects on hyenas’ net energy gain (Hofer and East 2003; Smith et al. 2008). Birthrates and survivorship are so much greater for high- than for low-ranking hyenas (Watts et al. 2009) that dominants tend to have many more surviving kin in the population than do subordinates (Hole- Figure 1. Per capita energy gain as a function of foraging group kamp et al. 2012). As a result of these large networks of allies, size among adult (A) African wild dogs Lycaon pictus (reprinted high-ranking hyenas have the most social capital (e.g., Smith from Creel 1997 with permission from Elsevier) and (B) spotted et al. 2010; Van Horn et al. 2004). hyenas Crocuta crocuta (reprinted from Smith 2008 with per- Compared with most other carnivores, spotted hyenas have mission from Elsevier). Points in A represent mean numbers of a prolonged period of fetal development, are of unusually wild dogs, with point size proportional to the number of ob- large mass at birth, and are remarkably precocial; they are servations, and the dashed line represents the linear regression; born with open eyes and fully erupted canine and incisor points in B represent individual hyenas found in subgroups of various sizes. teeth (Drea and Frank 2003). Nevertheless, cubs undergo an exceptionally long period of nutritional dependence after As in these species of monkeys, individual hyenas within each birth, and dependence on the mother continues long after clan can be ranked in a linear dominance hierarchy based on cubs are weaned because their feeding apparatus develops very outcomes of agonistic interactions (Frank 1986; Kruuk 1972; slowly, and this handicaps their feeding (Watts et al. 2009). Smith et al. 2008; Tilson and Hamilton 1984). Dominance Maternal capital is extremely influential in determining the relationships are extremely stable across years and ecological pace of development and reproduction (Holekamp et al. contexts (Frank 1986; Smith et al. 2011), but rank itself is 2012). Cubs usually nurse for over a year and may nurse for not correlated with size or fighting ability (Engh et al. 2000). up to 2 years. Because it takes juveniles years of practice to Instead, as in many monkeys (e.g., Chapais 1992; Cheney become proficient at hunting and at cracking through bone 1977; Horrocks and Hunte 1983; Walters 1980), coalition for- to access marrow (Holekamp et al. 1997; Mills 1990; Tanner mation plays an important role in acquisition and mainte- et al. 2010), mothers use coalitionary aggression to help their nance of social rank among spotted hyenas (Engh et al. 2000; offspring gain access to ungulate kills long after weaning. Holekamp and Smale 1993; Smale, Frank, and Holekamp Among nonkin, adult female hyenas preferentially tolerate 1993; Smith et al. 2010; Zabel et al. 1992). feeding at shared kills by those nonkin with which they as- S440 Current Anthropology Volume 53, Supplement 6, December 2012 sociate most often (Smith, Memenis, and Holekamp 2007). ciprocal support among nonkin). Instead, hyenas gained di- Dominants engage in reciprocal trading for services provided rect benefits from joining forces to attack subordinates and by subordinates, such as help hunting and defense of territory monitored the number of dominant bystanders in the “au- boundaries. In exchange, dominants withhold aggression dience” at fights to minimize costs to themselves. Taken to- from those unrelated hyenas with which they maintain the gether, the combined evolutionary forces of kin selection and strongest relationships. In this respect, spotted hyenas differ direct benefits appear to favor flexible decisions regarding from most carnivores, because most species of mammalian whether or not adult female hyenas intervene in fights (Smith carnivores allow only their kin to feed at kills. For example, et al. 2010). lions and African wild dogs (Creel and Creel 1995; Packer, Local ecology determines whether hyena clans maintain Pusey, and Eberly 2001) only hunt cooperatively and share well-defined and vigorously defended territories (e.g., Masai meat with relatives or mates (reviewed by Clutton-Brock Mara, Kenya; Boydston, Morelli, and Holekamp 2001) or 2009b). Individual differences in the extent to which spotted more permeable territorial boundaries with considerable hyenas tolerate one another in feeding contexts suggest some range overlap and tolerance of outsiders (e.g., the Kalahari degree of meat sharing among unrelated individuals (Smith, Desert; Mills 1990). Populations that engage in territory de- Memenis, and Holekamp 2007). fense form large intergroup coalitions against members of Although all adult female hyenas breed, rates of reproduc- other social groups. These intergroup disputes over territory tion vary based on social rank and prey density (Frank, Hole- boundaries or kills may involve up to 56 group mates joining kamp, and Smale 1995; Hofer and East 2003; Holekamp, forces against a common enemy (fig. 2; Smith et al. 2008). Smale, and Szykman 1996). Rank-related variation in females’ Individuals within hyena clans are on average more closely ability to access food (e.g., Frank 1986; Smith et al. 2008) has related to one another than to individuals belonging to neigh- striking effects on the growth rates of their cubs; high-ranking boring clans, but relatedness among hyena clan members is cubs grow faster than their low-ranking peers (Hofer and East low (Van Horn et al. 2004). Thus, as in chimpanzees (e.g., 1996, 2003). Dominant females start breeding at younger ages Pan troglodytes; Goldberg and Wrangham 1997), spotted hy- than do subordinates (Frank, Holekamp, and Smale 1995; enas on average derive large net direct fitness benefits from Holekamp, Smale, and Szykman 1996; Watts et al. 2009). joining forces with large numbers of nonrelatives during in- Interestingly, above and beyond the effects of rank, larger tergroup conflicts despite the risk of serious injury or death female hyenas produce more offspring over their lifetimes (Boydston, Morelli, and Holekamp 2001; Henschel and Skin- than do smaller females, suggesting that large body size con- ner 1991; Hofer and East 1993; Kruuk 1972; Mills 1990). fers an evolutionary advantage (Swanson, Dworkin, and Hole- Several other social carnivores, including white-nosed coatis kamp 2011). (Nasua narica; Gompper, Gittleman, and Wayne 1998) and gray wolves (Canis lupus; Lehman et al. 1992), also engage in lethal intergroup conflicts at territorial borders. However, in Evolutionary Forces and Mechanisms Promoting Intragroup contrast to most social carnivores who only join forces with and Intergroup Coalitions genetic relatives during intergroup conflicts (reviewed by As in most monkeys and great apes, spotted hyenas bias their Clutton-Brock 2009b), spotted hyenas do so with large num- social support toward kin during intragroup disputes (re- bers of unrelated group mates. viewed by Smith et al. 2010). We recently elucidated the evo- Whereas both cognitive and noncognitive (emotional and lutionary forces favoring intragroup coalitions among adult temperamental) factors promote cooperation and tolerance female spotted hyenas (Smith et al. 2010). First, we tested the in living chimpanzees and humans (Hrdy 2009; Melis and prediction from kin selection theory (Hamilton 1964a, 1964b) Semmann 2010; Tomasello et al. 2005), all available evidence that individuals should bias helpful behavior toward relatives to date suggests that cooperation among extant carnivores is and harmful behavior away from relatives if doing so provides facilitated by noncognitive mechanisms. For example, greeting inclusive fitness benefits. Second, we examined the hypothesis ceremonies facilitate intra- and intergroup cooperation that natural selection might favor interventions on behalf of among hyenas, helping potential allies to reach the same mo- nonkin via reciprocal altruism if the projected future benefits tivational state before cooperating (Smith et al. 2011). Greet- to the donor outweigh the immediate costs (Trivers 1971). ings occur when two hyenas stand parallel to one another Finally, we asked whether females gain direct benefits from and sniff each others’ anogenital regions (East, Hofer, and cooperative acts through better access to food or by rein- Wickler 1993; Kruuk 1972). These signals allow hyenas to forcing the status quo (Brown 1983; Connor 1995; West- quickly confirm relationship status in a society in which group Eberhard 1975). As predicted by kin selection theory, female members spend much of their time apart (Smith et al. 2011). spotted hyenas support close maternal and paternal kin most Similarly, in African wild dogs (Creel 1997; Creel and Creel often, and the density of cooperation networks increases with 2002) and gray wolves in North America (Mech 1970), greet- genetic relatedness. As is the case in most animal societies ings function to promote group hunting. (reviewed by Clutton-Brock 2009a), we found no evidence Because cooperation is vulnerable to cheaters, theory pre- of reciprocal altruism (e.g., enduring alliances based on re- dicts that punishment and threats should evolve, but there is Smith et al. Carnivore Cooperation S441

SE subgroup size (left vertical axis, histogram bars) and proportion of observations in which spotted hyenas ע Figure 2. Mean were found in subgroups containing more than one individual (right vertical axis, circles) in each of the following contexts: (1) hunting: one or more resident hyenas chased a prey animal for at least 50 m, regardless of the outcome; (2) natal den: one or more resident hyenas observed at an isolated den used by only one mother for shelter of a single litter until her cubs are 2–5 weeks old; (3) kills: one or more resident hyenas observed feeding on at least one fresh ungulate carcass; (4) courtship/mating: immigrant male(s) direct mating tactics toward a sexually mature female; (5) communal den: one or more resident hyenas observed at a den used concurrently by several litters; (6) border patrols: residents engaged in high rates of scent marking and defecation along territory boundaries; (7) clan wars (intergroup conflicts, called “clan wars” by Kruuk 1972): agonistic interactions between resident and alien hyenas at territory boundaries; (8) conflict with lions: agonistic interactions observed between resident hyenas and at least one lion; (9) other: none of the contexts above applied. Sample sizes, shown below each bar, represent numbers of observation sessions assigned to each context. Different letters indicate statistically significant differences between contexts after correcting for multiple testing. The shaded bar represents the baseline value of subgroup sizes occurring in “other” sessions against which other groups were compared. Figure adopted with permission from Smith et al. (2008). limited evidence of effective threats against “free riders” malian carnivores. To test competing hypotheses, we assessed among carnivores (reviewed by Cant 2011). Spotted hyenas the extent to which anatomical, life history, ecological, or use unprovoked aggression to reinforce dominance status, yet behavioral variables coevolved with cooperation among all there is no evidence that these attacks promote coalition for- species (N p 87 ) of carnivores for which all of the salient mation (Engh et al. 2005; Smith et al. 2010). Lions similarly predictor variables of interest were currently available. This fail to punish cheaters in the context of group hunting data set (see CAϩ online supplement A) captures the diverse (Packer, Pusey, and Eberly 2001) despite their ability to rec- suite of social and ecological traits exhibited by members of ognize laggards (Heinsohn and Packer 1995). Finally, al- the order Carnivora. Whenever possible, we extracted all data though banded mongooses Mungos mungo and meerkats do for a single variable (e.g., diet or forms of cooperation ex- enforce cooperative breeding, the threat of eviction is inef- hibited) from the same source. fective at preventing cheating in the first place (Cant et al. 2010; Clutton-Brock, Hodge, and Flower 2008). Forms of Cooperation Exhibited by Carnivores

Testing Ecological Models Using Data from We based the current analysis on reports from the literature Extant Mammalian Carnivores to calculate a composite score of cooperation by counting and summing the number of different forms of cooperation ex- We next used phylogenetic comparative methods to evaluate hibited by each species from among the following possibilities: the extent to which each of the competing ecological models (1) alloparental care, (2) group hunting, (3) intragroup co- of human evolution explains cooperation among extant mam- alition formation, (4) coalition formation during intergroup S442 Current Anthropology Volume 53, Supplement 6, December 2012 contests or warfare among conspecifics, and (5) cooperative distances before capturing them. Noncursors were those spe- protection from predators. Most cooperation data were ex- cies that relied on stealth while stalking and capturing prey tracted from Creel and Macdonald (1995). Intragroup coa- at short distances or that displayed no hunting whatsoever. lition data were from Smith et al. (2010). Finally, we assigned a cohesion index to reflect the increasing Each of our five cooperation types was assigned a value of degree of sociality for each focal species ranging from (1) 0 if it did not occur and 1 if it did occur in a particular solitary (only with conspecifics for mating), (2) pair living species. The only exception to this rule was alloparenting; (stable bond between adult male and female of the same following Creel and Creel (1991), intermediate species were species), (3) fission-fusion dynamics, and (4) obligately gre- assigned a score of 0.5 for alloparenting if they shared a com- garious (always found in close proximity to conspecifics). munal den (e.g., home base at which young born to more than one mother are raised) but did not engage in true allo- Anatomical and Physiological Predictors of Cooperation parental care such as allonursing or provisioning of the off- spring of others. Although this composite “cooperation score” Sexual dimorphism was measured as the body mass ratio of assumes values ranging from 0 to 5, in some analyses, we adult males to adult females. We corrected brain volume 3 simply asked whether or not a species engaged in any of these (mm ) for body size by taking the residuals from phyloge- five forms of cooperation. netically corrected regressions of log-transformed brain vol- Alloparental care is defined here as all aspects of care in ume on log-transformed mass. We used basal metabolic rates which individuals guard, groom, carry, play with, feed, or corrected for body mass as a measure of energy expenditure nurse the offspring of others (Creel and Creel 1991). We define because existing field metabolic data are rarely available for group hunting as concurrent attack by more than one con- carnivores. specific directed toward a selected prey item regardless of its outcome or fitness consequences (Holekamp et al. 1997). Co- Life History Predictors of Cooperation alition formation occurs when two or more individuals join Longevity was the maximum life span (in years) in the wild forces to direct aggression toward the same target(s). Intra- for each species. Gestation length was the number of days group coalitions are directed toward group mates, whereas between conception and birth. Litter size, a measure of re- intergroup coalitions are directed toward conspecifics be- productive investment, was the mean number of offspring longing to a different social group. Cooperative defense born in a single litter. Neonate mass was offspring weight at against predators includes mobbing of predators (e.g., group birth (kg) corrected for adult mass. Lactation duration was members collectively fend off potential predators by attacking the mean number of days between birth and cessation of them) or cooperative vigilance, defined here as any behavioral lactation in nursing females, and did not include subsequent adjustments that reduce the risk of predation for members periods of offspring dependence. of the group. Comparative Methods and Phylogenetic Generalized Ecological Predictors of Cooperation Least Squares Regression We defined two binary variables based on diet. First, we cat- Phylogenetic comparative methods represent powerful tools egorized species as “meat eaters” using an absolute definition to study adaptation because they account for potential au- based on whether their diet was comprised mainly of any tocorrelation due to shared evolutionary history (e.g., Clut- form of meat, including small prey (e.g., rodents, birds). ton-Brock and Harvey 1977; Felsenstein 1985; Gittleman and “Meat eaters” excluded primarily insectivorous, omnivorous, Luh 1992; Swanson et al. 2006). We considered shared an- piscivorous, or herbivorous species. Second, we inquired cestry of these 87 species by building a phylogeny primarily whether species with diets comprised mainly of large verte- based on Bininda-Emonds et al. (2007) and adjusting some brate prey (110 kg; Gittleman 1989) had the highest coop- relationships based on updated phylogenies or phylogenies eration scores. Habitat types increased in vegetative cover focused on smaller taxonomic subgroups (Finarelli 2008; from open (e.g., savannah) to mixed (e.g., woodland savan- Flynn et al. 2005; Gottelli et al. 1994; Johnson et al. 2006; nah) to closed (e.g., forest) habitats. Population density was Koepfli et al. 2006, 2007, 2008; Patoua et al. 2009; Perini, the number of individuals per square kilometer. Russo, and Schrago 2009; Sato et al. 2009; Yoder et al. 2003). We resolved polytomies wherever possible, assigning branch lengths of1 # 10Ϫ6 million years ago when branch lengths Behavioral Predictors of Cooperation were not estimated in the source. The only unknown rela- Home range sizes were average values for adults of both sexes. tionships for our phylogeny were those of gray wolves, Ethi- We also assigned a binary variable based on whether or not opian wolves Canis simensis, and coyotes Canis latrans;this a species hunted cursorially regardless of hunting group size. polytomy was retained for regressions and randomly resolved. Cursorial hunters were defined as carnivores that primarily The resulting branch lengths were set to 0 for estimation of used endurance to exhaust targets by chasing them for long phylogenetic signal and ancestor reconstruction. Unless stated Smith et al. Carnivore Cooperation S443 otherwise, all analyses were carried out in R version 2.12.1 species display weakly similar residual errors. Our data set (R Foundation for Statistical Computing 2010). was limited toN p 57 andN p 46 species, respectively, for We estimated the strength of the phylogenetic signal using which data on longevity in the wild and mass-corrected basal Blomberg’s K and tested whether it differed from that pre- metabolic rates were available. We first inquired whether each dicted by a null model specifying no effect of phylogeny. of these variables predicted our cooperation score. After cor- ע SE p .139 ע Specifically, we asked whether K estimated for the actual tip recting for phylogeny, neither longevity (b arrangement differed from that generated based on 100,000 .564,t p .246 ,P p .806 ) nor mass-corrected basal metabolic t p .187 ,P p .852 ) significantly, 521. ע SE p .098 ע randomized tip arrangements (Blomberg, Garland, and Ives rate (b 2003) using the “picante” package in R (Kembel et al. 2010). predicted cooperation across Carnivora. Therefore, we re- Our estimate of K revealed a moderate phylogenetic auto- moved these predictors from our final analysis because doing correlation that was significantly different from 0 (K p so permitted us to test the remaining variables using the sta- 0.195,,).Z p Ϫ1.58 P p .032 tistical power of our full data set (N p 87 species). Phylogenetic generalized least squares regression (PGLS) We used AICc to recover our best model explaining vari- allows for simultaneous consideration and estimation of the ation in the cooperation scores among carnivores (table 1). degree of phylogenetic nonindependence using Pagel’s lambda After correcting for the effects of phylogeny, the results from (l). Allowing character evolution through modes other than our best model suggest that the greatest number of cooper- Brownian motion is one of the main advantages of PGLS over ative behaviors occurs among cursorial hunters in species phylogenetically independent contrasts (PIC), another com- lacking strong male-biased size dimorphism that have large mon approach (Felsenstein 1985). Lambda represents a con- litters and engage to some extent in hunting big game (table tinuous variable for which 0 describes a trait that displays no 1). In addition, we have some evidence that species that are phylogenetic signal and 1 describes a trait that has evolved tall for their size (e.g., have large relative shoulder heights under Brownian motion. PGLS is equivalent to PIC for char- compared with their mass) display a greater number of co- acters evolving under Brownian motion with completely re- operative behaviors but only in species that exhibit cursorial solved phylogenies (Rohlf 2001). hunting (table 1). The only additional model that is statis- We built general linear models in a PGLS framework using tically indistinguishable from our best model (within 2 dAICc; the “nlme” package in R with the composite cooperation score Burnham and Anderson 2002) further suggests that species as the response variable and behavioral, ecological, morpho- living in open habitats engage in a greater number of co- logical, and life history variables as predictors. We allowed l operative behaviors than do those in dense habitats. to take its Maximum Likelihood Estimate (MLE) in each In general, the degree of social cohesion was an important model. We sequentially entered and dropped all potential ex- determinant of the cooperation score assigned to each species planatory terms, including two-way interactions predicted by (table 2). We excluded solitary species from this analysis be- our hypotheses. We deemed the candidate model with the cause these animals had no group members with which to smallest Akaike Information Criterion corrected (AICc) for cooperate. Even after correcting for multiple testing (Storey small sample size to be the best while retaining any models and Tibshirani 2003), fission-fusion and obligately gregarious with dAICc (difference between the AICc of the best model species had significantly greater cooperation scores than did and the model being considered) values of less than 2 as species living in pairs (table 2). Interestingly, our finding that essentially equivalent (Burnham and Anderson 2002). We ob- species with fission-fusion lifestyles were just as cooperative tained statistics for terms removed from our best model by as those species always found in cohesive social groups sug- individually adding each term to the minimal model. We only gests that fission-fusion dynamics permit species to avoid report interaction terms that improved the fit of our best costly competition without sacrificing benefits accruing from model. cooperation with group mates. We also used phylogenetic generalized estimating equations The overall tendency for carnivore species to cooperate was , 0.14 ע SE p 0.76 ע Paradis, Claude, and Strimmer 2004) with a binary response generally low (cooperation score:mean) variable to estimate the effect of each predictor on the five range 0–5,N p 87 species), but our results indicate strong binary cooperation variables, including the alloparenting var- variation both within and among families regarding coop- iable for which animals were cooperative if they either allo- erative tendencies (fig. 3). The proportion of species that parented or shared a communal den. Because some MLE engaged in each form of cooperation contributing to the co- estimates of models failed to converge, we estimated univar- operation score was also variable. A higher proportion of -inter ,( 0.04 ע iate models for each predictor variable. species participated in alloparental care (0.20 ע and group hunting ( 0.18 ,( 0.04 ע group contests (0.18 0.04) than in cooperative protection from predators Factors Predicting Composite Cooperation CAϩ ; 0.03 ע or intragroup coalitions ( 0.07 ( 0.04 ע 0.13) Scores in Carnivora supplement A). The MLE for the strength of phylogenetic signal for the final We found no evidence of cooperation among Ailuridae, model (l) was 0.060, suggesting that more closely related Ursidae, or Viverridae (fig. 3). In contrast, most members of S444 Current Anthropology Volume 53, Supplement 6, December 2012

Table 1. Best candidate model and the only model !2 dAICc of the best model explaining the composite cooperation score across Carnivora

b SE tPAICc dAICc Best candidate model: Intercept 1.719 .790 2.176 .032 247.2 Relative shoulder height Ϫ.736 .515 Ϫ1.429 .157 0 Cursorial hunting 1.691 .484 3.492 .001** Litter size (log) .488 .233 2.092 .040** Sexual dimorphism (log) Ϫ2.162 .935 Ϫ2.312 .023** Hunting of big game .462 .297 1.557 .123 Relative shoulder height: cursorial hunting 4.340 2.414 1.798 .076** Only model !2 dAICc of the best model: Intercept 1.441 .766 1.881 .064 249.1 Relative shoulder height Ϫ.718 .478 Ϫ1.502 .137 1.9 Cursorial hunting 1.701 .481 3.535 .001** Litter size (log) .419 .220 1.910 .060** Open vs. mixed habitat .265 .238 1.115 .268 Open vs. closed habitat .763 .334 2.282 .025** Mixed vs. closed habitat .498 .303 1.641 .105 Sexual dimorphism (log) Ϫ2.061 .916 Ϫ2.249 .027** Hunting of big game .420 .284 1.475 .144 Relative shoulder height: cursorial hunting 4.237 2.425 1.747 .085** Note. dAICc p difference between the AICc of the best model and the model being considered. Addition of these variables failed to improve the fit of our best candidate model: log neonate mass corrected for log adult mass; log brain size corrected for log adult mass, log mass, log duration of lactation, log home range size, log gestation length, and diet. In addition, none of these variables were significant ata ! .10 when added to the best model. The addition of log population density to the best model did not significantly improve the model, resulting in a model with a t p 2.07 ,P p .042 ). Results of ANOVA for overall habitat, 061. ע dAICc 1 2, but the variable was statistically significant when added (b p .125 p p formodelBareF 3.052,80 ,P .0846 . *.a ! .10 **a ! .05 (in bold).

Canidae and Herpestidae investigated here were highly co- erative hunters produced larger litters and were less sexually operative, engaging on average in at least one form of co- dimorphic than noncooperatively hunting species (table 3). operation (fig. 3). In particular, African wild dogs engaged in Additional meat gained from cooperative hunting, therefore, all five types of cooperation. Lions, cheetahs, and snow leop- appears to permit mothers to increase their investment in ards (Panthera uncia) represent interesting outliers because current reproductive effort by increasing offspring number they are the only cooperative species in the family Felidae. and also increasing their own body size relative to that of Interestingly, although Hyaenidae had a low mean coopera- males. Similarly, mothers of species that cooperatively de- -N p 4 species), spotted hyenas were fended themselves from predators also invested more in cur, 1.09 ע tion score (1.25 far more cooperative than any other members of their family rent reproduction, weaning offspring at later ages than did (score p 4.5). Members of Eupleridae, Mephitidae, and Pro- mothers of noncooperative species. Species living in dense cyonidae had low mean cooperation scores and high variation populations were also the most likely to cooperatively defend in the degree of cooperation among family members. themselves from predators, presumably because cooperative defense is mainly a numbers game, requiring a large number Factors Predicting Each Form of Cooperation in Carnivora of individuals to detect and cooperatively mob predators. Next, we used univariate tests to consider the effects of each of the predictor variables on each unique form of cooperation. Table 2. Effects of sociality on composite cooperation Perhaps because cooperation among carnivores is generally scores across nonsocial species of Carnivora rare, some models failed to converge. Thus, those variables Effect b SE tP not explicitly stated here as either having a significant or nonsignificant effect on each form of cooperation failed to Intercept .759 .518 1.466 .154 successfully converge (table 3). Overall, the results of these Pair bonding vs. fission-fusion 1.788 .597 2.995 .015** Pair bonding vs. obligately social 1.869 .679 2.754 .015** tests resembled the general patterns found for our composite Fission-fusion vs. obligately social .082 .717 .114 .910 cooperation scores; the tendency to cooperate generally in- Note. Solitary species were excluded from this analysis because these creased with cursorial hunting of big game (table 3). species had no group members with which to cooperate. P values are This analysis also revealed coevolution of particular traits presented in their corrected form to account for multiple comparisons. with each specific form of cooperation. For example, coop- **a ! .05 (in bold). Smith et al. Carnivore Cooperation S445

Figure 3. Cooperation scores among and within families in the order Carnivora. Dark horizontal lines in box plots represent medians, with boxes spanning the middle 50% of the data for each family group. Whiskers stretch to any values that are outside boxes but within 2.5 quartiles from the median. Families are ranked by mean cooperation scores from least cooperative to most cooperative (left to right). Outliers within each family are those values greater than 2.5 quartiles away from the median and are indicated by circles.

Moreover, because predators often aggregate in areas of high Our ancestor reconstruction suggests that extant species of prey density (known as the “pantry effect”; Ford and Pitelka carnivores probably evolved from noncooperative ancestors 1984), prey in dense populations are under strong selection (fig. 4). Furthermore, the same is generally true at the family to evolve effective antipredator behavior. Interestingly, our level, with the most recent common ancestors of most families data suggest that increased brain size might have coevolved displaying very low probabilities for any cooperation with the with alloparenting, an important finding consistent with com- exceptions of Canidae, Herpestidae, Hyaenidae, and Mephi- parative data on primates suggesting that alloparenting en- tidae. In particular, Felidae, Ursidae, Eupleridae, and Viver- hances energy required to sustain expensive neural tissue (Isler ridae exhibit almost no suggestion of cooperative behavior in and van Schaik 2012). the family’s ancestral state. Interestingly, cooperative species appear in every extant family except for Ailuridae, Ursidae, Evolutionary Losses and Gains of Cooperation in Carnivora and Viverridae. We next used each binary cooperation variable in an ancestor reconstruction using MLE to ask whether the data support a Insights into the Evolutionary Origins of greater likelihood of cooperation arising or being lost across Cooperation in Homo evolutionary transitions within Carnivora. Using the “ape” Multiple Factors Coevolve with the Emergence of Cooperation package in R, we estimated ancestral values for the common ancestors of the species present in our phylogeny. For every Overall, the results of comparative analysis revealed that mul- ancestral node, each signifying the ancestor of a pair of taxa, tiple factors are important correlates of cooperation in mam- we estimated the probability that the last common ancestor malian carnivores. These data therefore suggest that mean- at that node was cooperative. ingful links exist between cooperation and changes in S446 Current Anthropology Volume 53, Supplement 6, December 2012

Table 3. Factors influencing the tendency to engage in each fully predicted by a singular referential model evaluated here. of the five forms of cooperation across Carnivora Our analysis underscores the need for paleoanthropologists to consider a multitude of factors (rather than a single or Factor b SE tPrelatively small number of factors) simultaneously when at- Cooperative hunting:a tempting to explain the evolution of cooperation in hominins. Hunting of big game 1.74 .63 2.75 .013** This notion of a multifaceted approach to hominin evolution Litter size (log) 1.34 .59 2.26 .037** has been suggested previously (e.g., Potts 1994), but here we Sexual dimorphism Ϫ5.02 2.74 Ϫ1.83 .084* Intragroup coalitions:b provide new lines of evidence to support it. Briefly, as pre- Cursorial hunting 4.23 .99 4.26 .001** dicted by the hunting-scavenging model involving persistence Hunting of big game 2.77 1.14 2.43 .026** running, we found that carnivores engaging in cursorial hunt- Litter size (log) 1.82 .91 2.00 .060* ing of large-bodied prey are most likely to cooperate. More- Flesh diet 2.02 1.13 1.78 .092* over, morphological traits important for hunting, such as large Territory defense:c Cursorial hunting 1.57 .79 1.98 .064* relative shoulder height, and those theorized to result from Predator protection:d reduced male-male competition (e.g., Plavcan 2012), such as Hunting of big game 1.87 .67 2.80 .012** a reduction in sexual dimorphism, were most common in Cursorial hunting 1.89 .80 2.40 .027** highly cooperative species. These morphological changes are Population density (log) .33 .15 2.13 .047** of particular relevance because such factors may be evaluated Weaning age (log) .96 .55 1.74 .099* Alloparenting (none vs. in the fossil remains of early Homo. Nevertheless, those species any form):e of carnivores that were most cooperative in breeding generally Flesh diet 1.34 .50 2.68 .015** had larger relative brain sizes and greater reproductive in- Hunting of big game 1.20 .53 2.27 .036** vestment than did noncooperative carnivores. Relative brain Relative brain size 1.55 .89 1.74 .099* size failed to predict cooperative defense against predators, Note. Results from generalized estimating equations with each cooper- which does not support the prediction of the predator pro- ation variable as a binary response for significant variables that converged. tection model. Species that weaned offspring at the oldest Each test given is from a univariate model. a P 1 .10 for relative brain volume, flesh diet. ages (enhanced reproductive investment) and lived at the b P 1 .10 for sexual dimorphism, log gestation length, log weaning age, highest population densities (presumably in areas with neonate mass corrected for adult mass, relative brain volume. clumped resources) were most likely to cooperate in defense c P 1 .10 for log home range, sexual dimorphism, log litter size, log against predators. population density, log gestation length, relative shoulder height, neonate mass corrected for adult mass, relative brain volume, big game. d P 1 .10 for log home range, sexual dimorphism, log litter size, log Relevance of Extant Carnivores for Understanding gestation length, relative shoulder height, neonate mass corrected for Behavioral Shifts in Hominins adult mass, relative brain volume, flesh diet. e P 1 .10 for log-log home range, sexual dimorphism, log population Large mammalian carnivores might have coexisted with Homo density, log gestation length, log weaning age, neonate mass corrected by as early as 2.6 Ma. However, tooth marks on bones suggest for adult mass, cursorial hunting. *.a ! .10 that carnivores only started to regularly visit butchery sites **a ≤ .05 (in bold). by roughly around 2.0 Ma (Domı´nguez-Rodrigo and Mar- tinez-Navarro 2012). Despite the surprisingly high number of tooth marks on animal bones around this time, extrinsic morphology (e.g., relative height at shoulder for body mass, mortality of early Homo apparently declined, a pattern that reduced sexual dimorphism, increase in relative brain size), has been attributed to either increased cooperative defense foraging and ranging behaviors (e.g., endurance hunting of against predators (Hart and Sussman 2009) or cooperative big game in open landscapes, fission-fusion sociality), and life breeding (Hrdy 2009). Both forms of cooperation occur in history traits (e.g., increased age of weaning, increased re- extant carnivores reviewed here. Evidence from carnivores productive output), all of which are relevant to early homi- more broadly indicates that both the emergence of cooperative nins. These findings extend earlier studies suggesting a pos- defense against predators and the pace of reproduction can itive relationship between hunting large game in open habitats respond in a flexible fashion to variation in the availability and the emergence of sociality in carnivores (Gittleman and and acquisition of energy-rich foods. Thus, it is possible that Harvey 1982; Packer, Scheel, and Pusey 1990). Early Homo similar flexibility influenced shifts in reproductive investment apparently exhibited larger body and brain sizes and perhaps and rates of reproduction among early hominins. Interest- slower growth rates than did Australopithecus (Anto´n 2012). ingly, just as flexibility in female reproduction among spotted Our data suggest that meaningful inferences about social evo- hyenas exceeds that of most extant carnivores, the plastic lution are possible based on these morphological shifts. reproductive responses typical of early Homo appear to sur- Whereas each of the factors elucidated here for extant car- pass those of chimpanzees or gorillas (Bribiescas, Ellison, and nivores likely played some role in hominin evolution, only Gray 2012; Isler and van Schaik 2012; Wells 2012). Thus, some of them depend on meat eating, and none of them are maternal capital might have played a central role in hominin Figure 4. Phylogeny of the carnivore species used in our study. Tip labels display species names. At tips of the phylogeny are circles shaded to varying degrees indicating for each cooperation variable whether or not the species exhibits the trait. Black indicates trait presence, whereas white indicates that the species does not exhibit that trait. For alloparenting, gray indicates communal denning. Circles representing composite cooperation scores (a continuous measure of cooperation) are shaded, with dark shading representing the highest cooperation score. Pie charts are given for each binary variable for select taxonomic groups indicating the probabilities that common ancestors were uncooperative (white) or cooperative (black). Superscripts for each taxonomic grouping refer to labeled nodes on the phylogeny. S448 Current Anthropology Volume 53, Supplement 6, December 2012 evolution of large brains and slow life histories, although the insults more effectively than can most other large carnivores precise timing of each remains enigmatic. with more restricted dispersal abilities or less versatile mor- Around 2.3–1.7 Ma, a major shift in a suite of behaviors phological adaptations (Holekamp et al. 2012). In this respect, became persistent in the fossil record of early Homo (Potts data on spotted hyenas are consistent with the notion that 1998a, 2012); these included stone transport, tool making, natural selection favors species living in variable habitats that and access to large animals. In the Turkana and Olduvai ba- are best able to cope with and respond to changing environ- sins, stone transport distances increased, artifacts were dis- mental conditions. tributed more widely, and processing of animal tissues inten- Fission-fusion sociality may have played an underappre- sified, including the extraction of meat and marrow from large ciated role in reducing the costs confronted by early hominins animals (e.g., Blumenschine 1995; Bunn and Kroll 1986; Potts in changing environments. That is, hominin communities 1988). Although no evidence currently exists of tool use might have retained their ability to cooperate with group among extant carnivores, most carnivores are well endowed mates despite their splitting into more and more complex with massive jaws that permit them to capture prey and gain levels of temporary subgroups as the total area required per access to animal tissues without tool use. Nonetheless, most group increased (e.g., from those occupied by Australopithecus mammalian carnivores are unable to capture prey exceeding and Homo habilis to that occupied by Homo erectus; reviewed 10 kg (Gittleman 1989). Those that capture large prey hunt by Grove, Pearce, and Dunbar 2012). Our comparative data cooperatively when doing so, but there is no evidence of are consistent with the notion that fission-fusion sociality advanced planning before hunts by carnivores. In contrast, permits the maintenance of cooperation; extant carnivores modern hunts by the Ache of Paraguay (Kaplan and Hill 1985) living in societies structured by fission-fusion dynamics en- and subsistence whale hunters of Lamalera, Indonesia (Alvard gaged in just as many forms of cooperation as species in highly and Nolin 2002; O’Connell, Hawkes, and Blurton Jones 1988), cohesive groups and were more cooperative than those re- regularly capture prey of much larger than 10 kg in hunts stricted to living in pairs. Despite spending much of their requiring advanced planning. Recent comparative data sug- time apart from group members, most gregarious carnivores gest that cumulative culture, the summation of innovations regularly meet up with conspecifics for protection from pred- over time, may indeed be unique to modern humans (Dean ators, reinforcement of social bonds, and sharing of spoils et al. 2012). Altogether, these data suggest that cooperative from hunts. Evolution of an increasingly complex multilevel capture of some prey items might have been possible before fission-fusion society beyond that observed in any extant the evolution of large brains, but complex forms of coop- mammalian carnivore may have similarly helped early hom- erative hunting requiring advanced planning probably inins cope with increased foraging demands attributed to emerged later in hominin evolution. ranging over large areas as they migrated toward high latitudes Around 1.9–1.5 Ma, landscape instability likely promoted (Grove, Pearce, and Dunbar 2012). Taken together, evidence carrying of stones and meat over greater distances (e.g., 2– from extant mammalian carnivores reviewed here as well as 13 km; Potts 1998a). Selection favoring other behavioral traits, that from nonhuman primates (e.g., Wrangham, Gittleman, including sociality, of early hominins was also likely driven and Chapman 1993) and modern small-scale hunter-gathers by intense variation in ecological and climatic conditions (e.g., Marlowe 2005) suggests the most parsimonious inter- (Potts 1998b, 2012). Similarly, spotted hyenas, the most abun- pretation of the fossil record is that development toward an dant large carnivore in sub-Saharan Africa, may have also increasingly complex multilevel fission-fusion society allowed been subject to strong selection for their behavioral flexibility for both cooperation and range expansion at key transitional to cope with demands of life in a socially and ecologically stages of hominin evolution. dynamic landscape (Holekamp and Dloniak 2010; Holekamp In conclusion, it has long been recognized that understand- et al. 2012). The ecological dominance of spotted hyenas over ing the evolution and mechanisms of cooperation among other carnivores in Africa may in large part be attributed to mammalian carnivores might shed light on the factors shaping the behavioral flexibility that their impressive morphology hominin evolution (Hill 1982; Kaplan and Hill 1985; Schaller affords them (Holekamp and Dloniak 2010). Adult spotted and Lowther 1969). Our study confirms that meaningful links hyenas are efficient hunters (Holekamp et al. 1997) and ex- are possible between measurable morphological traits and tractive foragers (Tanner et al. 2010) capable of fully exploiting seemingly elusive behavioral traits. New analyses on coop- a wide array of foods ranging from termites to large ungulate erative breeding and predator protection for these species, prey. These hyenas effectively crack through bones as large as some but not all of which also happen to eat meat, make this giraffe leg bones to access marrow, allowing them to efficiently taxonomic group relevant today even if Homo was not sub- consume entire carcasses. In the face of burgeoning human stantially carnivorous. Our results also move the field forward populations across Africa, their behavioral flexibility has per- by emphasizing the need for the consideration of multiple mitted these animals to persist at high densities despite the factors rather than predictions from a single existing model energetic demands of being a top predator (Boydston et al. when explaining social evolution of early hominins. New in- 2003). It might be this behavioral flexibility with respect to sights suggesting convergent evolution between extant mam- foraging that permits spotted hyenas to cope with ecological malian carnivores and early hominins will undoubtedly Smith et al. 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Comments Pleistocene hominids at Olduvai Gorge, Tanzania. Current Anthropology 27: 431–452. from Rick Potts were particularly instrumental in this process. Bunn, Henry T., and Travis R. Pickering. 2010. Bovid mortality profiles in We are grateful to Laurie Obbink for helping to organize this paleoecological context falsify hypotheses of endurance running-hunting meeting. We thank John Finarelli for assisting us with ac- and passive scavenging by early Pleistocene hominins. Quaternary Research 74:395–404. quiring an accurate phylogeny and for his helpful suggestions Burnham, Kenneth P., and David R. Anderson. 2002. Model selection and for pruning it for our use here. We are also grateful to our inference: a practical information-theoretic approach. 2nd edition. New York: colleagues at the University of California, Los Angeles (UCLA) Springer. Byrne, Richard R. 1995. The thinking ape: evolutionary origins of intelligence. Center for Behavior, Evolution, and Culture and those par- Oxford: Oxford University Press. ticipating in the Modeling Social Complexity Investigative Cant, Michael A. 2011. The role of threats in animal cooperation. Proceedings Workshop at the National Institute for Mathematical and Bi- of the Royal Society B: Biological Sciences 278:170–178. Cant, Michael A., Sarah J. Hodge, Matthew B. V. Bell, Jason S. Gilchrist, and ological Synthesis (NIMBios; sponsored through National Sci- Hazel J. Nichols. 2010. Reproductive control via eviction (but not the threat ence Foundation (NSF) Award EF-08325858 and the Uni- of eviction) in banded mongooses. Proceedings of the Royal Society B: Bi- versity of Tennessee, Knoxville) for rich discussions on this ological Sciences 277:2219–2226. Carbone, Chris, Lory Frame, George Frame, James R. Malcolm, John H. topic. This research was funded by postdoctoral fellowships Fanshawe, Clare D. FitzGibbon, George B. Schaller, Iain J. 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How Our Ancestors Broke through the Gray Ceiling Comparative Evidence for Cooperative Breeding in Early Homo

by Karin Isler and Carel P. van Schaik

The “expensive brain” framework proposes that the costs of an increase in brain size can be met by any combination of increasing the total energy turnover or reducing energy allocation to other expensive functions, such as maintenance (digestion), locomotion, or production (growth and reproduction). Here, we explore its implications for human evolution. Using both comparative data on extant mammals and life-table simulations from wild extant apes, we show that primates with a hominoid lifestyle face a gray ceiling that limits their brain size, with larger values leading to demographic nonviability. We argue that cooperative care provides the most plausible exaptation for the increase in brain size in the Homo lineage.

For a change in any character to be adaptive, it must bring found among great apes (Schoenemann 2006). This increase a net fitness benefit relative to the ancestral state. To explain in brain size has no doubt brought various cognitive benefits, the evolution of larger brains, many hypotheses have been perhaps to do with tool use or cooperative hunting or other devised that focus on the adaptive benefits without consid- forms of cooperation. The question pursued here, however, ering the costs (e.g., Dunbar 1998). Here, following the early is how the increasing encephalization could be afforded (Ai- proponents of an energetic viewpoint (e.g., Aiello and ello and Key 2002; Aiello and Wells 2002; Leonard et al. 2003). Wheeler 1995; Martin 1981), we argue that the high costs of Thus, following the first pathway, a part of the brain-size brain tissue relative to those of other organs (Rolfe and Brown increase in early Homo may be attributed to an increase in 1997) should also be considered because they may limit the metabolic turnover. Supportive evidence comes from the find- net benefits to those situations where the survival benefits of ing that the positive correlation between basal metabolic rate larger brains outweigh the demographic consequences of the (BMR) and brain size is most pronounced in primates (Isler increased allocation of energy. Indeed, given that absolute and van Schaik 2006b). Although the BMRs of humans and brain size is tightly correlated with overall cognitive perfor- chimpanzees are similar and near the value predicted from mance (Deaner et al. 2007; Reader, Hager, and Laland 2011), the Kleiber line for their respective body mass (Kleiber 1961), most lineages would be able to derive a great variety of cog- humans exhibit a higher percentage of body fat compared nitive benefits from larger brains (e.g., Shettleworth 2010), with most primates (reviewed in Wells 2006), and thus BMR suggesting the possibility that the ability to overcome the costs relative to lean body mass is likely to be higher than in chim- may in fact be limiting and thus may explain most of the panzees (Aiello and Wells 2002). In addition, there is growing brain-size variation in homeothermic vertebrates. evidence for a pronounced difference in daily energy expen- The “expensive brain” framework notes that evolutionary diture between humans and great apes (Pontzer 2012; Pontzer increases in brain size can be paid for in two complementary et al. 2010). but nonexclusive ways (fig. 1): (i) by increasing energy turn- Environmental conditions should affect the potential re- over or (ii) by reducing allocation to other targets, such as action space for stabilizing the energy throughput on a higher maintenance, locomotion, and production (Isler and van level. Increased metabolic turnover may only be possible in Schaik 2009a). This framework can be applied to hominin habitats that allow for a continuous food supply. Thus, when evolution. Early Homo is associated with the first increase in periods of unavoidable food scarcity recur, we expect most brain size among hominins outside the range of brain sizes species to be forced to evolve smaller brains than their sister taxa in less seasonal environments. Indeed, we found that Karin Isler is Senior Lecturer and Carel P. van Schaik is Professor seasonality in food (and hence energy) intake is negatively and Director of Museum at the Anthropological Institute and correlated with brain size in strepsirrhine and catarrhine pri- Museum, University of Zurich (Winterthurerstrasse 190, CH-8057 mates (van Woerden, van Schaik, and Isler 2010; van Woerden Zurich, Switzerland [[email protected]]). This paper was submitted et al. 2012) as predicted by the expensive brain framework. 12 XII 11, accepted 3 VII 12, and electronically published 17 X 12. Work on birds, however, had earlier suggested that habitat

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0015$10.00. DOI: 10.1086/667623 S454 Current Anthropology Volume 53, Supplement 6, December 2012

Schaik 2006a), may also have played a role in human evo- lution when in early Homo an energetically less efficient, aus- tralopithecine-like form of bipedalism evolved into a modern striding gait. The abandonment of the energetically very ex- pensive climbing also freed these hominins from the anatom- ical compromise between climbing and walking (Isler and van Schaik 2006a). Apart from reducing costs of locomotion, this change in the locomotor habits may also have induced a reduction of maintenance costs during rest, as humans are Figure 1. Expensive brain framework. From an ultimate per- reported to have relatively less muscle mass than great apes spective, any increase in brain tissue must be paid for either by (Leonard et al. 2003; Snodgrass, Leonard, and Robertson any combination of increased energy turnover or by reduced 2009). However, this seeming difference could arise because energy allocation to other expensive body functions. of the higher amount of fat stores in humans. At present, hypotheses explaining increased encephalization in the hu- seasonality imposes selection on increased brain size (e.g., Sol man lineage with metabolic trade-offs through a shift in body 2009), a view known as the “cognitive buffer” hypothesis. This effect was also found among catarrhine primates in that composition are only weakly supported by empirical data relatively large-brained species show a larger difference be- (Muchlinski, Snodgrass, and Terranova 2012). tween the seasonality of their habitat and the annual variation In this paper, we explore the trade-off between brain size in food intake (van Woerden et al. 2012). Nevertheless, the and production, which includes growth and reproduction. relationship between relative brain size and habitat seasonality This effect is well established among birds (e.g., Iwaniuk and is neutral, indicating that the cognitive buffering may at best Nelson 2003) and mammals (Isler and van Schaik 2009a, level out the energetic constraint (van Woerden et al. 2012). 2009b). Here, we will use correlations between life history The habitats invaded by early Homo were clearly more sea- characteristics and thus reproductive capacity and brain size sonal than the gallery forests, lacustrine edges, and woodlands in extant primates to shed light on the evolutionary history inhabited by their ancestors (Potts 1998; Reed 1997). From of early hominins. Briefly, we will argue that great apes have the comparative evidence, we tentatively conclude that the brain sizes that are close to the maximum achievable with increasing habitat seasonality was an important selective force their lifestyle and that our hominin ancestors could only break in the early Homo lineage, although the primate data suggest through this so-called gray ceiling after they had adopted that at this point it had not yet led to an increase in brain cooperative breeding. size. Rather, increasing habitat seasonality may have shaped the unique human combination of storing body fat in com- bination with cognitive solutions to survive irregular star- vation periods (Navarrete, van Schaik, and Isler 2011; see also Table 1. Phylogenetic regressions of life history traits versus Kuzawa 1998; Wells 2010). female brain and body mass data in nonhuman primates Turning to the second pathway, are there trade-offs between (N p 86 species) the brain and other expensive body functions that may explain early human encephalization? In a classic study, Leslie Aiello Female Female and coworkers proposed that energetic effects on human brain brain mass body mass size were mainly linked to reduced allocation to intestinal Life history parameter l P Effect P Effect tissues because of increased meat eating (Aiello and Key 2002; Neonate body mass .959 !.0001 .674 .014 .209 Aiello and Wheeler 1995). However, comparative support for Gestation .996 .0005 .071 .095 Ϫ.084 this “expensive tissue” hypothesis is limited. Early studies had Lactation .737 !.0001 .811 .396 Ϫ.12 found no evidence for it in bats or birds (Isler and van Schaik Interbirth interval .925 .013 .461 .688 Ϫ.054 Ϫ 2006a; Jones and MacLarnon 2004). A recent study of a large Litter size .999 .017 .242 .166 .097 Annual fertility .955 .002 Ϫ.702 .355 .148 sample of mammals, including 23 species of primates, with Age at first reproduction .848 .0009 .573 .111 Ϫ.198 matching brain and organ mass data (Navarrete, van Schaik, Maximum life span .864 .0004 .425 .051 Ϫ.167 and Isler 2011) also failed to support it. These results put the Maximum reproductive life span .815 .001 .412 .064 Ϫ.171 Ϫ general validity of this hypothesis in doubt. Moreover, for the rmax .950 .0004 .688 .172 .186 specific case of humans, we argue that the currently available Source. Primate life history and female brain and body mass data are data on great-ape digestive tract anatomy (Chivers and Hladik taken from the compilation described in van Schaik and Isler (2012). 1980) are not sufficiently clear to claim reduction of the gut Note. Phylogenetic least squares regressions were calculated with pglm.est in the R-package CAIC (Orme et al. 2010; Purvis and Rambaut in the human lineage (Hladik, Chivers, and Pasquet 1999). 1995; R Development Core Team 2010). A l value close to 1 indicates Another trade-off, that between the energy used for lo- a strong phylogenetic influence on the respective parameters (Garland, comotion and for the brain as shown in birds (Isler and van Harvey, and Ives 1992). Isler and van Schaik Cooperative Breeding in Early Homo S455

Brain Size and Life History Traits: ing reproduction, or both). We have shown that relatively How Do Humans Differ? large-brained precocial mammals exhibit a reduced fertility rate by producing much larger offspring after longer interbirth From the expensive brain framework it follows that an in- intervals (Isler and van Schaik 2009a). This is probably be- crease in relative brain size could be paid for by reduced cause relatively large-brained immatures are highly vulnerable investment in production (i.e., slowing down growth, reduc- to temporary shortfalls in energy supply (the “brain mal-

Figure 2. Residuals of life history traits versus residuals of endocranial volume in primates (N p 86 species; Homo sapiens was excluded while calculating the regressions). Residuals were obtained from least squares regressions of the respective trait versus female body mass. A color version of this figure is available in the online edition of Current Anthropology. S456 Current Anthropology Volume 53, Supplement 6, December 2012

Table 2. Life history parameters of humans and other great apes

Parameter Gorilla gorilla Pan troglodytes Pan paniscus Pongo pygmaeus Pongo abelii Human mean 14 Female body mass (kg) 71.5 40.4 33.2 36.9 41.1 45.26 Female brain size (cm3) 434 357 326 337 346 1,213 Gestation length (m) 8.45 7.73 7.6 8.22 8 8.9 Neonate body mass (g) 2,124 1,846 1,447 1,968 1,969 3,319 Twinning rate 1/100 2.8/100 ? ? ? 1/100 Interbirth interval (years) 5 5.43 4.8 7.35 9.3 3.331 Weaning age (years) 3.5 4 3 5.3 5.5? 2.83 Female age at first reproduction (years) 10.2 13.25 14.2 15.7 15.4 18.84 Maximum life span 55 59.4 54.5 56.3 59 85 Sources. Values are taken from van Schaik and Isler (2012), from Ely et al. (2006) for chimpanzee twinning rate, from Walker et al. (2006) for the mean of 14 human subsistence populations, and from Barrickman et al. (2008) for human brain size. nutrition risk” hypothesis of Deaner, Barton, and van Schaik other primates, the main human characteristic is a distinctly 2003), so that a relatively large neonatal body mass is needed shortened period to weaning, and thus an increased annual to buffer this risk. In addition to larger newborns, the reduced fertility rate, for its brain size. On the other hand, humans allocation to production slows down development and delays exhibit considerably smaller neonates but only a slight de- the age at first reproduction in relatively large-brained pre- crease in gestation length and a perfectly normal age at first cocial mammals and especially in primates (table 1). Indeed, reproduction for their brain size. a recent analysis for a carefully compiled data set of wild Thus, the main deviation from expectation is that humans primates showed that brain size is the best predictor of the manage to have much higher investment in reproduction duration of all stages of developmental life history except the (both pre- and postnatally) than expected for their brain and (poorly delineated) lactational period and that taking body body size. The same conclusion is reached when we compare size into account does not improve the fit (Barrickman et al. the life history of human foragers directly with that of extant 2008). nonhuman hominoids (table 2). This difference points to To assess to what extent this effect of brain size on life major changes in lifestyles adopted by hominins, which will history also characterizes humans, we should look at human be explored after we determine that a given lineage has a life history traits in relation to relative brain size. Although maximum brain size it can achieve. some have questioned whether extant human foragers rep- resent the “natural” condition for our species, they are cer- Brain Size and Maximum Population tainly situated at the lower end of the spectrum of human Growth Rates reproductive capacity and can thus serve as a conservative estimate for comparison with extant ape species. In large-brained mammals and primates, the developmental If we plot life history traits versus relative brain size in slowdown and reduced reproductive rate are accompanied by nonhuman primates (fig. 2) and assess the values of human an increased adult life span (Isler and van Schaik 2009a), but foragers and horticulturalists based on those expected for the question arises whether the increased life span can con-

Figure 3. Maximum population growth rate rmax as a function of (A) endocranial volume (ECV) and (B) body mass in nonhuman primates (N p 85 species; Homo is shown for comparison but is not included in the calculation). A color version of this figure is available in the online edition of Current Anthropology. Isler and van Schaik Cooperative Breeding in Early Homo S457

Table 3. Maximum population growth rates of humans and other great apes

Rate Gorilla gorilla Pan troglodytes Pan paniscus Pongo pygmaeus Pongo abelii Human mean 14 Interbirth interval (years) 5 5.43 4.8 7.35 9.3 3.331 Female age at first reproduction (years) 10.2 13.25 14.2 15.7 15.4 18.84 Maximum life span 55 59.4 54.5 56.3 59 85 rmax .054 .049 .047 .031 .025 *

DTmin (years) 12.8 14.1 14.7 22.4 27.7 * Maximum age at last birth 45? 45 45 45? 45 47 rmax** (using maximum age at last birth) .051 .044 .043 .025 .017 .047

DTmin** (years) 13.6 15.8 16.1 27.7 40.8 14.7 Sources. Maximum age at last birth for apes (Emery Thompson et al. 2007; Wich et al. 2004); for humans (Hill and Hurtado 1996; Howell 1979).

Note. The human rmax and DTmin values calculated from maximum life span would be artificially high (*). Because of midlife menopause in humans, rmax and DTmin are more realistically calculated using maximum age at last reproduction instead of maximum life span (**). Then, however, the p same rationale must be followed for the other apes. These values should not be compared with those of other primates or mammals. DTmin minimum time to double population size. tinue to fully compensate the reduced production per unit be a better estimate of body size than body mass itself by time as brain size increases. On average, females of every being less prone to error variance (Economos 1980) and be- species leave roughly two viable adult offspring per lifetime, cause the relationship is found only for brain mass and not but species vary dramatically in their maximum reproductive for the mass of other organs, which also show a low degree capacity under ideal conditions. We need a measure of re- of variation (see Isler and van Schaik 2009b, app.). What is productive capacity that represents maximum possible life- especially striking is that great apes, in particular orangutans, time reproductive success. The net reproductive rate (R(0))of show the lowest possible rmax, quite possibly close to what is extant populations is derived from life tables and will hardly minimally viable demographically. ever represent optimal conditions. A far better estimate of Similarly, although rmax is based on an average annual fer- maximum reproductive capacity is maximum population tility rate, we may expect that using a maximum fertility rate growth rate (rmax). Additionally, in contrast to a rough product would only strengthen the observed relationship, as small- of average fertility and maximum fertile life span, rmax takes brained species probably exhibit a higher plasticity of repro- generation time into account. To give a stark example, if two duction in response to ecological conditions. In this case, rmax otherwise identical species differed because in one, females would underestimate the maximum reproductive capacity start to reproduce at age 1 and die at age 21, whereas in the mostly in small-brained species, yielding an even stronger other, females start to breed at age 21 and die at age 41, the negative correlation between maximum reproductive capacity

first species would soon outcompete the second (Lewontin and brain size. Using rmax is therefore a conservative approach

1978). The value of rmax is defined as for our purpose. 1 p eϪr ϩ beϪra Ϫ be,Ϫr(wϩ1) The Gray Ceiling in Primates where a p age at first reproduction, w p age at last repro- The negative relationship between r and brain mass, con- duction, or maximum life span, and b p birth rate (of female max trolling for body mass, indicates that as brain size increases, offspring) per year (Cole 1954). We can calculate r from max the increase in life span is increasingly unable to fully com- age at first reproduction, maximum life span, and annual pensate for the costs incurred by long developmental periods fertility rates by solving Cole’s (1954) equation numerically (Ross 1988, 1992). Enough reliable data for its calculation Table 4. Multiple regression of variables affecting r exist for many extant primate species. From r , the mini- max max simultaneously in nonhuman primates (N p 85 species, mum number of years needed to double population size r2 p 0.869) (DTmin) is calculated as Variable Estimate t ratio P ln(2) DT p . min r Intercept .083 .22 .829 max ln female endocranial volume Ϫ.663 Ϫ5.24 !.0001 We have shown previously (Isler and van Schaik 2009b) ln female body mass .067 .69 .495 that this r shows a very strong negative correlation with Terrestriality .168 3.91 .0002 max Nocturnality Ϫ.131 Ϫ2.40 .019 brain mass in mammals and precocial birds, and indeed, that Hominoidea vs. others Ϫ.232 Ϫ3.53 .0007 brain mass is a better predictor of r than is body mass. The max Note. Parametrization of the covariates was chosen empirically in order same is found within primates as a group (fig. 3) and if we to explain as much variation of rmax as possible as follows: terrestriality control for phylogenetic nonindependence (table 1). This and nocturnality were coded as binary variables (none or !5% vs. 15% finding is not a statistical artifact because brain mass might of terrestriality; nocturnal vs. diurnal or cathemeral). S458 Current Anthropology Volume 53, Supplement 6, December 2012

risk of local extinction in such conditions. Indeed, a popu- lation’s maximum reproductive capacity directly affects the maximum rate of environmental change that it can adapt to without going extinct (Lynch and Lande 1993). Second, low reproductive potential even under perfect conditions also im- plies a limited ability of a species to recover from population crashes and thus a species that is less likely to build up enough individuals to colonize new areas or habitats until the next crisis period. We can therefore use this reproductive potential as an estimate of the ability to stave off population or species extinction.

A major consequence of this rule is that ever-lower rmax with increasing brain size should lead us to expect a particular maximum brain size, which we call the gray ceiling. As brains exceed this size, population extinction becomes increasingly likely, leading eventually to the extinction of the population or species whenever major changes in habitat (e.g., due to climate change) take place. Given that among primates, great apes are at the minimum of demographic viability, we must conclude that in this lineage no major increase in brain size should be possible. Nonetheless, humans, of course, achieved exactly this, raising the question how this was possible.

Calculating rmax of extant humans is complicated by the existence of midlife menopause, which is unique among pri- mates. If instead of maximum life span we use maximum observed age at last reproduction (for females) and do the

same thing for great apes, the rmax of humans lies between the values of gorillas and chimpanzees (table 3) instead of far lower, as one would expect based on the brain-size effect on

Figure 4. Relationship between maximum population growth rmax. Notice that Sumatran orangutans have a potential DTmin rate rmax versus endocranial volume (ECV) in nonhuman pri- of over 25 years, which may well be the lowest value observed mates as affected by (A) terrestriality and (B) nocturnality. To for all extant mammals (the actual value itself is not to be illustrate the magnitude of differences, slopes of the regression taken too seriously because it refers to a theoretical construct; lines were forced to be identical in both groups. Symbols as in it is only meant to be used for comparative purposes). In the figure 3; multivariate statistics in table 5. A color version of this more seasonal African environments, such a value may not figure is available in the online edition of Current Anthropology. be realistic, and the observed values of the African great apes (between 13.6 and 16.1 years) suggest a realistic value of the and lower reproductive rates. The most likely reason is that potential DTmin of around 20 years. there is a realistic minimum mortality rate set by freak ac- cidents and freak environmental events (droughts, floods, Predicting Human r fires, epidemics, lightning strikes, etc.) that are truly unavoid- max able regardless of niche or behavior. Thus, as this minimum In comparison with other hominoids, humans exhibit a much mortality level is approached, further increases in brain size larger rmax than expected for our extremely large brain size will of course continue to yield lower production but will (fig. 3A). But what value of rmax would be predicted for a inevitably lead to only a modest improvement in survival and typical hominoid of humanlike brain and body mass? To an- thus maximum life span. As a result, rmax declines. swer this question, we must consider possible correlates of

It is likely that such a low reproductive potential as found either brain size or rmax to construct a multivariate linear in great apes compromises demographic viability for two rea- model that explains as much variation in primate rmax as pos- sons. First, where survival must be near perfect just to main- sible. tain population stability, there is virtually no room for selec- In a multivariate analysis within nonhuman primates p tive mortality. This means that drastic changes in the (N 85 species; table 4), rmax is affected by arboreality (spe- environment must be met with phenotypically plastic re- cies that are at least partly terrestrial have a higher rmax;fig. sponses (including individual learning and innovativeness and 4A) and by nocturnality (nocturnal species have a lower rmax socially learned innovations, i.e., culture) rather than selective than diurnal or cathemeral species; fig. 4B) but not by diet mortality and that populations are almost certainly at higher (percentage of leaves or fruit or animal matter in the diet). Isler and van Schaik Cooperative Breeding in Early Homo S459

Table 5. Hypothetical life history traits of Homo sapiens predicted from primate and hominoid trends

Trait Model A: primate Model B: hominoid Actual values: mean 14 Litter size !1 !1 1.011 Neonate mass (g) 7,377 6,865 3,319 Gestation length (months) 10.2 10.9 8.9 Lactation length (years) 5.46 7.57 2.83 Interbirth interval (years) 5.89 7.89 3.33 Age at first reproduction (years) 17.3 22.6 18.8 Maximum life span (years) 68.7 79.1 85

rmax .027 .022 .047

DTmin (years) 25.4 32.3 14.5 Source. For comparison, the actual mean values of 14 extant human populations are taken from Walker et al. (2006). Note. Model A includes terrestriality, nocturnality, and female endocranial volume and body mass, whereas model B additionally takes membership to Hominoidea into account. Using the predicted values for interbirth interval and age at first reproduction

and setting litter size to 1 and maximum age at last reproduction to 47 years, rmax values for Homo sapiens can also be calculated directly, yielding .031 (model A) and .014 (model B).

But even if these covariates are controlled for, hominoid spe- populations under the unstable African conditions in which p cies exhibit a lower rmax than other primates (P .0007 in a humans evolved. multiple regression; table 4). These hypothetical human rmax values, assuming a lifestyle

If humans followed the general primate trend, their rmax like that of other primates, are lower than those found for would be estimated as 0.027 (predicted from a multivariate any extant mammalian species. The lowest observed rmax val- model including terrestriality, nocturnality, and female body ues are found in species that experience very low adult mor- mass and endocranial volume [ECV]; table 5). If we take into tality rates (i.e., live in extremely stable habitats and hardly consideration that we are hominoids too, the predicted rmax suffer from predation), such as orangutans: 0.025 (Pongo abe- would be even lower, about 0.022. This means that the DTmin lii) and 0.031 (Pongo pygmaeus); killer whales: 0.028 (Pseu- under optimum conditions would be around 30 years, which dorca crassidens) and 0.046 (Orcinus orca); chimpanzees: 0.049 would almost certainly not lead to demographically viable (Pan troglodytes) and 0.047 (Pan paniscus); gorillas and Af- rican elephants: 0.054; and dugongs: 0.058. In conclusion, regardless of which model we use, a species with human brain and body mass would not be able to survive if it otherwise adheres to a primate or hominoid lifestyle let alone whether it was not completely arboreal and living in African woodland or savanna.

Why Could Humans Break through the Gray Ceiling? Up to this point, we have shown that a human brain–body size relationship would not be demographically feasible in a primate following a typical hominoid lifestyle even if we take differences in diet and locomotor patterns into account. The main distinction affecting interbirth intervals and weaning age is our system of cooperative care for infants and mothers (Burkart, Hrdy, and van Schaik 2009; Burkart and van Schaik 2010; Hrdy 2005). Callitrichids are the only other primates Figure 5. Maximum population growth rate rmax versus brain size (endocranial volume [ECV]) in nonhuman primates for spe- that exhibit cooperative breeding to a similar extent. Indeed, cies that exhibit cooperative breeding (Homo sapiens is excluded the maximum reproductive rate of callitrichines is, because from the calculation); species that show at least some amount of twinning, on roughly the same grade as Homo sapiens (fig. of allomaternal care such as paternal care, communal nursing, 5). or babysitting; and species that show no allomaternal care at all. A multivariate regression yields a clear additional effect of To illustrate the magnitude of differences, slopes of the regression lines were forced to be identical in the three groups. Symbols as this very rough measure of the extent of allomaternal care in in figure 3; multivariate statistics are given in table 7. A color nonhuman primates taking into account the known covariates version of this figure is available in the online edition of Current such as terrestriality, nocturnality, and diet (table 6). A more Anthropology. quantitative measurement of the extent and dimensions of S460 Current Anthropology Volume 53, Supplement 6, December 2012

Table 6. Multiple regression of variables affecting rmax 2010), and they may pull the estimates for humans down. simultaneously in nonhuman primates including a rough On the other hand, the heavily terrestrial gorillas may bias measure of allomaternal care (N p 72 species,r2 p 0.897 ) the estimates in the opposite direction, and the chimpanzee values are actually predicted quite well by the hominoid Variable Estimate t ratio P model. For now, therefore, we present both sets of results and Ϫ Ϫ Intercept .580 1.39 .168 expect that the true values may be intermediate. ln female endocranial volume Ϫ.540 Ϫ4.32 !.0001 ln female body mass .100 1.01 .317 Table 7 shows that the predicted age at first reproduction, Terrestriality .106 2.40 .019 fertility rates, interbirth intervals, and rmax are fairly accurate Nocturnality Ϫ.001 Ϫ.01 .989 in both models. Note that in both models C and D, interbirth Ϫ Ϫ Hominoidea vs. others .316 4.86 !.0001 intervals are anomalously shorter than lactation periods, Cooperative breeding: Cooperative vs. some allomaternal care .385 4.07 .0001 which is due to the result that in nonhuman primates, allo- Some vs. no allomaternal care .301 4.41 !.0001 maternal care reduces interbirth intervals more than it short- Note. Allomaternal care was assigned to three categories: “cooperative ens lactation periods. We are thus confident that cooperative care”: cooperatively breeding species (callitrichines); “some allomaternal care is indeed responsible for the observed differences between care”: species in which at least a modest amount of help for the mother human and ape life history traits. This interpretation is sup- is provided through paternal care, babysitting, allonursing, or passive ported by another result in table 7. Human life span is some- food sharing; “no allomaternal care”: the remaining species. For the other covariates, see table 4. If the variable “Hominoidea vs. others” is excluded, what longer than predicted, which may be linked to our ten- the effect of allomaternal care on rmax is still significant. In comparison dency to support the sick and injured, which should improve to the model in table 4, nocturnality does not affect rmax in this model. survival relative to the baseline situation of no support, as in This indicates that the difference in r between nocturnal and diurnal max great apes, and thus over time maximum life span. primates is better explained by the differences in the breeding system than by their activity pattern. There is one major discrepancy between model and ob- servation that may therefore reflect another effect than co- operative breeding. Neonate mass is much smaller and ges- allomaternal help confirms this relationship (van Schaik and tation length somewhat shorter than the very large values Isler 2012). predicted (largely due to our very large brain size). This dis- The inclusion of allomaternal care in the model to predict crepancy may be linked to the obstetrical dilemma, caused hypothetical human life history traits yields values that are by the narrowing of the pelvic canal as a result of bipedalism much closer to the actual values of extant human subsistence populations (table 7). It is not clear a priori which of the two (Montagu 1961; Trevathan 1987; Washburn 1960), which at models (general primate [C] or hominoid [D] in table 7) some point has become limiting for the size of the human provides the most accurate answer. neonate. It is certainly consistent with the secondary altri- Southeast Asian hominoids (gibbons, orangutans) live in ciality of human neonates. Note, however, that a more altricial regions that were at least in part affected less by the series of state at birth can explain only this one minor difference be- Pleistocene glaciations than Africa (Whitmore 1984). This tween the life histories of humans and great apes, whereas relative stability may have allowed for slower viable rmax (per- the overall difference can be attributed to the extensive allo- haps in part achieved through lower BMRs; Pontzer et al. maternal care in humans.

Table 7. Hypothetical life history traits of Homo sapiens predicted from a primate trend includ- ing cooperative breeding

Model C: Model D: Actual values: Trait primate and help hominoid and help mean 14 Litter size !1 1.036 1.011 Neonate mass (g) 6,824 6,476 3,319 Gestation length (months) 11.1 11.8 8.9 Lactation length (years) 3.78 5.28 2.83 Interbirth interval (years) 3.16 4.41 3.33 Age at first reproduction (years) 16.6 20.9 18.8 Maximum life span (years) 67.5 76.7 85

rmax .057 .042 .047

DTmin (years) 12.2 16.5 14.5 Source. For comparison, the actual mean values of 14 extant human populations are taken from Walker et al. (2006). Note. Model C includes female brain and body mass, terrestriality, and the allomaternal care category, whereas model D additionally takes membership to Hominoidea into account. Using the predicted values for litter size, interbirth

interval, age at first reproduction, and maximum age at last reproduction set to 47 years, rmax values for Homo sapiens can also be calculated directly, yielding .054 (model C) and .035 (model D). Isler and van Schaik Cooperative Breeding in Early Homo S461

Figure 6. Minimum population doubling time versus endocranial volume (ECV) in nonhuman primates (Homo sapiens is excluded from the calculation). The vertical line represents an ECV of 655 cm3. Note that values are not log transformed here. A color version of this figure is available in the online edition of Current Anthropology.

When Did Humans Break through (table 8). If we assume cooperative breeding, the predicted the Gray Ceiling? AFR is between 10.9 and 22.6 years, while the predicted IBI In this section, we aim to predict maximum potential pop- is 3.4 for A. afarensis and 4.7 for Qafzeh H. sapiens. Estimating ulation growth rates of extinct hominins from the primate twinning rate from our models is not feasible because the model to find out when they would have reached the region twinning callitrichines introduce a strong body-mass depen- of demographic nonviability without a change in the breeding dency of twinning rates. To estimate population growth rates, we therefore set litter size to 1.01; that is, twinning occurs in system. In a first attempt, we plot DTmin of nonhuman pri- mates versus their ECVs (fig. 6). To get a reasonable estimate 1% of births. The results of the model are illustrated in figure of a threshold value, we conservatively assume that a doubling 7. p time beyond 30 years (rmax 0.023 ) would not yield viable We assume that a DTmin of somewhere between 15 years populations. This is a very conservative estimate, as no other (extant chimpanzees) and 20 years would still be feasible. It living mammal exhibits such a low maximum reproductive is apparent that no help for mothers (as in orangutans) results rate. From the relationship between DTmin and ECV, we con- in a very steep relationship between population doubling clude that this value would be reached with an ECV of about times and brain size. Species are included in the category of 3 650 cm . If terrestriality is included in the model, which is “some help” even if they exhibit minimal helping behaviors, rather likely for all early hominins (remember we do not such as passive food sharing or babysitting, with only minimal require a high percentage of terrestrial locomotion here), the frequency. Extant African apes (gorillas and chimpanzees) are threshold would be even lower, about 610 cm3. This crude at this lower end of the spectrum. From our model, it seems first attempt suggests that the first species to break through that an ECV of more than 700 cm3 would not yield sustainable the gray ceiling was early Homo, which must therefore have populations with such an intermediate system of allomaternal had extensive allomaternal care. Using the more sophisticated care. Only with full cooperative breeding (as in extant humans model D—which was specific for the hominoids and included not only brain size but also body mass, terrestriality, and the or callitrichines) would fossil hominins have been able to level of allomaternal care—the effect of a change in breeding provide sufficient energy for a sustainable population growth 3 system can be specified in greater detail. rate and support a brain that is larger than 700 cm . Table 8 lists predicted interbirth intervals and the corre- In conclusion, a gradual change in lifestyle toward a sub- stantial increase in allomaternal help (including provisioning sponding DTmin for fossil hominin taxa groups. If we assume no allomaternal help, the predicted age at first reproduction of mothers and weaned offspring) may have evolved early in, (AFR) ranges from 12.6 years in Australopithecus afarensis to or even before, the genus Homo. (For the challenge of allo- 26.1 years in the very large-brained Qafzeh Homo sapiens,and cating the earliest Homo fossils to meaningful clusters, see the predicted interbirth interval (IBI) is from 6 to 8.4 years Anto´n 2012.) S462 Current Anthropology Volume 53, Supplement 6, December 2012

Were Early Homo Cooperative Breeders? (van Schaik and Burkart 2010). Indeed, among mammals, carnivores are more likely to be cooperative breeders (Smith We believe that Homo erectus (p ergaster), as it emerged at et al. 2012; Solomon and French 1997; Spencer-Booth 1970). around 1.8 Ma, was a good candidate for having extensive allomaternal care for two major reasons. First, they were likely Second, the weaned juveniles were less likely to make a living the first systematic hunters of large game (Foley and Lee 1991; on their own and would have strongly benefited from allo- Pobiner et al. 2008). Large-game hunting requires cooperation maternal support. They lived on the savanna, where resources during the hunt, cooperative defense against other dangerous harvested as efficiently by juveniles as adults, such as soft fruits, carnivores, extremely high tolerance around kills, and fre- are much scarcer than in forests (Hawkes et al. 1998), leading quent food sharing, perhaps even to the point of provisioning. to reduced juvenile foraging efficiency. The latter is especially These features are all more likely among cooperative breeders likely if they had already acquired a great reliance on meat

Table 8. Predicted life history and demographic parameters of early hominins

Allomaternal care during predicted Allomaternal care interbirth interval during predicted

(years) DTmin (years) Female endocranial Species and sample Time (Ma) volume Female body mass No Some CB No Some CB Australopithecus afarensis: A.L. 333-105 3.2 343 29.3 6.04 4.59 3.43 17.7 14.0 10.3 A.L. 444-2 3.2 550 51.3* 6.88 5.24 3.91 23.4 17.7 12.6 Australopithecus africanus: STS 71 2.75 428 26.6 6.21 4.73 3.53 20.1 15.6 11.4 STW 505 2.5 560 46.8 6.85 5.21 3.89 23.8 18.0 12.7 Australopithecus boisei: KNM-ER 732 female 1.7 500 32.0 6.48 4.93 3.68 22.1 17.0 12.2 OH 5 male 1.8 530 57.6 6.91 5.26 3.93 22.8 17.3 12.4 Early Homo: KNM-ER 1813 1.89 509 34.9 6.56 4.99 3.72 22.4 17.1 12.3 KNM-ER 1805 1.89 580 30.3* 6.61 5.03 3.76 24.6 18.6 13.1 KNM-ER 1470 1.89 752 45.6 7.18 5.46 4.07 30.0 21.8 14.8 Homo erectus: Africa: KNM-ER 42700 (Ileret) 1.55 690 45* 7.06 5.38 4.01 27.9 20.5 14.2 KNM-ER 3733 1.8 850 59.2 7.50 5.71 4.26 33.4 23.7 15.7 Georgia: D3444 1.77 638 47* 7.00 5.33 3.97 26.2 19.5 13.6 D2280 1.77 775 52.6* 7.31 5.56 4.15 30.7 22.2 15.0 Asia: Zhoukoudian XI female .42 1,015 51.8 7.64 5.81 4.34 41.2 27.9 17.6 Zhoukoudian X male .42 1,225 65.6* 8.06 6.13 4.57 53.2 33.3 19.8 Archaic Homo sapiens: Steinheim .25 1,110 60.5 7.86 5.98 4.47 45.9 30.1 18.6 Jebel Irhoud .09 1,305 80.5 8.3 6.31 4.71 58.0 35.2 20.5 Homo neanderthalensis: Saccopastore female .12 1,245 66.6 8.09 6.16 4.59 54.6 33.9 20.0 Le Moustier male .041 1,565 81.2 8.56 6.52 4.86 89.3 45.8 23.8 H. sapiens: Zhoukoudian 102 female .015 1,380 43.2 7.91 6.02 4.49 74.5 41.7 22.5 Qafzeh 9 female .1 1,531 64.6 8.35 6.36 4.74 89.5 46.1 23.8 Extant females 0 1,213 45.3 7.79 5.93 4.42 55.1 34.3 20.1 Sources. Endocranial volumes (cm3) and body mass (kg) estimates of fossils are taken from Gabunia et al. (2000), Kappelman (1996), Spocter and Manger (2007), Spoor et al. (2007), and Ruff (2010). Note. As sex determination is notoriously difficult for early hominins, we list both a small and a large morph from reasonably complete crania. Body mass estimates denoted with an asterisk do not correspond to the same fossil as the endocranial volume. The body mass for a small African H. erectus (45 kg) is very roughly estimated from comparing other estimates with the size of the Ileret cranium. Interbirth intervals and age at first reproduction are estimated using model D from table 6 (excluding the effect of nocturnality). For calculating minimum population doubling time ! p (DTmin), maximum age of reproduction is set to 47 years and twinning rate to 1/100. Values 20 years are highlighted in boldface. CB cooperative breeding. The predictions for 1.9 Ma Australopithecus sediba would be very similar to A. africanus min. (endocranial volume of 420 cm3 in a juvenile male, body mass of the adult female estimated at 27 kg; Berger et al. 2010). Isler and van Schaik Cooperative Breeding in Early Homo S463

Figure 7. Minimum population doubling time (DTmin; years) of fossil hominins predicted from model D (individual values listed in table 8). We assume that a DTmin of somewhere between 15 years (extant chimpanzees) and 20 years would still be feasible (shaded bar). The lack of smoothness results from the inclusion of body mass in the model. A color version of this figure is available in the online edition of Current Anthropology.

(Domı´nguez-Rodrigo and Pickering 2003), because the diffi- to a reduction in rmax in larger-brained organisms. There comes culty of learning how to hunt means that provisioning meat a point where no further increases in brain size are possible has strong positive effects on the fitness prospects of the young. because the long-term viability of populations is severely com- More seasonal habitats are more likely to contain cooperative promised. This point we call the “gray ceiling.” For great apes breeders (Hatchwell 2007; Rubenstein and Lovette 2007). The living a great-ape lifestyle, we put this conservatively at 600– argument is further supported by H. erectus (p ergaster)oc- 700 cm3. This explains why extant great apes and extinct cupying a much larger geographic range than earlier hominin australopithecines seem to have converged on similar brain species. Hrdy (2005, 2009) has argued convincingly that colo- sizes, but it makes the “escape” from great-ape level brain nizing hostile new habitats is facilitated by cooperative breeding. sizes by Homo even more striking. Assigning a distinct bound- Identifying the source of extensive allomaternal care in early ary to a highly fragmentary fossil record is tricky, but Homo Homo is difficult, as the defining feature of human caretaking rudolfensis (i.e., KNM-ER 1470) is a likely candidate for such seems to be its large flexibility (Hrdy 2009). In present-day hu- a change in lifestyle. The first well-documented hominin to man societies, grandmothers and males, but also not directly show brains that exceed this size was Homo erectus (p erg- related adults (Hill and Hurtado 2009), play a major role. As aster), which arose in Africa at around 1.8 Ma, occupied midlife menopause is extremely rare in mammals (Packer, Tatar, savanna habitats, hunted large game, and rather quickly had and Collins 1998), we cannot apply comparative evidence to the moved into other geographic regions. evolution of grandmothering. However, males were almost cer- Allomaternal care tends to lead to higher female repro- tainly involved in meat sharing and thus allomaternal care as ductive output in both primates (Mitani and Watts 1997; Ross soon as confrontational scavenging or hunting of large game was and MacLarnon 2000) and carnivores (Isler and van Schaik present (Marlowe 2007). In sum, while the brain size of H. erectus 2009a). We propose that as in other mammals and birds, the and various other indicators suggest that females of this species adoption of cooperative breeding (Hrdy 2005, 2009) had al- received much allomaternal care, we assume that male-female lowed H. erectus (p ergaster) to increase its r , which, given pair bonds accompanied by selective food sharing were sources max its value near the gray ceiling, made possible an expansion of of this care, but we can make no conclusions about the role of grandmothers. its brain size. As a conservative estimate, our gray ceiling value of 600–700 cm3 provides an upper boundary to brain size if a species is adhering to an apelike lifestyle. Of course, we Discussion cannot exclude the possibility that cooperative breeding pre- The analyses reported here suggest that the inability of survival dated a pronounced increase of encephalization by several to keep up with reduced production as brain size increases leads million years, as suggested in Lovejoy’s (2009) scenario for S464 Current Anthropology Volume 53, Supplement 6, December 2012 the adaptive suite of characters assigned to Ardipithecus ram- Burkart, Judith M., and Carel P. van Schaik. 2010. Cognitive consequences of cooperative breeding in primates? Animal Cognition 13(1):1–19. idus. In this case, however, another explanation would be Chivers, David J., and Claude M. Hladik. 1980. Morphology of the gastro- needed for the long time lag between the onset of provisioning intestinal tract in primates: comparisons with other mammals in relation and increase in brain size. Australopithecines were adept bi- to diet. Journal of Morphology 166:337–386. Cole, Lamon C. 1954. The population consequences of life-history phenom- peds without sectorial canine complexes, but there is no evi- ena. Quarterly Review of Biology 29(2):103–137. dence for a shift in life history traits and developmental tra- Dean, M. Christopher. 2006. Tooth microstructure tracks the pace of human jectories before Homo (Dean 2006; Dean and Lucas 2009; life-history evolution. Proceedings of the Royal Society B 273:2799–2808. Dean, M. Christopher, and Victoria S. Lucas. 2009. Dental and skeletal growth Schwartz 2012; but see DeSilva 2011). in early fossil hominins. Annals of Human Biology 36(5):545–561. In conclusion, if we rely on estimating the effect of evo- Deaner, Robert O., Rob Barton, and Carel P. van Schaik. 2003. Primate brains lutionary processes known to operate in primates or in ver- and life histories: renewing the connection. In Primate life histories and socioecology. Peter Kappeler and Michael E. Pereira, eds. Pp. 233–265. Chi- tebrates in general, there is evidence for several factors that cago: University of Chicago Press. allowed for brain-size expansion throughout the evolutionary Deaner, Robert O., Karin Isler, Judith M. Burkart, and Carel P. van Schaik. history of the human lineage. A more seasonal environment, 2007. Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain, Behavior and Evolution a change in diet toward higher-quality food sources, and more 70:115–124. efficient locomotion all may have played a role (Potts 2011). DeSilva, Jeremy M. 2011. A shift toward birthing relatively large infants early Instead of a comprehensive but unique “adaptive suite” of in human evolution. Proceedings of the National Academy of Sciences, U.S.A. 108(3):1022–1027. human traits (Lovejoy 2009), however, we find broad com- Domı´nguez-Rodrigo, Manuel, and Travis R. Pickering. 2003. 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The Capital Economy in Hominin Evolution How Adipose Tissue and Social Relationships Confer Phenotypic Flexibility and Resilience in Stochastic Environments

by Jonathan C. K. Wells

The global distribution of our species indicates a biology capable of adapting to an extraordinary range of ecosystems, generating interest in how such a biology evolved. Whereas much attention has been directed to genetic adaptation and developmental plasticity as adaptive strategies, ecological stochasticity within the life course may be addressed by additional strategies such as bet hedging and phenotypic flexibility. Both social relationships and adipose tissue may be considered as “energy capital” conferring reversible phenotypic flexibility across the life course. Evidence from primates and contemporary humans demonstrates the value of such energy capital in accommodating ecological uncertainty. The fact that Homo sapiens is characterized by high levels of both cooperative sociality and adiposity compared with extant apes suggests that ecological stochasticity may have been a key ecological stress in the evolution of our genus. The benefits of phenotypic flexibility for ecological risk management may have preceded and enabled the emergence of traits such as carnivory, encephalization, colonizing, and the maintenance of a single breeding species across diverse environments.

To understand the particular characteristics of extant humans, has generally been considered an integrated shift in many of much work has focused on physical traits readily discernible these trends, this perspective is now undergoing reappraisal in the fossil record, such as cranial capacity, dentition, and in the light of more comprehensive skeletal evidence (Anto´n postcranial anatomy. Such investigation enables the recon- and Snodgrass 2012). struction of trends in functional traits such as encephalization, The study of ecogeographical and temporal variability within locomotion, and reproduction (e.g., Anto´n 2003; Bramble and contemporary humans plays a key role in these reconstructions. Lieberman 2004; Bruner, Manzi, and Arsuaga 2003; DeSilva For example, substantial research has been conducted on the 2011; Rosenberg and Trevathan 2002). Evolutionary changes association between climate and morphology in humans (Hier- in such traits are typically considered physical or physiological naux and Froment 1976; Katzmarzyk and Leonard 1998; Rob- “solutions” to ecological stresses, such as climate trends or erts 1953; Wells 2012b). Such work then informs understanding shifts in the availability of resources (Klein and Edgar 2002; of past variability in hominin morphology (Perry and Dominy Vrba 1985), although neutral evolution and genetic drift may 2009; Ruff 2002). Similarly, variability in contemporary or re- also contribute to phenotypic trends. Much attention has been cent human dentition can be used to infer past dietary stresses directed, for example, to understanding what might have and to evaluate evolutionary patterns (Anto´n, Carter-Menn, driven the trend toward bipedal locomotion in earlier hom- and DeLeon 2011; Kaifu et al. 2003). inins (e.g., Crompton, Sellers, and Thorpe 2010) or progres- Although not addressed explicitly by all authors, nonpath- sive encephalization in the genus Homo (e.g., Bruner, Manzi, ological anatomical variation in the fossil record has tradi- and Arsuaga 2003). Dental analysis offers the capacity to re- tionally tended to receive a genetic interpretation (e.g., Hol- construct how hominins responded to changes in the avail- liday 1997; though see Ruff 2002). First, phylogenetic analyses ability of food sources (Organ et al. 2011), indicating, for typically show good agreement between molecular and mor- example, a postaustralopithecine shift to a broader diet base phological data (Gibbs, Collard, and Wood 2000; Gilbert and (Ungar 2012). Although the emergence of the genus Homo Rossie 2007; Pilbeam 2000), potentially implying a similar scenario for within-species variability. Second, the long-stand- ing attention directed to long-term ecological trends as key Jonathan C. K. Wells is Professor of Anthropology and Pediatric stresses (e.g., the “savannah hypothesis”; Dart 1925; Klein and Nutrition at the Childhood Nutrition Research Centre, University College London Institute of Child Health (30 Guilford Street, London Edgar 2002) would also match with a genetic model of ad- WC1N 1EH, United Kingdom [[email protected]]). This aptation. Consistent with such a perspective, climate has in- paper was submitted 12 XII 11, accepted 3 VII 12, and electronically deed been associated with genetic variability among contem- published 23 X 12. porary humans (Hancock et al. 2010, 2011).

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0016$10.00. DOI: 10.1086/667606 Wells The Capital Economy in Hominin Evolution S467

More recently, however, the contribution of developmental since the origin of our species. However, the interpretation plasticity to phenotypic variability has been recognized in of such phenotypic variation in the fossil record as adaptation extant primates and humans, suggesting that a similar ap- is possible only because each adaptation of genotype and de- proach is required for the fossil record (e.g., Ruff 2002). Ex- velopmental plasticity may generate relatively irreversible phe- perimental work on primates has demonstrated rapid trans- notypic effects within the life course. generational shifts in body proportions in populations Natural selection acts not on traits but on strategies (Hous- exposed to novel thermal environments (Paterson 1996) or ton and McNamara 1999), for example, not on tall height, to shifts in the availability of energy (Price, Hyde, and Coe but on growing faster or for longer. In contrast to the ex- 1999), clearly demonstrating a contribution of plasticity to amples described above, some adaptive strategies are relatively phenotypic change across generations. Similar work in hu- reversible, which in turn tells us about the kind of ecological mans has shown that both nutritional experience and psy- stresses that drive them. Such plasticity may relate either to chosocial stress in early life can exert long-term effects on the instability of phenotype within individuals or to pheno- multiple aspects of phenotype (e.g., Bogin et al. 2002; Ellis et typic relationships between individuals. In this article, I first al. 2009). A more comprehensive approach must therefore describe how stochastic environments favor such phenotypic assume that variability in the hominin fossil record reflects flexibility, which may emerge in different formats. I then re- the influences of both genotype and developmental plasticity view how both primates and humans benefit from such flex- (Kuzawa and Bragg 2012; Ruff 2002; Wells and Stock 2007). ible traits, focusing in particular on two generalized stores of The fundamental connection between contemporary hu- energy. Finally, I consider what role such energy stores may man variability and past evolutionary change may also apply have played in human evolution. to phenotypic traits that leave, at best, weak signals in the fossil record. Recently, for example, much interest has been Modes of Adaptation directed to why and when the unusual life history profile of humans (lengthy life spans and developmental periods but short interbirth intervals) emerged in our evolutionary history Phenotypic plasticity embraces many forms that can vary both (Aiello and Key 2002; Anto´n 2003; Hawkes 2006; Hrdy 2009). in their relative speed of response to ecological stresses and in Life history variability among contemporary humans is as- their degree of reversibility. At one extreme, developmental sumed to incorporate adaptation to stresses such as energy plasticity tends to be relatively irreversible, reflecting interac- availability and mortality risk, though the associations are tions between genotype and environment in early life, whereas complex (Ellis et al. 2009; Migliano and Guillon 2012; Perry at the other extreme, some aspects of metabolism and behavior and Dominy 2009; Walker and Hamilton 2008; Walker et al. can alter on a second-by-second basis (Gabriel et al. 2005; 2006). In turn, humans per se have an unusually lengthy Piersma and Drent 2003). In turn, the time lag of plastic re- period of development, suggesting that the Homo niche fa- sponse following the environmental cue may also vary (Gabriel vored a progressive reorganization of the tempo of devel- et al. 2005). Most work has focused on the two extremes, using opment in response to diverse ecological pressures, some of quantitative genetic models to address the norms of reaction them potentially compounded by hominin traits such as in- underlying developmental plasticity or optimality theory to ad- creasing brain size (Isler and van Schaik 2012; Robson, van dress behavioral ecology (Gabriel et al. 2005). Schaik, and Hawkes 2006; Schwartz 2012). Such variability in the form of plasticity reflects variability Information on some life history traits can be gleaned from in the frequency and regularity of ecological stresses relative the fossil record, though others, such as interbirth interval to the life span of the organism (Piersma and Drent 2003). and total fertility rate, may leave no material signal. For ex- Although attention has traditionally been directed to long- ample, dental eruption patterns represent markers of matu- term ecological shifts affecting hominin evolution, there is ration rate across species, though interpretation is complex increasing interest in the diversity of ecological stresses, some (Schwartz 2012), while age at weaning can potentially be es- of which are short-term but frequent and unpredictable (Bobe timated from isotopic enrichment ratios (e.g., Herring, Saun- and Behrensmeyer 2004; Potts 1996, 2012). ders, and Katzenberg 1998). Furthermore, plasticity in such Genetic adaptations can develop over variable time spans. developmental traits may be revealed by traits such as body There is increasing recognition that specific traits underlying proportions; for example, leg length appears particularly vul- the complex life history profile of humans have a polygenetic nerable to poor childhood nutrition, and short leg length may basis (Elks et al. 2010; Hirschhorn and Lettre 2009; Yang et al. therefore act as a skeletal marker for slowed development (e.g., 2010); hence, phenotypic variability in such traits may derive Li, Dangour, and Power 2007), though other ecological in large part from variability in gene frequencies within and stresses such as cold climates may generate similar effects between populations (Hancock et al. 2010). Although often (Katzmarzyk and Leonard 1998). assumed to require hundreds of generations, genetic change This overall approach is thus proving very valuable for can occur rapidly during periods of rapid population growth, understanding both when and why human traits emerged and and hence it may have been particularly important since the also how they have come to vary across ecological conditions Neolithic revolution (Cochran and Harpending 2009). S468 Current Anthropology Volume 53, Supplement 6, December 2012

Developmental plasticity represents a faster mode of phe- explicitly address the concepts of risk and uncertainty, which notypic change, theoretically capable of fine-tuning pheno- to variable degrees challenge both organisms and financial type to more recent or local conditions (Stearns 1992; West- institutions. Such uncertainty requires “decisions” to be made Eberhard 2003). A key mechanism underlying such plasticity on the basis of imperfect information. For biological organ- is epigenetic variability in gene expression in response to en- isms, such decisions are shaped by the forces of selection into vironmental factors occurring during early development a coherent “adaptive strategy” (Laubichler, Hagen, and Ham- (Youngson and Whitelaw 2008). Such epigenetic marks are merstein 2005). then broadly maintained through the life course, though with Consider an environment that flips irregularly between two progressive attrition over time (Fraga et al. 2005). It is tempt- states of contrasting quality, such that the phenotypic traits ing to assume that developmental plasticity is adaptive; how- that maximize fitness in one environment are very different ever, in long-lived species there may be a systematic shift in to those that maximize fitness in the other. A number of ecological conditions between the life course periods of de- responses are possible, depending on the timescale of change velopment and reproduction, potentially resulting in costly and the availability of cues. maladaptation. If the rate of flipping is low, each generation of organisms Many ecological stresses are not systematic, however, and can search for cues of environmental quality and use these occur irregularly through the life course while still exerting to guide ontogenetic development. Here, risk is addressed by powerful effects on biology. Potts (2012) has argued that stud- acquiring up-to-date information. Such developmental plas- ies using single markers of past ecological change have tended ticity is certainly important in promoting phenotypic vari- to bias interpretation toward particular climatic trends (e.g., ability, some of it potentially adaptive, among contemporary temperature or aridity) and that a more integrative approach human populations, such as brain sparing in response to fetal emphasizes temporal fluctuations in the overall level of eco- undernutrition (Hales and Barker 1992). An enhanced level logical variability and hence shifts attention from “ecological of such plasticity may plausibly have emerged during recent stress” to “ecological uncertainty.” hominin evolution. This hypothesis remains untested, how- As the frequency of stochasticity accelerates relative to the ever, because of inadequate information on plasticity in non- duration of the life course and hence the level of uncertainty human apes. increases, systematic adaptations of the kind described above If the rate of environmental flipping is high, another po- are neither especially valuable nor indeed easy to develop. At tential response of the organism is “stochastic phenotype the simplest level, the environment may “flip” between two switching” across generations, more commonly known as “bet extremes, generating a dilemma for the organism: adapt to hedging” (Beaumont et al. 2009; Philippi and Seger 1989). one, the other, or neither, in which case it will be maladapted Here, no information is sought; rather, environmental ran- in both situations. In unstable environments, therefore, “com- domness is addressed directly by phenotypic randomness. Bet mitment” to any simple adaptive strategy is problematic, and hedging may be further subdivided into a conservative strat- a more sophisticated strategy is required. egy (avoiding phenotypic extremes and opting for an inter- Already in early hominin evolution, australopithecines were mediate phenotype) versus a diversified strategy (producing able to tolerate substantial environmental variability between multiple phenotypes; Philippi and Seger 1989). In each case, 3.4 and 2.9 mya, during which temperature and rainfall fluc- the variance in parental fitness is decreased by increasing the tuated, and they appear to have done so without favoring one likelihood that at least a subset of offspring will prove adapted ecosystem over another (Bonnefille et al. 2004). The greater geographical range of early Homo suggests even greater ca- to whatever environment is encountered. Consistent with pacity to tolerate diverse environments. What kinds of adap- such theory, recent experiments in bacteria have demon- tive strategy could have enabled such versatility? strated the emergence of bet-hedging phenotypes in popu- lations exposed repeatedly to contrasting conditions (Beau- mont et al. 2009). Evolutionary Economics The success of developmental plasticity and bet hedging is To investigate the challenge of ecological uncertainty, it is influenced by the rate of generation time relative to the rate useful to draw on concepts from the discipline of economics. of environmental flipping. In any ape or hominin past or Economic ideas have long been widely used in biology, given present, requiring at least a decade to grow to reproductive implicit or explicit recognition of common ground between maturity, neither developmental plasticity nor bet hedging are “rational decision making” and the process of natural selec- satisfactory solutions to high levels of ecological stochasticity. tion (Vermeij 2004). Classic work addressed parental invest- Information accessed in early life loses value because it cannot ment (Trivers 1972), evolutionary game theory (Maynard refer to the multiple ecological states that may occur in suc- Smith 1982), and optimal foraging theory (MacArthur and cession, while each of the bet-hedged variants may be selected Pianka 1966), but a “second wave” of evolutionary economics out when in the “wrong” environment. This is not to suggest is now seeing a range of new ideas tested on biological phe- that bet hedging and developmental plasticity do not con- nomena (Hammerstein and Hagen 2005). Many of these ideas tribute to overall adaptive strategy in humans but simply that Wells The Capital Economy in Hominin Evolution S469 they do not comprise an adequate response to increasing negate such negative correlations on an immediate basis, ecological stochasticity. breaking down the simple association between phenotype and An additional strategy is therefore required by organisms selection. By introducing a time lag between energy income with lengthy developmental periods if they are to tolerate en- and energy utilization, life history decisions may be detached vironments with high levels of stochasticity. A key feature of from the immediacy of ecological stochasticity. It is the buf- this alternative strategy is reversibility; in other words, a re- fering of life history “investment decisions” from selective duction in life course “commitment” to any specific phenotypic pressures that is key to the value of energy capital. While state (Wells and Stock 2012). Phenotypic flexibility meets this developmental plasticity primarily affects the rates of growth requirement by increasing the breadth of environmental tol- and maturation, phenotypic flexibility is of particular im- erance, that is, the range of viable ecological conditions (Gabriel portance for maintaining flexibility in the trade-off between et al. 2005). In the following section, I discuss the generic role current and future reproduction in adult life. of “capital,” another concept derived from evolutionary eco- At the level of the cell, energy needs are relatively constant nomics, in conferring such phenotypic flexibility. although still subject to influences such as physical activity and infection. Cellular needs are maintained by regulatory The Evolutionary Economics of Capital processes that can balance shortfalls against reserves and hence maintain function even as the environment varies. Clas- In seminal work, Kaplan and colleagues (Kaplan, Lancaster, sically, for example, ecologists distinguish between “income and Robson 2003; Kaplan et al. 2000) proposed that devel- breeders,” which capture the energy needed for reproductive opment be considered as “a process in which individuals and effort from the environment on a daily basis, and “capital their parents invest in a stock of embodied capital” (Kaplan breeders,” which accumulate energy stores before breeding et al. 2000:164). They (Kaplan et al. 2000:164) proposed that (Jo¨nsson 1997; Stearns 1992). The key difference is that capital “in a physical sense, embodied capital is organized somatic breeders can breed in a range of ecological circumstances tissue. In a functional sense, embodied capital includes because they are buffered from uncertainty in energy avail- strength, immune function, coordination, skill, knowledge, ability (Pond 1984; Stearns 1992). Most attention has focused and social networks, all of which affect the profitability of on adiposity as the primary source of capital for funding allocating time and other resources to alternative activities reproduction, but using the concept of the extended phe- such as resource acquisition, defense from predators and par- notype (Dawkins 1982), social networks likewise provide en- asites, mating competition, parenting and social dominance.” ergy capital, as in the case of cooperative breeding (Hrdy This broad approach is instrumental in integrating a variety 2009). of raw inputs and phenotypic outputs relevant to life history Storing energy physically in the body and behaviorally in variability. I propose to build on this approach here by em- the social group represents complementary strategies with dif- phasizing two components of embodied capital representing ferent implications for addressing uncertainty. Social capital energy stores. Previously, I differentiated “illiquid” and “liq- stored in networks allows energy to be differentially distrib- uid” capital specifically to distinguish between components uted across a group of individuals. At any given time, a single of embodied capital that represent commitment to a given individual may fail to achieve daily energy balance without phenotype and those that offer reversibility (Wells 2010b). experiencing penalties because of the role of others in sub- Energy represents liquid capital that may be gained and lost sidizing total energy requirements. For periods of high energy from two primary stores, social capital and adipose tissue. demand such as reproduction, this social distribution of en- Each of these stores allows the conversion of diverse raw ergy supply reduces the need of any individual to capture substrates (e.g., discrete food parcels, behavioral interactions) directly from the environment or to store within the body into generalized energy currencies. While Kaplan and col- the total energy required. However, such social stores also leagues (Kaplan, Lancaster, and Robson 2003; Kaplan et al. make possible social competition over access to energy. An 2000) discussed social networks as an example of embodied assumed relationship of reciprocity might fail to materialize capital, they paid minimal attention to adipose tissue as a when most needed. Equally, an adverse ecological event might functional tissue in the same context. substantially reduce the energy content of an entire social The capacity to store energy buffers strongly against fluc- network, placing all individuals at risk. Obligations or prom- tuations in energy supply and demand (Pond 1998). Classi- ises of producing energy might therefore become relatively cally, life history strategy is assumed to comprise a series of worthless in a low-productivity environment. trade-offs, most importantly between the functions of main- Adipose tissue offers greater individual control of energy tenance, growth, reproduction, and immune function, but by maintaining it in physical form but at the cost of having also between current and future reproduction (Hill 1993; Zera to transport it as additional body weight. This could increase and Harshman 2001). The traditional model of resource al- the risk of predation as demonstrated empirically in some location assumes that investment in one function is at the species and hypothesized for hominins (Speakman 2007). cost of investment in another because of limited overall re- Lipid stores allow some functions, or tissues, to fail to achieve sources (van Noordwijk and de Jong 1986). Energy stores can daily energy balance, their requirements being met instead S470 Current Anthropology Volume 53, Supplement 6, December 2012 through lipolysis in adipose tissue (Pond 1998). Somatic en- panzees have also been subject to more positive selection than ergy stores are essentially ring-fenced for individual use, humans (Bakewell, Shi, and Zhang 2007). While there is in- though that does not preclude targeting them at particular creasing evidence for multiple recent species of Homo (Homo social relationships, for example, investing in offspring. In- neanderthalensis, Homo floriensis; Brown et al. 2004) and a creasing internal energy storage is favored when the energy new type recently reported from Siberia (Krause et al. 2010; needs of a social group are heterogeneous, so that the value Reich et al. 2010), only one species exists in the contemporary of energy likewise differs between individuals. world. Although a reduced level of genetic variation is pre- Generically, organisms occupying more stochastic environ- dicted in modern humans given our relatively recent speci- ments are predicted to benefit from such energy capital, lead- ation (Cann, Stoneking, and Wilson 1987) and potentially ing to species differences in traits such as adiposity and so- due to culturally mediated migration patterns (Premo and ciality (Pond 1998). On the one hand, energy capital is a Hublin 2009), a proportion of the genetic variability of other highly effective form of phenotypic flexibility, allowing capital Homo species is also assumed to have passed into our own to be stored or invested in good conditions and used to buffer species (Garrigan and Hammer 2006; Green et al. 2010; Reich poor conditions. This reversibility reduces the need for ex- et al. 2010). pensive permanent traits that are only suited to particular Regardless of the timescale and mode through which ge- ecological conditions. On the other hand, the magnitude of netic variability might have accumulated, what is arguably capital in any given individual may guide life history strategy, most notable in humans is our relatively low level of genetic as demonstrated in other species (e.g., Liao et al. 2011; Zera differentiation in proportion to the extraordinary diversity of and Zhao 2003). Energy capital may, for example, affect de- habitats we now occupy. This contrasts markedly with much velopmental plasticity but may further enable energy parti- greater genetic differentiation in apes despite their inhabiting tioning between different life history functions during adult- relatively homogeneous environments (Gagneux et al. 1999). hood, such as meeting the costs of immune function during The relative genetic unity in Homo sapiens implies continued infection and funding reproduction when infection is absent interbreeding between regional populations even as they oc- (Wells 2010a). As with other traits reviewed in the introduc- cupied diverse habitats and ecological niches. Indeed, some tion, we can therefore consider how capital stores vary within studies also suggest a degree of recent interbreeding with other and between contemporary populations and attempt to re- contemporaneous Homo species (Green et al. 2010; Reich et construct the evolutionary history of capital stores in past al. 2010; though see Eriksson and Manica 2012). populations. It is clear that some adaptive strategies have become in- corporated into the human genome, such as the elongation Variability in “Commitment” across Species of growth and its division into several distinct developmental periods (Bogin and Smith 1996), that therefore represent The concepts of phenotypic reversibility versus irreversibility commitment to a generic human niche. Beyond this com- match closely with the more established terminology of plas- mitment, the within-population genetic variability that is evi- ticity and canalization. These latter traits are integrally related dent in any human life history trait (e.g., stature, birth weight, (Flatt 2005) precisely because the plasticity of some traits in age at menarche, longevity; see Wells and Stock 2011) may the face of ecological stresses underlies the relatively invariant be considered to represent diversified bet hedging—that is, phenotype of others. In mammals, for example, growth of the maintenance of phenotypic diversity among offspring to the brain is relatively protected from environmental stresses, increase parental fitness (Ellis et al. 2009; Wells 2009)—while and other traits are more plastic in response to nutritional or each of these life history traits also shows substantial plasticity climatic stress (e.g., Barbiro-Michaely et al. 2007). Organisms (Wells and Stock 2011). However, my argument here is that are therefore more committed to brain growth than they are the limited genetic commitment of humans is complemented to other components of growth. Beyond such within-organ- not only by developmental plasticity but also by extensive use ism contrasts, species also vary among themselves in the ex- of energy stores that may be allocated flexibly between com- tent of genetic specialization versus phenotypic plasticity, that peting phenotypic traits and between individuals and hence is, in their commitment to specific niches. alleviate ecological stochasticity. The next section considers The lack of commitment in the human genome is already the contribution of energy capital to phenotypic flexibility in evident from comparisons with the genomes of other apes. nonhuman primates. Although subject to continued gene flow between popula- tions, chimpanzees, gorillas, and orangutans have been con- Capital and Flexibility in Nonhuman Primates sidered to comprise two different species or subspecies despite occupying relatively small geographic ranges compared with Primates have high levels of sociality, and their tendency to humans (Becquet and Przeworski 2007; Hey 2010; Warren et solve ecological problems in social ways is well established al. 2001), and furthermore, the degree of genetic variability (Hrdy 2009; Lee 1999; Sussman, Garber, and Cheverud 2005). in each such species is greater than in the entire human ge- A review of primate activity budgets suggested the proportion nome (Gagneux et al. 1999; Kaessmann et al. 2001). Chim- of time directed to sociality ranged from 1% to 8% in pro- Wells The Capital Economy in Hominin Evolution S471 simians, from1% to 22% in New World monkeys, from 1% food stores are known in some bird and mammal species, to 28% in Old World monkeys, and from 2% to 25% in apes while adiposity is a widespread somatic adaptation to eco- (Sussman, Garber, and Cheverud 2005). Importantly, the ma- logical uncertainty (Pond 1984, 1998). jority of such social behavior was cooperative and affiliative In primates, the use of adipose tissue to resolve seasonal rather than antagonistic. fluctuations in energy availability was elegantly demonstrated Individuals may invest in social relationships and accu- in a study of orangutans where urinary ketones indicated the mulate social capital that may be converted back into bene- metabolism of fat during periods of negative energy balance ficial physical resources (Isler and van Schaik 2009). For ex- (Knott 1998). The highest levels of ketones were observed in ample, female chacma baboons who formed stronger and pregnant or lactating females, highlighting the value of adi- more stable social bonds with other female baboons had pose tissue in buffering reproduction from ecological sto- greater longevity (Silk et al. 2010) and also produced offspring chasticity. Greater adiposity or leptin levels have been reported who themselves had greater longevity through increasing the in females compared with males in baboons (Rutenberg et rates of offspring survival (Silk et al. 2009). Similarly, social al. 1987), macaques (Schwartz and Kemnitz 1992), chimpan- relationships may benefit male fitness, as demonstrated in zees (Bribiescas and Anestis 2010), and orangutans (Morbeck Assamese macaques, where strong bonds between males were and Zihlman 1988), but information on adiposity and its linked to the formation of coalitions, dominance rank, and regulatory effects remains surprisingly scarce in the primate the number of offspring sired (Schulke et al. 2010). literature considering how important the trait appears in Such social investments make their maximal contribution hominin evolution (Wells 2010a). Intriguingly, the males of to flexibility when they enable cooperative breeding, a be- some marmoset and tamarin species have been shown to gain havior evident in some primate species as well as other mam- weight during their mate’s pregnancy, a strategy suggested as mals and birds (Isler and van Schaik 2009) and involving a adaptive given their key alloparental role after delivery when continuum of behavior ranging from carrying or protecting they may carry offspring equivalent to 20% of their own body offspring to “babysitting,” provisioning, or suckling them weight (Ziegler et al. 2006). (Hrdy 2004, 2009). Here, social capital contributes directly to Importantly, a rapidly growing literature has demonstrated the capacity of reproducing females to meet the total energy that adipose tissue is not only a fuel store but also the source demands of their offspring. In Hanuman langurs, infants were of numerous signaling molecules that coordinate energy observed to be carried by females other than the mother for trade-offs between competing biological functions such as up to half of daylight hours, which has sufficient effect on growth, immune function, and reproduction (Wells 2010a). the maternal energy budget to reduce the time to the next The role of adipose tissue in such functions has been dem- conception (Hrdy 2004). Among marmosets and tamarins, onstrated in a variety of species (Bartness, Demas, and Song males may carry offspring for the majority of the time and 2002; Demas 2004; Pond 1998). Among the hormones se- also supplement maternal milk in the offspring diet with creted by adipose tissue is leptin, signaling the availability of small-prey items (Garber 1997). Collectively, maternal fitness energy to the brain, and studies in a variety of species have in these species is positively correlated with the number of shown that it helps regulate the allocation of energy between male helpers, and in cotton-top tamarins, such help appears competing functions (Demas and Sakaria 2005; Drazen, De- obligatory, with mothers lacking assistance tending to aban- mas, and Nelson 2001; Schneider 2004). Adipose tissue also don their young (Hrdy 2004). Such cooperative behavior not provides both the energy and the molecular precursors for only increases the flexibility in provisioning offspring but also immune function, and it does so in tissue-specific fashion, permits flexibility in mating arrangements (Hrdy 2004). indicating differential preparation of specific tissues for dif- Such social interactions reduce the strength with which ferent types of pathogen (Pond 2003). The emergence of ad- energy turnover is a function of a single organism’s body size ipose tissue has been proposed to have aided control over the and instead increase the strength with which it reflects social dynamics of energy supply and demand between tissues, for relationships (Kramer and Ellison 2010; Reiches et al. 2009). example, to allow high energy processes such as lactation to Recent exploration of such communal energy budgets has occur during periods of minimal energy intake in primitive emphasized “activity subsidies” (e.g., babysitting) as well as mammals (Pond 1984). redistributions of food and multiple and changing contri- These data from primates and other mammals illustrate butions from ascendant and descendant kin across the life for both sexes how accumulating energy capital can confer course (Kramer and Ellison 2010; Reiches et al. 2009). By diverse fitness benefits while increasing resilience to ecological enabling energy dynamics to be temporarily invested extra- factors operating at the level of the individual. However, how corporeally, social relationships promote maximal flexibility these strategic decisions are enacted at the molecular level in in reproductive energetics. diverse species remains to be established in detail. Impor- Such energy transfers need not necessarily be maintained tantly, the use of energy capital by marmosets and tamarins in social relationships and may instead be converted to phys- affects not only immediate reproduction but also demogra- ical capital, either extracorporeal, in the form of food hoards, phy. These primates have a powerful ability to increase pop- or physiological, in the form of adipose tissue. Extracorporeal ulation size and colonize new niches (Hrdy 2009), indicating S472 Current Anthropology Volume 53, Supplement 6, December 2012 that the adaptive strategy of phenotypic flexibility that can Through adulthood, gender differences in fat distribution buffer individuals from energy stress in harsh conditions can slowly decrease, so that by old age the genders converge in furthermore drive population growth beyond that feasible in body shape, and central adiposity in both sexes is increased individual income breeders in good conditions. relative to peripheral adiposity (Wells, Cole, and Treleaven 2008). Both sexes lose lean mass such that in later life the Capital Investment and Humans body becomes more “economical” (Zafon 2007). These shifts in fat distribution have been interpreted as life history strategy Recent work has highlighted a variety of ways in which the in which increased prioritization of central adiposity with storage, mobilization, and transfer of capital within and be- increasing age promotes immune function at the expense of tween individuals confer significant flexibility in contempo- reproduction (Wells, Griffin, and Treleaven 2010). rary humans. Adipose tissue can supply energy for growth, The ratio of fat to lean tissue therefore emerges as a key reproduction, and immune function, and a number of hor- adaptive strategy in which growth can be tailored to ecological mones have been shown to contribute to this strategic par- conditions under the transducing effect of maternal pheno- titioning of energy. Paradoxically, the evidence that leptin type. The magnitude of lean mass has long-term implications levels correlate with energy stores in humans and hence or- for energy requirements, while the magnitude of adiposity chestrate such trade-offs is currently inconsistent and better can respond by providing appropriate “risk management” supported in females than in males (Bribiescas 2001; Kuzawa, (Wells 2012c). For example, the low birth weight characteristic Quinn, and Adair 2007; Sharrock et al. 2008). It is likely that of contemporary Indian populations, poorly nourished for leptin makes up only one of a range of molecular signals many generations, incorporates a low level of investment in involved in the regulation of biological functions (Schneider lean mass balanced by an increased investment in adiposity 2004); for example, insulin is increasingly recognized to play (Yajnik et al. 2003). Collectively, these traits represent an eco- a key role in coordinating life history trade-offs (Harshman nomical and resilient phenotype capable of tolerating high and Zera 2007; Watve and Yajnik 2007). uncertainty in infant energy supply. The life course trajectory of human body composition in- More broadly, many environmental factors generate vari- dicates the changing value of fat during development, breed- ability in the fat-lean ratio, indicating that the strategy for ing, and aging. High neonatal adiposity of humans compared accumulating and using energy capital is sensitive to multiple with other mammals has been hypothesized to buffer the life course and ecological signals, including physical (e.g., cli- obligatory energy demands of the large Homo brain (Kuzawa mate), ecological (e.g., diet, disease), social (e.g., maternal 1998). However, this need not represent the only or even the rank), and demographic (e.g., parity, interbirth interval) fac- primary function of such adiposity. Unpublished data from tors (Wells 2011, 2012b). The magnitude of sexual dimor- Ethiopia (n p 255 ) show that over the first 6 months, infants phism in adiposity has likewise further been shown to vary first increase disproportionately in adiposity and then accrete in relation to ecological factors (Wells 2012d). Capital ac- disproportionately lean mass (Andersen, Friis, and Wells, un- quisition also reflects a multitude of dynamic social inter- published data). The magnitude of infant energy stores may actions in which energy is passed to and from individuals therefore guide the early accretion of lean tissue, which has through a complex set of relationships. One might consider less capacity to oscillate in response to energy fluctuations. the high adiposity of infants as a temporary accumulation of Adipose tissue may be important in supporting, regulating, capital favored by the sum total of maternal and alloparental and protecting each of somatic growth, immune function, provisioning during pregnancy, a source of income less guar- and brain development during infancy when mortality risk is anteed as the offspring matures. Thus, energy capital may be highest (Kelly 1995) while furthermore accommodating the rapidly moved between individuals not only to boost the initiation of sex differences in life history strategy. Because stores of some individuals but also as “loans” physically pro- early energy supply derives primarily from the maternal bud- tected from those with competing interests. get, such regulatory effects of adipose tissue are ultimately a Research on diverse human populations has demonstrated transgenerational maternal effect (Ong et al. 2007; Wells an extraordinary degree of variability in the nature and structure 2010b), as discussed below. of relationships that underlie the distribution of energy capital During development, the two sexes show contrasting so- (Kaplan, Lancaster, and Robson 2003; Sear and Mace 2008). matic capital accumulation, with adult males achieving greater In 10 foraging societies, on average men acquired ∼68% of the height and relative lean mass and less fat mass than females calories and ∼88% of the protein and hence were by far the (Wells 2007b). These differences in adiposity are particularly dominant supplier of calories to weaned offspring as well as evident for fat distribution, with the enhanced peripheral fat protein and fat to women, though there was also variability of females both signaling reproductive capacity and meeting between populations in these contributions (Kaplan et al. 2000). the energy costs of lactation (Wells 2010a). Humans are capital This highlights the sexual division of labor as another key com- breeders and hence can breed across a range of ecological ponent of human flexibility in capital acquisition. Hrdy (2009) conditions and seasons, though in good conditions they use argued that while male provisioning is critical for cooperative daily “energy income” rather than drawing on energy stores. breeding, the specific contribution of the father cannot be guar- Wells The Capital Economy in Hominin Evolution S473 anteed, resulting in a range of strategies for mothers to acquire “additional fathers” and hence bet-hedge across multiple male providers. Similarly, in relation to females, maternal grand- mothers have been shown in several societies to be important alloparental provisioners of grandoffspring and hence to pro- mote their survival (Hawkes, O’Connell, and Blurton Jones 1989; Sear and Mace 2008). Cooperative breeding and pooled energy budgets therefore offer unprecedented flexibility in humans as they impose min- imal constraints on the social relationships generating energy supply at the individual level (Hrdy 2009; Reiches et al. 2009). More broadly, social capital may be distributed across multiple social relationships, which may be accumulated through the life course. No single social relationship may prove a reliable source of support in every circumstance; hence, bet hedging across multiple relationships may again prove the optimal strategy. Because a group of humans must inevitably compete Figure 1. Alternative and complementary strategies for accom- for the sum total of available energy in the local environment, modating ecological stochasticity. The brain integrates social and networks of social support can never be entirely benign but behavioral information, influencing physiological regulatory sys- must rather contain a variety of different relationships, some tems. Adipose tissue integrates ecological information and influ- based on kinship and others on political alliances. For ex- ences on neuroendocrine regulatory systems. Both of these organs ample, studies of the !Kung bushmen of southern Africa show provide “risk management” of life history strategy in the face of that relationships of reciprocity are key to the management ecological stochasticity. of nutritional risk (Howell 2010), a scenario also observed in many other nonindustrialized societies (Couper-Johnston Zukowska 2012; Soares et al. 2010). Each of these hormones 2000). Such social capital distributes risk across rather than in turn affects adiposity and metabolic traits such as appetite within individual bodies and hence buffers uncertainty in (Hirsch and Zukowska 2012; Maejima et al. 2011). Thus, the individual foraging returns. brain contributes to the regulation of life history strategy and The combination of variable dynamics of cooperative does so in response to social and ecological stresses. breeding and life course flexibility in adipose tissue stores With respect to adipose tissue, hormones such as leptin means that humans are uniquely undercommitted to any spe- and insulin signal the level and consistency of lipid stores to cific niche, which helps us to understand our unusual capacity the brain (Benoit et al. 2004) and in doing so affect many to colonize. Such undercommitment is backed up by other life history functions, including reproductive behavior (Cun- generalized subsistence strategies such as meat eating and ningham, Clifton, and Steiner 1999; Watve and Yajnik 2007). cooking (Foley 2001; Sullivan, Hagen, and Hammerstein Preliminary evidence from rodents suggests that levels of ad- 2008), each of which reduces the need to adapt physiologically iposity may influence oxytocin (Flak et al. 2011) and hence to specific diets. Social capital likewise underpins a wide va- potentially social behavior. Thus, while further research is riety of human relationships, including coalitions and alli- required, it is already apparent that adipose tissue likewise ances and other forms of cooperative behavior. contributes to the regulation of life history strategy and again In the context of ecological uncertainty, one could argue does so in response to diverse ecological stresses. that energy capital is not “for” anything in particular. Its Clearly these two risk-management systems differ in their purpose might be seen instead as a way of avoiding com- receptivity to specific signals, their timescale of response, their mitting energy to any specific function at any specific time, degree of flexibility, and their functional targets. Together, instead providing sophisticated “risk management” of life his- however, they represent an important link between the level tory strategy by integrating a cumulative array of individual of capital and life history strategy and thereby highlight the signals from the physical and social environment. The brain importance of capital from an evolutionary perspective. and adipose tissues both play a part in such integrative reg- ulation and hence emerge as important “control centers” for Capital in Hominins life history strategy (Wells 2010a, 2012c). Intriguingly, each of these organs acts strongly on the other (fig. 1). Reconstructing energy capital dynamics in hominins is at With respect to the brain, recent research on the neuroen- present difficult because of the potential transiency of energy docrine basis of social behavior has demonstrated the effects capital per se and the lack of clear markers in the fossil record. of a range of hormones; for example, oxytocin plays a key Phenotypic flexibility to some extent must remain hidden role in cooperative behavior, while neuropeptide Y plays an from preservation. equally fundamental role in the stress response (Hirsch and Intriguingly, however, both adipose tissue and bone are S474 Current Anthropology Volume 53, Supplement 6, December 2012 increasingly being reinterpreted as dynamic rather than inert tissues, and growing awareness of endocrine links between these tissues may aid novel interpretation of the fossil record in due course. For example, bone is now known to contribute to the regulation of energy metabolism (Fernandez-Real and Ricart 2011), while leptin mediates skeletal turnover (Ducy et al. 2000). Osteocalcin, which can be recovered from some fossilized material (Nielsen-Marsh et al. 2002), shows an in- verse correlation with adiposity in living humans (Fernandez- Real and Ricart 2011). Further work in this area may generate more robust findings. Given that both adiposity and social capital vary substantially within and between contemporary human populations, we can assume that they represented Figure 2. Positive feedback cycle in which the capacity to tolerate stochastic environments promotes the capacity to colonize new dynamic adaptive strategies in Homo evolution, but the details environments. Both social and physical forms of energy capital remain to be established (see Wells 2010a for a preliminary may have provided the necessary phenotypic flexibility. estimation of adiposity in prehuman hominins). Both adiposity and social capital enable variation in the Capital and Transgenerational Effects mode and breadth of environmental tolerance; that is, they can vary in relation to average environmental conditions (e.g., As discussed above, capital reduces exposure to ecological hot vs. cold climates) but also provide phenotypic flexibility stresses and hence to selection, which aids in understanding to buffer variability in any given environment. Recently, Na- our species’ limited local genetic commitment. However, the varrete, van Schaik, and Isler (2011) reported an inverse cor- implications of energy capital in Homo go much further be- relation across ∼100 mammal species between brain and ad- cause of the particular sensitivity of developmental trajectory ipose tissue masses. These authors suggested that storing in- to environmental factors operating in early life. formation in the brain or energy in the body represent two As in most mammals, hominin fetuses must initially ex- alternative strategies for accommodating uncertainty in en- perience ecological pressures under the transducing effect of ergy availability. The fact that our own species is a positive maternal phenotype (Wells 2003, 2007c). Most perspectives outlier for both traits offers a powerful indication that eco- on developmental plasticity emphasize how developing off- logical stochasticity has been a key stress in the evolution of spring adapt to the ecological environment (e.g., Bateson the genus Homo. 2001; Kuzawa 2005). Some argue that offspring use environ- In turn, the phenotypic flexibility that emerged under such mental cues adaptively by anticipating the future environment selective pressures appears to have conferred on Homo an in which breeding will occur (Gluckman and Hanson 2004; extraordinary capacity to colonize new niches (Wells and Gluckman, Hanson, and Beedle 2007). This model fits poorly Stock 2007). The energy capital that provides resilience against with the observation that human mothers substantially buffer tough conditions also favors successful probing of novel such cues through both physiological and social mechanisms niches and demographic expansion as demonstrated by rapid (Wells 2003), and the anticipatory model has been criticized recovery from population crashes (Hill and Hurtado 1996). by several authors (Bogin, Varela Silva, and Rios 2007; Rickard Through positive feedback loops, colonizing, with its popu- and Lummaa 2007; Wells 2007a, 2011, 2012a). lation booms and busts, can become its own selective pressure, I have argued that given ecological stochasticity, offspring as shown in figure 2. Thus, withstanding “ecological feast and should respond not to short-term external cues but to ma- famine” may have made possible “reproductive feast and fam- ternal phenotype, which represents the cumulative effect of ine.” “an extensive period of time, with short-term fluctuations Cooperative breeding is also notable in many social car- smoothed out to provide a more reliable rating of environ- nivores (Smith et al. 2012), which likewise benefit from a mental quality” (Wells 2003:152). This smoothing effect was social means of buffering individuals’ risk of failure in cap- subsequently labeled “intergenerational inertia” by Kuzawa turing prey. According to this perspective, the emergence of (2005), but Kuzawa’s approach, like that of Gluckman and energy capital as an adaptive response to ecological uncer- Hanson, does not address the dynamics deriving from parent- tainty in early Homo may have opened up carnivory as a new offspring conflicts of interest (Haig 1993, 1997; Trivers 1974), subsistence niche, making use of two types of bet hedging: which these authors reject (Gluckman et al. 2009). across individuals (e.g., buffering variance in productivity be- Clearly the offspring requires information in order to select tween individual hunters or gatherers) and across the genders a developmental trajectory, but in the absence of direct cues (diversifying the resources harvested by the whole group). from the external environment, the offspring must use those Similarly, cooperative breeding may have made possible the deriving from maternal phenotype. In accepting such cues, funding of larger brains (Hrdy 2009; Isler and van Schaik however, the offspring must also submit to maternal strategy 2012). (Wells 2003, 2010a), and this strategy is particularly important Wells The Capital Economy in Hominin Evolution S475 in human life history because it initially falls to the mother Acknowledgments to meet the high costs of offspring brain growth (Aiello and I very much appreciate the invitation from Susan Anto´n and Key 2002; Martin 1983, 1989) and to allocate resources be- Leslie Aiello to participate in this workshop and their critical tween several competing offspring during much of the re- comments on the manuscript as well as the comprehensive productive career (Wells 2003). Closure of the critical window discussions with the other participants. of physiological sensitivity in early infancy, despite the ex- tended period of growth, results in the canalization of off- spring growth trajectory in the second year of life (Smith et References Cited al. 1976) and allows the mother to “fix” her own investment Aiello, Leslie C., and Cathy Key. 2002. Energetic consequences of being a strategy in each offspring at the time of weaning (Wells 2003). Homo erectus female. American Journal of Human Biology 14:551–565. The cues received by developing offspring before weaning Anto´n, Susan C. 2003. Natural history of Homo erectus. Yearbook of Physical therefore refer not to ecological conditions per se but to the Anthropology 37:126–170. Anto´n, Susan C., Hannah Carter-Menn, and Valerie B. DeLeon. 2011. 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Pregnancy weight gain: marmoset and tam- A. Swan, Linda Vigilant, and Jonathan L. Heeney. 2001. Speciation and arin dads show it too. Biology Letters 2:181–183. Current Anthropology Volume 53, Supplement 6, December 2012 S479

Origins and Evolution of Genus Homo New Perspectives

by Susan C. Anto´n and J. Josh Snodgrass

Recent fossil and archaeological finds have complicated our interpretation of the origin and early evolution of genus Homo. Using an integrated data set from the fossil record and contemporary human and nonhuman primate biology, we provide a fresh perspective on three important shifts in human evolutionary history: (1) the emergence of Homo, (2) the transition between non-erectus early Homo and Homo erectus, and (3) the appearance of regional variation in H. erectus. The shift from Australopithecus to Homo was marked by body and brain size increases, a dietary shift, and an increase in total daily energy expenditure. These shifts became more pronounced in H. erectus, but the transformation was not as radical as previously envisioned. Many aspects of the human life history package, including reduced dimorphism, likely occured later in evolution. The extant data suggest that the origin and evolution of Homo was characterized by a positive feedback loop that drove life history evolution. Critical to this process were probably cooperative breeding and changes in diet, body composition, and extrinsic mortality risk. Multisystem evaluations of the behavior, physiology, and anatomy of extant groups explicitly designed to be closely proxied in the fossil record provide explicit hypotheses to be tested on future fossil finds.

Recent fossil and archaeological finds have complicated our They also raise questions about when a modern pattern of interpretation of the origin and early evolution of genus life history might have emerged and what role, if any, it played Homo. It now appears overly simplistic to view the origin of in our early evolution. Homo erectus as a punctuated event characterized by a radical Modern humans have diverged in numerous ways from the shift in biology and behavior (Aiello and Anto´n 2012; Anto´n life history patterns seen in other primates, and this “human 2012; Holliday 2012; Pontzer 2012; Schwartz 2012; Ungar package” seems linked to our ability to support larger brains 2012). Several of the key morphological, behavioral, and life and to disperse widely. Our unique suite of life history traits history characteristics thought to first emerge with H. erectus includes altricial birth, a large energy-expensive brain, long (e.g., narrow bi-iliac breadth, relatively long legs, and a more juvenile dependency with relatively late reproduction, short “modern” pattern of growth) seem instead to have arisen at interbirth intervals (IBIs) with high fertility, and a long post- different times and in different species. Further, accumulating reproductive life span (Bogin 1999; Flinn 2010; Hill and Hur- data from Africa and beyond document regional morpho- tado 1996; Kaplan et al. 2000; Leigh 2001). With this package logical variation in early H. erectus and expand the range of we appear to have been able to circumvent several of the key variation in this species. These new finds also make the dif- constraints that affect other species. Many of the life history ferences between H. erectus (s.l.) and Homo habilis (s.l.) less traits that define modern humans serve to decrease age-spe- stark and suggest that regional variation in the former may cific reproductive value (i.e., the contribution to the growth reflect local adaptive pressures that result from inhabiting of the population) early in life and greatly increase the costs diverse environments in Africa and Eurasia. The mosaic na- of reproduction and somatic maintenance. What is most strik- ture of these acquisitions and the greater range of intraspecific ing about contemporary human biology is that we are able variation, especially in H. erectus, call into question previous to produce numerous high-quality offspring that experience inferences regarding the selective factors behind the early evo- relatively low mortality, grow slowly, and live long lives. In lution of our genus and its eventual dispersal from Africa. essence, we are able to “have our cake and eat it too” by avoiding some of the life history trade-offs seen in other mammals and having a life history pattern that is both “fast” Susan C. Anto´nis Professor, Department of Anthropology, New York and “slow” and that emphasizes quantity and quality (Kuzawa University (25 Waverly Place, New York, New York 10003, U.S.A. [[email protected]]). J. Josh Snodgrass is Associate Professor, and Bragg 2012). Department of Anthropology, University of Oregon (1321 Kincaid This life history shift in humans was almost certainly Street, Eugene, Oregon 97403, U.S.A.). The authors contributed facilitated by substantial behavioral and cultural shifts, in- equally to this work. This paper was submitted 4 V 12, accepted 8 cluding (1) cooperation in foraging (e.g., hunting/division of VII 12, and electronically published 28 XI 12. labor), which maximizes the ability to obtain a stable, high-

᭧ 2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0017$10.00. DOI: 10.1086/667692 S480 Current Anthropology Volume 53, Supplement 6, December 2012 quality diet; and (2) cooperation in reproduction (e.g., allo- H. erectus that reveal great variation in the species, including parenting and midwifery), which allows the compression of small-bodied members from both Africa and Georgia (Ga- the IBI and the consequent stacking of offspring as well as bunia et al. 2000; Potts et al. 2004; Simpson et al. 2008; Spoor the care for and provisioning of the secondarily altricial off- et al. 2007), and suggest a previous overreliance on the Na- spring necessitated by our unique obstetrical dilemma (Tre- riokotome skeleton (KNM-WT-15000) in reconstructions of vathan 1987). Several key questions about these behavioral H. erectus. Additionally, reassessments of the Nariokotome shifts remain unanswered, including when these traits material have concluded that he would have been considerably emerged, whether they evolved together as a package or piece- shorter than previous estimates (∼163 cm [5 feet 4 inches], meal in different hominin species, and the particular selective not 185 cm [6 feet 1 inch]; Graves et al. 2010), younger at pressures that drove their evolution. death (∼8 years old, not 11–13 years old; Dean and Smith To address these distinct data sets, we bring together ideas 2009), and with a life history pattern distinct from modern raised at the Wenner-Gren workshop “Human Biology and humans (Dean and Smith 2009; Dean et al. 2001; Thompson the Origins of Homo” in Sintra, Portugal, 2011. To the papers and Nelson 2011), although we note that there is substantial presented in this special issue we add new data and perspec- variation in the modern human pattern of development (Sˇe- tives, summarize the fossil and archaeological records (tables sˇelj 2011). Further, the recent discovery of a nearly complete 1, 2), and consider what research on contemporary primate adult female H. erectus pelvis from Gona, Ethiopia, which is life history trade-offs, developmental plasticity, and regional broad and has a relatively large birth canal, raises questions adaptive patterns can help us infer about behavioral and cul- about the narrow-hipped, Nariokotome-based pelvic recon- tural changes in early Homo (tables 3–5). These data give us struction and whether H. erectus infants were secondarily al- a fresh perspective on three important shifts in human evo- tricial (Graves et al. 2010; Simpson et al. 2008).2 lutionary history: (1) the emergence of genus Homo, (2) the In addition to recent changes in our understanding of H. transition between non-erectus early Homo and H. erectus, erectus, new discoveries and reanalyses have complicated the and (3) the appearance of regional morphological variation picture of earliest Homo by documenting its diversity and in H. erectus (including Homo ergaster). Using this integrated emphasizing underappreciated differences and similarities data set, we consider the implications for understanding the with H. erectus (Blumenschine et al. 2003; Spoor et al. 2007). changing selective pressures that led to the transition to and Finally, a new view of Australopithecus has begun to emerge evolution of early Homo. in which it shares many postcranial characteristics with Homo, including a somewhat large body and relatively long legs How What We Now Know from the Hard (Haile-Selassie et al. 2010; Holliday 2012; Leakey et al. 2012; Evidence Differs from What We Thought Pontzer 2012). These results suggest a previous overreliance We Knew on the very small “Lucy” (A.L.288-1) skeleton to characterize that species/genus. Over the past several decades, a consensus had emerged that Brains, Bodies, and Sexual Dimorphism the shift to humanlike patterns of body size and shape—and at least some of the behavioral parts of the “human pack- Although recent discoveries reveal a larger Australopithecus afa- age”—occurred with the origin of Homo erectus (e.g., Anto´n rensis and a smaller, more variable H. erectus than previously 2003; Shipman and Walker 1989). This was seen by many known, there still appear to be important differences between researchers as a radical transformation reflecting a sharp and the species. Even when including the largest of the new Aus- fundamental shift in niche occupation, and it emphasized a tralopithecus fossils and the smallest of the new early Homo distinct division between H. erectus on the one hand and non- fossils, estimates suggest an average increase in body mass of erectus early Homo and Australopithecus on the other.1 Earliest 33% from A. afarensis to early Homo (in this case H. habilis ϩ Homo and Australopithecus were reconstructed as essentially Homo rudolfensis ϩ early H. erectus; Holliday 2012; Pontzer bipedal apes, whereas H. erectus had many of the anatomical 2012). The difference is more modest—on the order of 10%— and life history hallmarks seen in modern humans. To some, when comparing A. afarensis to only non-erectus early Homo the gap between these groups suggested that earlier species (table 1). The fossil record also suggests a body mass increase such as Homo habilis should be excluded from Homo (Collard of ∼25% between early non-erectus Homo in East Africa and and Wood 2007; Wood and Collard 1999). early H. erectus (Africa ϩ Georgia). This expanding fossil record Recent fossil discoveries paint a picture that is substantially documents marked regional variation, with early African H. more complicated. These discoveries include new fossils of erectus being ∼17%–24% larger on average than Georgian H.

1. While it is recognized that Australopithecus may be paraphyletic, for the purposes of the comparisons in this paper, the genus is considered 2. We note that there is some disagreement regarding the specific status to exclude Paranthropus species but to include the best-represented spe- of the Gona pelvis, including suggestions that it may not be Homo (Ruff cies commonly assigned to Australopithecus, i.e., A. anamensis, A. afa- 2010). Nonetheless, other reconstructions of the KNM-WT 15000 pelvis rensis, A. garhi, A. africanus, and A. sediba. When the data for specific were narrower than the original, suggesting that its breadth may not be comparisons come from a single species, that species is indicated by name. a strong anchor point for neonate head size. Anto´n and Snodgrass Origins and Evolution of Genus Homo S481 erectus of approximately the same geological age (table 1; Anto´n transitions in early Homo. As has been well documented, pos- 2012). terior teeth decrease in average size and increase in occlusal Recent fossil evidence and reinterpretation of known speci- relief from Australopithecus to Homo (Ungar 2012). The trend mens also documents a more mosaic pattern of evolving limb is somewhat more pronounced in H. erectus, which shows proportions, which has implications for locomotor reconstruc- substantial third molar reduction (Gabunia et al. 2000; In- tions. New work shows that despite absolute size differences and driati and Anto´n 2008; Spoor et al. 2007). There is, however, contrary to conventional wisdom, relative hind-limb length does substantial size overlap in jaw and tooth size among all early not differ from Australopithecus to Homo or among Homo (Hol- Homo (Anto´n 2008). In contrast, preliminary evidence sug- liday 2012; Holliday and Franciscus 2009; Pontzer 2012). The gests that incisor row length may be larger in non-erectus forelimb, however, is relatively stronger and slightly longer in early Homo than in Australopithecus and intermediate in size both Australopithecus and non-erectus early Homo than it is in in H. erectus (Ungar 2012). This may suggest dietary differ- H. erectus (Ruff 2009). Further, the Georgian forelimb is slightly ences relating to incisal preparation. shorter than in early African H. erectus, which may reflect a Dental topography and microwear for all early Homo are temporal, climatic, or even secular shift (Holliday 2012; Pontzer more complex than in Australopithecus. Although early Homo 2012). likely ate a fairly generalized diet, this signal suggests they Cranial capacities show an increase of 130% from A. afa- also consumed less brittle foods (Ungar and Scott 2009; Ungar rensis (mean p 478) to non-erectus early Homo (i.e., 1813 ϩ et al. 2012). Homo erectus shows more variation and more 1470 groups; mean p 629 cm3). This marks the first time that small features than non-erectus early Homo, indicating greater hominin cranial capacity expands beyond the range of variation dietary breadth in the former (Ungar and Sponheimer 2011). seen among great apes (Schoenemann 2006). Also, although The signal is similar across regional samples of H. erectus. the ranges overlap, average cranial capacity increases by ∼25% Thus, dental morphology suggests consumption of a gener- from early non-erectus Homo to early H. erectus in Africa and alized diet in early Homo but with a modestly increased dietary Georgia (combined mean p 810 cm3)orby130% when com- breadth compared with Australopithecus. pared with just early African H. erectus (mean p 863 cm3). Although sample sizes are extremely small, there is some Among regional samples, both early African H. erectus and early evidence that the emergence of the first permanent molar Indonesian H. erectus are ∼25% larger on average than Georgian (M1), a variable that correlates with many life history traits, H. erectus of about the same geological age, a similar difference occurs about a year later in H. erectus than in A. afarensis as for body size (tables 1, 2). (Dean et al. 2001; Schwartz 2012). This finding is consistent Despite the problems of assigning sex to individual fossils, with a recent analysis that documents relatively minor growth preliminary patterns of sexual dimorphism can be considered and life history differences in H. erectus compared with earlier for different species using brain and body size estimates (An- hominins and living African apes (Thompson and Nelson to´n 2012; Plavcan 2012). The ratio of male to female mean 2011). However, the pattern of skeletal and dental develop- values for brain and body size suggests that H. erectus is ment in Nariokotome is not much outside the range of “tall” modestly less dimorphic than is A. afarensis. However, sex is modern human children (Sˇesˇelj 2011), hinting perhaps at the hard to estimate for fossils, and the degree of dimorphism modularity (i.e., independence) of developmental systems. inferred depends on the particular variable considered, the Unfortunately, there are no data for M1 emergence for non- means of comparison, and the specimens included in the erectus early Homo, and we caution that M1 development can sample (table 1; Plavcan 2012). For example, A. afarensis and be decoupled from somatic growth rates (Dirks and Bowman early H. erectus show no difference in size variation (CVs) for 2007; Godfrey et al. 2003). Thus, life history reconstructions body mass or endocranial capacity (table 1; and see table 3 suggest a pattern of growth modestly different from Australo- in Anto´n 2012). By other measures, H. habilis (exclusive of pithecus yet distinct from later Homo species such as Nean- 1470) is more dimorphic in body mass estimates than Aus- derthals and modern humans. tralopithecus but less dimorphic in brain size (table 1; Plavcan 2012). And H. erectus is more dimorphic than H. habilis in Climate and Environment brain size but less dimorphic in body size. Unfortunately, H. habilis values are particularly suspect given the small samples Although populations of early Homo likely lived in a variety and uncertainty regarding numbers of included species. These of specific environments, Potts (2012) reviews how multiple data are equivocal as to the degree of dimorphism present independent paleoclimatic records show an increase in the but do not provide strong support for decreasing dimorphism amplitude of the climate shifts and an increasing unpredict- in H. erectus (see Plavcan 2012). ability in their timing during the origin and early evolution of Homo. He suggests that this inherent variation in climate placed a premium on developmental plasticity—the capacity Teeth, Development, and Diet for developing individuals to respond phenotypically to en- Examination of dental evidence such as tooth size, microwear, vironmental conditions (Lasker 1969; Wells 2012)—and likely and developmental pattern can provide a window onto key behavioral plasticity as well. The result of developmental plas- 13 / 31.9) 55.8/ 924; 50/51; & p ( ( ( H. erectus 56.7; c ( 33) 590) & Homo habilis & vs. 46; 625; ( ( more dimorphic: 1.2 ( Homo rudolfensis H. erectus less dimorphic: 1.06/1.0 ( more dimorphic: 17.8/15.9 vs. less dimorphic: 8.7/5.8 vs. larger: 2,224–2,568 vs. 2,026–2,264 less dimorphic: 1.20/1.25 ( less dimorphic: 19.3/18.5 vs. 33 larger: 1,308–1,351 vs. 1,192 larger: 52/55 vs. 44 larger: 863 vs. 629 46.2/48.2) vs. 1.77 ( & species based on hard evidence African 770) vs. 1.05 ( 47/51) vs. 1.39 ( 12.2 & & 60.4; H. erectus H. erectus Homo erectus H. erectus Relatively less strong humerus in H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus Homo b H. / 400) & 39; 29.5) ( & 507; ( H. erectus 39; Homo ergaster / ( and within early Homo less dimorphic: 1.06/1.0 less dimorphic: 1.15/1.2 less dimorphic: 8.7/5.8 vs. larger: 1,308–1,351 vs. 1,134 larger: 2,224–2,568 vs. larger: 52/55 vs. 40 larger: 810/863 vs. 478 less dimorphic: 1.20/1.25 Homo erectus 46.2/48.2) vs. 1.32 ( and 730/770) vs. 1.3 ( & vs. & 47/51) vs. 1.32 ( & H. ergaster H. ergaster H. ergaster H. ergaster H. ergaster H. ergaster H. ergaster H. ergaster / / / / / / / / 50/51; 840/924; 55.8/60.4; 29.5) ( ( ( A. afarensis ( ( & 16.3 ergaster 1,927–2,153 ( H. erectus H. erectus Relatively less strong humerus in H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus Australopithecus a 33) & Homo 46; 56.7; 625; ( ( ( 29.5) 400) vs. early & & 39; 507; ( 29.5) ( & Pan 39; ( more dimorphic: 1.39 ( less dimorphic: 12.2 vs. 15.7 No difference: 17.8/15.9 vs. 15.9 more dimorphic: 1.77 ( less dimorphic: 1.05 ( more dimorphic: 33 vs.more 20.2 dimorphic: 13 vs. 16.3 No difference: 19.3/18.5 vs. 20.2 larger: 1,191.7 vs. 1,134 larger: 2,026–2,264 vs. 1,927–2,153 larger: 44 vs. 40 larger: 629 vs. 478 590) vs. 1.3 ( 31.9) vs. 1.32 ( vs. 1.32 ( & & Australopithecus afarensis Homo Homo Homo SameSameHomo Same Same Same Same Both similar to Homo Homo Homo Homo Homo Homo ´n 2012) ´n 2012) ´n 2012) ´n 2012) ; Anto 3 ´n 2012) d d ´n 2012) Pontzer 2012) 2012; Pontzer 2012) as per Anto 2009) Using associated skeletons (Anto Using sex estimates of Pontzer (2012) Of body mass dataOf (Anto femur length data (Anto Male/female mean: CVs (Anto Male/female average brain size (sex designations CVs: Bodies: Brains: Humerofemoral length proportions (Holliday 2012; Hind-limb length relative to body mass (Holliday Sexual dimorphism: Humerofemoral strength proportions (Ruff 2008, TDEE (kcal/day) Table 1. Differences that may relate to life history inferences compared between Average brain size (cm BMR (kcal/day) Average body mass (kg; Holliday 2012; Pontzer 2012)

S482 Pan 545) ϩ H. habi- 4.4–4.5 A. africanus r p H. habilis weight # H. erectus ; thinner? enamel than perhaps transports rock ; smaller M’s than as a conservative comparison with across Old World by 1.6 Ma I’s intermediate between unknown; A. afarensis H. erectus verage of male (16 and farther? years substantial variation and moretures small fea- lis H. habilis with third molar reduction y published. H. erectus 12:368) are used. Lower mean values for Similar? H. erectus H. habilis Unremarkable M surface complexity with H. erectus does not physical activity level (PAL). A range of PALs from apelike A. afarensis # after 1.95 Ma vative values previousl BMR A. afarensis are included in body size estimates. p ; less bunodont M’s e complexity with sub- H. habilis ; smaller M’s than more conser : 4.4–4.5 vs. 2.9–3.6 years A. afarensis H. rudolfensis Acheulean after 1.76 Ma Similar tools or divided by taxon? and possibly across Old World by 1.6 Ma ϩ H. erectus A. afarensis transport rock 12–13 km; stantial variation and more small features with more occlusal reliefthan and thinner enamel Oldowan H. erectus Ubiquitous after 2.5 Ma Similar? Ubiquitous after 2.5 Ma H. erectus Later in Larger I’s than sp.thatmaybe 2.9– Homo ity Unremarkable M surfac p A. afar- ; less buno- A. afarensis values are presented as the combined means for Georgian and early African A. afarensis probably does not ; overlapping ranges he high range of variation, we opt for the A. afarensis 10sto100sofmfrom2.5to unknown; H. erectus A. afarensis A. afarensis pears occurrence with 2.3 Ma and possiblyMa; farther after 1.95 move stone 3.6 years but smaller average M’s than ensis dont M’s with morethan occlusal relief None before 2.6 Ma when Oldowan ap- H. habilis Similar? H. habilis –only values. Age at M1 eruption is available only for the early African remains. H. erectus r et al. 2012) Unremarkable M surface complex er, Hare, and Pontzer 2012), but given t 558) equations is reported. Total daily energy expenditure (TDEE) range is calculated as TDEE ϩ is used for comparative purposes because its cranial capacities (Holloway and Yuan 2004) and body mass (Pontzer 2012) values are greater than those fo weight is not included in brain size estimates, but postcrania assigned to the # followed by the early African 2003) 2012) 1994) Basal metabolic rate (BMR) is calculated by using the Oxford equations for prime adults (18–30 years) and the average body weight of each species. The a Given the small size of the Georgian remains, where available, Australopithecus afarensis Homo rudolfensis Tool technologies (Lepre et al. 2011; Semaw et al. Cut-marked/percussion-marked bone (Potts 2012) Ubiquitous after 2.5 Ma; one possible Stone transit distances? (Braun et al. 2008; Potts Site distribution (area/home range; Swisher et al. Age at M1 eruption (Schwartz 2012) Dental microwear (Ungar 2012; Unga and thus provide a conservative comparison for differences in size. Cranial capacity of KNM-ER 1470 is excluded. Tooth size and shape (Ungar 2012) Larger I’s than a b c d A. afarensis (1.7; Pontzer and Kamilar 2009) to humanlike (1.9, being the mean of male, 1.98, and female, 1.82, averages for subsistence populations; Snodgrass 20 and female (13.1 have been reported (1.5; Schroepf

S483 S484 Current Anthropology Volume 53, Supplement 6, December 2012

Table 2. Regional differences between early Homo erectus samples related to important variables of life history

African Homo erectus/Homo ergaster Georgian H. erectus/ (1.8–1.5 Ma)a H. ergaster (1.8–1.7 Ma)b Asian H. erectus (11.5 Ma)c Average brain size (cm3) X p 863 (n p 5) X p 686 (n p 3) 908 (n p 1) Average body size (kg) X p 57 (n p 4); X p 54 (n p 5) X p 46 (n p 3) ? BMR (kcal/day)d 1,352 1,221 ? TDEE (kcal/day)d 2,298–2,568 2,075–2,319 ? Sexual dimorphism: Brains (male/female mean values) ?1.2 (( p 924, & p 770) ?1.07 (( p 700, & p 655) ? (( p 908) Bodies (male/female mean values) 1.0/1.25 (( p 51/60.4, & p 51/48.2) ?1.21 (( p 48.8 [1], & p ? 40.2 [1]) Age at M1 eruption (years) 4.4 (KNM-WT 15000) ? 4.5 (n p 1) Forelimb to hind-limb length pro- Similar to earlier hominins or a Georgian has slightly ? portions little shorter shorter forelimb Forelimb and strength proportions Less strong relative to hind limb ?? than in H. habilis Tooth size/shape H. erectus/H. ergaster I’s intermediate ?; largest of the H. erectus/ ?; larger than African, slightly (Anto´n 2008; Indriati and An- between Homo habilis and Austra- H. ergaster teeth, smaller smaller than Georgian, with to´n 2008; Ungar 2012) lopithecus; smaller average M’s than than H. habilis and with M3 reduction H. habilis or Australopithecus and M3 reduction with M3 reduction Tooth microwear Unremarkable M surface complexity Unremarkable M surface ? (Ungar 2012; Ungar et al. with substantial variation and more complexity with substan- 2012) small features tial variation and more small features Transit distances? 12–13 km ? ? a Cranial capacities for KNM-ER 3733, 3883, 42700, KNM-WT 15000, OH 9; body mass values for KNM-ER 736, 737 1808, KNM-WT 15000 (n p 4 ) and BSN49/P27 (n p 5 ). Sexes are unknown; however, KNM-ER 1808, 3733, 42700, and BSN 49/P27 are presumed females for this table; KNM-ER 736 and 737 are not assigned to sex. Two sex dimorphism estimates are provided for body size: the first calculates body mass for male skeleton KNM-WT15000 and female skeletons KNM-ER 1808 and BSN 49/P27; the second follows Pontzer’s sex designations for postcranial elements, includes more specimens, and moves KNM-ER 1808 to male. South African H. erectus do not preserve endocranial capacity. Body mass data for South African H. erectus are not included, but the few that are available are comparable to East African H. erectus and would not change the results here (see Anto´n 2012). b Cranial capacities for D2280, 2282, 3444; body mass values for large and small adult and D2021. Sexes are unknown; however, D2282 and the small adult are presumed females for this table; D2021 is unsexed. c Statements reflect Asian H. erectus older than 1.5 Ma only. Cranial capacity for Sangiran 4; dental dimensions for Sangiran 4 and S27; M1 emergence from Dean et al. (2001). While some postcranial size estimates have been made for mid-Pleistocene Asian H. erectus (Anto´n 2003), no postcranial fossils are available from the early Pleistocene. d BMR (basal metabolic rate) and TDEE (total daily energy expenditure) calculated as in table 1, using an average African H. erectus weight of 55 kg as per table 1. ticity is seen in recent secular trends in size in humans (e.g., thought to signal a foraging shift and to be associated with Boas 1912; Bogin 1999; Kaplan 1954; Shapiro 1939; Stinson the origin of Homo (Leakey, Tobias, and Napier 1964). The 2012) and is a critical means by which humans balance the first unambiguous tools appear at 2.6 Ma, with cut-marked high costs of growing large-brained offspring while adjusting animal bone ubiquitous in sites after this time (Potts 2012); to environmental change at the generational or multigener- however, one occurrence of cut-marked bone has been argued ational timescale (Kuzawa and Bragg 2012; Walker et al. 2006; to occur before the emergence of Homo (McPherron et al. Wells 2012). If developmental pattern, particularly plasticity, 2010, 2011; but see Domı´nguez-Rodrigo, Pickering, and Bunn is the target of selection (Kuzawa and Bragg 2012), a means 2010, 2011). Although the Oldowan is linked to carcass pro- of assessing how to visualize this pattern in the skeletal record cessing, other uses related to plant food processing are im- of extant taxa is needed to lay a foundation for doing so in portant (Roche, Blumenschine, and Shea 2009). This emerg- the fossil record. A similar means is needed for identifying ing picture is consistent with dental evidence and supports a behavioral plasticity from the archaeological record. modest dietary shift to more carnivory in Homo and increased dietary breadth compared with Australopithecus. Material Culture A second noteworthy change occurs at approximately 1.95 The archaeological record provides evidence of several key Ma with an increase in stone transport distances that suggests behaviors—including changes in dietary niche, ranging, and the movement of rock over ∼12 km intervals (Braun et al. cognition—that are often associated with the rise of genus 2008; Potts 2012). Further, by 1.76 Ma, Acheulean tools ap- Homo. The manufacture and use of stone tools has long been pear in the record (Lepre et al. 2011). These changes are often Anto´n and Snodgrass Origins and Evolution of Genus Homo S485 attributed to H. erectus and are used to suggest increased body size increases and dietary differences, occur with the range, although it is worth noting that this temporal asso- origin of Homo. Still other changes, such as pelvic narrowing ciation may be coincidental and that increased transit dis- and marked encephalization, occur considerably later in time tances may be characteristic of all post-2.0-Ma Homo. Cer- than previously believed, with several of these traits not ap- tainly after 1.6 Ma, H. erectus, but not other Homo,is pearing until the origin of modern humans. distributed across the Old World, suggesting even greater While the nature of the fossil record makes any interpre- ranging. tation preliminary, current evidence is consistent with the view that there was not a radical shift in the biology and What Changes in Fossil Homo May Mean for Energetics behavior of H. erectus but instead that the full suite of mor- phological and life history traits that characterize our own Changes in brain and body size and ranging have important species first emerged in modern humans. The shift from Aus- implications for daily energy expenditures that must in turn tralopithecus to Homo was marked by body and brain size be balanced by shifts in energy input (i.e., dietary quantity increase, dental and other indicators of a dietary shift, and or quality) and/or shifts in allocation to somatic functions. changes in ranging behavior that imply increased TDEE. Total daily energy expenditure (TDEE), or an individual’s total These shifts became more pronounced in H. erectus, but sub- metabolic cost per day, encompasses the energy required for basic bodily survival and maintenance (thermoregulation, im- stantial intraspecific variation exists. It also appears that the mune function, physical activity, etc.) and that required for developmental shift to the modern human condition occurred growth and reproduction. If basal metabolic rate (BMR) and piecemeal. Homo erectus development (based on the timing physical activity level (PAL) are known, TDEE can be esti- of M1 eruption) was later relative to Australopithecus but was mated (TDEE p PAL # BMR). BMR has a strong correlation quicker than that seen in later Homo. This delay may have to body weight, and average PALs have been measured for been present in non-erectus early Homo as well. An important subsistence populations of humans and some great apes point that has emerged especially from Schwartz’s (2012) (Pontzer et al. 2010; Schroepfer, Hare, and Pontzer 2012; work is that there were diverse life history patterns among Snodgrass 2012). Thus, we can calculate a range of TDEEs fossil hominins, and an approach to human life history evo- for each fossil hominin species by using alternately an ape lution that considers only “ape” versus “human” or “slow” (1.7) or human (1.9) subsistence average for PAL and human versus “fast” is overly simplistic (see also Leigh and Blomquist equations for BMR (tables 1, 2). 2007, 2011; Robson and Wood 2008). When data from contemporary humans and other primates The increasing variability of climate over time suggests that are used to estimate key energy parameters for fossil species, both developmental and behavioral flexibility may have been TDEE increases in all early Homo over the condition in Aus- prized and that the apparent variation seen in the past needs tralopithecus because of body size increases. If we assume that to be carefully compared and parsed against extant variation. different species and genera shared similar PALs (i.e., are ei- These data imply that the extant record should be plumbed ther all apelike or all humanlike), then H. habilis TDEE in- in new ways for evidence of how the skeletons of living hu- creases only modestly (5%) over the condition in A. afarensis. mans and nonhuman primates reflect their environments, life Homo erectus increases by 15% over A. afarensis. African H. histories, and behaviors. These analyses require the devel- erectus TDEE estimates are 10% greater than those for Geor- opment of data sets in which the extant and fossil records gian H. erectus. Alternatively, if suggestions of increased rang- can be more fully integrated. ing in H. erectus (or early Homo) are considered to indicate that Homo species can be attributed more humanlike PALs compared with A. afarensis, then the differences between the Human Biology and the Origins of Homo: genera would be greater. In either case, Homo appears to have required more energy input than Australopithecus or perhaps Implications for Understanding the a shift to a higher throughput system (i.e., more calories Fossil Record consumed and expended per day) than Australopithecus such as is seen in humans versus great apes (see Pontzer 2012). Here we integrate recent advances in the study of contem- porary human and primate biology with the fossil record to better interpret the evidence discussed above (tables 3, 4). We Summary of Fossil Changes in Early Homo concentrate on inferences regarding (1) the emergence of ge- The suite of morphological and behavioral traits that char- nus Homo, (2) the transition between non-erectus early Homo acterize modern humans does not first appear with the origin and Homo erectus, and (3) the appearance of regional mor- of H. erectus, at least not to the extent previously believed. phological variation in H. erectus. We outline predictions that Some critical changes such as hind-limb elongation occur at we hope will help guide future research and suggest areas in the base of the hominin lineage (i.e., well before the origin which additional data from extant taxa would be particularly of genus Homo). Other traits, including modest brain and useful. S486 Current Anthropology Volume 53, Supplement 6, December 2012

Table 3. Inferences regarding behavioral/cultural differences between Australopithecus and Homo

Australopithecus vs. Homo erectus/ H. erectus vs Homo habilis/ Australopithecus vs. early Homo Homo ergaster Homo rudolfensis Energetic requirements: Brains Homo larger on average H. erectus/H. ergaster larger H. erectus larger on average Bodies Homo larger on average H. erectus/H. ergaster larger H. erectus larger on average Developmental rate: Brains ? ? ? Teeth (Schwartz 2012) ? H. erectus/H. ergaster slower than ? Australopithecus but still fast compared with Homo sapiens? Bodies (Dean et al. 2001; ? H. erectus/H. ergaster body relatively ? Graves et al. 2010) faster than teeth intermediate be- tween Pan and H. sapiens Diet (from teeth; Ungar Tougher, less brittle food items Tougher, less brittle food items in Tougher, less brittle food items 2012; Ungar et al. 2012) in Homo; more incisal preparation H. erectus/H. ergaster; greater diet in H. erectus; greater diet in Homo? breadth in H. erectus/H. ergaster breadth in H. erectus than than Australopithecus H. habilis/H. rudolfensis Nutritional environment/diet: From brains/bodies Homo somewhat higher-quality diet H. erectus/H. ergaster higher-quality H. erectus probably higher- diet quality diet From archaeology Homo greater use of animal prod- H. erectus/H. ergaster more signifi- H. erectus likely greater use of ucts? cant use of animal products animal than H. habilis/H. rudolfensis Locomotor repertoire Both have significant arboreal com- H. erectus/H. ergaster strongly ter- H. erectus more terrestrial ponent restrial Home range (HR): Bodies Somewhat larger because of larger H. erectus/H. ergaster larger because H. erectus larger because of body size? of body size body size Site distribution Similar? H. erectus/H. ergaster larger HR H. erectus larger HR Stone transport ? H. erectus/H. ergaster larger HR H. erectus larger HR Note. Based on hard-evidence differences in table 1.

The Emergence of Early Homo plasticity that leads to early maturation and small adult body size (see Migliano and Guillon 2012). While we focus mainly The fossil record for earliest Homo is especially sparse, and on body size, we note that cranial characteristics and brain inferences from it must be made cautiously. Nonetheless, size are subject to similar developmental plasticity (e.g., Boas available fossil evidence suggests that non-erectus early Homo 1912), and we note that nondietary variables also contribute species were somewhat larger in average brain and body size to growth and adult outcomes. and had slower developmental patterns than Australopithecus Recent work has provided extensive evidence that extrinsic (Anto´n 2012; Holliday 2012; Pontzer 2012; Schwartz 2012). If confirmed, the extant record indicates that this brain and mortality risk is a primary contributor to life history variation body size increase was most likely to result from an increase both within and between species, with faster growth and ear- in food availability and dietary quality and a reduction in lier reproduction in environments of high (especially juvenile) extrinsic mortality risk. mortality (Charnov 1993; Kuzawa and Bragg 2012; Stearns Considerable evidence exists that improved diet quality and 1992; Walker et al. 2006). For example, arboreal nonhuman nutrient availability during growth influences adult body size primates tend to have relatively protracted life histories that (Kuzawa and Bragg 2012). In contemporary human popu- appear to result from the relatively low predation risk and lations, secular trends to larger body size and earlier repro- mortality they experience (Borries et al. 2011). And in hu- ductive maturation occur quickly via developmental shifts mans, extremely high mortality environments with pro- that alter energy allocation during improved environmental nounced juvenile and adult risk may help explain the fast conditions such as higher-quality and more stable food re- developmental life history pattern and small adult body size sources and reduced infectious disease exposure (Boas 1912; of “pygmy” populations such as the Aeta and Batak of the Bogin 1999; Kaplan 1954; Shapiro 1939; Stinson 2012). For Philippines (Migliano 2005; Migliano and Guillon 2012; Mig- example, in a single generation, Mayan children growing up liano, Vinicius, and Lahr 2007). in the United States experienced a 10-cm population-level Thus, proximate environment-related shifts in life history increase in stature compared with those in Guatemala (Bogin can influence morphology and are potentially identifiable in and Rios 2003). Conversely, under stable yet extremely poor the fossil record. Further, these developmental shifts may pro- environmental conditions, there is evidence for a reduced vide a foundation for longer-term population-level adaptation Anto´n and Snodgrass Origins and Evolution of Genus Homo S487

Table 4. Regional behavioral/cultural differences inferred between early Homo erectus samples

African Homo erectus/Homo Georgian H. erectus/H. ergaster ergaster (1.8–1.5 Ma) (1.8–1.7 Ma) Asian H. erectus (11.5 Ma) Inferred energetic requirements: Brains (TDEE) Increased contribution of brain size Increased contribution of brain size Increased contribution of brain to metabolism to metabolism over condition size to metabolism in H. habilis TDEE Higher in Africa because of body Lower in Georgia, with seasonal ? size differences upregulation of metabolic expenditures? Inferred developmental rate Same as Asia ? Same as Africa Inferred diet (teeth) Tougher, less brittle food items in Tougher, less brittle food items in ? H. erectus/H. ergaster H. erectus/H. ergaster Greater diet breadth than Homo Greater diet breadth than Homo habilis/Homo rudolfensis habilis/Homo rudolfensis Inferred nutritional environment: Anatomy High quality Nutritionally less sufficient during High quality given brain size growth given small size Archaeology High quality Perhaps more seasonal? ? Transit distances? 12–13 km ? ? Extrinsic mortality? Lower than Australopithecus based Lower than Australopithecus but Lower than Australopithecus on body and brain size possibly higher than other H. based on brain size erectus Note. Inferred from primary data in table 2. TDEE p total daily energy expenditure. through natural selection (Kuzawa and Bragg 2012). The prediction on archaeological and paleontological evidence for complicated web of interactions means that shifts in body dietary change in earliest Homo as well as modest body size size, for example, may result from a variety of different inputs increase over the condition in Australopithecus. Additional working together or at cross-purposes (Kuzawa and Bragg studies of dental macro- and microstructure will help lay a 2012; Migliano and Guillon 2012). It is nonetheless possible foundation in extant taxa for understanding the relationship to begin to make some predictions regarding the expected of tooth form (especially molars) to diet. While we acknowl- outcomes that various kinds of changes to extrinsic mortality edge that proxies for life history patterns are more compli- and other proximate factors might have on skeletal size and cated to reconstruct than proxies for other types of shifts, shape. In particular, increases in overall body size might result studies that consider how dental developmental profiles and from several different decreases in, for example, extrinsic mor- their variation are correlated with life history attributes within tality. These could include reduced susceptibility to predation populations of living human and nonhuman primates will be or decreased infectious disease or parasite burden, for ex- an important means of contextualizing fossil data. ample. Future research should develop means of assessing Another hypothesized contributor to the emergence of early from separate records (i.e., archaeological, paleontological, Homo is related to the influence of increasing climatic vari- geological, and contemporary biological) the presence and ability on biology. The geological record indicates increased rate of these various sources of mortality. climatic variability during the rise of early Homo, which, based If decreases in extrinsic mortality and increases in energy on extant human and primate biology, hints at the possibility availability and dietary quality are driving factors in the origin that greater developmental plasticity than in Australopithecus of Homo, then we can predict that if further evidence of may have facilitated adjustments to short-term environmental multiple early non-erectus Homo taxa is found, each will be change and initiated a cascade of events leading to greater larger in average body size than Australopithecus. However, capacity for phenotypic plasticity as well as increased dispersal these multiple Homo species, while showing anatomical evi- capability. Given the paucity of the Homo record from 2.5 to dence of niche partitioning, may or may not differ from one 1.5 Ma, part of the primary research agenda should be an another in body size. emphasis on exploring sediments from this time period with The fossil record also suggests that non-erectus early Homo a particular focus on differentiating between early non-erectus was smaller and developed more quickly than H. erectus,al- and early H. erectus lifeways. However, additional work on though again the early Homo record is quite sparse. When the substantial fossil record of Australopithecus afarensis, additional fossils of early Homo are available, we predict that which shows distinct temporal changes in morphology (Lock- non-erectus early Homo will be found to have had a life history wood, Kimbel, and Johanson 2000), might be useful in pro- pattern intermediate between Australopithecus and H. erectus viding a comparative hominin data set for testing the idea of with a modestly extended growth period, including the pres- increased developmental plasticity in Homo. Studies that focus ence of short childhood and adolescent periods. We base our on comparing variation potentially related to developmental S488 Current Anthropology Volume 53, Supplement 6, December 2012

Table 5. Tertiary inferences regarding life history and behavior between Australopithecus and Homo

Australopithecus vs. Australopithecus vs. Homo erectus/ H. erectus vs. Homo habilis/ early Homo Homo ergaster Homo rudolfensis Extrinsic mortality Possibly lower in Homo given Lower in H. erectus Lower in H. erectus body size Developmental plasticity ? Greater in H. erectus Greater in H. erectus Body composition Larger brains in Homo but Larger brains in H. erectus/H. ergaster Larger brains in H. erectus/H. ergaster similar adiposity and greater adiposity and greater adiposity Cooperative breeding Possibly more cooperative H. erectus/H. ergaster more coopera- H. erectus/H. ergaster more coopera- (alloparenting; Isler breeding in Homo tive breeding necessitated by larger tive breeding necessitated by larger and van Schaik 2012) average brain size average brain size Cooperative hunting Possibly greater in Homo Likely greater cooperative hunting Likely greater cooperative hunting based on diet shift in H. erectus/H. based on diet shift in H. erectus/H. ergaster ergaster Note. Based on hard-evidence differences in table 1. plasticity (e.g., variation in body size or dimorphism at a given logical skills such as in foraging as well as the refinement of time) among time packets of this taxon and with early Homo social behaviors (Bogin 1999). would facilitate the identification of genus-level differences in In order to assess, interpret, and characterize a species’ life biology. If increased developmental plasticity is present in history pattern, we need to study multiple somatic systems Homo, one should find greater variation in the genus at any simultaneously (Leigh and Blomquist 2007, 2011; Sˇesˇelj 2011). given time than in other well-represented genera. While non- While multisystem studies have only begun to be applied to erectus Homo samples are currently insufficient for such com- the fossil record, in large part because of a dearth of associated parisons, H. erectus provides more opportunities for such skeletal remains, they point to the need for extensive research investigations. on extant taxa for which somatic and physiological data are knowable. So far, these integrative studies have focussed on The Transition between Non-erectus Early Homo and the hard tissues of the extant and fossil record (Clegg and Homo erectus Aiello 1999; Guatelli-Steinberg 2009; Sˇesˇelj 2011), and many more such studies are needed. Further, there is a critical need Even though recent fossil and archaeological discoveries chal- for studies that reach across both living and skeletal popu- lenge the idea that the origin of H. erectus involved a punc- lations to combine hard-tissue parameters (e.g., age, sex, and tuated transformation of biology and behavior, present evi- size proxies), soft-tissue measures, and physiological data in dence suggests that this species did diverge from other living humans, nonhuman primates, and other mammals (see hominins in several important ways. The life history pattern http://bonesandbehavior.org; Smith et al. 2012). Work that of H. erectus appears to have been more protracted than that links conditions of nutritional stress to variation in both skel- of Australopithecus and Paranthropus and possibly non-erectus etal maturation (e.g., Frisancho, Garn, and Ascoli 1970) and early Homo. Despite this, when compared with modern hu- dental emergence patterns (e.g., Gaur and Kumar 2012) sug- mans and later Homo (e.g., Neanderthals), H. erectus appears gests that multiple modalities are influenced by this devel- to have had a more rapid life history, with less pronounced secondary altriciality, an earlier maturation, and a less pro- opmental process. A key step forward will be to define data nounced adolescent growth spurt (Dean and Smith 2009; sets in extant taxa that are explicitly designed to be collected Graves et al. 2010; Guatelli-Steinberg 2009; Thompson and and/or closely proxied in the fossil record in order that phys- Nelson 2011). ical or archaeological clues can be identified as signals for Present evidence suggests that a childhood phase of de- development of behavioral or physiological shifts in deep time velopment (i.e., “early childhood”), with offspring being (see http://bonesandbehavior.org). weaned yet still dependent for food and experiencing rapid The other significant life history shift that arguably emerged brain growth but slow somatic growth, was in place by the in early H. erectus is the extended time to maturity through time of H. erectus (Bogin 2006; Thompson and Nelson 2011). an elongated adolescence coupled with the development of a Contemporary human biology suggests that this life history pronounced late adolescent growth spurt (Bogin and Smith shift in H. erectus most likely would have involved a short- 1996). The extant record indicates that this most likely would ening of infancy with earlier weaning and probably also have involved a reduction in extrinsic mortality risk and shorter IBIs. Importantly, this pattern would have resulted in greater nutritional access and stability than in early hominin higher fertility and greater potential for population increase. species (e.g., Robson and Wood 2008). Fossil and archaeo- Extending childhood by even a year would allow more time logical evidence is consistent with increased access to higher- for cognitive development, including the development of eco- quality foods (i.e., those with relatively high energy and nu- Anto´n and Snodgrass Origins and Evolution of Genus Homo S489 trient density; Potts 2012; Ungar 2012), resulting in potentially in non-erectus Homo (Bribiescas, Ellison, and Gray 2012; Gett- fewer periods of nutritional inadequacy that would have re- ler 2010; Key and Aiello 2000; Swedell and Plummer 2012). duced associated declines in immune function. Additionally, once cooperative breeding is present, we ex- Beyond diet, the extant record strongly implicates reduced pect a fundamental shift in social organization that may be extrinsic mortality as a means of increasing size and delaying visible in the archaeological record (Potts 2012; Smith et al. development; however, it remains unclear just how mortality 2012; Swedell and Plummer 2012). This may be reflected in risk might have been lowered for H. erectus. An important evidence for greater or more complicated extractive foraging clue may come from the extensive system of cooperative be- (Swedell and Plummer 2012) or in the aggregation of multiple havior and breeding seen in modern humans. Cooperative individuals (Potts 2012; Smith et al. 2012). Future archaeo- behavior, defined here as behaviors that provide a benefit to logical endeavors should aim to identify material cultural sig- another individual and may or may not have a cost to the natures reflecting these shifts. This research could potentially actor, occurs widely in the natural world, yet the degree of be coupled with stable isotope studies, which have shown cooperation between unrelated individuals is unique to hu- great potential for identifying signatures of population move- mans (Clutton-Brock 2009; Melis and Semmann 2010). In ment during the lifetime of an individual (e.g., Copeland et cooperative breeders, allocare (including paternal care) allows al. 2011). Finally, we suggest that future studies focus on other the mother to channel resources to her own somatic main- aspects of extrinsic mortality relevant to shaping body size tenance and reproduction; thus, allocare should generally be and shape, including predation rates as well as contributors favored evolutionarily when the risk to the offspring is not to intrinsic mortality rates such as dietary breadth, quality, too high (Lappan 2009; Ross and MacLarnon 2000). Among and availability. mammalian species, those with greater allocare exhibit rela- tively rapid infant growth with earlier weaning and faster Regional Variation, Climatic Adaptation, and Dispersal in reproductive (birth) rates, although these infants are not Homo erectus larger at birth (Borries et al. 2011; Isler and van Schaik 2009; Mitani and Watts 1997; Ross and MacLarnon 2000; Smith et By the time of H. erectus, the trend toward greater ranging that may have started at the base of the genus had blossomed al. 2012). The well-developed system of cooperation in hu- into long-range dispersals into a variety of different climatic mans plays a critical role in supporting the high costs of contexts (e.g., the Republic of Georgia and tropical southeast encephalization that must be paid during pregnancy and lac- Asia; Anto´n and Swisher 2004). Widely dispersed living mam- tation (Ellison 2008; Kramer 2010; Wells 2012) and is a major mals face a number of similar challenges and tend to share factor in enabling early weaning, relatively low extrinsic mor- a number of attributes including behavioral plasticity, soci- tality, extended subadult dependence, and high fertility ality, and relatively high rates of reproduction (i.e., high in- (Gurven and Hill 2009; Hill and Hurtado 2009; Kaplan et al. trinsic rates of natural increase; Anto´n, Leonard, and Rob- 2000; Lancaster and Lancaster 1983). Thus, cooperative breed- ertson 2002). In addition, contemporary humans add greater ing was almost certainly a critical contributor to brain size adiposity that buffers individuals in shifting environments and increase in the Homo lineage, although the timing of this also allows maintenance of brain metabolic requirements, occurrence is elusive. both of which are critical to successful dispersal (Kuzawa An important observation related to the likely presence of 1998; Leonard et al. 2003; Wells 2010). And humans exhibit cooperative breeding in H. erectus is the link between de- great developmental plasticity that preserves flexibility in the mographic viability and encephalization. Isler and van Schaik face of short-term environmental changes (Walker et al. (2012) suggest that demographic viability in primates is un- 2006). As such, it seems likely, based on what we know of 3 tenable at average cranial capacities over 700 cm (i.e., a “gray the extant record, that H. erectus (1) had a different body ceiling”) because of low fertility related to a protracted sub- composition than earlier hominins, with higher levels of ad- adult period characterized by rapid brain growth but slow iposity; (2) possessed a level of developmental plasticity sim- somatic growth. Smith (2012) and colleagues also found sup- ilar to that seen in modern humans, which may help explain port from the carnivores for the idea of the co-occurrence of the long existence of this species; and (3) may have had greater brain size expansion and cooperative breeding. Cooperative behavioral plasticity, which would have favored their success breeding in the form of direct care and the provisioning of over less versatile members of genus Homo (see Smith et al. juveniles with high-quality resources (e.g., animal fat and pro- 2012). tein) would have enabled early H. erectus to circumvent this To see how body composition might have changed, we look demographic constraint and evolve a relatively large brain to humans who differ from other mammals (including non- while also having a life history pattern with early weaning human primates) by having particularly high levels of fat, and short IBI that led to greater fertility and facilitated pop- large brains, small guts, and low muscularity (Aiello and ulation growth. Thus, a system of cooperative breeding, al- Wheeler 1995; Leonard et al. 2003; Wells 2010). These dif- though not as well developed as in modern humans, seems ferences in body composition structure variation in energy likely to have been in place by the time of H. erectus if not demands because of marked differences in organ-specific met- S490 Current Anthropology Volume 53, Supplement 6, December 2012 abolic rates. While most internal organs—such as the heart, dictions of body composition in fossil hominins as well as lungs, kidneys, liver, and spleen—appear to be tightly scaled tests as to when in our lineage adiposity and sex-specific with body mass (Calder 1984; Stahl 1965), the brain, gut, patterns of adiposity arose. skeletal muscle, and adipose tissue vary according to func- Plavcan (2012) notes that because of the difference between tional demands (Aiello and Wheeler 1995; Calder 1984; total body mass and lean body mass in humans and the dif- Muchlinski, Snodgrass, and Terranova 2012; Schmidt-Nielsen ferential distribution of fat in human females, degrees of cra- 1984; Wells 2010). Nonhuman primates are “undermuscled” nial and postcranial skeletal variation differ in humans but when compared with other mammals, which likely reflects not other apes. As in all other primates, postcranial variation the arboreal heritage of the order. Humans, and especially (as reflected in CVs of linear dimensions) is similar to that human females, appear to be even less muscular (Muchlinski, of lean body mass variation (excluding adipose tissue) in Snodgrass, and Terranova 2012; Snodgrass, Leonard, and Rob- humans. But unlike other primates, these CVs are greater than ertson 2009). Although this could be an adaptation to reduce cranial CVs. Cranial variation in humans is similar to that of energetic costs associated with bipedal locomotion, it is more total body mass variation (including adipose tissue, which likely a reflection of our high levels of adipose tissue for a may indicate the importance of adipose tissue to brain main- primate of our size. tenance). Presumably this reflects increased adiposity in hu- Thus, besides the brain, the single most important com- mans and differential fat distribution in human females versus ponent of body composition for understanding human evo- males. Thus, finding the point at which measures of cranial lution is arguably adipose tissue (Wells 2010, 2012). This tissue and postcranial skeletal dimorphism diverge may provide a is closely linked to brain development and immune function, preliminary clue as to when greater (or at least differential) likely underpins the exceptional dispersal abilities of our ge- adiposity arose in the lineage. At present, endocranial and nus, and helps explain our ability to withstand seasonal and femoral length CVs are similar to one another within early periodic fluctuations in food availability (Kuzawa 1998; Wells non-erectus Homo, early H. erectus, and A. afarensis. Thus, at 2010, 2012). Humans are exceptional in having fat stores least the differential fat distribution seen in human males and considerably larger than most free-living primates and ter- females had yet to develop by the time of early H. erectus, restrial tropically living mammals, and this is true for non- although we currently have no window on to whether in- Western human populations as well (body fat levels average creased adiposity was present in both sexes (table 1; and see 25% for adult females and 13% for adult males; Pond 1998; table 5 in Anto´n 2012). Wells 2006, 2010). Humans are extremely fat at birth (∼15% Our inference of greater developmental plasticity in H. fat) and during infancy (peaking at ∼25%–30% fat), which erectus is supported by the variation seen in size across re- contrasts markedly with wild primates (baboons, 3%), do- gional samples but is also an insight that requires that we use mesticated species (pigs, 1.3%), and even seals (harp seals, caution in interpreting the meaning of morphological differ- 10.4%; Kuzawa 1998). Adipose tissue in humans serves pri- ences among samples in body proportions, size, and sexual marily as a nutritional buffer against long-term (e.g., seasonal dimorphism. Caution is required for several reasons. First, or periodic) decreases in energy availability, and fat is an some of the size variation shows a temporal trend in H. erectus important adaptation for preserving cerebral metabolism in (see Plavcan 2012). Second, total variation in H. erectus is not the face of the high and obligate metabolic demands of the particularly remarkable relative to extant primates (Plavcan large human brain (Kuzawa 1998; Leonard et al. 2003). Fur- 2012). Third, it is well established that developmental plas- ther, human sex differences in adiposity are shaped by dif- ticity can shift these signals rapidly in extant human and ferences in reproductive strategies—in particular, the enor- nonhuman primates (e.g., Bogin and Rios 2003) and for a mous energetic costs of pregnancy and lactation borne by variety of different reasons (Kuzawa and Bragg 2012). females (Snodgrass 2012; Valeggia and Ellison 2001). This shift To test the extent to which developmental plasticity was in body composition and concomitant increased energetic present in H. erectus and how similar it was to the human buffering (i.e., “somatic capital” of Kaplan et al. 2000) may form, we need to understand how such plasticity is reflected have played a central role in the ability of H. erectus to suc- in the skeletons of humans and nonhuman primates. Sur- cessfully disperse into new environments, especially those with prisingly, the extent of variation in developmental plasticity seasonal and periodic variation in climate and food avail- among primates is not well studied, and the lack of these data ability. is a barrier to interpreting variation in the human fossil rec- Our ability to identify shifts in body composition in the ord. One study of baboons demonstrates the potential for fossil record is, of course, limited, and we are further con- dramatic shifts in growth, reproduction, and body size with strained by the surprisingly little body composition data avail- altered environmental conditions (Altmann and Alberts able for living primates and other mammals. Refining our 2005). Garbage-foraging baboons Papio cynocephalus show understanding of body composition in extant species will help faster maturation and larger body size than other savannah to identify which aspects of body composition in humans are baboons as a result of better food availability during ontogeny. derived and to outline adaptive scenarios related to their di- Given their generalized ecologies and broad geographic dis- vergence (Wells 2012). It may also allow more nuanced pre- tributions, papionin monkeys (baboons, mandrills, and ma- Anto´n and Snodgrass Origins and Evolution of Genus Homo S491 caques) and modern humans are arguably the best analogues Robertson 2009). For this reason, poor growth resulting from for early Homo, especially H. erectus (Jolly 2001; Swedell and environmental conditions disproportionately affects limbs Plummer 2012), and should prove a fruitful area of focus for and their distal segments, which grow at a more rapid rate future studies. than the trunk during infancy. At ∼2–3 years of age, declining A related issue with importance for interpreting the hom- growth rates and more developed immune and digestive sys- inin fossil record is the influence of developmental plasticity tems reduce the risks of permanent growth disruptions (Bogin on sexual dimorphism (see Bribiescas, Ellison, and Gray 1999; Kuzawa 1998). As a result, the secular increase in height 2012). Although both sexes experience developmental plas- experienced by most human populations in the twentieth ticity, males are disproportionately able to capitalize on high- century was associated with disproportionate gains in limb quality environments, whereas females are more environ- length, particularly distal segments (Stinson 2012). In fact, mentally buffered and less negatively influenced by poor relatively short legs are interpreted as reflecting an adverse environments (Altmann and Alberts 2005; Kuzawa 2007; Stin- early developmental environment (Bogin and Varela-Silva son 1985). Thus, sexual dimorphism can shift rapidly over 2010). Although genetic factors related to ultimate causes such time with reduced sexual dimorphism in bad times and ac- as climatic adaptation (Katzmarzyk and Leonard 1998; Rob- centuated sexual dimorphism under more optimal environ- erts 1978) are important contributors to body proportions, mental conditions (Stini 1972, 1975). This may hint at the proximate factors such as nutrition during development cause of the apparent reduction in dimorphism in Georgian clearly play an important role in humans (Bogin and Rios H. erectus (see table 2). Additionally, environmental condi- 2003; Eveleth and Tanner 1990; Stinson 2012). Studies of how tions experienced during development influence testosterone the skeleton is affected by nutritional insufficiency during the and thus shape sexually dimorphic traits, including stature, longer weaning period of great apes will be important to bone growth, and muscle mass (Bribiescas, Ellison, and Gray considering the applications to the fossil record. 2012; Kuzawa et al. 2010). This topic has not been system- Further, exposure to persistent and ubiquitous stressors atically studied across primates, but we believe it should form that are not effectively buffered by cultural/behavioral mech- the basis for future investigations as it has important impli- anisms will lead to adjustments initially through develop- cations for making inferences from morphological variation. mental plasticity and later, if experienced at a population level Although we recognize that other, longer-term forces such over multiple generations, by genetic changes resulting from as mate competition are critical to shaping differences in sex- polygenic adaptation (Kuzawa and Bragg 2012). Thus, studies ual dimorphism across taxa (see Plavcan 2012), a more sys- that combine dental, cranial, and postcranial analysis can po- tematic understanding of intraspecific variation across geo- tentially expand our ability to interpret variation in body size graphic, environmental, and nutritional contexts in primates and proportions seen among regional samples of H. erectus. is critical to contextualizing variation in the fossil record. While the state of the fossil record is currently quite far from Evaluations of specific skeletal responses (e.g., brow devel- adequate for such purposes, regional samples of H. erectus opment) to environmental signals in extant taxa may help may begin to be probed using integrative studies, and addi- elucidate the meaning of sexual dimorphism in the fossil rec- tional research on extant taxa will help provide the compar- ord (Bribiescas, Ellison, and Gray 2012). More systematic ative foundation for this work. studies of geographic variation in nonhuman primate sam- We could hypothesize, for example, that the smaller overall ples, both skeletal and living, that pay particular attention to size of Georgian H. erectus is due to decreased nutritional how the adult form of skeletal traits (including overall size sufficiency during development or increased extrinsic mor- but also secondary sex characteristics such as robusticity) is tality (due to predation or disease; Anto´n 2012; Migliano and affected by developmental plasticity and how the sexes are Guillon 2012). Or, we might predict it results from small- differentially affected in different environments will greatly packet resources that are widely dispersed in a topographically improve our ability to differentiate adaptation from epiphe- challenging area with little selective pressure for large body nomenal variation in the fossil record (Plavcan 2012; see Fer- size—an explanation offered for the small adult body size of nandez-Duque 2011 for an example of the use of skeletal Late Stone Age humans of southern Africa (Pfeiffer 2012). proxies from living animals). Or, the apparently shortened arms of the Dmanisi group may Another means of differentiating among hypotheses for perhaps reflect climatic adaptation (Pontzer 2012). intraspecific variation in body size and shape considers dif- We could test these hypotheses by considering the specific ferences in proportions due to the timing of growth disrup- anatomical and archaeological signatures each implies. For tions. Poor growth related to environmental conditions typ- example, nutritional stress-related small adult body size likely ically occurs during infancy when growth rate is rapid and would be accompanied by shortened distal limb segments and the body is uniquely vulnerable to insult. In humans, this marked enamel hypoplasias, the latter of which provide a heightened vulnerability is associated with the introduction permanent record of systemic physiological stress, whereas of supplemental, often low-quality foods, which usually begins climatic adaptation might result in shortened arms but not at ∼4–6 months of age. These foods may also inadvertently necessarily differentially short distal limb segments in both introduce pathogens (Sellen 2001; Snodgrass, Leonard, and arms and legs. Alternatively, increased extrinsic mortality such S492 Current Anthropology Volume 53, Supplement 6, December 2012

Figure 1. A positive feedback loop between cooperative behavior (initially in breeding), diet quality and stability, cognitive abilities (brain size), and extrinsic mortality risk drove life history evolution and contributed to cultural change in genus Homo. Gradual, self-reinforcing shifts in these central elements had consequences for life history traits including extending the developmental period, increased fertility, and larger body size; body composition including increased adiposity, reduced gut size, and reduced muscularity; communication including eventually the development of language; and cultural change including more complex extractive foraging. Early Homo showed only modest increases in the central elements. The fully modern package of life history and other consequences may not have emerged until recent humans. as predation and parasites should lead to differences in neo- A Model for the Origins and Evolution of natal size (Kuzawa and Bragg 2012) relative to nonstressed Genus Homo groups but not necessarily to indicators of nutritional stress and may also yield archaeological signals. Evidence of packet The integration of paleoanthropological data with informa- size may come from archaeological evidence. Surprisingly, tion from primatology and human biology leads us to the research of this nature in contemporary humans and non- conclusion that the origin and evolution of early Homo was human primates is fairly limited. However, a study among characterized by a positive feedback loop that drove life his- Aboriginal Australians—which found that permanent stunt- tory evolution and contributed to cultural change. The central ing was seen only in individuals with enamel defects that were elements of this model are cooperative behavior, diet, cog- early (within the first 18 months of life), severe (enough to nitive abilities, and extrinsic mortality risk (fig. 1). The model produce paired enamel defects), and repeated (during infancy postulates gradual self-reinforcing shifts in these central ele- and childhood; Floyd and Littleton 2006)—shows the poten- ments with consequences for life history traits (e.g., extended tial of multisystem studies. Such an integrative approach may developmental period, increased fertility, and larger body help us interpret body size and proportion variation in Homo size), body composition (e.g., adiposity, gut size, and mus- and to differentiate adaptive variation from responses to prox- cularity), communication abilities (the development of lan- imate environmental factors such as diet and disease. guage), and cultural change (tool use). The model expands Finally, we suggest that from other records, local environ- on Hrdy’s (2009) cooperative breeding hypothesis, which pos- mental signals should also be plumbed and developed to un- tulates that beginning with the rise of the genus Homo, allo- derstand the specific as well as the regional and global context maternal care and provisioning drove life history evolution, of fossil groups. If extrinsic mortality has such important and it recognizes, as does Kaplan et al. (2000), that reducing consequences for size and shape variation, then additional mortality rates, investing in embodied capital (fat), and in- means of assessing extrinsic mortality must be pursued. As creasing cooperation are in a positive feedback loop with brain mentioned earlier, these include archaeological means for as- size. However, it does not rest on a particular kind of food sessing predation and diet as well as geochemical means for resource or social structure but recognizes that increasing diet reconstructing plausible climates and diets. Thus, we advocate quality and/or throughput and cooperation remain critical to a multipronged approach to future research agendas that (ob- growing big brains and large bodies. viously) includes collection of new fossil hominins and a focus At present, it is impossible to identify the initial evolu- in extant mammals on skeletal end results of environmental tionary change or changes, but it seems most likely that be- and physiological parameters, especially in widely dispersed havioral changes related to diet and perhaps cooperation were taxa. early additions. In contrast, encephalization would likely have Anto´n and Snodgrass Origins and Evolution of Genus Homo S493 been a secondary change, because comparative studies suggest of the behavior, physiology, and anatomy of extant groups. that alterations in diet quality and body composition were These data sets must be explicitly designed to be measurable necessary preconditions of hominin brain expansion. Further, or closely proxied in the fossil record. reductions in mortality risk (both intrinsic and extrinsic) most likely would have been substantially influenced by dietary shifts and increased cooperative behavior and thus would Acknowledgments likely have been downstream changes. Present fossil and archaeological evidence suggests sub- We benefited greatly from the lively discussions at the Wenner- stantial changes in diet occurred initially with non-erectus Gren Foundation workshop “Human Biology and the Origins early Homo and were followed by marked dietary change in of Homo” held in Sintra, Portugal, in March 2011. We thank Homo erectus. In particular, earliest Homo likely consumed a Leslie Aiello, who co-organized the workshop with S. C. An- substantially higher-quality diet than Australopithecus and to´n, our fellow participants, and Laurie Obbink for making Paranthropus, as the result of the consumption of high-quality the Sintra meeting such a productive, stimulating, and con- plant foods (e.g., underground storage organs) as well as an- vivial week. Following Sintra, Chloe, Bill Leonard, and Her- imal source foods. Homo erectus appears to have occupied a man Pontzer engaged in critical discussions of energetics and new ecological position for hominins that almost certainly organ-specific metabolism, Leslie Aiello and Tom Schoene- involved a considerable increase in access to animal foods. mann provided important input on the early conception of This dietary shift to more energy- and nutrient-dense foods this paper, Chris Kuzawa provided critical feedback on a later would potentially have allowed for an increase in brain size iteration, and Leslie Aiello and the reviewers greatly improved by removing constraints on brain growth; in addition, this the final paper. Emily Middleton and the Current Anthro- dietary change may have selected for increased brain size and pology staff provided expert editorial advice. cognitive capacity related to increased foraging, extraction, and processing abilities associated with higher-quality diets. 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