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An afarensis Infant First Metatarsal from Hadar,

A thesis submitted to the Miami University Honors Program in partial fulfillment of the requirements for University Honors with Distinction A thesis submitted to the Miami University Department in partial fulfillment of the requirements for Departmental Honors

By

Heather A. Hillenbrand

May 2009 Oxford, Ohio, USA Abstract An Australopithecus afarensis Infant First Metatarsal from Hadar, Ethiopia By Heather A. Hillenbrand The story of early evolution centers largely on the adaptation of bipedality. “The hallux clearly plays so fundamental a role in locomotion that any relevant fossil specimen would have great significance for the assessment of locomotor patterns in hominids” (Latimer and Lovejoy, 1990: 125). The hallux, or first toe, consists of the first metatarsal and the proximal and distal phalanges (White and Folkens, 2000). The most important indication of bipedality in this digit is the hallucal tarsometatarsal joint (the joint at which the first metatarsal articulates with the medial cuneiform). Though significant fossil evidence of Australopithecus afarensis has been documented, controversy over interpretation of the species’ anatomical adaptations, and thus its locomotor patterns, still exist. This work addresses an Australopithecus afarensis infant first metatarsal from the A.L. 333 site in Hadar, Ethiopia, never before described nor accessioned to the Hadar catalogue. The fossil was compared to the first metatarsals of modern human and infants, and, in measurements where these groups differed, the fossil was found to be morphologically similar to . This anatomy suggests the potential for fully modern bipedal locomotion, which implies profound behavioral changes by 3.5 million years ago. This provides further evidence of obligate bipedality in Australopithecus afarensis.

2 Table of Contents Abstract 1 Preface 3 Acknowledgements 4 Introduction 5 Materials and Methods 13 Description of Fossil 15 Results 19 Discussion 22 Conclusion 23 Future Work 24 References 25

3 Preface In late June 2008, I groggily made my way into the office of Bruce Latimer, then Director of the Cleveland Museum of Natural History. Having gotten off a plane from the United Kingdom just 12 hours before, I was about to start my internship as an Adopt-A- Student in the Department of Physical Anthropology at the museum. I had proposed a project for my internship, but was open to other work. To my great astonishment, Dr. Latimer reached into a safe behind his desk and pulled out a small bag with a tiny bone in it. He asked me what I thought it was, and I responded that it looked like a baby’s toe. He then informed me that it was 3.5 million years old. Holding this fossil in my for the first time will remain one of the most profound moments in my life. The odds of this project, and this thesis, existing are infinitesimal (see the Taphomony section), and I was extremely privileged to be able to conduct this research. This fossil was hidden in a piece of matrix from the A.L. 333 (First Family) site at Hadar, Ethiopia, but had remained undiscovered in the museum since the 1970’s. A geologist who was analyzing the sample at the Cleveland Museum of Natural History came across the bone, and took it to Dr. Latimer, asking if it was “anything important.” I imagine Dr. Latimer was as surprised as I was—this fossil had been hiding in the museum for more than 30 years! My summer project, and this resulting thesis, focuses on the analysis of one very tiny toe bone that tells a very big story.

4 Acknowledgements Most importantly, I would like to thank my advisor and mentor, Dr. Linda Marchant of Miami University, who directed this thesis, Dr. Scott Suarez of Miami University, the co- advisor, and Dr. Yohannes Haile Selassie, of the Cleveland Museum of Natural History, my external reader.

I would like to thank the Kirtlandia Society and the Cleveland Museum of Natural History for the opportunity to conduct this research. I am grateful to Bruce Latimer, former Director of the Cleveland Museum of Natural History, and currently professor in the department of Anthropology at Case Western Reserve University, for his advice and guidance throughout this project and to Lyeman Jellema for his help and patience with every aspect of my internship.

I would also like to thank Owen Lovejoy for his comments, Linda Marchant, Bill McGrew, Tim Webster and Mercedes Okumura for their continued support.

I would like to thank the Miami University Dean’s Scholars program for funding this project during the academic year, the Miami University Honors Department for thesis guidance, and the past, current, and future Miami Biological Anthropology Laboratory

(Upham 65) workers for academic and social support.

Last, but not least, I would like to thank my parents, John and Sandra Hillenbrand, for their support in all of my endeavors.

5 Introduction Bipedality and Upright walking is a fundamental trait that separates humans from the other great . Habitual bipedality (walking on two legs) is a relatively rare form of locomotion, and has appeared in a very limited number of lineages. Humans are the only extant with extensive morphological adaptation for striding bipedality. Skeletal changes affecting the skull, spine, , leg, and foot were required for the human lineage to make the transition from quadrupedal (four-legged) to bipedal locomotion (Stanford et al., 2009). Such adaptations are considered markers of early hominids, as the other significant characteristic of humans, increased , did not occur until relatively late in the human story (Lewin and Foley, 2004). ( troglodytes) are the closest living relatives of modern humans ( sapiens), and their anatomy represents an excellent basis of comparison to determine the morphological affinity of extinct hominids. Chimpanzee anatomy is adapted for a combination of arboreality (tree-climbing), suspensory behavior (brachiating), and mainly quadrupedal knuckle walking while on the ground. While the locomotor patterns of chimpanzees may or may not be analogous to those of the last common ancestor, chimpanzees certainly exhibit a suite of skeletal traits that differ significantly from those of modern humans, and thus can be used for comparison to find locomotory affinity in hominid fossils. Compared to chimpanzees, modern humans have a foramen magnum (the opening through which the spinal cord passes) nearer to the center of the basicranium, an S-shape spinal curvature (as opposed to C-shaped), a shorter, broader pelvis and a more angled femur with reorganized musculature, longer lower limbs with greater joint surface area, and a platform foot with an adducted, enlarged hallux (first toe) (Lewin and Foley, 2004). While evolution from quadruped locomotion to fully committed bipedality may seem extreme, the shift is not as great as it initially appears. The primate order is

6 characterized by the ability to sit upright, and some are able to walk on two legs for short periods of times. Still, the commitment to bipedality is unique to humans, and must result from selective pressures (Lewin and Foley, 2004). Prominent explanations for this shift include: Energy Efficiency—While walking bipedally is not more efficient than walking quadrupedally like a horse or dog does, it is more efficient than quadrupedal knuckle-walking. If hominids evolved from a knuckle-walking ancestor (Washburn, 1967, Begun, 1993, Richmond et al., 2001), a shift to an erect posture would have been a move toward greater efficiency when walking (Rodman and McHenry, 1980; Pontzer et al., 2009), though not necessarily greater efficiency when (Bramble and Lieberman, 2004). Thermoregulation—Bipedality has been posited as a more efficient way of dissipating heat from the brain (Falk, 1990) and avoiding sun exposure at midday (Wheeler, 1991). However, avoiding overheating could easily be a happy outcome of bipedality rather than a cause. Ecological Changes—The emergence of bipedality coincides with a major cooling and drying trend in Africa between 6 and 8 million years ago (Cerling et al, 1997). This produced the widespread savannah environment still seen in eastern Africa today.

Climate change caused an expansion of grassland and a decrease in forests, which would have resulted in greater distances between food trees. This could have favored bipedality as a more efficient way of traveling long distances. Bipedal hominids would have also had the advantage of being able to see over tall grasses, and thus both view food sources from further distances and spot and avoid potential predators (Stanford et al., 2009). While changing habitat clearly influences evolution, it is unlikely to be the sole cause of this major shift. Moreover, fossil remains of the earliest known hominids (see below) such as

7 ramidus (White et al., 1994, 1995), Ardipithecus kadabba (Haile- Selassie, 2001) and tchadensis (Brunet et al., 2002, 2005) have been found in closed wooded habitats, not savannah habitats. Dietary Benefits leading to locomotory behavior shifts—Tuttle (1981), Jolly (1970), and Hunt (1996) independently observed non-human primates that sometimes assumed a bipedal posture when feeding on fruit or nuts. While this behavior only lasted seconds at a time for a few minutes a day, these researchers suggest (differing slightly on details) that proto-hominids became more and more bipedal because of the feeding advantages this posture offered, and eventually became habitual bipeds. Mating Strategies—Lovejoy (1981) proposes a behavioral model that integrates interpretations of climate change, anatomy, and reproductive physiology as causes of bipedality. Arguing that humans and their hominid ancestors have a slow reproductive rate that would cause extinction without a way of increasing survival rates of offspring, Lovejoy suggests that a monogamous mating system increases infant survival due to male provisioning of females. For this system to be successful, males must be certain of paternity of the offspring, and females must be certain of continued male support. Climate change would require males to travel further to provision their offspring and mates, and bipedality would be a more efficient way of doing so. Not only would it allow males to travel greater distances, it would also free the arms for carrying food. Females did not display estrus, which necessitated males to stay nearby or return frequently to increase the chances of mating during the window of fertility. Provisioned by the male, the female could reduce interbirth intervals and decrease infant mortality. Though several aspects of this theory are difficult to prove and thus controversial, Lovejoy’s holistic approach provides a useful example of the many factors involved in hominid evolution.

8 These theories are not mutually exclusive, and it is likely that several selective pressures converged to cause the evolution of bipedality. An integrated theoretical approach combined with careful analysis of fossil evidence will lead to a better understanding of the evolution of bipedality. Taphonomy One of the reasons why the evolution of bipedality is so unclear is the paucity of the available fossil evidence. Fossil hominid remains are rare in the Plio- fossil record for a variety of reasons. Taphonomy is the study of all the transitional processes an organism undergoes between death and scientific recovery (Lyman, 1994). Often called burial science, taphonomy deals with both biological and geological processes that affect the probabilistic of deposition. A hominid (or any other ) may die from injury, disease, or predation, which may or may not leave signs on the body. After death, microorganisms accelerate decomposition, while and insects scavenge tissues. Remains are also exposed to the possibility of being scattered by weathering and trampling (Behrensmeyer and Hill, 1980). To become part of the fossil record, bones must be covered in sediment. In sediment burial, biological decomposition and scattering are interrupted, and minerals from the surrounding sediments are absorbed into the bone, replacing its original organic tissue. In order to be discovered, a fossil must eventually be re-exposed through geologic processes. Then it is once again vulnerable to weathering, trampling, and erosion. Only prompt discovery upon exposure will make it available for scientific research (Lyman, 1994). Fossil Evidence of Early Hominids Despite these challenges, fossil evidence of the human lineage is fairly abundant in its late history, and progressively sparser toward its origin. However, fossil hominids of any time period are very rare compared to those of other vertebrate taxa, likely due to the low population density of hominids and the relative size and fragility of their bones

9 (Lewin and Foley, 2004). Molecular genetic evidence suggests that there was an African monophyletic that includes , Pan, and Homo, and that the chimpanzee-human lineage split between 5 and 7 million years ago (Stanford et al., 2009). The first hominids are largely identified by indications of bipedality. The past twenty years have been extremely exciting, though confusing, for . The search for fossil evidence of the last common ancestor (LCA) between humans and chimpanzees, and evidence of the earliest in the human lineage has expanded both geographically and temporally. In 1994, White et al. announced the discovery of 17 hominid fossils from Ethiopia, dating to 4.4 million years ago, with extremely primitive morphology and limited hominid traits. Initially dubbed Australopithecus ramidus, the of the fossils was later changed to Ardipithecus based on their primitive attributes (White et al., 1994, 1995). In 2001, Haile-Selassie announced a subspecies, Ardipithecus ramidus kadabba, later elevated to Ardipithecus kadabba (Haile-Selassie et al. 2004), dated between 5.2 and 5.8 million years old. More publications addressing the bipedality of Ardipithecus are in preparation (Lovejoy, personal communication). In the meantime, other scientists have also discovered other potential early hominids. In 2000 tugenensis, a Kenyan fossil from the Tugen hills, was declared a unique genus and species by Senut et al. (2000), and was claimed as a human ancestor based on proximal femora and other fossils. At 6.1 to 5.8 million years old, it is the second oldest contender for the root of the human lineage (Senut et al., 2000). The oldest potential early human is biochronologically dated to between 6 and 7 million years ago and comes from Chad. Named Sahelanthropus tchadensis, this ancestral claim is based entirely on a taphonomically deformed cranium. Brunet et al. (2002, 2005) suggested the position of the foramen magnum indicates a habitual bipedal posture. However, the presence of lower limb fossils would increase the strength of these

10 claims. The evolutionary relationships between these early potential hominids and , the likely ancestors of humans, remain uncertain (see Figure 1). The earliest yet found, Australopithecus anamensis, is still poorly known. Fossils attributed to this genus were discovered in Kenya, and date between 3.8 and 4.2 million years old. Proximal and distal ends of the tibia suggest bipedality. The species has mix of primitive traits (such as canine size) and derived traits (such as the anatomy of the aforementioned tibia), and is currently considered to be basal to the genus Australopithecus (Leakey et al., 1995, Ward et al., 2001). Figure 1: Potential Hominid Evolutionary Tree (from Zimmerman, 2005)

11 The Australopithecus afarensis Story Before the discovery of Australopithecus anamensis, Australopithecus afarensis was considered a basal australopithecine, and possibly very close to the LCA. The specimen of A. afarensis, a mandible found in , , dates to 3.6-3.8 million years ago (Johanson et al., 1978). However, the vast majority of A. afarensis fossils have been discovered since the mid 1970’s at Hadar, Ethiopia (see Figure 2). The most spectacular of these, A.L. 288-1 (), is the 40% complete skeleton of an adult female whose anatomy combines an apelike cranial capacity and limb proportions with largely humanlike pelvic bones and lower extremities (Johanson et al., 1982). Several authors, (Johanson et al. 1982, Latimer and Lovejoy, 1990, White and Suwa, 1987) suggest the postcranial anatomy is indicative of fully modern bipedal locomotion, while others (Stern and Susman, 1983, Jungers, 1988) suggest that finger curvature and upper limb proportions that differ from modern humans mean that the species was not a fully modern biped. Figure 2: Hadar, Ethiopia

(GNU, FSF) The more recently discovered fossil DIK-1-1, also hailing from the Hadar Formation in Ethiopia, is highly relevant to this question. At 3.3 million years old, this

12 well-preserved juvenile specimen is nearly complete (the cranium, mandible, teeth, torso, and lower limbs are largely intact, and fragments of the upper limbs), though it is being recovered slowly due to encasement in matrix. Much information remains to be gained from this juvenile individual, who was only three years old at death (Alemseged, 2006). The fossil analyzed in this work comes from the A.L. 333 of Hadar, Ethiopia, popularly known as the “First Family” site (see Figure 2). This site contains fragmentary remains of at least 13 A. afarensis individuals and dates to 3.5 million years ago (Johanson et al., 1982). This specimen, an infant metatarsal from an individual of approximately 1 year old at death, gives further insight to the growth and development of Australopithecus afarensis and may shed light on the bipedality debate. Materials and Methods The original specimen, A.L. 333-?, is currently housed at the Physical Anthropology Laboratory of the Cleveland Museum of Natural History. All morphological observations made and measurements taken were on the original specimen. A.L. 333-? was compared to modern human (n=50) and chimpanzee first metatarsals (n=28) at a similar developmental stage (see Figure 3). All modern human and chimpanzee material was obtained from the Hamann Todd Osteological Collection at the Cleveland Museum of Natural History. The right first metatarsals of the comparative material were measured unless that side was not present or was damaged, in which case the left metatarsal was measured. Individual age for the human sample was as recorded at death; chimpanzee age was approximated using the dental eruption averages described by Conroy and Mahoney (1991) when possible. Based on the individual ages of the specimens in the comparative sample, A.L. 333-? is estimated to be approximately one year old at time of death. Eleven metric measurements were taken on each metatarsal with digital calipers according to standards established by Stock (2007) to document variation (see Table 1).

13 Table 1: Measurements (after Stock, 2007)

Measurement of Metatarsal Definition maximum length maximum length of first metatarsal maximum length measured with 1 caliper arm flush with the total length medial side of proximal articular surface distance from center of the articular surface to most distal articular length point on distal articular surface maximum diameter at midshaft midshaft calculated at 50% of the metatarsal minimum diameter at midshaft midshaft calculated at 50% of the metatarsal dorso-plantar diameter at midshaft midshaft calculated at 50% of the metatarsal transverse diameter at midshaft midshaft calculated at 50% of the metatarsal maximum diameter (dorso-plantar) of the proximal articular proximal maximum height surface maximum transverse diameter of the proximal articular proximal maximum breadth surface projected distance between the most plantar points on plantar diaphyseal chord proximal and distal articular surfaces diaphyseal curvature maximum subtense of the plantar diaphyseal chord

Description of the Fossil A.L. 333-?: immature (infant) right first metatarsal (see Figure 3) Preservation This specimen is an immature right first metatarsal in good condition. The distal surface and shaft are complete, but the proximal metaphysis is absent. It is completely preserved by permineralization. Morphology The bone has a short, wide proximal metaphyseal surface with minimal rugosity. There is slight abrasion on the dorsal side. The shaft is moderately tapered and

14 has moderate curvature. The distal surface has no metaphysis and is covered by a cartilaginous cap. Figure 3, a-e, illustrates the anatomy of A.L. 333-? compared to a modern infant human and infant chimpanzee.

Figure 3: Infant modern human, A.L. 333-?, and chimpanzee first metatarsal, from left to right.

a) Dorsal Aspect

15 b) Lateral Aspect

c) Medial Aspect

16 d) Ventral Aspect

e) Proximal Aspect

17 Results In early development, though morphologically different, modern chimpanzee and modern human first metatarsals did not show substantial differentiation in all measurements (midshaft diameter, diaphyseal curvature). However, ratios and proportions show noticeable differences between humans and chimpanzees. The chimpanzees in the sample had longer metatarsals that were narrower at the articular facet (see Figure 4). Within each species (humans, chimpanzees) the correlation value of the maximum length of the first metatarsal to the maximum width of the unfused proximal surface is strong, and the groups remain noticeably disparate. Therefore, the maximum length of the first metatarsal is an excellent predictor of the maximum width of the unfused proximal surface. When the fossil’s maximum length value is entered into the equation for the human trend line, the calculated value of the proximal surface falls . 829 away from the expected value for human, while when entered into the equation for the chimpanzee trend line, it falls 1.899 away from the expected value. This difference of more than 100%, shows the fossil is more humanlike than chimpanzee-like in maximum dimensions.

18 The shape of the proximal surface also differed significantly; the ratio of the proximal height of the proximal surface to its width was greater than one in chimpanzees and less than one in humans (see Figure 4). This is particularly visually striking (see Figure 3e). A.L. 333-? groups with the human specimens in both of these measurements.

19 Discussion

It is not surprising that human and chimpanzee infants do not differ in all traits measured, as morphological similarities are to be expected in closely related taxa, particularly at an infant stage. However, the morphology of the human first toe is unique (Langdon, 2005) because every other extant primate has an opposable first toe (Latimer and Lovejoy, 1990). Articular anatomy of the first toe strongly distinguishes African apes from modern humans, and thus is a particularly important trait to analyze in fossil hominid material.

20 The relatively and absolutely small size of human toes is essential for walking, where the long, grasping toes of climbing primates are a hindrance to bipedal locomotion. The human first toe, instead of grasping, has been converted to a stout, immobile structure that supports the entire body weight during the final thrust of the walking gait (Langdon, 2005). As shown pictorially in Figure 3(a-e) and graphically in Figure 4, the Australopithecus afarensis fossil (A.L. 333-?) is closer in size to human fossils of a similar age than it is to chimpanzees. The non-grasping human first toe is in line with the other toes, unlike the grasping first toe of other primates. This is most evident in the joint between the first metatarsal and the medial cuneiform, one of the “most functionally telling features of the hominoid pedal skeleton” (Latimer and Lovejoy, 1990: 125). While curved in other primates, the surface of this joint in humans has been flattened (Langdon, 2005). The proximal articular surface of the first metatarsal in humans has a marked invagination that locks the first metatarsal with the medial cuneiform, which aids in inhibiting movement (Latimer and Lovejoy, 1990). Unfortunately, this fossil individual was too young at death to have a fused first metatarsal and the metaphysis was not recovered, so the joint surface cannot be analyzed. However, the proximal end of an adult first metatarsal (A.L. 333-54) was previously recovered from this site (Latimer et al., 1982). Latimer and Lovejoy (1990) suggest that the articular surface of A.L. 333-54 is extremely similar to that of humans, On the other hand, Proctor et al. (2008), based on microscribe analysis of 17 distinct landmarks, concluded that A.L. 333-54 is morphologically similar to the articular surface of metatarsals in other apes. However, Proctor et al. (2008) did not use the original fossil material. The most obvious anatomical trait separating an articulated human first tarsometatarsal from that of an is the angle at which it articulates. In humans, “the shaft of the first metatarsal has been rotated so that the phalanges now face the ground, as

21 in other toes” (Langdon, 2005: 109). As shown in Figure 6, this is highly visible even at a young age. Even when the metaphysis and articular surface are not present, the rotation of the bone is visibly present (see Figure 3). The shape of the proximal end of the first metatarsal appears rotated in humans, and in the fossil, relative to the chimpanzee specimen (Figure 3e). This trait was metrically analyzed by comparing the proximal height and width of the proximal surface of infant metatarsals. In infant chimpanzees, the height to width ratio was greater than one, while in human infant this ratio was less than one, indicating metatarsal rotation. The fossil also exhibited a proximal surface height to width ration of less than one (See Figure 5). Figure 6: Articulated infant human (left) and infant chimpanzee (right) feet

The suite of traits exhibited by this fossil described above suggests that Australopithecus afarensis did not have an opposable hallux. This is in accord with the findings of previous researchers on related fossils (Latimer and Lovejoy, 1990, McHenry and Jones, 2006). However, more questions emerge from these data. For example, would

22 it be necessary to carry an infant who could not grasp with her or his hind limbs? What percent of an adult’s activity budget was spent in bipedal posture or locomotion? Insight into the first question may emerge when a more complete description of the Australopithecus afarensis juvenile DIK-1-1 is available.

Conclusion Australopithecus afarensis had a humanlike hallucal tarsometatarsal joint. Observation of this feature in an immature individual supports this interpretation. Presence of this diagnostic anatomy in an infant suggests bipedality as its primary locomotory pattern. This is relevant to human evolution, as Australopithecus afarensis is widely considered to be ancestral to modern humans (Figure 1). Human ancestors, functionally bipedal at 3.5 million years ago, still have many secrets to reveal, but further analysis and discoveries will help to resolve current questions.

23 Future Work I am currently preparing a manuscript on this research to be submitted for publication in a scientific journal, most likely the Journal of Human Evolution. This research was recently presented at the 78th annual meeting of the American Association of Physical Anthropologists, where a colleague interested in foot development contacted me to discuss this project and to suggest the possibility of collaborative research on DK-1-1, whose foot bones have not yet been analyzed. Dan Proctor (cf. Proctor et al., 2008) is conducting further research on the potential for analysis of the articular surface of metatarsals 2-5, which will further highlight strengths and weaknesses of this method (pers. comm.). Upon graduation, I intend to continue research in human skeletal anatomy and bone biology. The 2009 Joanna Jackson Goldman Memorial Prize will allow me to spend one year in the Duckworth Laboratory at the Leverhulme Centre for Human Evolutionary Studies (Department of Biological Anthropology, University of Cambridge) researching a different topic in human osteology: osteoporosis. Though this research may seem unconnected, I feel that understanding the dynamics of the human skeletal system is integral to understanding both fossil evidence and modern human evolution. Upon completion of my Goldman project, I intend to enter graduate school in hopes of earning a doctoral degree in anthropology and eventually attaining a teaching/research position.

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