Patterns of Variance and Covariance in Anthropoid Limb Proportions: Implications for Interpreting the Hominin Fossil Record

by Vance C. R. Powell

B.A. in Anthropology, December 2011, University of South Florida M.Phil. in Hominid Paleobiology, June 2016, The George Washington University

A Dissertation submitted to

The Faculty of The Columbian College of Arts and Sciences of the George Washington University in partial fulfillment of the requirements for the degree of Doctor of Philosophy

August 31, 2018

Dissertation directed by

Bernard A. Wood University Professor of Human Origins

The Columbian College of Arts and Sciences of The George Washington University certifies that Vance C. R. Powell has passed the Final Examination for the degree of

Doctor of Philosophy as of May 11, 2018. This is the final and approved form of the dissertation.

Patterns of Variance and Covariance in Anthropoid Limb Proportions: Implications for Interpreting the Hominin Fossil Record

Vance C. R. Powell

Dissertation Research Committee:

Bernard A. Wood, University Professor of Human Origins, Dissertation Director

Sergio Almécija, Assistant Research Professor of Anthropology, Committee Member

W. Andrew Barr, Visiting Assistant Professor of Anthropology, Committee Member

Dedication

This dissertation is dedicated to all those instructors who are responsible for instilling in me a love of science and the motivation to pursue an advanced degree in a STEM field.

To my high school science instructor, Robert Geach, who encouraged the friendly rivalry for best grades between myself and classmate Nia Mapp. Despite being a Christian private school instructor, Mr. Geach always answered questions about evolution directly and honestly.

To my instructors from the University of South Florida, Melissa Pope, Edgar Amador,

Michelle Raxter, and Thomas Pluckhahn. For me, these individuals laid the founding knowledge about the four fields of anthropology, and I thank them for dealing with my endless questions.

To my family, my mother, my sister Nikki (aka, Peyton), my brothers Khnum (aka,

Mark) and Terry, and my partner Desiree. Without your influences early in my life, and your encouragement and support throughout my academic career, I would not have made it this far.

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Acknowledgements

I would like to begin by thanking my graduate school advisor, Dr. Bernard A.

Wood. Bernard’s is among the first paleoanthropological research with which I became familiar during undergraduate studies. I will never underestimate how fortunate I am to have worked under his guidance, and to have had his support during the emotionally, intellectually, and financially trying graduate school experience. I have not been an easy student to work with, but I am immensely grateful.

I would also like to thank my other committee members and examiners, Drs.

Sergio Almécija, W. Andrew Barr, Ashley Hammond, and Adam Gordon, who, despite having no obligation to me as an individual or student, dedicated countless hours to reviewing, editing, and offering comments on my thesis. In the time we worked together I have learned more about producing good research than I can account for here.

I also acknowledge the students and other faculty at the George Washington

University (GWU), and especially in the Center for the Advanced Study of Human

Paleobiology (CASHP). Like my committee members, many offered ideas to help me form my thesis topic, reviewed drafts of other projects, and others offered their companionship. I am particularly thankful for the latter, as the last 5 and a half years, during which I’ve seen my family only very rarely, have proven to be particularly lonely, especially considering the “social butterfly” I had frequently been described as during my undergraduate.

Finally, I would like to thank the George Washington University and the National

Science Foundation, which funded my research and studies.

Abstract of Dissertation

Patterns of Variance and Covariance in Anthropoid Limb Proportions: Implications for Interpreting the Hominin Fossil Record

Interpreting the taxonomic and behavioral implications of variation in the inferred limb proportions of fossil hominin taxa is contingent upon assessing how much variation exists in extant primate taxa and, by extension, how much of that variation is associated differences in their locomotor behaviors. However, the majority of evidence linking limb proportions to behavior in extant primates is based on taxonomically-restricted samples, or on species means as opposed to individual values, or does not account for field observations that capture the complexity of locomotor behavior in a primate taxon (see

Napier & Napier, 1967; Fleagle, 1988; see also Preuschoft, 2002). With regards to extinct taxa, the problem is compounded by a necessary reliance on relatively few associated skeletons, most of which are incomplete, or fragmented or both.

This thesis addresses the aforementioned issues using a) multivariate methods to quantify the relationships between limb proportions and behavioral repertoires in extant anthropoids; b) machine-learning methods to select relevant extant models with which to interpret the limb proportions of extinct taxa; and c) resampling methods to evaluate hypotheses regarding major adaptive shifts in inferred locomotor behavior.

Table of Contents

Dedication iii

Acknowledgements iv

Abstract of Dissertation v

List of Figures viii

List of Tables ix

Chapter 1: Introduction 1 Extant primate locomotion 3 Primate limb proportions 4 Inferring behavior from fossil hominin 5 skeletons Thesis outline and goals 18

Chapter 2: Phylogenetic and functional signals of anthropoid limb 21 proportions Abstract 21 Introduction 22 Materials and Methods 27 Sample 27 Analytical methods 29 Results 38 Discussion 46

Chapter 3: Are extant apes appropriate models for hominin limb proportions? 75 Insights from machine learning analyses Abstract 75 Introduction 77 Materials and Methods 80 Extant training sample 80 Fossil sample 80 Analytical methods 84 Results 89 Discussion 91

Chapter 4: Evaluating hominin locomotor grades 113 Abstract 113

Introduction 114 Materials and Methods 117 Fossil specimens 117 Comparative sample 118 Analytical methods 118 Results 121 Discussion 125 Chapter 5: Conclusion 135

Bibliography of References 141

Appendix 181

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List of Figures

Chapter 2 figures 54

Figure 2.1. Measurements 54

Figure 2.2. Phylogenetic tree 55

Figure 2.3 a&b. Box plots 56

Figure 2.4 a&b. PCA 58

Figure 2.5 a-c. 2-BPLS 60

Figure 2.6. Phylomorphospace 63

Chapter 3 figures 98

Figure 3.1 a-d. CART decision trees 98

Figure 3.2. Comparative PCA 102

Figure 3.3 a&b. Comparative box plots 104

Chapter 4 figures 129

Figure 4.1 a&b. Genus distributions 129

Figure 4.2. Putative “grade” distributions 131

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List of Tables

Chapter 2 tables 64

Table 2.1. Anthropoid sample 64

Table 2.2. Average percent inter-observer error per taxon 65

Table, 2.3. Tukey’s HSD results 66

Table 2.4. PCA loadings 67

Table 2.5. Percent locomotor behavior 68

Table 2.6. Percent positional behavior 70

Table 2.7 a-c. 2-BPLS scores 71

Table 2.8. Phylogenetic signal 74

Chapter 3 tables 106

Table 3.1. CART validation results 106

Table 3.2. Published fossil sample 107

Table 3.3. Fossil regression estimates 108

Table 3.4 a-d. Regression formulae 109

Chapter 4 tables 132

Table 4.1. Extant sample 132

Table 4.2. Fossil specimens 133

Table 4.3. Arithmetic index differences and percentile values 134

Chapter 1: Introduction

Two of the major competing hypotheses about variation in the inferred limb length proportions of hominins have posited either taxic diversity, or major adaptive shifts from more ape-like to more modern human-like ancestors with occasional

“reversals” to more ancestral phenotypes (Hartwig-Scherer and Martin, 1991; Wood and

Richmond, 2000; Richmond et al., 2002; Harcourt-Smith and Aiello, 2004; Berger, 2010;

Harcourt-Smith, 2015). However, testing hypotheses about the significance of variation for interpreting fossil behavioral differences is hampered by uncertainty about hominin alpha taxonomy (i.e., the number of taxa represented in the hominin fossil record) and how morphology (e.g., limb proportions) is related to locomotor behavior in extant taxa

(see Wood & Boyle, 2016; Villmoare, 2018; Hunt et al., 2016). To address these points, comparative approaches are used to investigate the relationship between variation in limb proportions and behavior in extant primate taxa, and then these relationships are used as reference points against which to interpret the variation among fossil hominins (see

Ackermann & Smith 2007).

Research addressing these points must contend with the fact that most of the critical fossil evidence about the limb proportions of early hominins comes from incomplete and fragmentary skeletons (e.g., OH 62, BOU-VP 12/1) (Johanson et al.,

1987; Asfaw et al., 1999; see also Harcourt-Smith, 2007). Moreover, some of these skeletons, such as those assigned to Homo habilis (OH 62) and Australopithecus garhi

(BOU-VP-12/1), suggest reversions to more primitive or ‘ape-like’ body proportions

(e.g., relatively longer forelimbs and radii) when compared to Australopithecus afarensis

(Johanson et al., 1987; White, 1980; White et al., 1981; White & Suwa, 1987; Asfaw et

1 al., 1999; but see Stern & Susman, 1983; Tuttle, 1984, 1990, 1991; and Harcourt-Smith

& Hilton, 2005 for alternative interpretations). However, those claims have not been carefully evaluated against appropriate comparative samples to determine if the fossil variation actually exceeds extant variation (White, 2003; Ackermann & Smith, 2007).

Others have suggested that limb proportions might be informative about major changes in locomotor behavior within the hominin clade. For instance, Wood and Collard (1999) suggested that the major locomotor adaptations of Ardipithecus, Australopithecus,

Paranthropus, and Homo habilis are characterized by facultative or habitual bipedalism and arboreal competence, whereas that of later Homo (i.e., Homo erectus and subsequent taxa) is characterized by obligate bipedalism (Wood and Collard, 1999; Collard 2002).

Quantitative approaches capable of addressing this claim were not implemented until

Richmond et al., (2002), which assessed fossil variation of limb proportions in the context of variability in extant hominoid species. Richmond and colleagues, however, did not address overall traditional limb proportions (and instead focused on humerofemoral length and shaft proportions), or use comparative samples that only captured genus- or grade-level variation.

This thesis, which builds on these previous efforts, develops methods that estimate how much variation should be accepted within a fossil hominin genus and within a fossil hominin locomotor grade (see Wood and Collard, 1999; Collard, 2002).

The remainder of this introduction focuses on: 1) hypotheses about categories of extant primate locomotor behavior and morphology, 2) the postcranial evidence supporting hypotheses of categories of fossil hominin locomotor behavior, and 3) the goals of the dissertation.

EXTANT PRIMATE LOCOMOTION

The relationship between limb proportions and locomotor behavior has been recognized since at least Mollison (1911), and has thereafter been developed, especially influentially by A.H. Schultz’s observations about variation in the limb proportions of extant primates (e.g., 1930, 1933, 1937). Two of the most influential subsequent contributions to these discussions were Napier’s “Evolutionary aspects of primate locomotion” (1967), and observations in Napier and Napier’s Handbook of Living

Primates (1967). The latter proposed four primate locomotor categories (i.e., vertical clinging and leaping, quadrupedalism, so-called “brachiation”1, and bipedalism; N.B.,

“climbing” is not discussed), plus various locomotor “sub-types” that further distinguish forms of quadrupedalism and the since-revised “brachiation” category. For each of the first three locomotor modes the authors provide ranges of corresponding intermembral indices (i.e., the forelimb/hindlimb*100): 50-80% for vertical clingers and leapers, 80-

100% for quadrupeds, 100-150% for brachiators. These important early contributions, which were generally supported by later research (e.g., Fleagle, 1988), have been fundamental to discussions about the inferred locomotor behaviors of fossil hominin taxa

(Asfaw et al., 1999; Richmond et al., 2002; Lordkipanidze et al., 2007; Lovejoy et al.,

2009).

The years following the contributions of Mollison, Schultz, and Napier saw continued interest in describing and categorizing the locomotor behaviors of extant primates, as well as focused kinematic studies of localized and complex anatomy (see

1 True brachiation, characterized by pendulous and ricochetal swings, has since been distinguished from other kinds of suspensory behavior and restricted to the Hylobatidae (see Hollihn, 1984; Chang et al., 2000).

3 below). With the introduction of more precise locomotor categories, researchers began to pose questions regarding how often and how long taxa used the different locomotor modes within the repertoire of that taxon (see Preuschoft, 2002). Napier and Napier’s

(1967) patterns of locomotor variation were generally corroborated, but other work suffered from observational biases and lack of descriptive continuity among researchers

(particularly regarding categories like “climbing”), resulting in incompatible estimates of behavioral frequencies from one researcher to the next (see Prost, 1965; Hunt et al.,

1996). Addressing this shortcoming, Hunt et al., (1996) detailed 32 positional modes subdivided into 74 locomotor sub-modes and 52 postural sub-modes. Later, Hunt (2016) reported frequencies of use and characteristic morphologies for postural modes in a large sample of extant primates. The standardized locomotor mode descriptions provided by

Hunt are invaluable resources used in this thesis to quantify the relationships between traditional limb proportions and locomotor modes (see Chapter 2).

PRIMATE LIMB PROPORTIONS

Napier and Napier (1967) described the relationships between limb proportions and locomotor behavior in primates in terms of mechanical function (see also Napier &

Napier, 1967; Fleagle, 1988; Preuschoft, 2002). In summary, taxa that rely on the use of the forelimbs to propel themselves between branches (i.e., brachiation) have longer forelimbs (relative to hindlimbs) that allow them to reach further and perform pendulum- like motions. Conversely, those taxa that employ more leaping behaviors tend to have relatively longer hindlimbs, which enable them to maintain contact with substrates for a longer period of time and thus generate greater propulsive forces during these maneuvers.

Quadrupeds, on the other hand, have limbs of approximately equal length, allowing the

4 forelimbs and hindlimbs to work together on horizontal substrates and more equally distribute body weight. Arboreal quadrupeds have relatively shorter limbs in order to keep their centers of mass low and near the substrate for stability on precarious supports.

Terrestrial quadrupeds have longer limbs that lengthen the stride and reduce the energetic costs of locomotion. In obligate bipeds (the only extant representative of which is Homo sapiens) the hindlimbs are elongated relative to forelimbs to allow for a longer stride (see also Fleagle 1988). Thus, taxa practicing forelimb-dominated behaviors have generally longer forelimbs, and those practicing hindlimb-dominated behaviors have generally longer hindlimbs. However, the relationships between primate limb proportions and locomotor behavior described by the Napiers were not quantified. Instead, many studies have focused on variables such a joint size, shaft robusticity, bone curvature, and trabecular architecture, in part because these variables are more responsive to in vivo loading regimes and thus may be more informative of actual behaviors during life

(Schafﬂer et al., 1985; Ruff, 1987, 1988, 2002; Demes and Jungers, 1989, 1993; Ruff and

Runestad, 1992; Jungers and Burr, 1994; Rafferty and Ruff, 1994; Runestad, 1997;

Jungers et al., 1998; Connour et al., 2000; Llorens et al., 2001; Kimura, 2003; Marchi,

2005; Yamanaka et al., 2005). Limb length proportions, and their correlates, however, should be quantitatively evaluated in extant primates to understand their variation in fossil hominins.

INFERRING BEHAVIOR FROM FOSSIL HOMININ SKELETONS

This section summarizes the available skeletal evidence about limb proportions that has been used to generate hypotheses about the locomotor behavior of fossil hominins. Only those taxa that are represented by associated skeletons, or that are of

5 particular importance for understanding the evolution of hominin grades, are discussed.

Thus, Paranthropus and archaic humans (e.g., Homo heidelbergensis, H. neanderthalensis) are not discussed.

Putative hominins

Three putative hominins from the late Miocene and Early Pliocene of Africa,

Sahelanthropus tchadensis from Chad at 7 Ma (Brunet et al., 2002), Orrorin tugenensis from Kenya at 5.7-6 Ma (Senut et al., 2001), and Ardipithecus ramidus from Ethiopia at

4.4 Ma (Lovejoy, 2009; Lovejoy et al., 2009) provide the earliest purported evidence of bipedalism in the hominin lineage. Of these, only O. tugenensis and Ar. ramidus are represented by any long bone material.

Sahelanthropus tchadensis

Sahelanthropus tchadensis is known from a remarkably complete, though fragmented and deformed, hominin cranium (TM 266-01-060-1) that preserves the alveolar process for the incisors, the roots of the premolars, and molar and premolar crown fragments. TM 266 also preserves portions of the basicranium and foramen magnum, the latter of which is oriented at 95o to the orbital plane in virtual reconstructions provided by Zollikofer and colleagues (2005). This angle is similar to that observed in H. sapiens, Au. afarensis (AL 444-2) and Australopithecus africanus (Sts 5), and is indicative of orthograde (i.e., upright trunk) posture in which the head is held directly above the cervical vertebrae during bipedal locomotion. This contrasts with other primates that have more acute angles between foramen magnum and orbital plane that reflects the more horizontal orientation of the cervical vertebrae relative to the basicranium. Zollikofer et al. (2005) also interpret the flat nuchal plane and downward

6 lipping of the nuchal crest of TM 266 (the result of nuchal musculature pulling downward on the occipital region to hold the head erect) as additional evidence for bipedalism. This review focuses on postcranial morphology, but at present TM 266 is regarded as the earliest potential evidence of bipedalism in hominins.

Orrorin tugenensis

Orrorin tugenensis (holotype BAR 1000’00) is a slightly younger (c. 6 Ma;

Pickford and Senut, 2001; Sawada et al., 2002) potential hominin that is known from several unassociated mandibular and maxillary teeth, which distinguish the taxon from later Australopithecus species, as well as a partial distal humerus, proximal manual phalanx, and three partial proximal femora (one of which, a left femur, retains the femoral head: BAR 1002’00). Evidence for bipedalism is found in the surface and cross- sectional morphology of BAR 1002’00, including cortical bone distributions around the femoral neck that are thicker inferiorly to counter downward forces of body weight during bipedal locomotion, supposedly unlike that of African apes (Galik et al., 2004; but see Rafferty, 1998; Stern and Susman, 1991; Stern 2000 for alternate interpretations), a femoral head-to-shaft ratio intermediate to modern humans and Australopithecus

(Richmond et al., 2008), presence of an intertrochanteric groove for the obturator externus tendon, and a short femoral neck (Galik et al., 2004; but Senut says it is

“elongated”). Dispute persists over whether some of these features are diagnostic of bipedalism (e.g., similar cortical bone distribution and intertrochanteric groove may be found in other primates, and the latter is not found in all bipeds; Stern & Susman, 1991;

Rafferty 1998; Stern 2000), and other aspects of the BAR 1002’00 femur are interpreted

7 as similar to Miocene apes (Almécija et al., 2013), but the general consensus is that O. tugenensis was at least partially bipedal.

Forelimb features (e.g., robust humeral brachioradialis flange and curved proximal manual phalanx) associated with BAR 1000’00 also suggest a capable climbing repertoire comparable to that of Pan (Richmond & Jungers, 2008). Considering the derived evidence for bipedalism in the femur and the primitive climbing features of the humerus and phalanx, Richmond et al. (2008) interpret O. tugenensis as an example of an australopith-like locomotor repertoire characterized by bipedalism and climbing behaviors.

Ardipithecus ramidus

The most complete potential hominin associated skeleton belongs to the 4.4 Ma

Ar. ramidus (ARA-VP-6/500), discovered in the Middle Awash of Ethiopia (Lovejoy,

2009; Lovejoy et al., 2009). Nine long bones belonging to ARA-VP-6/500 were recovered, in addition to a fragmented face, anterior maxillary fragment, anterior mandibular fragment, fragmented cranium, several teeth, and nearly complete right and left hands and feet (i.e., carpals, metacarpals, tarsals, metatarsals, and phalanges). No humerus has been recovered for ARA-VP-6/500, but humerus length was regressed from the conspecific ARA-VP 7/2 using relative forelimb proportions (see Lovejoy et al., 2009 supplementary information). The preservation of the right and left radii allowed estimates of hominin inter-limb proportions.

When on the ground, its discoverers interpreted Ar. ramidus as a biped that could balance its weight while walking without having to shift laterally as extensively as extant apes (Lovejoy et al., 2009; Lovejoy, 2009). Its pelvis is shorter and broader than the

8 pelves of extant apes, with a laterally flared ilium that repositions the gluteal muscles as in later hominins. Several features of the tarsals and metatarsals suggested to the researchers that the foot of Ar. ramidus was rigid like that of monkeys and humans, and dissimilar from the derived, pliant condition of the African apes (Lovejoy et al., 2009).

However, like the African apes, the hallux remained abducted for climbing, a feature considered lost by the time of Au. afarensis (Latimer and Lovejoy, 1990; but see Clarke and Tobias, 1995 who suggest the later Au. africanus retained a partially opposable hallux). Likewise, the ischia and femoral surface morphology are more similar to extant

African apes or Miocene apes (e.g., tall ischia, positioning of the linea aspera and femoral gluteal complex). On the other hand, Ar. ramidus had approximately balanced intermembral proportions, like an arboreal quadruped and intermediate between modern humans and extant apes. Also suggesting arboreal locomotor habits, the hands and wrists of Ar. ramidus have been interpreted as Ekembo2-like adaptations to above-branch quadrupedalism while in the trees, due to the primitive retention of a flexible wrist and long, curved phalanges. The postcranium of Ar. ramidus is thus interpreted as representing adaptations for facultative bipedalism on the ground combined with substantial arboreal ability (see also Prost, 1980; Lovejoy, 2009; Lovejoy et al., 2009; see also Harcourt-Smith, 2007). While some similarities with Australopithecus are evident,

Ardipithecus seems to have exhibited a unique locomotor repertoire. If Ardipithecus did employ a locomotor repertoire distinct from Au. afarensis, it must be considered just how

2 Ekembo is the revised generic allocation for the postcrania and other specimens previously allocated to Proconsul (see McNulty, et al., 2015).

9 different it may have been, and whether both taxa belong within a single grade as had been suggested before the discovery of ARA-VP-6/500 (Collard, 2002).

Australopithecus

Australopithecus afarensis

The locomotor affinities of Australopithecus species have been the subject of strong debate for decades, due primarily to the morphological diversity of the locomotor skeleton in taxa of this genus (Ward, 2002; Haile-Selassie et al., 2010; Harcourt-Smith,

2007). The focus of this thesis is limb proportions, but the overall postcranial evidence for behavior in this genus is briefly reviewed. Australopiths exhibit a mosaic of primitive

(i.e., ‘ape-like’) and derived features that suggest increased reliance on bipedalism compared to other African apes (i.e., Pan and Gorilla), but the shoulders, pelvic girdles, feet, and major long bones also suggest arboreal capability. Most of what is known about the early Australopithecus postcranium derives from the associated skeleton A.L. 288-1

(A. afarensis, “Lucy”, ca. 3.2 Ma; Johanson et al., 1978; Johanson et al., 1979; Walter,

1994). This skeleton represents the majority of bony elements in the body, including craniomandibular fragments, vertebrae and ribs, a nearly complete hemipelvis, sacrum, nearly complete left femur, broken but nearly complete humeri, as well as fragmented radii, ulnae, and tibiae. Other regions of the postcranium (e.g., scapula, hands, and feet) are known from other specimens attributed to Au. afarensis (e.g., the Hadar material, and

DIK-1-1; Drapeau et al., 2005; Green et al., 2012).

Much of the postcranial skeleton is consistent with the hypothesis that Au. afarensis was a habitual biped. For instance, most authors interpret the feet as lacking an opposable hallux (Latimer and Lovejoy, 1990; but see Harcourt-Smith et al., 2004). This

10 conclusion is supported by the Laetoli footprints, which appear to have short toes and an adducted hallux (Harcourt-Smith, 2005). But some features of the Au. afarensis cheiridia

(i.e., hands and feet) also imply a strong arboreal behavioral component. The manual and pedal phalanges of the Hadar specimens are long, and curved with strong flexor ridges, which are epigenetic results of climbing and suspensory behaviors in vivo (Marzke, 1983;

Stern & Susman, 1983; Richmond, 2007). It is worth noting here that Clarke and Tobias

(1995) interpret the contemporary Stw 573 (see Granger et al., 2015) as retaining an opposable hallux, which if correct indicates that “primitive” hominin phenotypes persisted into the time of Au. afarensis.

The pelvis of A.L. 288-1 exhibits some of the most convincing evidence for bipedalism. The pelvis is arguably similar to modern humans in that it is short, wide, and deep antero-posteriorly (versus other primates), with a large, upright-weight-bearing sacrum translated far behind the enlarged acetabulum, and a prominent anterior inferior iliac spine implying a strong leg extensor (i.e., rectus femoris) as in modern humans

(Harcourt-Smith, 2007). However, the iliac flaring (which helps to reposition the gluteal muscles antero-laterally to act as hip abductors during locomotion) is greater than that observed in later Homo and modern humans, and may have served to provide support to an ape-like, cone-shaped rib cage with a large inferior thoracic aperture. The functional relevance of the extreme iliac flaring is debated, but the other features are commonly thought to assist in balancing the trunk vertically above the legs during locomotion, and consensus on the overall Au. afarensis pelvic morphology is adaptation for bipedal locomotion (Lovejoy, 2000; Ward, 2002).

Features of the hindlimb are central to discussions about hominin locomotion because, in bipeds, the hindlimb alone contacts the substrate during walking, and thus it should most directly reflect relevant adaptations and epigenetic alterations. Proximally, the femur of Au. afarensis has many traits that suggest habitual bipedalism, including a long neck (although this may be related to trunk girth) and inferiorly thickened cortical bone in the femoral neck as exhibited by A.L. 128-1 and the Maka femora (Lovejoy et al., 2002). On the other hand, attachments on the femoral greater trochanter for the gluteus minimus muscles (important for walking in extant humans) are more ape-like, with a proximo-distally elongated insertion, contra the localized, ovoid insertion in modern humans. The knee region also displays a mosaic of primitive and derived morphology (Ward, 2002). For example, the A.L. 129 knee (i.e., distal femur and proximal tibia) has a strong bicondylar angle, which is an epigenetic feature developed by frequent bipedal loading of the knee (Taieb et al., 1974; ShefelbIne & Tardieu, 2002).

Likewise, the talar surface of the distal tibia is horizontal and perpendicular to the major axis of the tibia, implying that the knee passes directly over the center line of the foot, unlike the inclined talar surface of apes that shift their weight during bipedalism (Ward,

2002). Conversely, the tibial insertions for gracilis, semitendinosus, and sartorius are more similar to the apes.

The forelimb of Au. afarensis also implies considerable arboreal competence. The lateral trochlea of the distal humerus is large and well-developed, and the glenoid fossa of the DIK-1-1 scapula is cranially-oriented (Alemseged et al., 2006; Green et al., 2012; however, Haile-Selassie et al., 2010 recovered an Au. afarensis male scapula, KDS-VP 1-

1, that is more similar to the modern human condition). The former trait helps prevent

12 dislocation of the elbow during climbing and suspension, while the latter pre-disposes the arm for reaching above the head during the same behaviors. There is also some debate over the proposed presence of a “dorsal ridge complex” of the radius that helps lock the wrist to prevent hyperextension injuries during knuckle walking, as is seen in the knuckle walking African apes (Richmond and Strait, 2000), but considering the lack of other knuckle walking adaptations other authors dispute its relevance (Dainton, 2001; Lovejoy et al., 2001).

Based on A.L. 288-1, the within- and between-limb proportions of Au. afarensis suggest derived, bipedally-adapted, lower limbs and primitive, arboreally-adapted, upper limbs. The femora were short compared to later hominins, but the lower limbs were longer in comparison with the upper limbs than is the case in extant hominoids (Ward,

2002). It is reasonable to conclude, then, that Au. afarensis used its hindlimbs differently than its presumably more ape-like ancestors. On the other hand, within the limbs, both crural and brachial proportions remained primitive. This pattern of limb proportions is distinct from that of modern humans, and although the exact behavioral significance is unclear, it is not suggested that they preclude some form of bipedalism (Jungers, 1982;

Wolpoff, 1983). The unique pattern of primitive and derived features has led authors to conclude that Australopithecus used a form of bipedalism dissimilar to anything seen in modern hominoids, although many dismiss the bent-knee-bent-hip bipedalism suggested by some (see Stern & Susman, 1983; Susman, 1984).

Australopithecus garhi

Australopithecus garhi is the name currently assigned for the c. 2.5 Ma fossil material recovered from the Bouri Hata formations of Ethiopia (Asfaw et al., 1999).

Several individuals belonging to this group have been recovered since 1990, but the most important for this thesis is the partial skeleton BOU-VP-12/1, which preserves “fairly complete shafts of a left femur and the right humerus, radius, and ulna […] partial fibular shaft, a proximal foot phalanx, and the base of the anterior portion of the mandible”

(Asfaw et al., 1999). According to the authors, the long bones are complete enough that lengths can be accurately estimated. Using their estimates, Asfaw et al., reported that while the humerofemoral ratio is an indication of a human-like elongation of the femur, the elongated forearms meant that the brachial ratio fell toward the higher range of Pan and overlapped with Pongo. While some authors have disagreed with the estimated brachial ratios (Reno et al., 2005), if taken at face value such primitive upper limb proportions indicate arboreal capabilities, and are potential evidence for a reversal from an earlier, more modern human-like bauplan (see Richmond et al., 2003), but the condition of BOU-VP-12/1 makes estimates of its limb proportions unreliable.

Australopithecus sediba

Unfortunately, no fore- and hindlimb elements are complete enough to estimate intermembral limb proportions from a single individual of Au. sediba (Berger et al.,

2010). The adult female MH 2 skeleton lacks sufficient hindlimb material to estimate either femur or tibia length, and too few long bone lengths of the juvenile MH 1 are published to use it as a model to regress missing lengths for MH 2. For this reason, Au. sediba is excluded from the analyses of this thesis. However, this taxon is potentially important for assessing the diversity of locomotor form and presumed function in hominin evolution. For example, other aspects of the postcranial morphology of Au. sediba, such as a gracile calcaneal tuber with a superiorly positioned lateral process

(similar to hominoids), and a convex fourth metatarsal base, which together indicate that

Au. sediba would have landed simultaneously on the heel and lateral edge of the flexible foot, further indicate a unique form of bipedalism characterized by a hyper-pronated foot with a mid-tarsal break (DeSilva, 2013). Arboreal proficiency is demonstrated by a similar pattern of forelimb morphology as that observed for A.L. 288-1, including cranially-oriented scapular glenoid fossae, high brachial index (in the range of Au. afarensis and the later Homo habilis, and at the upper ranges of H. sapiens and G. gorilla), distal humerus trochlear morphology, as well as the proximal and distal ulnar morphology. In combination these features suggest bipedalism combined with an even stronger signal of arboreal locomotion than that seen in Au. afarensis.

Homo

Homo habilis

Hominin phylogeny is particularly uncertain around the emergence of Homo prior to 2 Ma, and at present there is debate whether early Homo is represented by one sexually dimorphic species (H. habilis sensu lato) or two species (H. habilis sensu stricto and H. rudolfensis) (Wood, 1992; Spoor et al., 2015). Hereafter, Homo habilis is referred to in the latter sense. The most complete associated skeleton representing early Homo is OH

62, which preserves fragmented teeth, partial maxillae and other facial fragments, as well as poorly-preserved major long bone shaft fragments (none of which retain articular surfaces) (Johanson et al., 1987). Other important elements potentially belonging to H. habilis include the hand remains of the holotype OH 7 (Leakey et al., 1964; see also

Susman & Creel, 1979; but see Almécija et al., 2009), and the foot of OH 8 (but see Gebo

& Schwartz, 2006), which some have suggested may belong to the same individual

(Susman et al., 1982; Susman 2008).

The cheiridia provide evidence about the locomotor behavior of H. habilis.

Specifically, the hands are derived toward the modern human condition in having a strong, thick pollex and long distal manual phalanges (Susman et al., 1982). However, the proximal and intermediate phalanges are robust with thick cortices, strong flexor attachments, and marked curvature, all of which suggest an ape-like climbing repertoire.

Almécija et al., (2009; see also Moyà-Solà et al., 2008) concluded that the robust morphology of the OH 7 phalanges was more consistent with an attribution to robust australopiths (Paranthropus) rather than early Homo.

What has been recovered of the OH 8 foot is perhaps even more derived than the hands. Although the fossil preserves no phalanges, it has a stout, adducted and fixed hallucial metatarsal, and close packing of the tarsals that prevents mobility at the midfoot

(Susman & Creel, 1979; Susman et al., 1982). On the basis of talar morphology, however, Gebo and Schwartz (2006) disagree that OH 8 belongs to early Homo, and suggesting its closer similarity to the TM-1517 talus attributed to Australopithecus boisei

(Wood, 1974).

The appendicular skeleton is best known from OH 62, but the OH 35 tibia and fibula (which may also belong to the OH 7/OH 8 individual) are also assigned to H. habilis by some researchers (Susman et al., 1982). The fibula of OH 35 has been described as resembling the modern human condition whereas the tibia appears more primitive. Ruff’s (2009) analysis of cross-sectional dimensions (which are known to respond to epigenetic effects of locomotor loading) of the OH 62 humerus and femur

16 indicate that compared to the femur, the humerus experienced more mechanical loading than is the case for later Homo, and thus a relatively greater role of climbing locomotion.

Although the OH 62 skeleton is poorly-preserved, analysis of limb proportions based on published length estimates was provided by Richmond et al. (2002), who suggested that the differences between the humerofemoral proportions of OH 62 and A.L. 288-1 are rare within a single extant primate taxon. Furthermore, some estimates of OH 62 suggest even more ape-like upper-to-lower limb ratios, with a relatively longer humerus than apparent for Au. afarensis (Hartwig-Scherer & Martin, 1991). The results of Richmond et al.

(2002) and Ruff (2009) indicate that forelimb dominated arboreal locomotor behaviors survived late into the lineages that gave rise to H. sapiens, and may have involved at least one reversal to more primitive body proportions and positional repertoires. Further assessment of the grade classification of A.L. 288-1 and OH 62 is in order.

Homo ergaster

The earliest evidence of modern human-like body proportions appears with an especially well-preserved associated skeleton of Homo ergaster, KNM-WT 15000 (c.

1.55 Ma). It includes nearly complete representatives of most major long bones

(excluding the radius, but retaining a nearly complete ulna), as well as remarkably well- preserved axial and cranial elements (Brown et al., 1985; Lordkipanidze et al., 2007).

Researchers have also recovered other associated skeletons attributed to H. ergaster or H. georgicus (c. 1.77 Ma) from the Dmanisi region of Georgia (Lordkipanidze et al., 2007).

These also exhibit modern human-like postcranial morphology and body proportions, but are combined with small stature and small, close to australopith-sized, brains.

Like modern humans, KNM-WT 15000 has long femora and tibiae, but short forearms, with crural, brachial and humerofemoral ratios falling just within the upper end of modern human variation. No forearm elements are recovered in sufficient condition to provide length estimates for the Dmanisi hominins, but its humerofemoral and crural ratios are also similar to modern humans. The Dmanisi tibia is relatively short, which some suggest is an adaptation to the colder northerly climates of Georgia (Pontzer et al.,

2010), whereas the longer tibiae of KNM-WT 15000 are consistent with an elongated body that facilitates thermoregulation (Bergmann, 1848; Allen, 1877). Both Dmanisi and

KNM-WT 15000 are interpreted as fully committed terrestrial bipeds, as evidenced by their long legs, short arms, high femoral bicondylar angles, and the rigid, lever-like foot of Dmanisi, with its straight and robust metatarsals, and fully adducted hallux. On the other hand, both the African and European specimens retained cranially-oriented glenoid fossae, and the Dmanisi specimens display a uniquely oriented tibio-talar articulation.

The overall postcranial morphology and limb proportions of the Dmanisi and African specimens have been interpreted as indicating hunting/pursuit behaviors not seen in earlier hominins (Lordkipanidze et al., 2007; Pontzer, 2010).

THESIS OUTLINE AND GOALS

The effective analysis of the evolution of hominin body form since the most recent common ancestor of modern humans and Pan cannot proceed without a better understanding of how body form varies within and among extant primate taxa, and how any such variation relates to the locomotor repertoires of those taxa. These types of comparative data are also necessary if researchers are to better understand the extent to

18 which the hominin clade can be subdivided into grades. These questions inform the content and organization of this thesis.

● Chapter 2: Phylogenetic and functional signals of anthropoid limb proportions

● Goal 1: To quantitatively characterize extant anthropoid taxa according to the

variation in their overall limb proportions.

● Goal 2: To test hypothesized relationships between limb proportions and

behavioral repertoires.

● Goal 3: To test the presence and strength of phylogenetic signal in limb

proportions.

● Chapter 3: Are extant apes appropriate models for fossil hominin limb

proportions? Insights from machine-learning analyses

● Goal 1: To test whether extant hominoids are appropriate models for

reconstructing hominin limb proportions.

● Goal 2: To use multiple regression to estimate and re-estimate missing fossil

hominin long bone lengths.

● Chapter 4: Evaluating hominin locomotor grades

● Goal 1: To evaluate the variation in limb proportions in extant hominoid

genera and grades.

● Goal 2: To use variation in limb proportions to test hypotheses of grade shifts

among hominin taxa.

These analyses expand upon the work of Napier and Napier (1967) and Fleagle

(1988), as well as Richmond et al., (2002) by using multivariate, machine learning, and

19 resampling methods to explore the variation in anthropoid limb proportions to improve methods for deciphering the behavioral and taxic significance of fossil hominin variation.

Chapter 2: Phylogenetic and Functional Signals in Anthropoid Limb Proportions

ABSTRACT

Limb proportions have been used to sort early hominins (i.e., human lineage members of tribe Hominini post-dating the last common ancestor of Pan and Homo) into grades (Collard & Wood, 1999; Collard, 2002), but the degree to which limb proportions discriminate among extant anthropoid taxa, and how they correlate with the locomotor behaviors of those taxa, is not completely understood (but see previous discussions on the topic by Napier, 1967; Napier & Walker, 1967; Napier & Napier, 1967; Fleagle, 1988;

Richmond et al., 2002). Here, multivariate approaches (e.g., principal components analysis, two-block partial least squares analysis) and phylogenetic comparative methods

(e.g., phylomorphospace) are used to investigate the taxic, behavioral, and phylogenetic patterning of limb proportions in a sample of extant anthropoids.

The results of multivariate analyses demonstrate that extant hominoid genera can be distinguished from one another in morphospace (i.e., the graphical representation of the body shapes a taxon may display) the defined by either overall traditional limb indices or Mosimann size-adjusted long bone lengths. Significant covariance between limb proportions and locomotor behavior is also demonstrated for anthropoids. However, phylogenetic comparative methods suggest that although there is a strong phylogenetic signal in limb proportions, several extant hominoid and non-hominoid anthropoids that practice specialized locomotor habits (e.g., Homo sapiens, Pongo, the Hylobatidae, and the Atelidae) also have specialized phenotypes. These results will be crucial to testing hominin locomotor grade hypotheses.

INTRODUCTION

Napier and Napier (1967) implied that there is a positive correlation between primate limb proportions and the use of forelimb dominated behaviors (see also Napier,

1967; Napier & Walker, 1967). Thus, Collard and Wood (1999) wrote that fossil hominin limb proportions may also be used to evaluate the evolution of two major phases of hominin locomotor behavior (i.e., ‘grades’ or ‘adaptive types’: groups of taxa sharing functionally consistent adaptations; Huxley, 1958; Collard 2002). They also suggested that because a genus should be both a clade and a grade, grade affinities should be used to evaluate hypotheses of genus-level alpha taxonomy (i.e., the number of taxa represented in the hominin fossil record). If limb proportions are to be used to understand locomotor behavior, and for grade hypotheses (as Collard & Wood, 1999 suggested), quantifying their relationship with locomotor behaviors should be a primary concern for researchers investigating the origins and patterning of early hominin locomotor behavior.

Napier and Napier (1967; see also Napier & Walker, 1967) suggested that extant non-human primates can be allocated to one of three broad, grade-like, patterns based on limb proportions and dominant locomotor behaviors: The first group would include relatively small-bodied vertically clinging and leaping so-called ‘prosimians’3 that have long hindlimbs relative to forelimbs (50-80% intermembral index). The second pattern of

Napier and Napier includes non-hominoid anthropoid quadrupeds (i.e., ‘monkeys’) that have limbs of approximately equal length (80-100% intermembral index). Within this grouping the more terrestrial taxa have absolutely longer limbs relative to body length

3 The category ‘prosimians’-- which included lemurs, lorises, bushbabies, and tarsiers-- is now considered obsolete. Lemurs, lorises, and bushbabies are now placed in the revised category, Strepsirrhini. Tarsiers have been placed beside the Anthropoidea in the Haplorrhini.

22 enabling longer strides and faster progress, and the more arboreal taxa have shorter limbs for stability on narrow supports like branches. But the publications of Napier and colleagues also placed the Atelidae into the quadrupedal monkey locomotor pattern, with the sub-type ‘New World semi-brachiation’, which recalls their similarities with apes

(Mittermeier & Fleagle, 1976; Mittermeier, 1978; Fleagle et al., 1981). The ‘brachiating’4 third pattern of Napier and Napier included the larger-bodied non-human hominoids that have relatively longer forelimbs (100-150% intermembral index) (but see below, and

Fleagle, 1988; Fleagle & Meldrum, 1988). By Napier and Napier’s (1967) classification, genus Homo is a fourth, bipedal, pattern within Hominoidea, with intermembral proportions (70-72%) that overlap with the ‘prosimian’ grade (see also Schultz, 1930).

Thus, primate intermembral proportions appear to be tied to forelimb- versus hindlimb- dominated behaviors. But whether the limb proportions of fossil hominins were more like the extant hominoids, modern humans, or another hitherto unknown group was not addressed (see Collard & Wood, 1999; Collard, 2002).

Young et al., (2010) inferred from patterns of forelimb and hindlimb integration that the Pan-Homo last common ancestor (PHLCA) was ape-like. They wrote that a monkey-like PHLCA would require multiple episodes of convergence in hominoids. This is consistent with other research that has suggested the precursor of the hominin clade had long forelimbs and practiced forelimb-dominated arboreal locomotor behaviors (see

Morton, 1926; Collard, 2002; see also Keith, 1923; Schultz, 1930). This scenario implies one or more shifts of behavior and limb proportions (and subsequently, grade) toward the

4 True brachiation is now recognized as a highly specialized locomotor behavior practiced only by the Hylobatidae (see Hollihn, 1984; Chang et al., 2000).

23 modern human phenotype, during which hominins would “pass through” a period of balanced, monkey-like proportions. This period may be captured in the limb proportions of known fossil hominins.

However, before paleoanthropologists can use inferred limb proportions as evidence of different locomotor adaptations within the hominin clade (see Hartwig-

Scherer & Martin, 1991; Collard & Wood, 1999; Wood & Richmond, 2000; Richmond et al., 2002; Harcourt-Smith & Aiello, 2004; Reno et al., 2005; Haeusler & McHenry,

2007), researchers must quantify the patterns of variation in the limb proportions of extant taxa, the extent of any association between overall limb proportions and locomotor mode, and the potential influence that phylogenetic relatedness may have on limb proportions.

Napier and Napier (1967) described in detail the various modes of extant primate locomotion, but they did not have access to subsequent field observations that suggest substantial behavioral plasticity and overlap among locomotor modes (see Mittermeier &

Fleagle, 1976; Hunt et al., 1996; Hunt, 2016). More recent behavioral data have been related back to some relevant morphology (e.g., Almécija et al., 2015), but limb proportions have not had the same treatment. The initial studies of Napier and Napier

(1967) (see also Jouffroy & Lessertisseur, 1979; Fleagle, 1988) were followed by efforts to link differences in behavior with the proportionate lengths of limbs and body segments in specific taxa (Jungers, 1980; Fleagle & Meldrum, 1988; Garber, 1991; Doran, 1993;

Gebo & Sargis, 1994). But these studies lacked comparable behavioral categories and compatible methods for collecting locomotor data (see Hunt et al., 1996, which reviews the development of an improved methodology). Instead of limb proportions, other

24 researchers have focused on the lengths of modern human hindlimbs and how they influence the energetics of bipedalism or running (Bramble & Lieberman, 2004; Pontzer,

2005; Steudel-Numbers, 2006; Steudel-Numbers & Weaver, 2007), or the relationships between more plastic aspects of long bone diaphyseal and articular morphology with loading regimes and locomotor behaviors (Ruff, 1991; Ruff, 2000; Lieberman et al.,

2001; Ruff, 2002; Carlson, 2005; Shaw & Ryan 2012). Thus, it appears that no previous research has quantified intra- and interspecific variation in overall limb proportions in extant anthropoids or made multivariate comparisons of these patterns with observations about locomotor behavior. Doing so will provide a comparative context for assessing the taxic and behavioral significance of observed differences in limb proportions among fossil hominin skeletons.

In summary, this study investigates the extent of variation in limb proportions of extant anthropoid groups; quantifies the degree to which limb proportions are associated with behavioral repertoires across a large, taxonomically inclusive anthropoid sample; and evaluates the presence and strength of phylogenetic signal in limb proportions. Thus, to build on the work of Napier and Napier (1967), Napier and Walker (1967), Fleagle

(1988), and others (e.g., Richmond et al., 2002; Almécija et al., 2015), the following steps were followed:

1) First, the degree to which limb proportions can discriminate among extant

anthropoid groups (i.e., species, genera, superfamilies) is determined. As per the

findings of previous authors (Schultz, 1937; Napier, 1967; Napier & Napier,

1967; Fleagle, 1988), hominoids are expected to show more variation in limb

proportions than New and Old World monkeys. For example, monkeys should

cluster around equal or sub-equal intermembral indices (80-100%), whereas non-

Homo hominoids should have longer and more varying intermembral indices

(100-150%).

2) Next, the relationships between species overall mean limb proportions and

behavioral repertoires are quantified using Two-Block Partial Least Squares

analyses (2B-PLS; Rohlf & Corti, 2000). Limb proportion differences among

extant groups are anticipated to reflect differences in behavioral repertoires. For

instance, those taxa with nearly equal intermembral indices (e.g., monkeys)

should exhibit locomotion more heavily dominated by quadrupedality, whereas

hominoids should have relatively longer forelimbs and increased forelimb

dominated behaviors. Taxa practicing similar proportions of locomotor behaviors

should have more similar limb proportions.

3) Finally, phylogenetic comparative methods (PCMs) are used to test the strength of

the phylogenetic signal present in the limb proportions of various anthropoid

groups. Because constraints imposed by ancestry also influence limb proportions,

PCMs will help avoid any misleading conclusions that might be drawn if

phylogenetic patterning is not taken into account (O’Neil and Dobson, 2008;

Collyer et al., 2015). Therefore, PCMs are used in conjunction with 2B-PLS to

differentiate the degree to which limb proportions are influenced by phylogeny as

opposed to adaptation.

MATERIALS AND METHODS

Sample

Extant non-human species were chosen to provide a taxonomically-broad sampling from each of the anthropoid grades described by Napier and Napier (1967). It is important to include multiple representatives from all of the hominoid groups for which a diverse range of locomotor behaviors are available in order to capture as much variation among closely related taxa as possible.

The total sample (N = 1,825) consists of a large, regionally heterogeneous sample of modern humans (n = 1,270) (789 males, 481 females), plus a taxonomically diverse sample of non-human anthropoids (n = 555), with each taxon having, where possible, approximately balanced numbers of adult males and females (Table 2.1). The non-human anthropoid sample comprises five genera of hominoids (n = 305), nine genera of cercopithecids (n = 153), and 12 genera of ceboids (n = 90). The modern human data came from the online Goldman Osteometric Dataset (Auerbach & Ruff, 2004, 2006), and the Terry collection of the Smithsonian Institute’s National Museum of Natural History

(the latter collected by Powell). It includes skeletons 5,500 years old to present, from the following locations: Alaska, the Andaman Islands, Argentina, Arizona, Australia,

Austria, Belgium, California, the Canary Islands, Chile, the Democratic Republic of

Congo, Ecuador, Egypt, England, France, Germany, Hawaii, Illinois, Italy, Japan,

Kentucky, Madagascar, New Jersey, New Mexico, Ohio, Peru, Philippines, Russia,

Scotland, South Africa, South Dakota, Sudan, Utah, and Washington. Additional information is provided on the Goldman Osteometric Dataset website

(https://web.utk.edu/~auerbach/GOLD.htm; (Auerbach & Ruff, 2004, 2006).

Data collection

Excluding a major contribution of Homo sapiens (n=1,169) from the Goldman

Osteometric Dataset, Powell collected the majority of the remaining data using measurement protocols set out in the Goldman Osteometric Dataset methodology

(Auerbach & Ruff, 2004, 2006). Only specimens with all four major long bones in a good state of preservation were included in the sample, and measurements were collected from the right side of the skeleton. Data for the balance of the non-human anthropoids, including surface scans and linear measurements, was generously contributed by Dr. J.

M. Plavcan (University of Arkansas), Dr. C. B. Ruff (Johns Hopkins University), and Dr.

M. Tocheri (Lakehead University). The data collected by Powell were either recorded directly from skeletons using Mitutoyo Corporation digital calipers and an osteometric board, or they were collected as inter-point distances on three-dimensional surface scans

(contributed by Dr. J. M. Plavcan, University of Arkansas; collected by J. M. Plavcan,

Mike Lague, and Adam Gordon; funded by NSF BCS-0647557) using Landmark Editor

3.0 (University of California, Davis’ Institute for Data Analysis and Visualization, Wiley et al., 2005). Because of the multiple sources of data, an error study was performed on a sample of specimens for which data were collected by both Powell (both from skeletal collections, and from 3D surface scans contributed by Plavcan) and Ruff. Using the error formula (|x1 – x2|/x1 )*100, Powell found the inter-observer error for most specimens to be minimal (<5%). However, Powell’s 3D surface scans for several Gorilla specimens were consistently approximately 10% different from those Powell collected by hand, and this error may be due to improperly scaled surface scans. Therefore, only Powell’s hand-

28 collected Gorilla specimens are used herein. Results of the error study are provided in

Table 2.2.

Measurements

Humerus maximum length (HML) - distance between the most superior point on the humeral head to the most distal point of the medial projection of the trochlea; Radius maximum length (RML) - distance between the most superior point on the radial head to the most distal point of the styloid process; Femur maximum length (FML) – distance from the most superior point on the femoral head to the most inferior aspect of the medial condyle; Tibia maximum length (TML) - distance from most superior point of the intercondylar eminence to the most distal aspect of the medial malleolus. Outliers were not removed unless they were clearly due to data recording errors, such as impossibly small or large long bone length values. See Figure 2.1 for visualizations of each measurement.

Analytical methods

Size adjustment

Body size, which varies significantly across primates, influences variables like feeding habits and positional behavior (Gaulin, 1979; Sailer, 1985; Cant, 1987; Doran,

1993; Hunt, 1996), so any consideration of body proportions must account for differences in body size among the individuals and taxa studied. A number of variables (e.g., trunk or vertebral column length, or body mass) have been used as proxies for body size (Jungers et al., 1995; Jungers, 2009), but these data were not available for the majority of the present sample. Instead, the geometric mean (GM) is used here, which combines size information from all available linear variables into a single variable that is then used as a

29 size proxy for body size or, in this case, overall skeletal size, without completely removing relative size (Mosimann, 1970; Jungers et al., 1995). The GM must be calculated on no fewer than three input variables (Coleman, 2008), which in this case are the four maximum lengths of humerus, radius, femur, and tibia. For every individual, each variable is divided by the GM - calculated as the nth root of the product of n measurements - to generate four Mosimann shape ratios: HUM, RAD, FEM, TIB. Using

GM to obtain dimensionless proportions is commonly used in paleontological contexts

(e.g., Lockwood et al., 1996; Green & Gordon, 2008; Kivell et al., 2013) because alternatives like allometric residuals have been demonstrated to consistently fail to identify known isometric individuals of different size (Jungers, 1995).

Four traditional indices were also calculated: humerofemoral (HFI;

100*HML/FML), brachial (BRI; 100*HML/RML), crural (CRI; 100*TML/FML), and intermembral [IMI; 100*(HML+RML)/(FML+TML)]. These dimensionless indices have a long history of significance in the study of limb proportions and positional behavior in primates (Mollison, 1911; Erikson, 1963; Napier, 1967; Napier & Napier; 1967; Fleagle,

1988; Hunt, 2016), and together with the previously described Mosimann shape ratios, were the variables used for the following analyses.

Boxplots and Tukey’s HSD

Inter-group (i.e., species, genus, and superfamily) differences in limb proportions are tested using Analysis of Variance (ANOVA) with Tukey’s post-hoc “Honestly

Significant Difference” (HSD) at a confidence level of 95%. Boxplots were used to illustrate the ranges of variation of each of the four traditional limb indices at the genus and superfamily levels. Boxplots were produced using function ‘qplot’ from the ggplot2

(Wickham, 2009). Tukey’s HSD was performed with function ‘TukeyHSD’. All analyses, including those below, were performed in R version 3.4.4 (R Core Team, 2017)

Principal Components Analysis

Principal Components Analysis (PCA) was used to explore inter- and intra-group variation and clustering patterns based on the simultaneous consideration of multiple limb proportion variables. PCA is an ordination technique that reduces multiple variables into a smaller number of indices (i.e., principal components - PCs) that are linearly uncorrelated combinations of the original variables represented in lower-dimensional space (Pearson, 1901). This method detects major patterns of variation (i.e., the PCs) among individuals in a sample without a priori group information. The method also provides loadings for each PC indicating to what degree the original individual variables contribute to each axis of variation. Due to its multidimensional summary properties,

PCA is traditionally applied to the study of complex shape variation of individual bones

(e.g., mandible, scaphoid) or combinations of bones (e.g., skull, cranium) (Franklin et al.,

2006; Yang et al., 2006; Lague et al., 2008; Bonneau et al., 2012; Kivell et al., 2013).

Only rarely has PCA been used to explore variation in the overall postcranial morphology of anthropoids (e.g., several limb segments simultaneously) (but see Holliday, 1997;

Young, 2003). PCA is used here because it treats multiple potentially correlated limb proportions as simple overall shape data, and clustering patterns indicate which limb proportions drive variation on each axis.

Here, PCA is performed separately on the overall Mosimann shape ratios and the overall traditional limb indices. The PCAs were produced using the ‘prcomp’ function and resulting biplots were generated with ggplot2 (Wickham, 2009).

Two-Block Partial Least Squares (2B-PLS)

To quantify the degree to which limb proportions covary with locomotor repertoire Two-Block Partial Least Squares analyses (2B-PLS) were performed on subsets of the sampled taxa. 2B-PLS uses singular value decompositions between datasets to construct linear combinations of pairs of variables from one dataset (e.g., anthropoid limb proportions) such that a second dataset (e.g., percent locomotor mode) accounts for as much of the covariance between the original pairs of variables as possible

(Rohlf & Corti, 2000). This method of exploring covariance between variables differs from regression analyses in that the two datasets representing the shape and covariate blocks are treated symmetrically. That is to say, neither set of variables is assumed to be dependent or predictive of the other (Rohlf & Corti, 2000). 2B-PLS, which is a particularly appropriate means of describing covariance between behavior and limb proportions precisely because it does not assume a priori directional relationships between variables (Adams et al., 2014), was performed using function ‘two.b.pls’ of the package Geomorph (Adams et al., 2017).

Two-Block PLS has been used previously to investigate cranial integration in hominoids (Singh et al., 2009), patterns of integration in the appendicular skeleton in mammalian carnivores (Martín-Serra et al., 2014), forelimb-to-hindlimb shape covariance in hominoids and hominins (Tallman, 2013), and to evaluate the covariance between hamate shape and proportions of arboreal locomotor modes used by a sample of extant Homo sapiens, hominoids and a sample of monkeys (Almécija et al., 2015). The results of the latter indicate significant relationships between locomotion and hamate shape in anthropoids. Following Almécija and colleagues (2015), a subset of the

32 complete anthropoid dataset is here used to characterize evolutionary patterns of covariance between overall limb proportions with associated published locomotor behavior data matrices. The reduced anthropoid subset comprises limb proportions for 22 species from 17 genera for which data about the frequencies of arboreal locomotor behavior were available. The taxa included for 2B-PLS are Alouatta caraya, Ateles geoffroyi, Cebuella pygmaea, Cebus albifrons, Cebus paella, Cercopithecus albogularis,

Cercopithecus mitis, Colobus guereza, Gorilla beringei, Gorilla gorilla, Hylobates lar,

Lagothrix lagotricha, Macaca fascicularis, Macaca nemestrina, Pan paniscus, Pan troglodytes, Papio cynocephalus, Pongo pygmaeus, Presbytis rubicunda, Procolobus badius, Saimiri sciureus, and Symphalangus syndactylus (Table 2.5).

Published locomotor data were gathered primarily following the compiled data of

Hunt (2016) (see also Thorpe & Crompton, 2006; Almécija, et al., 2015; and references therein). All other sources of locomotor data are cited in Table 2.5. The initial locomotor block variables were the same six modes of arboreal locomotion used by Almécija et al.

(2015): quadrupedal/tripedal walking (QTW), vertical climbing and descent (VCD), bipedal walking (BW), orthograde clamber and transfer (OCT), brachiation and forelimb swing (BFS), and drop and leap (DL) (see also Thorpe & Crompton, 2006; Hunt, 1996).

These locomotor modes allowed the inclusion of Homo sapiens (100% BW) (Prost, 1980;

Rose, 1984; Collard & Wood, 1999), and were the most similar to those locomotor variables used throughout the published literature (see Table 2.6). In practice, some adjustments were necessary to make the published data compatible. For instance, Hunt

(2016) referred to separate “clamber” and “transfer” locomotor categories, whereas

Almécija et al. (2015) refer to orthograde clamber and transfer (OCT). In this case,

Hunt’s (2016) “clamber” and “transfer” values were summed to produce an OCT value.

All behavioral values were converted to percentages of the sum total of available data for each taxon before analysis.

For comparison, a second 2B-PLS used only the 18 positional modes (Table 2.6) published in Hunt (2016) and a subset of 11 taxa from the anthropoid sample available in

Hunt (2016): Cercopithecus albogularis, Cercopithecus mitis, Colobus guereza,

Hylobates lar, Pan troglodytes, Papio cynocephalus, Pongo abelli, Pongo pygmaeus,

Presbytis rubicunda, Procolobus badius, Symphalangus syndactylus. The comparison, which uses data from a single source, should expose any potential error associated with gathering locomotor behavioral data from multiple publications. Although modern humans are considered obligate in terms of locomotion and are thus included in the first

2B-PLS, H. sapiens are not included in the second because percentage use for positional categories like “sit”, “lie”, and “squat” were unavailable (see Hunt, 2016). The matrices of locomotor and positional mode frequencies used in 2B-PLS analyses and literature sources for all data are provided in Tables 2.5 and Table 2.6.

Phylogenetic comparative analyses

The dataset used in this paper is broadly taxonomically inclusive, including multiple taxa from three anthropoid superfamilies, (i.e., macroevolutionary-scale).

Because species are not evolutionarily independent of each other it is important that where possible phylogenetic effects (i.e., the tendency of closely related taxa to resemble each other more than they do distantly related taxa) (Blomberg & Garland, 2002) are accounted for (Collyer et al., 2014). Phylogenetic comparative methods (PCMs) are thus used here to test for the signal of phylogeny in individual and overall Mosimann shape

34 ratios and traditional limb proportions to understand to what extent genetic propinquity influences the results of the foregoing analyses.

The phylogenetic relationships of the complete anthropoid dataset (Figure 2.2) were produced from a consensus tree based on molecular data and downloaded from

“The 10KTrees Project” (ver. 3; Arnold et al., 2010; http://www.10ktrees.fas.harvard.edu). If species were not available in 10K Trees the data for the nearest available sister species was substituted (i.e., Saguinus midas represents

Saguinus labiatus; Presbytis melalophos represents Presbytis rubicunda). Genus names from 10K Trees were also updated and edited to match the generic designations of the sample (i.e., Callithrix pygmea = Cebuella pygmea; Piliocolobus badius = Procolobus badius). The phylogenetic tree was produced using Mesquite 3.2 (Maddison & Maddison,

2017).

Phylomorphospace

To assess patterning in shape space due to phylogeny, a phylogenetic tree was mapped onto the morphospace defined by the first two axes of a PCA of the covariance matrix of the overall limb proportion means of extant species (Sidlauskas, 2008). The phylomorphospace approach is gaining popularity among evolutionary anthropologists because it succinctly visualizes evidence of homoplasy and adaptation in closely related clades (see Almécija et al., 2013; Almécija et al., 2015; Young et al., 2015; Prang, 2016).

Phylomorphospace methods have previously been used to investigate the correlation between morphological shifts, habitat, and diet (Klingenberg & Ekau, 1996), the order of shifts (Stone, 2003), partitioning of morphological diversity (Stayton & Ruta, 2006), and to visualize adaptive radiations (Clabaut et al., 2007).

Following the methods laid out by Rohlf (2002) the internal nodes of a phylogenetic tree represent hypothetical ancestral nodes that are reconstructed using maximum likelihood. A phylomorphospace is produced by plotting the ancestral node configurations onto a morphospace defined by species means and connecting the branches of the tree (Bookstein et al., 1985; Rohlf, 2002; Sidlauskas, 2008). For visualization purposes, this method is particularly suited to visually assess possible convergence among species in different parts of a tree, to see evidence of accelerated morphological change, and to analyze how taxa from separate lineages are distributed across the morphospace (Monteiro, 2013). Phylomorphospace plots were produced using the function ‘phylomorphospace’ of the package Phytools (Revell, 2012).

Care must be taken in interpreting phylomorphospace visualizations, however, as the approach is associated with several assumptions and caveats that can alter observations and drawn conclusions (reviewed in Sidlauskas, 2008). 1) Maximum likelihood estimates assume that ancestral reconstructions represented by any node must have been morphologically intermediate to the connected nodes. This can be problematic if only a few taxa are sampled, if many modern subclades are omitted, or if descendants are far derived versus ancestors. Only the last circumstance is likely to be of concern for the analyses at hand, as no fossils were included. 2) Ancestral state reconstructions are best when the morphological change of a given branch is moderate compared to the range of variation exhibited by the total clade, and when descendants have not been strongly drawn to an adaptive peak. Thus, large average distances between taxa, especially if due to strong selective forces, can make reconstructions of even recent common ancestors less informative. All great ape genera, and the most abundant available lesser ape genera,

36 were sampled. Thus, only the last circumstance may skew conclusions, as the Asian apes and Homo practice specialized forms of locomotion. 3) If branches are not calibrated according to time depth, the phylomorphospace may not be used to comment on the rate of change, only the mean magnitude of morphological change per phylogenetic branch.

4) Phylomorphospace output is entirely dependent on which morphologies were used to construct it. Thus, the results of the present analyses will be different if performed using, for instance, dental or articular morphology.

Phylogenetic Signal

Phylogenetic signal was estimated for Mosimann shape ratios and traditional indices using Blomberg’s K (Blomberg et al., 2003). Blomberg’s K has been applied to study phylogenetic effects on ecological communities and diversity (Kraft et al., 2007;

Flynn et al., 2011; Swenson et al., 2012), and the degree and pattern of phylogenetic signal in quadrupedal primate long bone structure (O’Neill et al., 2008). This statistic estimates phylogenetic signal as the ratio of the mean squared error of the tree tip data

(MSE0) measured from the phylogenetic corrected mean for a continuous variable, and the mean squared error of the variance–covariance matrix derived from the given phylogeny (Blomberg et al., 2003; Münkemüller et al., 2012). Blomberg’s K assumes a

Brownian Motion model of trait evolution in the absence of phylogenetic inertia, where

K<1 indicates less resemblance of closely related taxa than expected under Brownian motion, and a K closely approaching or exceeding 1 suggests a stronger resemblance between closely related taxa than expected.

A multivariate version of Blomberg’s K (hereafter called multiple K) was introduced recently by Adams (2014). This method allows for the estimation of

37 phylogenetic signal using multiple continuous traits simultaneously. Taking into account the multivariate shape of the overall limb skeleton and limb proportions is an important part of the present research effort and the introduction of the multiple K will therefore be an indispensable to conclusions. However, the original Blomberg’s K is also necessary to understand how individual limb proportions contribute to the overall phylogenetic signal.

Blomberg’s K and multiple K were derived at 10,000 permutations using the ‘physignal’ function of the Geomorph package (Adams et al., 2017).

RESULTS

Boxplots and Tukey’s HSD

Boxplots illustrating superfamily and genus-level variation for each of the four traditional indices are provided in Figure 2.3. Visual inspection of boxplots reveals differences in limb proportions between modern humans and other anthropoids consistent with those reported in previous studies (Schultz, 1930; Shea, 1981; Jungers, 1985;

Richmond, 2002). As anticipated by Jungers (2009), IMI (intermembral index) and HFI

(humerofemoral index) share nearly identical patterns and consistently separate taxa most effectively, as would be expected if these indices effectively characterize locomotor behavioral repertoires. Asian apes (i.e., Pongo, Hylobates, and Symphalangus: 125-

140%) and then African apes (i.e., Gorilla and Pan: 100-120%) have the highest values for these indices among anthropoids. Pongo, whose closest living relatives are the

African apes, falls within the range of the Hylobatidae for each index.

Genus Pan shows nearly identical values for both IMI and HFI (~100-110%), and both Pan species fall partially within the range of the monkeys (the latter having ~60-

105% for both indices). Here, the overlap between Pan and monkeys is due largely to the

Atelidae (i.e., Alouatta, Ateles, and Lagothrix). Compared to other platyrrhines, atelids have lower CRI (crural index) values that fall in the range of cercopithecoids, but only slightly overlap with hominoids. However, the atelids, which are the only non-hominoids to exceed 100% for IMI and HFI, are even more similar to hominoids, consistent with research recognizing their skeletal, muscular, and behavioral convergences toward apes in their “semi-brachiating” form of locomotion (Mittermeier & Fleagle, 1976;

Mittermeier, 1978; Fleagle et al., 1981). For both IMI and HFI, most New and Old World monkeys are similar, although New World monkeys exhibit a greater range of IMI values than Old World Monkeys (due to the Atelidae). In all, these superfamilies effectively span the range of values from Homo to Pan, but do not markedly exceed either genus.

On the other hand, BRI (brachial index) is largely consistent across anthropoids

(~80-110%). Exceptions are the lower values of Homo and Gorilla, and the higher values of Hylobates, Symphalangus, and Presbytis. The hominoid genera easily exceed the BRI range in monkeys, potentially indicating differences in the degrees to which hominoid genera rely on forelimb-dominated locomotor behaviors.

Crural index ranges from the nearly identical values for modern humans and the

African apes (~75-85%), to ~80-95% for the Asian apes, ~85-105% for

Cercopithecoidea, and ~90-110% for Ceboidea. Not only is the crural index consistent within each of the aforementioned groups, the differences between those groups are small and the values overlap markedly. The CRI values for all hominoids (including Homo sapiens) are separated from nearly all monkeys, and both Cercopithecoidea and Ceboidea are more variable for CRI than are the hominoids.

To quantify statistical differences visually demonstrated in the boxplots, ANOVA with post-hoc Tukey’s HSD multiple pairwise comparisons (p=0.05) was performed on the complete anthropoid sample at three taxonomic levels (i.e., species, genus, and superfamily). Results of these analyses are summarized below and provided in Table 2.3.

Anthropoidea: At the superfamily level, out of six pairwise comparisons, significant differences were found between 100% of pairs for IMI, HFI, and CRI, but only 5 out of 6 BRI comparisons were significant. The BRI result is due to non- significant difference between Hominoidea and Ceboidea. Out of 352 comparisons of anthropoid genera, significant differences were found between 87% of pairs for the IMI,

82% for the HFI, 67% for the BRI, and 66% for the CRI. At the anthropoid species level, significant differences exist for 82% of IMI, 75% of HFI, 54 % of BRI, and 60% of CRI, out of 821 pairwise comparisons.

Hominoidea: Of 10 hominoid generic pairs, significant differences were found between 100% of IMI, 90% of HFI and BRI, and 80% of CRI comparisons. Non- significant estimates usually involved pairs comprising the Asian apes (Pongo,

Hylobates, and Symphalangus).

Cercopithecoidea: Out of 79 comparisons of cercopithecoid species, significant differences were found between 70% of pairs for the IMI, 61% for the HFI, 54% for the

BRI, and 49% for the CRI.

Ceboidea: Out of 154 species comparisons, 73% of IMI, 67% of HFI, 28% of

BRI, and 23% of CRI pairs showed significant differences.

Principal Components Analysis

The majority of extant hominoid genera can be distinguished in PCA multivariate space using overall Mosimann shape ratios or overall traditional indices. This is supported by Tukey’s HSD, in which hominoid genera are statistically distinct (100%) for both Mosimann shape ratios and traditional indices, whereas ceboid genera (57%) and species (51%) are least distinguishable by traditional indices (see Table 2.3). The hominoid genera form three groups (i.e., Homo, African apes, Asian apes) in PCA space, whereas monkey taxa overlap markedly in PCA space. Using Mosimann shape ratios, PC

1 and PC 2 account for 99% of the explained variance, 84% and 15% respectively. PC 1 explains variance in FEM and TIB relative lengths in the positive direction, and RAD and

HUM relative lengths toward the negative end of the axis. The negative end of PC 2 explains HUM and FEM relative lengths, whereas the positive end explains variance in

TIB and RAD relative lengths. PC 1 is related to hindlimb versus forelimb variance, such that relatively long-legged Homo sapiens and some Saguinus and Callithrix individuals are the only taxa on the positive end of the axis, and the relatively long-armed Asian apes

(i.e., Pongo, Hylobates, and Symphalangus) are the most negative. PC 2 is related to differences in the lengths of proximal versus distal elements. Hominoids including H. sapiens show substantial overlap on PC 2, but Gorilla displays relatively longer HUM and shorter TIB than other groups; Presbytis and Saguinus have the longest TIB and shortest HUM.

The first two axes of the PCA of traditional indices explained 98% of the variance. Here, PC 1 explains 89% of observed variance, and PC 2 explains 9%. PC 1 is related to indices capturing between-limb relationships, whereas the Asian apes with

41 greater IMI and HFI due to relatively long forelimbs are most negative and separated from Homo sapiens by the African ape genera and monkey superfamilies. On the other hand, PC 2 is related to within-limb relationships, where Cercopithecoidea (e.g.,

Presbytis) and other monkey taxa with greater BRI and CRI are most positive and separated from Gorilla by all remaining taxa. On PC 2, Homo sapiens overlaps most notably with several monkeys, Pan, and the Asian apes.

2-Block Partial Least Squares (2B-PLS)

Results of Two-Block Partial Least Squares analyses (2B-PLS) confirm that positive and significant covariance exists between both the Mosimann shape ratios and the traditional indices with behavioral repertoires. Both Mosimann shape ratios and traditional limb indices showed comparable strength and fit with behavioral repertoire. In the following, 2B-PLS results for Mosimann shape ratios and traditional indices are summarized in the plots in Figures 2.7a-c. Results for individual anthropoid superfamilies and the monkeys are provided in the supplementary information.

Traditional indices

Two-block PLS based on traditional indices closely reflect the results for the

Mosimann shape ratios. Along PLS 1, IMI consistently fell at the extreme values and farthest from zero compared to all other traditional indices. Anthropoids exhibit strongly positive and significant correlations between traditional indices and locomotion (r-PLS =

0.77; P = 0.001). Along PLS 1 negative values in the locomotion block are related to

QTW, DL, and BW. These covary with greater CRI and BRI, and lesser IMI and HFI ratios. Conversely, positive values in the locomotor block are mostly related to BFS,

OCT, and VCD. These locomotor modes covary with greater IMI and HFI, but lesser

CRI and BRI.

Along PLS 2 negative values in the locomotion block comprise BW, VCD, and

OCT. In the shape block these covary with lesser HFI and greater BRI. In contrast, positive locomotor block values are related to DL and slightly less so to BFS. In the shape block, positive values covary with greater HFI, smaller BRI, with IMI and CRI intermediate (figure 2.7a).

Mosimann shape ratios

Anthropoids exhibit strongly positive and significant correlations between

Mosimann shape ratios and arboreal locomotion (r-PLS = 0.77; P = 0.003). Along PLS 1, negative values in the arboreal locomotion block are related to QTW, DL, and BW.

These covary mostly with long hindlimbs (especially longer TIB) and short forelimbs

(especially longer RAD). Conversely, positive values in the locomotor block are mostly related to BFS, OCT, and VCD. These locomotor modes covary primarily with positive values for longer forelimbs and shorter hindlimbs.

Along PLS 2, negative values in the locomotion block are related to BW, VCD, and OCT, and these covary in the shape block with longer proximal segments (HUM, in particular) relative to distal elements (especially RAD). In contrast, positive locomotor block values are related to DL, BFS, and QTW. Positive values covary with longer distal and shorter proximal elements in the shape block (figure 2.7b).

Comparative Two-Block Partial Least Squares

An additional Two-Block Partial Least Squares analysis (2B-PLS) was performed on traditional indices and percentage use of an extended suite of 18 positional behaviors for 11 species as published in Hunt (2016; see Table 2.6). This recovered a stronger correlation (r-PLS = 0.93, P = 0.002) than in the foregoing 2B-PLS analyses (see Table

2.6 and Figure 2.7c), with same close relationship between IMI, HFI and forelimb- dominated behavioral categories evident in the foregoing 2B-PLS analyses.

Along PLS 1 traditional indices IMI and HFI fall among the highest values and most closely covary in the shape block with forelimb-dominated behaviors like Hunt’s

(2016) “arm hanging” and “brachiating” but also “sitting”, whereas lower values of CRI and BRI covary with “quadrupedal walking”, “leaping”, and “quadrupedal standing” (see

Figure 2.7c). Positive values on PLS 2 were mostly related to BRI on the shape block, and covary with “arm hanging”, “leaping”, “quadrupedal walking”, “brachiating”, and

“vertical climbing” in the positional behavior block. HFI had the lowest PLS 2 value and covaries most with “sitting” on the positional behavior block.

Phylogenetic comparative methods

Values for K that closely approach or exceed 1 are more similar among closely related groups than expected under Brownian motion. Therefore, K statistics detected significant phylogenetic signals for most individual Mosimann shape ratios and for total

Mosimann shape ratios, and for most individual traditional indices and for total traditional indices. Exceptions include the CRI of Cercopithecoidea (K= 0.72, P= 0.15), which showed non-significant phylogenetic signal. BRI also showed moderate, but in one case non-significant, phylogenetic signal in all anthropoids (K= 0.61, P = 0.51) and non-

44 human anthropoids (K=0.64, P= 0.001). Results of Blomberg’s K and multiple K are provided in Table 2.8.

Mapping the molecular phylogeny onto the shape space defined by anthropoid traditional indices reveals a complex relationship. While monkeys occupy less shape space than hominoids (when modern humans are included), several species in each superfamily share more similar traditional indices with other more distantly related taxa

(Figure 2.6). For example, while sharing an inferred common ancestor with all hominoids

(LCAH) that is most like Gorilla along the first axis, the Asian apes (i.e., Pongo,

Hylobates, and Symphalangus) cluster towards the negative end. On the other hand, Pan species overlap with the monkeys and cluster slightly more positively of the LCAH reconstruction on the first axis. Relative to Pan, Homo sapiens falls roughly 3-4 times to the positive of the LCAH on the first axis, even beyond the monkeys. These results are consistent with expectations that limb proportions would share strong relationships with behavior as well as phylogeny (Napier & Napier, 1967; O’Neil & Dobson, 2008; Collyer et al., 2015), but care must be taken in interpreting these ancestral state reconstructions as primitive and derived phenotypes have not been calibrated by the inclusion of relevant fossil data.

The evidence from phylomorphospace provides several instances of greater phenotypic change (i.e., some taxa less like inferred common ancestors than their cousin lineages) within closely related taxa (e.g., Homo sapiens, Pongo, and the Hylobatidae), and potentially homoplastic similarity between distantly related taxa (e.g., Pan and

Atelidae).

DISCUSSION

How well anthropoids can be distinguished on the basis of their limb proportions, and the relationships of morphology with behavioral repertoires and phylogeny, are questions of importance for paleontologists who seek to understand the functional relevance of limb proportions in extinct taxa, especially hominins (see Napier & Napier,

1967; Fleagle, 1988; Ruff & Walker, 1993; Collard & Wood, 1999; Asfaw et al., 1999;

Collard, 2002; Richmond et al., 2002; Lordkipanidze et al., 2009). However, prior to this study no one had used quantitative methods to separate extant anthropoids according to their limb proportions, or had evaluated the amount of covariance between overall limb proportions and behavioral repertoires, or tested the phylogenetic signal present in traditional limb proportions in a large, taxonomically inclusive sample of extant anthropoids.

To address these questions post-hoc comparisons and various multivariate methods (i.e., Principal Components Analyses, Two-Block Partial Least Squares analyses, phylomorphospace, and multiple K) were used to evaluate the behavioral and phylogenetic significance of variation in overall limb proportions in a macroevolutionary- scale sample of 1,825 extant anthropoids (three superfamilies, 27 genera, 41 species).

Tukey’s HSD demonstrated that all hominoid genera and many monkey genera can be statistically separated on the basis of limb proportions alone (Table 2.3). These results are consistent with previous research in regards to variation in individual limb proportions

(Schultz, 1930; 1937; Napier & Napier, 1967; Fleagle, 1988), demonstrating that intermembral (IMI) and humerofemoral (HFI) indices most effectively separate extant anthropoids at the genus level, and that the hominoid brachial index (BRI) range exceeds

46 the range of the two monkey superfamilies combined. The crural index (CRI), which shows a distinctly narrow range of values, is far more consistent across anthropoids as compared to other traditional indices, but CRI is generally more consistent within genera than is the IMI, which may be due to the greater sexual dimorphism of the IMI (see

Schultz, 1937; Napier & Napier, 1967; Fleagle, 1988).

Principal components analyses (PCA) of both Mosimann shape ratios and traditional indices show that in morphospace hominoid genera (including Homo) exhibit relatively little intrageneric variation, but the intergeneric variation is such that they can be distinguished with almost no overlap. On individual axes, however, there is overlap among hominoid genera. Along PC 1, Homo, the African apes, and the Asian apes form three groups that likely reflect the close continuity of IMI and HFI with the functional demands of their respective habitats (see Schultz, 1930; 1937; Napier, 1967; Napier &

Napier, 1967; Hollihn, 1984; Chang et al., 2000). Hominoids mostly do not overlap with monkeys, with the exception that Pan overlaps with platyrrhines on PC1, due to the

Atelidae (Figure 2.4a, b; see also Schultz, 1930; Mittermeier & Fleagle, 1976;

Mittermeier, 1978; Fleagle et al., 1981). Unlike hominoids, both New World and Old

World monkeys are effectively indistinguishable within a region of the PCA space that is largely intermediate between Homo and African apes on the first axis. In other words, hominoids display more intergeneric shape disparity than the monkeys, even though the former are represented by far fewer genera than the latter (i.e., seven apes versus 20 monkeys). These differences were captured without the use of a priori discriminating methods, therefore demonstrating that multivariate analysis of traditional limb proportion data can identify genera, and thus this provides support for the hypothesis that overall

47 limb proportions capture meaningful and defining aspects of genus-level biology, especially in modern hominoids.

Two-Block Partial Least Squares analysis (2B-PLS) was used to quantify the covariation between overall limb proportions and behavior. The results are consistent with widely-accepted but previously unquantified relationships between overall limb proportions and behavior in extant anthropoids (Napier & Napier, 1967; Fleagle, 1988).

As expected, these relationships are dominated by the covariance of IMI and HFI with

BFS (brachiation and forelimb swing) behaviors. But the majority of limb proportions also exhibit strong phylogenetic signals, revealing the complex relationship between behavior and ancestry. Mapping the tree of phylogenetic relationships onto the PCA space defined by the distribution of species mean traditional indices shows that the scatter of points generally accords closely with phylogenetic relatedness, but several species mapped closer to other more distantly related taxa. For example, Homo sapiens is removed from the African apes and lies beyond the monkeys along PC 1 (due to a smaller

IMI value caused by relatively longer hindlimbs), whereas Pongo falls closest to

Hylobates and Symphalangus (due to larger IMI value caused by relatively longer forelimbs). Furthermore, Homo sapiens, Pongo, and Symphalangus all display the longest branch lengths since their reconstructed last common ancestor of hominoids (LCAH), indicating that taxa with exceptionally long fore- or hind-limbs have changed more than their closest extant relatives (i.e., the African apes). This contrasts with Schultz’s

(1937;1930) claim that limb proportions, especially IMI, of Symphalangus and Pongo had probably undergone greater change in one direction than had the proportions of modern humans in the other. Results suggest, instead, that modern humans show the

48 greatest change in IMI and HFI since the LCAH, followed by the Asian apes. The extent of phenotypic divergence between extant hominoid genera from the LCAH or their extant monkey cousins may reflect the extent of behavioral change required for modern apes to adapt to new ecological niches, and this accords with the results of 2B-PLS analyses.

Although all 2-BPLS analyses in this chapter show positive and significant covariance between phenotype and behavior, percentages of use are limited in their ability to capture the importance of given behaviors for the survival of individuals. The small percentage of time spent by Pan performing climbing and suspension behaviors according to the Hunt (2016) data may misrepresent the importance of those behaviors to the adaptive strategies of African apes. Limb proportions and other adaptations for arboreality may, thus, be more closely related to variables like phylogenetic inertia, energy efficiency, maneuverability and accessing food, predator avoidance, and injury prevention (Boesch & Boesch-Achermann, 2000; Pontzer & Wrangham, 2004; Hunt,

2016). Pontzer and Wrangham (2004) reviewed these points and tested hypotheses about energy efficiency. Their results supported the hypothesis that arboreal adaptations in Pan are the result of selection for safe climbing (i.e., avoiding falls from the canopy) (see also

Latimer, 1991; Hunt, 1991; Cartmill et al., 2002). Subsequent work on this topic should account for the potential risks and rewards of performing given behaviors.

The results of 2B-PLS and phylomorphospace analyses are generally in keeping with foregoing authors (e.g., Morton, 1926; Schultz, 1930; 1937), but are meaningfully distinct in several ways. For instance, Morton (1926) argued that the behavioral precursor to human bipedalism may have been similar to the brachiation employed by the

Hylobatidae. The phylomorphospace presented here, however, reconstructed the tentative

49 common ancestor of Pan and Homo (PHLCA) as relatively more similar to Pan, and falling in the range of monkeys on the first axis, suggesting that its limbs are of approximately equal length.

If the relationship between limb proportions and behavior quantified with 2B-PLS holds among extinct taxa, it is more likely that the LCAH behaved like a generalized quadruped than an extant brachiating hylobatid. This result is more in keeping with the arboreal precursor model proposed by Schultz (1930), and the conclusions of Lovejoy et al., (2009) in regards to the 4.4 Ma Ardipithecus ramidus. This specimen was argued to be more similar to extant generalized quadrupeds in aspects of morphology like limb proportions (but see also the “troglodytian” or Pan-like model proposed by Keith, 1923).

Regardless, the ancestral reconstruction in the phylomorphospace implies that the

PHLCA was monkey-like in terms of limb proportions, and considering Ardipithecus ramidus, perhaps some form of arborealist, but not likely as specialized as hylobatids in terms of morphology or behavior (see Hollihn, 1984; Chang et al., 2000). Considerable caution must be taken when interpreting the ancestral phenotypes reconstructed using the phylomorphospace method, however, as relevant fossil data were not available to calibrate ancestral states using the Maximum Likelihood method.

Schultz (1937) also wrote, on the basis of ontogenetic changes in limb proportions that the ancestors of Pongo may have had shorter forelimbs than their modern versions.

The present results generally support this conclusion, as the reconstructed ancestor of the two extant Pongo species (i.e., P. pygmaeus and P. abelli) has limbs of slightly more equal length. The LCAH, on the other hand is reconstructed to have Gorilla-like IMI and

HFI, but generally extant ape-like proportions on PC 2. There are no known postcrania

50 belonging to the recent ancestors of Pongo, but like the 2B-PLS LCAH reconstruction, the potential early great ape, Oreopithecus (dated to ca. 8.5 Ma; Azzaroli et al., 1986), has Gorilla-like IMI (Straus, 1963).

Richmond et al., (2002) tested whether the hominin fossil record is characterized by behavioral diversity, and whether there was any evidence of evolutionary ‘reversals’ to more primitive (i.e., ape-like) morphologies as compared to A.L. 288-1. They used resampling methods to create distributions of selected limb proportions (i.e., traditional humerofemoral index and humerofemoral midshaft circumference index) in extant hominoid species, and compared these to the differences between pairs of fossil specimens (including OH 62 and BOU-VP 12/1). They suggested the results were consistent with evidence of reversals in OH 62 and possibly BOU-VP 12/1. They showed that differences in length proportions between fossil pairs could not be matched in extant hominoid samples, but that midshaft circumference differences were not uncommon in extant taxa. The results of the present analyses support the hypothesis that apparent differences in the limb proportions of extinct hominin taxa are likely to indicate behavioral variation or reversals, but three issues stand out.

First, the fragmentary condition of many associated hominin skeletons means that intermembral proportions cannot be calculated without estimating the maximum lengths of some long bones. Authors have visually estimated incomplete or missing long bone lengths (e.g., BOU-VP 12/1) (Asfaw et al., 1999) or they have used regressions based on

Pan, Homo, or other African ape models (see the disparate radius estimates of A.L. 288-

1) (Schmid, 1983; Asfaw et al., 1999). Richmond et al., (2002) used these estimates for their tests (although they recognize the problems associated with OH 62 long bone length

51 estimates, noting that their conclusions may be premature), but whether fossil hominins were actually much like modern African apes in terms of overall limb proportions remains to be determined. The affirmative seems unlikely due in part to the long bone estimates of the potential early hominin Ar. ramidus, whose proportions may have been more like extant arboreal quadrupeds (Lovejoy et al., 2009; Richmond et al., 2002).

The second issue is that in the present work extant monkeys effectively fill the gap between Pan and Homo along PC 1, which suggests that none of the extant African apes nor Homo are likely to provide an appropriate model for estimating IMI and HFI in the available fossils. Young et al., (2010) suggested that a more monkey-like phenotype should be expected for hominins intermediate to modern humans and a suspensory

PHLCA with long forelimbs. However, they demonstrated that the inferred forelimb-to- hindlimb proportions of fossil hominins led them to cluster near modern humans, on the other side of the quadrupedal monkeys from apes, with respect to the forelimb-hindlimb length allometric relationship. Thus, there is no evidence from hominins that their earliest representatives, or the PHLCA, had ape-like phenotypes. Whether the PHLCA was ape- like or monkey-like, should extant apes be used as models for fossil hominin limb proportions? If researchers are to use regressions based on extant model taxa, they must determine, without bias, which of the extant groups is the most appropriate model for early hominin limb proportions.

The third issue is that because previous research had not quantified how much variation exists within the overall limb proportions of extant taxa and functional groups, it was not possible to assess the significance of any fossil differences.

The present analysis has demonstrated quantitatively that extant hominoid genera can be separated using limb proportions alone, and that limb proportions covary with behavioral repertoires. This relationship means that extant hominoid limb proportions accord closely with their genera, and thus limb proportions may be useful to determine the likelihood that two fossil hominin specimens belong to the same genus or grade (as suggested by Wood, 1997). In a subsequent study we will use patterns of limb proportions variation in extant anthropoids to a) estimate and re-estimate fossil hominin associated skeletons’ major long bone lengths (i.e., those used to calculate traditional limb indices; see Mollison, 1910; Schultz, 1930), and b) modify the methods of

Richmond et al., (2002) to test whether the variation in fossil associated skeletons is consistent with grade hypotheses.

Considerations

This project uses modern and traditional methods to analyze traditional data to address proposals that limb proportions can be used to identify patterns of, and variation among, locomotor behaviors within the hominin clade. These analyses should be modified using long bone maximum lengths adjusted by the actual body mass or vertebral length of each extant specimen, similar to the allometric investigations of

Jungers (1980). Secondly, larger samples of more platyrrhine taxa should be included, as well as strepsirrhines who share some limb proportions more similar to Homo.

Phylogenetic comparative methods should also be calibrated using reconstructed fossil limb proportions (see Chapter 3). Limb proportions are meaningful aspects of species biology that can be evaluated quantitatively to understand extant taxa, and should be researched more intensely to refine how fossil variation is interpreted.

CHAPTER 2 FIGURES

Figure 2.1. Measurements Figure 2.1. Measurements

Figure 2.1. Demonstrations of the methods of measurement for the four linear variables collected on each of the four major long bones. Measurement definitions derive from those described in the Goldman Osteometric Dataset documentation.

Figure 2.2. Phylogenetic tree Figure 2.2. Phylogenetic tree

Figure 2.2. Phylogenetic tree of anthropoids used herein. Consensus molecular phylogeny was downloaded from the 10K Trees website and produced using Mesquite ver. 3.4. Dates inferred using mean molecular branch lengths. Several species from our dataset were not available on 10K Trees, thus conspecifics were substituted, and names changed. See the Methods: Phylogenetic comparative methods section above.

Figure 2.3a. Box plots

Figure 2.3a & 2.3b. Box plots of anthropoid traditional indices displaying ranges, means, 1st and 3rd quartiles, extremes, and outliers at the genus level. Miniature box plots summarize results at the superfamily level. Hominoid genera are more widely dispersed between low and high values for all indices, excluding CRI. Representatives of family Atelidae are shifted toward ape-like values for IMI and HFI as the only monkeys that exceed 100%. Sample sizes are in parentheses beside genus names.

Figure 2.3b. Box plots, continued Figure 2.3b. Box plots, continued

Figure 2.4. (A) Principal Components Analysis of Mosimann shape ratios: femur (FEM), tibia (TIB), humerus (HUM), and radius (RAD). (B) Principal Components Analysis of traditional indices: intermembral (IMI), humerofemoral (HFI), brachial (BRI), and crural (CRI). Loadings are given below each plot. Both plots are effectively identical and demonstrate the same relationships. On both axes, hominoid genera are distinct with little overlap, whereas nearly the entire cercopithecoid superfamily is subsumed within the ceboid superfamily. Along PC 1 Pan overlaps heavily with the monkeys (due largely to the Atelidae), but other apes show almost no overlap with monkeys. Homo sapiens clusters on the other end of PC 1 from other African apes, and shows little overlap with monkeys.

Figure 2.4a. PCA- Mosimann ratios Figure 2.4a. Principal components analyses- Mosimann ratios

Figure 2.4b. PCA- Traditional indices Figure 2.4b. Principal components analyses- Traditional indices

Figure 2.4. (A) Principal Components Analysis of Mosimann shape ratios: femur (FEM), tibia (TIB), humerus (HUM), and radius (RAD). (B) Principal Components Analysis of traditional indices: intermembral (IMI), humerofemoral (HFI), brachial (BRI), and crural (CRI). Loadings are given below each plot. Both plots are effectively identical and demonstrate the same relationships. On both axes, hominoid genera are distinct with little overlap, whereas almost all of the cercopithecoid superfamily is subsumed within the ceboid superfamily. Along PC 1 Pan overlaps heavily with the monkeys (due largely to the Atelidae), but other apes show almost no overlap with monkeys. Homo sapiens clusters on the other end of PC 1 from other African apes, and shows little overlap with monkeys.

Figure 2.5a. 2-Block PLS- Locomotor behavior vs. Traditional indices Figure 2.5a. 2-BPLS- Locomotor behavior vs. Traditional indices

Figure 2.51. Two-Block Partial Least Squares showing the positive and significant association between locomotor behavior (block 1) and traditional indices (block 2). In the given plot, IMI and HFI exhibit the strongest covariation with Bimanual Forelimb Suspension, whereas CRI and BRI covary more closely with Quadrupedal/Tripedal Walking, Vertical Climbing and Descent, and Bipedal Walking Here appear to be three major behavioral/morphological groupings among anthropoids: Asian apes, African apes joined by Ateles and Lagothrix, and monkeys joined by Homo sapiens.

Figure 2.5b. 2-Block PLS- Locomotor behavior vs. Mosimann ratios Figure 2.5b. 2-BPLS- Locomotor behavior vs. Mosimann ratios

Figure 2.5b. Two-Block Partial Least Squares showing the positive and significant association between locomotor behavior (PLS block 1) and Mosimann ratios (PLS block 2). Results of 2-BPLS are similar whether the shape block (block 2) is traditional indices or Mosimann ratios.

Figure 2.5c. 2-Block PLS- Positional behavior vs. Mosimann ratios Figure 2.5c. 2-BPLS- Positional behavior vs. Mosimann ratios

Figure 2.5c. Comparative Two-Block Partial Least Squares showing the positive and significant association between positional behavior (PLS block 1) and Mosimann ratios (PLS block 2). Locomotor data are provided in Table 2.6, based on Hunt (2010).

Figure 2.6. Phylomorphospace

falls with the World New falls

Pan

e, e,

flect some overall phylogenetic patterning, but

falls with the Hylobatidafalls

Pongo

Phylomorphospace

Figure 2.6. Figure

falls beyondfalls the demonstrates monkeys. This that great apes have relaxed phylogenetic constraints

Homo

Figure 2.6. Figure Phylomorphospace plot displaying a consensus molecular phylogeny mapped onto thetwo first principal components of species mean traditional Limbindices. proportions re relationships are complex at finer resolution. For instance, although great apes are more closely related to one another than they are to the or Hylobatidae monkeys, along PC 1 Atelidae, and on limb proportions, likely reflecting a potential for behavioral adaptation.

CHAPTER 2 TABLES

Table 2.1. Anthropoid sample TABLE 2.1. Anthropoid sample Superfamily Genus Species Males Females Unknown Total Hominoidea Homo sapiens 4,5 789 481 1270 Pan troglodytes 1,4,5 53 28 14 95 paniscus 5 9 9 18 Gorilla gorilla 1,2,4,5 37 27 2 66 beringei 4,5 3 4 7 Pongo pygmaeus 2,4,5 14 15 5 34 abelli 4 3 2 5 Hylobates lar 5 39 34 7 80 Symphalangussyndactylus 4 3 3 1 7 Total = 1582 Cercopithecoidea Cercopithecusalbogularis 5 4 9 mitis 1 1 Colobus guereza 5 8 9 3 20 Macaca fascicularis 5 10 10 20 nemestrina 4,5 2 6 8 Nasalis larvatus 5 3 5 2 10 Papio cynocephalus 3 19 18 37 hamadryas 3 2 2 Presbytis rubicunda 5 5 5 10 Procolobus badius 2 11 13 Theropithecusgelada 13 13 Trachypithecuscristatus 5 5 5 10 Total = 153 Ceboidea 5 Alouatta caraya 2 3 1 6 palliata 3 2 5 Aotus trivirgatus 3 3 6 Ateles fusciceps 3 3 6 geoffroyi 1 1 2 4 Callicebus moloch 3 2 5 Callimico goeldii 2 3 5 Callithrix jacchus 2 2 4 Cebuella pygmaea 4 1 5 Cebus albifrons 3 3 6 apella 2 3 5 Lagothrix lagotricha 1 1 2 4 Leontopithecuschrysomelas 3 2 5 rosalia 2 2 1 5 Saguinus fuscicolis 2 1 3 labiatus 3 3 6 oedipus 1 3 4 Saimiri sciureus 3 3 6 Total = 90 Total (N) = 1,825 Extant anthropoid sample. Provenance: 1) the American Museum of Natural History; 2) the Cleaveland Museum of Natural History; 3) the Kenyan National Museum; 4) the Smithsonian Institute's National museum of Natural History; 5) the Museum of Comparative Zoology, Harvard; 6) the Goldmann Osteometric Dataset. All Ceboidea data were collected from the Smithsonian Institution's National Museum of Natural History.

Table 2.2. Average percent inter-observer error measures per taxon TABLE 2.2. Average percent inter-observer error measures per taxon Powell (3D) - Ruff

FML TML HML RML

H. lar 0.30 0.38 0.43 0.6

Powell - Ruff

FML TML HML RML

H. lar 0.65 0.91 0.60 0.42

P. 0.88 0.99 0.6 0.76 troglodytes

P. 4.82 6.80 0.65 3.76 pygmaeus

Powell – Powell (3D)

FML TML HML RML

G. gorilla 10.4 10.30 11.77 11.15 8

H. lar 1.56 0.94 1.11 0.42

P. 3.13 1.17 2.41 2.56 troglodytes

Powell (3D) indicates data collected by Powell from 3D scans provided by Plavcan. Error formula (|x1 – x2|/x1 )*100. Values are species averages. Humeral maximum length (HML), radial maximum length (RML), femoral maximum length (FML), tibial maximum length (TML). Due to the disparity of hand-collected and 3D-derived measurements for Gorilla, only hand-collected data were used for this taxon.

Table 2.3. Tukey’s HSD results TABLE 2.3. Tukey’s HSD results at various levels.

Anthropoidea Anthropoidea Anthropoidea Hominoidea Hominoidea Cercopithecoidea Ceboidea

(Superfamily) (Genus) (Species) (Genus) (Species) (Species) (Species)

Humerus/GM 83.3% 68.4% 64.5% 90.0% 68.9% 47.0% 50.3%

Radius/GM 100.0% 84.9% 70.1% 90.0% 64.4% 72.7% 69.3%

Femur/GM 83.3% 74.6% 63.4% 90.0% 75.5% 69.7% 57.5%

Tibia/GM 100.0% 82.6% 77.9% 100.0% 77.8% 77.3% 59.5%

All Mosimann 83.3% 61.8% 47.6% 100.0% 80.0% 62.1% 57.5% shape ratios

Intermembral 100.0% 86.6 % 81.7 % 100.0% 82.6 % 69.6 % 73.4 %

Humerofemoral 100.0% 82.1 % 75.2 % 90.0% 76.1 % 60.8 % 66.9 %

Brachial 83.3% 67.3 % 53.6 % 90.0% 76.1 % 54.4 % 27.9 %

Crural 100.0% 66.2 % 60.3 % 80.0% 37.0% 49.4 % 23.4 %

All indices 83.3% 79.5% 72.8% 100.0% 82.2% 65.2% 63.4%

PC1 100.0% 85.8% 80.8% 100.0% 82.6% 67.1% 73.4%

PC2 100.0% 61.4% 56.6% 90.0% 67.4% 55.7% 22.1%

Number of 6 352 821 10 46 79 154 Comparisons

Displaying percentages of pairs correctly distinguished using traditional indices and Principal Components (PCs) at superfamily, genus, and species levels. In this table, Anthropoidea includes Homo, but Hominoidea does not so that the long legs of Homo do not bias results. Crural index is typically least effective at separating between groups, except for two instances in which brachial index distinguished fewer pairs: anthropoid at the superfamily and species levels. PCs are derived from traditional indices. PC 1 closely matches the distinctiveness of the Intermembral index. Number of Comparisons provides the number of pairs of taxa analyzed by Tukey’s HSD.

Table 2.4. PCA loadings TABLE 2.4. PCA loadings

Mosimann shape ratio PC 1 PC 2

Femur 0.59 0.30

Tibia 0.42 -0.50

Humerus -0.26 0.74

Radius -0.64 -0.35

Traditional index PC 1 PC 2

Intermembral index -0.74 -0.14

Humerofemoral index -0.59 -0.33

Brachial index -0.33 0.84

Crural index -0.05 0.41

PCA loadings for Mosimann shape ratios and traditional indices. Regarding Mosimann ratios, PC 1 captures variation in forelimb versus hindlimbs, whereas PC 1 captures variation in proximal versus distal elements. Regarding traditional indices, PC 1 captures variation mostly in intermembral and humerofemoral indices, whereas PC 2 captures intra-limb variation versus inter-limb variation.

Table 2.5. Percent locomotor behavior TABLE 2.5. Percent locomotor behavior Taxa QTW VCD BW OCT BFS DL

Alouatta caraya 1 87.3 1.3 4.9 0.0 0.0 6.5

Ateles geoffroyi 2 3.9 0.8 0.3 53.3 32.3 9.4

Cebuella pygmaea 3 22.9 52.3 1.2 2.9 0.0 20.7

Cebus albifrons 1 81.9 5.0 9.6 0 1.5 2.0

Cebus apella 4, 5 39.6 17.5 0.0 17.5 0.0 25.3

Cercopithecus albogularis 59.0 28.7 0.8 0.0 0.3 11.2

Cercopithecus mitis 48.1 30.5 2.3 0.0 0.0 19.1

Colobus guereza 21.9 14.2 2.7 0.0 1.4 59.7

Gorilla gorilla 50.0 37.7 1.9 5.7 4.7 0.0

Gorilla beringei 20.4 51.6 5.4 18.3 3.2 1.1

Hylobates lar 0.0 16.0 2.4 0.0 73.1 8.5

Lagothrix lagotricha 8.4 1.8 0.0 60.3 11.7 17.8

Macaca fascicularis 6 74.1 0.0 16.2 4.3 0.0 5.4

Macaca nemestrina 77.5 11.1 3.5 0.0 0.0 8.0

Pan paniscus 25.7 42.6 0.8 20.5 7.2 3.2

Pan troglodytes 27.5 55.5 4.7 6.2 5.7 0.5

Papio cynocephalus 97.9 1.3 0.3 0.0 0.0 0.5

Pongo abelli 19.8 27.4 7.6 21.7 23.6 0

Pongo pygmaeus 6.3 12.5 16.8 25.4 39.1 0.0

Presbytis rubicunda 30.2 11.3 0.0 0.0 2.1 56.4

Procolobus badius 28.9 25.7 2.6 0.0 0.8 42.1

Saimiri sciureus 7 73.8 4.3 0.5 0.3 0.3 20.7

Symphalangus syndactylus 0.0 25.5 6.2 1.3 64.5 2.5

(Continued from Table 2.5) Taxa and percent locomotor behaviors used in 2BPLS analyses, after Almécija et al. (2016). Quadrupedal/tripedal walking (QTW); vertical climbing and descent (VCD); bipedal walking (BW); orthograde clamber and transfer (OCT); brachiation and forelimb swing (BFS); drop and leap (DL). Congener data was substituted if locomotor data were not available: Alouatta caraya (A. palliata), Ateles geoffroyi (A. belzebuth), Presbytis rubicunda (average P. obscura and P. melalophos), Cercopithecus albogularis (average of Cercopithecus species per Hunt, 2016), Colobus guereza (average of Colobus species per Hunt, 2016), Papio cynocephalus (average of Papio species per Hunt, 2016). Macaca nemestrina (M. mulatta). All data from Hunt, 2016 unless specified otherwise: 1) Bezanson, 2009; 2) Cant et al., 2003; 3) Youlatos, 1999; 4) Gebo, 1989; 5) Wright, 2007; 6) Chatani, 2003; 7) Fontaine, 1990.

Table 2.6. Percent positional behavior

PLS analyses.

TABLE 2.6. Percent positional behavior positional Percent 2.6. TABLE

Proportions for of use 18 positional described modes in Hunt (2016). were usedThese for comparative 2B

Table 2.7a. 2-B PLS scores- Traditional indices TABLE 2.7a. 2-BPLS scores- Traditional indices Locomotor block PLS[,1] 1 PLS [,2] 2 PLS[,3] 3 PLS [,4] 4 QTW -0.5476834 0.2006976 0.2847672 0.62133095 VCD 0.2054308 -0.4616107 0.3649308 0.06675728 BW -0.1666791 -0.5539092 -0.6718971 0.01545780 OCT 0.2276626 -0.1099745 0.4718914 -0.40817221 BFS 0.6596108 0.4695293 -0.2972837 0.29898129 DL -0.3783418 0.4552675 -0.1524086 -0.59435512

Shape block- Traditional indices PLS[,1] 1 PLS [,2] 2 PLS[,3] 3 PLS[,4] 4 IMI 0.76816466 0.1007718 -0.2629729 0.5749899 HFI 0.62652528 -0.2085375 0.4706308 -0.5852220 BRI 0.08735810 0.9304742 -0.1203427 -0.3348194 CRI -0.09878102 0.2838573 0.8335884 0.4634628

Table 2.7b. 2-B PLS scores- Mosimann ratios TABLE 2.7b: 2-BLOCK PLS scores- Mosimann ratios Locomotor block PLS [,1] 1 PLS [,2] 2 PLS [,3] 3 PLS [,4] 4 QTW -0.5109275 -0.2550624 -0.3726742 -0.55983557 VCD 0.1900748 0.4651324 -0.4154208 0.39809546 BW -0.2218513 0.5627403 0.6461102 -0.21374535 OCT 0.2358534 0.1097255 -0.3700980 -0.05237641 BFS 0.6782591 -0.4263675 0.2947340 -0.22660334 DL -0.3714086 -0.4561683 0.2173488 0.65446521

Shape block- Mosimann ratios PLS [,1] 1 PLS [,2] 2 PLS [,3] 3 PLS[,4] 4 Gfem -0.4374314 0.2955952 0.8447658 0.08745259 Gtib -0.5260518 -0.2688716 -0.2574735 0.76464696 Ghum 0.4397209 0.7211940 -0.0794619 0.52934917 Grad 0.5818666 -0.5658717 0.4623461 0.35701055

Table 2.7c. Comparative 2-BPLS scores TABLE 2.7c: Comparative 2-BPLS scores Locomotor block ( Hunt, 2016) PLS 1[,1] PLS 2 [,2] PLS 3 [,3] PLS 4 [,4] sit -0.141809344 -0.707244360 0.390281357 0.267146110 lie -0.053657330 -0.244147127 0.121127731 -0.252125125 q.stand 0.133732067 -0.070729333 -0.473831447 0.496877752 squat -0.001830852 -0.010864993 0.012094385 -0.004550146 cling 0.035335927 -0.032325248 -0.198279956 -0.052548529 b.stand -0.040855046 -0.058574250 -0.111685116 -0.126506227 armhang -0.575719074 0.467708694 0.235290070 0.399400094 ips.suspend -0.074204256 -0.072533067 -0.120646432 -0.203943207 q.walk 0.655537691 0.140839170 0.112474719 0.433587648 vert.climb 0.027120895 0.178134012 -0.374064160 -0.276620304 leap 0.376991071 0.288520135 0.544002885 -0.298966723 q.run 0.029278833 -0.020472214 -0.129629827 -0.023742705 b.walk -0.037120062 0.009340347 -0.007716719 -0.045743654 brachiate -0.199078713 0.257097486 0.093693458 0.046200568 clamber -0.061454180 -0.056328184 -0.104366821 -0.158283332 suspensory -0.030275897 -0.041477976 -0.039134804 -0.113467949 transfer -0.009934432 -0.016689840 -0.007808233 -0.040765322

Shape block- Mosimann ratios PLS[,1] 1 PLS [,2] 2 PLS [,3] 3 [,4]PLS 4 Gfem 0.4310970 0.0313472 0.71699660 -0.5468899 Gtib 0.5318632 0.2163677 -0.67861014 -0.4580336 Ghum -0.4483072 -0.6482194 -0.15621008 -0.5953408 Grad -0.5747152 0.7293928 0.03166339 -0.3697107

Table 2.8. Phylogenetic signal TABLE 2.8. Phylogenetic Signal – Blomberg’s K and Multiple-K

Variable K P K P K- P K- P K- P K- P (non- Hominoids Monkey Cerc. Ceb. Homo) (non- Homo)

Intermem 0.98 0.001 1.65 0.001 1.25 0.007 1.06 0.001 1.24 0.004 2.03 0.001 bral

Humerofe 0.87 0.001 1.40 0.001 1.04 0.020 0.87 0.001 0.97 0.006 1.83 0.001 moral

Brachial 0.61 0.510 0.64 0.001 1.70 0.002 0.80 0.001 1.00 0.018 1.20 0.004

Crural 1.11 0.001 1.07 0.001 1.46 0.004 0.82 0.001 0.72 0.149 1.60 0.001

All Indices 0.90 0.001 1.35 0.001 1.32 0.001 0.92 0.001 1.00 0.001 1.81 0.001

Humerus 1.07 0.001 0.92 0.001 0.88 0.053 0.88 0.001 0.95 0.01 1.90 0.001

Radius 0.78 0.001 1.88 0.001 1.70 0.002 1.05 0.001 1.31 0.005 1.80 0.001

Femur 0.52 0.001 1.49 0.001 1.25 0.008 0.72 0.001 0.93 0.02 1.48 0.001

Tibia 1.17 0.001 1.26 0.001 1.25 0.008 1.20 0.001 1.17 0.007 2.13 0.001

All 0.85 0.001 1.40 0.001 1.21 0.001 0.98 0.001 1.09 0.002 1.85 0.001 Mosimann

Blomberg’s K for individual Mosimann shape ratios and traditional indices, as well as multiple K (Adams, 2014) for all Mosimann shape ratios and all traditional indices, in several groups of anthropoids. Homo was excluded from several calculations to better understand the effect of the genus on results. K < 1 indicates less similarity among closely related taxa than expected under Brownian motion, whereas K > 1 indicates greater similarity than expected. Most groupings are at least as similar as expected under Brownian motion, but for many K approaches or exceeds 1.

Chapter 3: Are extant apes appropriate models for fossil hominin limb proportions? Insights from machine-learning analyses

ABSTRACT

Limb proportions, which are important indicators of a taxon’s locomotor and positional behavior (Napier, 1967; Napier & Walker, 1967; Napier & Napier, 1967;

Fleagle, 1988; Richmond et al., 2002; see also Chapter 2), are only available for early hominin taxa (i.e., tribe Hominini: human lineage members since the last common ancestor of Pan and Homo) whose fossil record includes well-preserved associated skeletons, such as ARA-VP-6/500 and KNM-WT 15000 (Lovejoy et al., 2009; Brown et al., 1985). But well-preserved associated skeletons are extremely rare, so researchers resort to reconstructing incomplete skeletons, which runs the risk of adding unknown error to estimates of variables such as the intermembral index (see Reno et al., 2005;

Vančata, 2005; Harcourt-Smith, 2007). Most existing reconstructions are based on regression estimates derived from modern human or extant African ape models (e.g.,

Schmid, 1983; Asfaw et al., 1999). However, evidence from Miocene apes and

Ardipithecus ramidus (e.g., Straus, 1963, Lovejoy et al., 2009), as well as results of

Chapter 2, suggest that other extant primate taxa may be more appropriate models for extinct hominin limb proportions.

In this study we use Classification and Regression Trees (or CART) – a non- parametric machine-learning classification technique – to examine whether any extant anthropoids are suitable models to estimate the maximum lengths of fragmentary or unavailable long bones of fossil hominin associated skeletons. After adjusting for size, some hominins (i.e., Ardipithecus ramidus, Australopithecus afarensis, and Homo

75 floresiensis) are most like Old World monkeys. Conversely, averagely larger-bodied members of Homo (i.e., Homo georgicus and Homo ergaster) are most like Homo sapiens. No hominin skeleton was found to be like an extant non-human hominoid. The estimates of missing long bones have implications for hypotheses about the prevalence of forelimb-dominated arboreal locomotor behaviors in hominins or their recent predecessors.

INTRODUCTION

Hypotheses about the functional relevance of the limb proportions of hominins

(Ruff & Walker, 1993; Ruff, 1994; Richmond et al., 2002; Lovejoy et al., 2009, see also

Collard & Wood, 1999; Collard 2002) have often cited Napier and Napier’s (1967) discussion that intermembral index is predictive of dominant locomotor mode (Napier &

Napier, 1967; Fleagle, 1988). In Chapter 2, multivariate methods were used to explore the behavioral covariates and phylogenetic patterning of limb proportions among extant anthropoids. Results showed that 1) limb proportions distinguish extant monkeys and extant ape genera from one another in multivariate space; 2) limb proportions exhibit strong phylogenetic signal, but extant Homo and Pongo are less like their closest extant relative, and more similar to other anthropoids (i.e., monkeys and hylobatids, respectively); and 3) overall anthropoid limb proportions and positional behavioral repertoires are strongly linked.

The results of previous analyses are consistent with many foregoing authors (e.g.,

Schultz, 1930; 1937; Napier, 1967; Napier & Napier, 1967; Richmond et al., 2000;

Richmond et al., 2002; Moyà-Solà et al., 2004; Lovejoy et al., 2009; Almécija et al.,

2015), suggesting that the extant hominoids have diversified to meet the unique behavioral requirements of their ecological niches, highlighting that the prevalence of forelimb and hindlimb dominated behaviors is closely linked to the intermembral and humerofemoral indices. The derived phenotypes of the extant hominoids imply that their ancestors may have had intermediate limb proportions and behavioral repertoires that were unlike those of living genera (see Schultz, 1930; Straus, 1963; Lovejoy et al., 2009).

However, with the exceptions of KNM-WT 15000 (Homo ergaster; Brown et, al., 1985)

77 and potentially LB 1 (Homo floresiensis; Brown et al., 2004, but see below), no early hominin associated skeleton is sufficiently complete to directly measure or reliably estimate the maximum lengths of all four major long bones (i.e., those traditionally used in the calculation of traditional limb proportions: humerus, radius, femur, and tibia). Each specimen lacks at least one published maximum length estimate. This is important because overall limb proportions (i.e., intermembral, humerofemoral, brachial, and crural indices) best distinguish extant anthropoid genera, but the relatively poor preservation of many early hominin associated skeletons makes calculating their traditional indices impossible. For example, BOU-VP-12/1 lacks sufficient material for any tibia length estimates (Asfaw et al., 1999), and many ends of the remaining long bones are missing, making estimates questionable (see Reno et al.,2005). OH 62 has published length estimates for the major long bones except the tibia (Hartwig-Scherer & Martin, 1991;

Richmond et al., 2002), but Harcourt-Smith (2007) is correct that the maximum length estimates of OH 62 are also probably unreliable due to their poor preservation (see also

Richmond et al., 2002).

Even many of the best-preserved associated skeletons that have been more informative about hominin limb proportions are incomplete, but without these skeletons, there is not much that can be said about limb proportions. For example, ARA-VP-6/500

(Ardipithecus ramidus) lacks an associated humerus; its published humerus length is estimated from the humerus of its conspecific, ARA-VP-7/2 (Lovejoy et al., 2009). A.L.

288-1 (Australopithecus afarensis) lacks sufficient forearm material to make reliable estimates of the length of either radius or ulna; its published radius length estimates vary significantly depending on whether a human-like or Pan-like regression model is used

(Schmid, 1983; Asfaw et al., 1999; Richmond et al., 2002). The most complete associated adult skeleton from Dmanisi also lacks forearm bones, but it is otherwise relatively well- preserved (Lordkipanidze et al., 2007). An even more complete specimen, LB 1, has nearly complete representatives of all of the major long bones of the limbs, potentially including a radius. However, the radius from which the published measurements come may not belong to the LB 1 individual (Brown, 2004; Vančata, 2005).

Estimates of the lengths of long bones that are missing or incomplete have either been based on visual guesswork, or on regressions that use the observed limb proportions of Homo sapiens, Pan, or a combination of African apes (Schmid, 1983; Hartwig-Scherer

& Martin, 1991; Asfaw et al., 1999). However, evidence from Miocene apes and Ar. ramidus postcrania suggests that the extant apes, like modern humans, are derived and consequently may not be the most appropriate extant models for early hominin limb proportions (e.g., Ward et al., 1993a, 1993b; Straus, 1963; Moyà-Solà et al., 2004;

Lovejoy et al., 2009; Almécija et al., 2013). The problem with assuming extant African ape or human models is exemplified, for instance, in the markedly differing estimates for forearm bones belonging to Au. afarensis (see Schmid, 1983; Asfaw et al., 1999; see also

Richmond et al., 2002; Reno et al., 2005). This is problematic because, as previous research shows, monkey intermembral and humerofemoral indices are intermediate between Homo and African apes (Young et al., 2010; see also Chapter 2). Therefore, genetic propinquity alone may not be the most appropriate way to select a reference model for reconstructing the body proportions of extinct hominins.

Because limb proportions separate extant hominoid genera and are closely related to anthropoid behavioral specializations (see Schultz, 1937; Napier & Napier, 1967;

Fleagle, 1988; Chapter 2), it is crucial that researchers have reliable estimates of limb proportions for fossil specimens if the behavioral relevance of fossil variation is to be interpreted to explain the origins of human-like morphology, behavior, or taxic affinities

(see Richmond et al., 2002; Collard 2002). But rather than assume that an extant hominoid is the most appropriate model for fossil hominin limb proportions, the present study uses a non-parametric multivariate machine-learning classification technique (i.e.,

Classification and Regression Trees, or CART) to select the most appropriate extant anthropoid model genus for each fossil hominin associated skeleton based on three available size-adjusted published reliable major long bone lengths. Multiple linear regression then estimates and/or re-estimates the unavailable long bone lengths.

MATERIALS AND METHODS

Extant training sample

The extant anthropoid training dataset (n=1825) comprises the same long bone maximum length data that was described in Chapter 2. The diverse dataset allows the machine-learning methods to select from a much broader range of possible primate body plans than if samples were restricted to hominoids. It includes modern humans (n =

1,270) (789 males, 481 females), non-human hominoids (n = 305), cercopithecids (n =

153), and ceboids (n = 90). Where possible, each taxon has approximately balanced numbers of adult males and females (see also Chapter 2: Table 2.1).

Fossil sample

The fossil sample is comprised of the five most complete hominin associated skeletons for which there are published maximum length data for any three of the four major long bones - ARA-VP-6/500, A.L. 288-1, KNM-WT 15000, the Dmanisi adult,

80 and LB 1. Associated skeletons assigned to other hominin taxa (e.g., Orrorin,

Sahelanthropus, Australopithecus africanus, Australopithecus sediba, and Homo naledi) are excluded from these analyses because none of them have sufficient published long bone data. Two fossil hominin associated skeletons with sufficient published maximum lengths (i.e., OH 62 and BOU-VP-12/1) are excluded from the main analyses because their poor preservation calls into question the reliability of the published estimates of the incomplete long bones, but we do explore the implications our study has for generating more reliable estimates of their missing data. Published length data and sources of associated skeletons are provided in Table 3.2.

ARA-VP-6/500

The 4.4 Ma ARA-VP-6/500 individual from the Middle Awash, Ethiopia has been attributed to Ar. ramidus (Lovejoy et al., 2009; Suwa et al., 2009). The forearm (i.e., radius and ulna) and tibia are nearly complete. A femoral shaft lacking epiphyseal ends was also recovered, and a reliable estimate of its length was derived from a combination of comparison to modern human and chimpanzee femora, as well as from further investigation of the crural proportions of extant hominoids. Maximum length of the humerus of ARA-VP-6/500 was estimated from the humerus of a conspecific individual,

ARA-VP-7/2, by comparing the ratios of the humerus to the remaining forelimb elements

(i.e., radius, carpals, metacarpals) (Lovejoy et al., 2009).

A.L. 288-1

The 3.2 Ma Au. afarensis individual, A.L. 288-1, was for a long time the most complete early hominin associated skeletons (Johanson & Taieb, 1976; Ward, 2002;

Harcourt-Smith et al., 2004; Harcourt-Smith, 2007; Haile-Selassie et al., 2010), but other

81 well-preserved hominin specimens now exist (e.g., Walker & Leakey, 1983; Lovejoy et al., 2009; Brown et al., 2004; Lordkipanidze et al., 2007). The A.L. 288-1 skeleton includes a largely intact femur, two nearly complete humeri and one tibia, all of which are missing only small sections of their shafts. Published estimates exist for all of the major long bones of interest for this study, but the relatively poor preservation of the radial and ulnar fragments has resulted in disagreement about their complete lengths

(Schmid, 1983; Asfaw et al., 1999; see also Richmond et al., 2002); the radial length estimates differ by approximately four centimeters (Johanson et al., 1982; Jungers et al.,

1982; Schmid, 1983; Hartwig-Scherer & Martin, 1991; McHenry, 1992; Pontzer et al.,

2010; Asfaw et al., 1999; Lordkipanidze et al., 2007). The average of the two largest and two smallest humerus maximum length estimates reported by Johanson, 1982 (236.8 mm), Jungers and colleagues, 1982 (239 mm), Richmond and colleagues, 2002 (238 mm), and Lordkipanidze and colleagues, 2007 (235 mm) will be used in the present analyses.

KNM-WT 15000

The first known hominin associated skeleton to have limb proportions estimated to be in the range of modern humans is the c.1.55 Ma KNM-WT 15000, assigned to early

African Homo erectus/Homo ergaster, (Ruff & Walker, 1993; see also Argue et al.,

2006). The remarkable preservation of this skeleton has inspired decades of inquiry about the behavior and morphology of early Homo (e.g., Walker & Leakey, 1993;

Lordkipanidze, 2007; Pontzer et al., 2010). Representatives of all major long bones or analogues are in excellent condition, allowing either direct measurement or reliable estimates of maximum lengths (Walker & Leakey, 1993; Richmond et al., 2002). Of

82 these, only the radii belonging to KNM-WT 15000 were not recovered, but two well- preserved ulnae have allowed radius length to be predicted with confidence.

Homo georgicus/ergaster

Several well-preserved individuals belonging to an early population of small- brained Homo ergaster-like hominins have been recovered from Dmanisi in Georgia

(Lordkipanidze et al., 2007). In order to distinguish these individuals from KNM-WT

15000 this dissertation follows the initial publication and refers the Dmanisi evidence to

Homo georgicus. One of the associated skeletons, that of a large adult, preserves the humerus, femur, and tibia for which two published length estimates are available, but no forearm elements are preserved.

LB 1

A hominin associated skeleton dated to at least 60-100 ka (Sutikna et al., 2016) was recovered from Liang Bua in Flores (Brown et al., 2004; van den Bergh, et al., 2016;

Brumm et al., 2016) was referred to Homo floresiensis. The LB 1 individual includes at least one nearly complete example of all four major long bones, and maximum length estimates have been published for all (Brown et al., 2004; Morwood et al., 2005; Vančata

2005). However, the radius currently thought to belong to LB 1 was initially thought to belong to a conspecific, but was said to be about the right size for LB 1 (Brown et al.,

2004; Morwood et al., 2005). Vančata (2005), on the other hand, suggests that the radius in question is too long to belong to LB 1. The small size of the Homo floresiensis remains complicates comparisons with most modern human skeletal collections (Gordon et al.,

2008; Holliday et al., 2009), but LB 1 is included in the present analyses to understand how the small overall body size of a hominin may affect limb proportions.

Analytical Methods

Data collection

This study uses exactly the same collected measurements and size adjustments as described in Chapter 2, and Table 2.1 and Figure 2.1. For extant taxa, four maximum length measurements (i.e., humerus, radius, femur, and tibia) were collected from museum specimens and 3D surface scans following the protocols set out in the Goldman

Osteometric Dataset methodology (Auerbach & Ruff, 2004, 2006). Available fossil data were collected from the published literature (see Table 3.2). The four raw long bone measurements were size adjusted using Mosimann’s method (Jungers et al., 1995). Four traditional indices (i.e., intermembral, humerofemoral, brachial, and crural indices) were also calculated (Mollison, 1911; Schultz, 1930; Erikson, 1963; Napier, 1967; Napier &

Napier; 1967; Fleagle, 1988; Hunt, 2016).

This paper will estimate or re-estimate a) the humeral length of ARA-VP-6/500; b) the radial lengths of A.L. 288-1, Dmanisi, and LB 1; and c) the femoral length of

KNM-WT 15000. Although the published estimates for KNM-WT 15000 are reliable, its femoral length is re-estimated because it is a strongly functional element closely tied to cost of locomotion (Pontzer, 2005), and because having the actual bone allows the new estimate provided herein to be validated.

Classification and Regression Trees

Multivariate classification techniques such as Canonical Variate Analysis (CVA; known as Discriminant Function Analysis when only two groups are included) (Fischer,

1936, 1938; Rao, 1948; Albrecht, 1980) are classic and well-known methods that have been used in paleontological research to discriminate artifact and fossil-bearing facies

84 according to composition (Buzas, 1972; Culley et al., 2013), stone tool types (Eren &

Lycett, 2012), sex identity (Giles & Elliot, 1963), “race” affiliation (Bidmos & Dayal,

2003), and aspects of behavior (Carlson & Van Gerven, 1977). CVA derives from multiple regression analyses and multivariate analysis of variance, in that it uses canonical functions (i.e., linear combinations of variables) from multiple independent variables to quantitatively group observations into previously defined categories by maximizing the differences between groups and minimizing those within (James &

McCulloch, 1990). However, CVA has requirements and limitations that cannot necessarily be met with the large, macroevolutionary-scale, biological dataset of this study (James & McCulloch, 1990; Johnson & Wichern, 1998). Specifically, 1) there must be homogeneity of variance-covariance matrices; 2) variables must have a multivariate normal distribution; 3) variables must not represent singularities (i.e., instances of perfect correlation between explanatory variables); 4) outliers are highly problematic; 5) prior probabilities for class assignments must be known before building discriminant models;

6) inter-variable relationships must be linear. The present study uses an alternative classification method, described below, to avoid introducing these sources of error.

A newer classification method called Classification and Regression Trees

(CART) provides an alternative to traditional discriminant techniques. Based on decision- tree machine-learning, CART uses non-parametric recursive binary partitioning of a set of descriptor variables to assign observations to one of several categories (Breiman et al,

1984; Clark & Pregibon, 1992; Ripley, 2007; Loh, 2011). CART predicts the categorical classification of samples based on series of if-then logical conditions. Ecologists have recently begun to take advantage of CART as a classification tool because of its

85 flexibility in handling multiple response variable types (e.g., continuous, categorical, or rank data) and its robustness against nonlinear relationships (i.e., invariance to transformations of explanatory variables), singularities (which actually strengthen CART by maximizing available information), high-order interactions (i.e., interactions between variables affected by one or more other variables), and missing values (De’ath &

Fabricious, 2000; Prasad et al., 2006). Researchers have used CART in the study of species and community distributions (Vayssières et al., 2000) and the effect on species abundance due to land use changes (De’ath & Fabricious, 2000). Here, CART predicts the categorical (i.e., extant anthropoid genus) classifications of fossil specimens according to their available long bone lengths. The regression describing the linear relationships of those variables with the fourth long bone length is then used as a model to estimate the lengths of unavailable long bones.

CART is used here to build regression trees from several extant anthropoid training datasets. Each training set is a version of the original anthropoid dataset that includes only three size-adjusted variables: the long bone lengths corresponding to those available for each hominin associated skeleton in the fossil sample. Each variable is size adjusted by the GM of only the three long bone lengths available. For example, this study seeks to estimate the lengths of the radii belonging to A.L. 288-1, Homo georgicus, and

LB 1, and thus will train CART predictions for these fossils using a training dataset comprising Mosimann shape ratios calculated on only the maximum lengths of the humerus, femur, and tibia. The tree that best defines extant taxa on the basis of those three Mosimann ratios is then used to predict the best comparative model with which to regress radius length.

CART for classification

The CART technique works by choosing one variable that best divides the entire dataset around a specific value for that variable, resulting in 2 child nodes that are, respectively, associated with all values below and above the parental node variable value

(De’ath & Fabricious, 2000; Loh, 2011); the resultant child nodes are more homogeneous within themselves than between. The process is recursively iterated for each child node, thereby progressively dividing the remaining data by choosing the values of the remaining variables that best divide the dataset until all further partitioning around any variable results in less optimal trees. Trees are then “pruned” (or “scaled-back”) based on the lowest recovered true prediction error estimate, which requires cross-validation approaches to choose the best tree for description or subsequent prediction (De’ath &

Fabricious, 2000).

Cross-validating CART

As with any model fitting procedure, cross-validation must be performed on

CART to assess the predictive performance of models to determine how well results can be generalized to independent datasets (i.e., datasets other than those used to train the model). There are currently two methods by which CART trees can be cross-validated.

The first, which uses a random subset of the data from every subgroup and requires a cross-validation sample that is one-half to two-thirds of all the data, results in a prediction error value calculated from the predicted and observed values (Breiman et al., 1984;

De’ath & Fabricious, 2000; Loh, 2011). The tree with the smallest prediction error is then selected as the best tree. However, this method requires large samples for each subgroup of the dataset, which cannot be met for several monkey taxa.

The second method, and the one employed in the present work, uses K-fold cross- validation to 1) divide the dataset into K subsets of equal size, where in this case K = 10;

2) drop one subset and use the remaining data to build a tree to predict the dropped subset, and repeat for each subset K; 3) calculate estimated error for each subset and sum over all subsets; and 4) select the tree with the smallest estimated error rate (De’ath &

Fabricious, 2000). CART analyses, including partitioning and cross-validation, were performed using the ‘RPART’ package (Therneau, 1997; Atkinson, 2000). All analyses, including those described below, were performed in R version 3.4.4 (R Core Team,

2017).

Multiple linear regression

Single-response multiple linear regressions of CART-selected extant model taxa produce regression equations to estimate or re-estimate unavailable or questionable hominin long bone lengths. To generate each equation, the predictor variables (X) are the three unadjusted long bone maximum lengths corresponding to those available for the hominin associated skeleton in question. The response variable (Y) is the unavailable or questionable long bone length of interest. All linear equations were produced using the

‘lme4’ package (Bates et al., 2015). Prediction intervals were calculated using the

‘predict’ function in base R.

Comparative analyses

Boxplots and Principal Components Analysis (PCA) were used to visualize the placement of reconstructed hominin specimens in the context of a macroevolutionary- scale anthropoid morphospace. Boxplots allow comparison of fossil specimens and extant genera using individual limb proportions (i.e., intermembral, humerofemoral, brachial,

88 and crural indices). PCA, on the other hand, allows visual comparisons using all traditional indices simultaneously by reducing the number of input variables to two indices (i.e., principal components) that are linear combinations of the original variables in lower-dimensional space. Boxplots and PCA biplots were produced using ‘ggplot2’

(Wickham, 2009). PCA was performed using the ‘prcomp’ function in base R.

RESULTS

To test whether any extant hominoid is a suitable model for fossil hominin limb proportions, Classification and Regression Trees (CART) and multiple regressions were used to choose the best available extant models with which to estimate and re-estimate a) the humeral maximum length for ARA-VP-6/500 (Ar. ramidus), b) radial maximum lengths for A.L. 288-1 (Au. afarensis), LB 1 (H. floresiensis), and the Dmanisi adult (H. georgicus), and c) the femoral maximum length for KNM-WT 15000 (H. ergaster).

Some of the predictions for missing long bones are close to the published estimates. For example, the predicted maximum length for the ARA-VP-6/500 humerus (245.5 mm, error = 4.5) is 6% shorter than the published estimate (261.5 mm; Lovejoy, 2009;

Lovejoy et al., 2009), and the KNM-WT 15000 femoral prediction (448.8 mm, error =

10.3) exceeds the mean published value (432 cm; Walker & Leakey, 1983) by only 4%.

On the other hand, some predictions were substantially different from the published values. The mean prediction for the maximum length of the A.L. 288-1 radius (251.9 mm, error = 4.7) was 31% longer than the published length obtained from an H. sapiens regression (174 mm; Schmid, 1983; Richmond, 2002), and 15% longer than an estimate based on a Pan regression (215 mm; Asfaw et al., 1999; Richmond et al., 2002).

Similarly, the predicted radius length of LB 1 (252.8 mm, error = 4.7) exceeds the

89 published value of 210 mm by 17% (Brown et al., 2004; see also Vančata, 2005, which suggests 210 mm is too long, although no alternative measurement is provided). Specific results of fossil hominin CART classifications and regressions are provided in Table 3.3.

These estimates are interpreted in the discussion below.

CART prediction found that most of the hominins (i.e., Ar. ramidus, Au. afarensis, and H. floresiensis) were most similar to extant generalized monkeys, independent of which of the forelimb bones were unavailable. CART repeatedly selected the genus Papio, but the marked overlap among monkeys may reduce the method’s precision in that regard. Thus, generic affiliation notwithstanding, available long bone length relationships of many hominins are more similar to those of extant generalized monkeys, and perhaps specifically genus Papio. The other two specimens belonging to

H. ergaster and H. georgicus are most similar to the long bone length relationships in H. sapiens.

Using the new predicted maximum lengths, when looking at box plots of intermembral, humerofemoral, and brachial proportions, the Ar. ramidus and Au. afarensis estimates, which are distinct from those of fossil Homo, substantially overlap the values of extant monkeys and have some overlap with the upper outliers of H. sapiens. The values for H. floresiensis fall among the non-Homo fossil hominins (Figures

3.3a, b). In a Principal Components Analysis (PCA) of overall limb proportions, the non-

Homo reconstructions plus LB 1 all fall well within the monkey region of the PCA space and are distant from the PCA space occupied by any extant hominoid. Both H. ergaster and H. georgicus are well within the H. sapiens cluster (Figure 3.2).

DISCUSSION

Limb proportions are closely tied to locomotor behavior and taxonomy in extant hominoids (Schultz, 1937; Napier and Napier, 1967; Jungers, 1985; see also Chapter 2).

Thus, reliable estimates of hominin limb proportions are an important component of interpreting the functional and taxic affinities of extinct taxa based on their inferred locomotion. However, the analysis of traditional limb proportions is hindered, in part, because hominin skeletons are typically recovered with damaged or incomplete long bones, requiring their lengths to be estimated by observation or regression. The observations of trained experts are invaluable, but they are inevitably qualitative.

Regression estimates require the selection of model taxa, the criterion of which has traditionally been phylogenetic relatedness, and Reno et al., (2005) showed how much estimates of individual specimens (e.g., OH 62, BOU-VP-12/1, and the radius of A.L.

288-1) can differ depending on a model’s taxic composition (Johanson, 1987; Asfaw et al., 1999; Richmond et al., 2002). Instead, this study used a multivariate machine- learning classification method (i.e., Classification and Regression Trees, or CART) to test which of the extant anthropoid genera in the available sample have limb proportions most similar to available overall hominin lengths, and then used regressions based on those genera to estimate unavailable fossil long bone lengths.

For Homo georgicus and Homo ergaster CART selected H. sapiens as the most appropriate model. Among the early hominins, with the exception of OH 62 for which

Pan was selected, CART consistently selected extant generalized monkeys, and not

African apes, as the most appropriate model for reconstructing limb proportions. This is consistent with over a century of investigations (Mollison, 1911; Schultz, 1930; 1937;

Napier & Napier, 1967; Fleagle, 1988) that have demonstrated that modern humans are much more similar to extant monkeys than to extant hominoids in terms of intermembral

(IMI) and humerofemoral indices (HFI). Monkeys fill the morphospace between modern humans and extant hominoids such that a phylomorphospace uncalibrated with relevant fossil specimens predicts the Pan-Homo last common ancestor (PHLCA), and the trajectory from it to modern humans on the first axis, as passing through ‘generalized monkey-like’ (i.e., symmetrical) IMI and HFI (but squarely within the range of extant hominoids for BRI and CRI) (Chapter 2; see also Young et al., 2010).

Although the differences between the new regression estimates and those published for A.L. 288-1 and LB 1 are substantial, they should not be rejected out of hand. The forearm bones of A.L. 288-1 are heavily damaged, and the radius attributed to

LB 1 may not belong to the LB 1 individual (see Brown et al., 2004; Vančata, 2005), so there is no material against which to reliably assess the new estimates. However, the new estimate for the femur of KNM-WT 15000, which is the only skeleton in the fossil sample that has nearly all of its long bones either well-preserved or their lengths reliably estimated, is consistent with the observed length, and the new estimate of the ARA-VP-

6/500 humerus was also close to the length regressed from the preserved forelimb proportions of a conspecific.

Considering the origins of hominin behavior

The results of this study suggest that the limb proportions of some fossil hominins

(and perhaps the PHLCA) are better characterized as generalized monkey-like rather than

African ape-like. CART consistently chose one monkey genus (Papio) as the most appropriate model for reconstructing hominin limb proportions. This accords with

92 ancestral state reconstructions (ASR) in phylomorphospace plots that predict a PHLCA in the IMI and HFI range of the Atelidae, and a trajectory through extant monkeys leading to modern Homo on PC 1 (Chapter 2: figure 2.6; see also Young et al., 2010). While the newly reconstructed overall fossil limb proportions were not available to calibrate primitive and derived traits for the phylomorphospace (thus ancestral reconstructions may be imprecise), the analyses are consistent with the hypothesis that obligate bipedalism arose from a generalized monkey-like hominoid ancestor.

Some Miocene postcrania (e.g., Afropithecus, Ekembo, Equatorius,

Pierolapithecus, and Nacholapithecus), as well as Ar. ramidus, retain limb length proportions and features of the trunk, hand, and wrist associated with monkey-like palmigrade quadrupedalism (Leakey & Leakey, 1986; Ward et al., 1993a, 1993b; Ward et al., 1999; Nakatsukasa, et al., 2003; Moyà-Solà et al., 2004; Lovejoy et al., 2009).

Considering these, Lovejoy et al., (2009) claimed that the extant apes represent so-called adaptive ‘cul-de-sacs’, having independently acquired their adaptations to orthograde climbing and suspension from an ancestor that was, in their view, almost certainly a predominantly palmigrade arboreal quadruped. Thus, instead of a series of adaptations toward, and then away from, extant ape-like forelimb-dominated climbing and suspensory adaptations, the most parsimonious conclusion is that hominin ancestors never had intermembral indices in the range of extant apes, and thus were never as adapted to forelimb-dominated behaviors (i.e., suspension) as modern hominoids appear to be. Under this scenario hominins and their precursors may have always had generalized monkey-like limb proportions, from which forms with elongated hind-limbs were derived (Lovejoy, 2009; Lovejoy et al., 2009).

On the other hand, the limb proportions of fossils like Oreopithecus (Straus, 1963;

Jungers, 1987) and Hispanopithecus (Moyá-Solá & Khöler, 1996) suggest that some early great apes had IMI in the ranges of the extant climbing hominoids (although lacking the specialized BRI of true brachiators like Hylobates). Whether or not forelimb dominated locomotion and associated phenotypes are ancestral in African apes remains unknown, but if adaptations to extant ape-like forelimb dominated behaviors characterize the great ape clade, hominins and their precursors may have passed through a period of monkey-like intermembral proportions as they acquired the short forelimbs and long hindlimbs of modern humans (see Young et al., 2010). Young et al., (2010) work from this hypothesis, but they demonstrated that intermembral proportions of selected fossil skeletons (i.e., A.L. 288-1, BOU-VP-12/1, and OH 62) are intermediate between extant monkeys and Homo, and are not intermediate between extant monkeys and apes, nor are they within the ape range. This accords with the Principal Components Analysis (PCA) presented in this thesis, which places all fossil hominins (excluding H. georgicus and H. ergaster) squarely within the extant generalized monkeys on the first two axes.

Although it has been demonstrated that overall limb proportions are closely tied to positional behavioral repertoires in extant taxa, the observation that fossil hominins share l intermembral and humerofemoral indices with generalized monkeys should not be taken to indicate that extant monkeys are literal models for the locomotor and positional behavior of fossil hominins. For example, other indicators of hominin locomotor and positional behavior, such as phalangeal, joint, muscle-attachment, and pelvic morphology

(Susman & Creel, 1979; Stern, 1982; Stern & Susman, 1983; Latimer & Lovejoy, 1990;

Richmond, 1998; Ward, 2002; Harcourt-Smith et al., 2004; Richmond & Jungers, 2008;

Susman & Susman 2008; Ruff, 2009; Lovejoy et al., 2009; DeSilva et al., 2013) are consistent with orthogrady. Evidence of orthograde adaptations (or of ‘pre-adaptations’ that could later be co-opted to orthogrady) is also apparent in several Miocene taxa, including Oreopithecus and Hispanopithecus (Straus, 1963; Moyà-Solà & Kholer, 1996).

Even the probable quadruped, Pierolapithecus, had an orthograde-like trunk (e.g., wide, antero-posteriorly-compressed thorax, and transverse processes arising from the junction of the vertebral pedicles and bodies), but also had short digits with palmigrade wrist morphology and only moderately-curved phalanges (Moyà-Solà et al., 2004).

Pierolapithecus is particularly interesting because its combination of ape-like trunk morphology and monkey-like wrists and digits suggest that it, like extinct hominins, exhibited behavior not seen in extant anthropoids (see also Almécija et al., 2009). Thus, whether hominins and their precursors maintained or secondarily acquired generalized monkey-like limb proportions, the evolution of orthograde trunk posture in hominoids could have promoted a radiation of unique behavioral repertoires and associated phenotypes that could have provided the basis for bipedal behaviors.

Because fossil long bone length proportions are rarely available, or can be reliably estimated, for fossil hominins, researchers have used other functionally relevant fossil anatomy (e.g., long bone articular and diaphyseal dimensions) to make inferences about fossil hominin behavior and locomotor adaptations (McHenry & Berger, 1998; Richmond et al., 2002; Green et al., 2007). Green et al., (2007) used Monte Carlo resampling methods to generate distributions and compare upper-to-lower limb joint size and diaphyseal dimensions for extant great ape genera, Au. afarensis, and Au. africanus. The results for extant taxa accord with the results of this thesis (see also Chapter 2 and

Figures 2.5a-c) demonstrating that the most arboreal taxon in their sample (i.e., Pongo) had the greatest upper-to-lower values, whereas bipedal H. sapiens had the smallest upper-to-lower values, with the African apes intermediate. Among the fossil sample, however, they found that Au. africanus had more ape-like upper-to-lower values, whereas

Au. afarensis was more modern human-like. Although long bone length proportions (e.g., traditional indices) are closely tied to locomotion in extant primates, joint and shaft dimensions are also functionally relevant and respond to mechanical demands and force transmission (Jungers, 1988; Godfrey et al., 1995; Ruff, 2002). Thus, the more modern human-like condition reported in Green et al., (2007) may indicate that the locomotor repertoire of Au. afarensis was forelimb-dominated, but the generalized monkey-like overall proportions may be primitive retentions that do not reflect its actual locomotor specializations. Considering the strong association between phenotype and behavior seen across extant anthropoids (see Figures 2.5a-c), it seems unlikely that fossil hominins with limb proportions unlike those of any H. sapiens (e.g., Au. afarensis and H. floresiensis) were bipedal in the sense that modern humans are.

Conclusions

This paper explored new methods to select appropriate models for estimating hominin limb proportions and showed that many fossil hominins share the morphospace occupied by extant monkeys, but the various implications remains to be determined (see Huxley,

1958; Wood & Collard, 1997; Collard & Wood, 1999; Collard, 2002; Richmond et al.,

2002; see also Villmoare, 2017; Wood & Boyle, 2016). The degree to which the limb proportions of individual hominin specimens differ must be evaluated in the context of the variation seen in extant taxa (see White, 2003; Ackermann & Smith, 2007). Omitting

96 the cladistic implications and focusing only on the link between phenotype and behavior, the next chapter explores the possible implications of these results for the locomotor component of the hominin grade scheme proposed by Collard and Wood (1999) and

Collard (2002).

CHAPTER 3 FIGURES Figure 3.1a. CART decision tree- No humerus Figure 3.1a. CART decision tree- No humerus

Figure 3.1a. Graphical representation of the decision tree constructed by CART analyses excluding the humerus. All long bones are size adjusted by the geometric mean. The variables used in the tree- building process, in order of importance, are radius, femur, and tibia.

Figure 3.1b. CART decision tree- No radius Figure 3.1b. CART decision tree- no radius

Figure 3.1b. Graphical representation of the decision tree constructed by CART analyses excluding the radius. All long bones are size adjusted by the geometric mean. The variables used in the tree-building process, in order of importance, are femur, humerus, and tibia.

Figure 3.1c. CART decision tree- No femur Figure 3.1c. CART decision tree- no femur

Figure 3.1c. Graphical representation of the decision tree constructed by CART analyses excluding the femur. All long bones are size adjusted by the geometric mean. The variables used in the tree-building process, in order of importance, are radius, tibia, and humerus.

100

Figure 3.1d. CART decision tree- No tibia Figure 3.1d. CART decision tree- no tibia

Figure 3.1d. Graphical representation of the decision tree constructed by CART analyses excluding the tibia. All long bones are size adjusted by the geometric mean. The variables used in the tree-building process, in order of importance, are femur, radius, and humerus.

101

Figure 3.2. Comparative PCA

Figure 3.2a. Comparative PCA

Figure 3.1. Comparative Principal Components Analysis of Mosimann ratios: femur, tibia, humerus, and radius (98.9% explained variation). In this PCA space, hominoid genera are distinct with little overlap, whereas nearly the entire superfamily Cercopithecoidea is subsumed within the superfamily Ceboidea. Most non-Homo specimens fall in the range of extant monkeys, regardless of their respective genera, whereas larger-bodied Homo species fall in the range of Homo sapiens.

102

Figure 3.2b. Comparative PCA

Figure 3.2. Comparative Principal Components Analysis of Mosimann ratios: femur, tibia, humerus, and radius (98.9% explained variation). In this PCA space, hominoid genera are distinct with little overlap, whereas nearly the entire superfamily Cercopithecoidea is subsumed within the superfamily Ceboidea. Most non-Homo specimens fall completely in the range of extant monkeys, regardless of their respective genera, whereas larger-bodied Homo species fall completely in the range of Homo sapiens. Fossil limb proportions used to produce the PCA are provided in Table 3.4.

103

Figure 3.3a. Comparative box plots Figure 3.3a. Comparative box plots

Figure 3.3a. Box plots of comparative anthropoid traditional indices, displaying ranges, means, 1st and 3rd quartiles, extremes, and outliers at the genus level. For each index, excluding the crural index, larger-bodied hominins fall within the range of extant Homo sapiens. Australopith-grade hominins (diamonds) overlap most consistently with monkeys, but their brachial indices also overlap with the Asian apes. The small-bodied LB 1, Homo floresiensis (green square) falls nearest the other non- Homo hominins in all cases. In terms of crural index, however, several fossil hominins fall with hominoids and H. sapiens, and between KNM-WT 15000 and Dmanisi. ARA-VP-6/500 falls within the humerofemoral range of H. sapiens, and very near Dmanisi, but the differences between most Homo and non-Homo hominins is reduced for this index as compared to intermembral and brachial indices. Taken together, these results indicate that differences in radius length are driving the gulf between body types hominins. Fossil limb proportions used to produce the PCA are provided in Table 3.4.

104

Figure 3.3b. Comparative box plots Figure 3.3b. Comparative box plots

Figure 3.3b. Box plots of comparative anthropoid traditional indices, displaying ranges, means, 1st and 3rd quartiles, extremes, and outliers at the genus level. For each index, excluding the crural index, larger-bodied hominins fall within the range of extant Homo sapiens. Australopith-grade hominins (diamonds) overlap most consistently with monkeys, but their brachial indices also overlap with the Asian apes. The small-bodied LB 1, Homo floresiensis (green square) falls nearest the other non-Homo hominins in all cases. In terms of crural index, however, several fossil hominins fall with hominoids and H. sapiens, and between KNM-WT 15000 and Dmanisi. ARA-VP-6/500 falls within the humerofemoral range of H. sapiens, and very near Dmanisi, but the differences between most Homo and non-Homo hominins is reduced for this index as compared to intermembral and brachial indices. Taken together, these results indicate that differences in radius length are driving the gulf between body types hominins. Fossil limb proportions used to produce the PCA are provided in table 3.4.

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CHAPTER 3 TABLES

Table 3.1. CART validation results TABLE 3.1. CART validation results Ar. ramidus Alouatta Ateles Nasalis Pan Papio 0.05 0.07 0.10 0.07 0.70 A. afarensis Cebus Colobus H. sapiens Nasalis Papio Procolobus Trachypithecus (a) 0.02 0.02 0.02 0.13 0.63 0.14 0.05 (b) 0.02 0.02 0.02 0.13 0.63 0.14 0.05 A. garhi Cebus Colobus Presbytis Procolobus Saguinus Saimiri Trachypithecus (a) 0.67 0.04 0.29 (b) 0.03 0.08 0.03 0.03 0.06 (c) 1 (d) 0.67 0.29 H. habilis Alouatta Ateles Cebuella Gorilla Lagothrix Leontopithecus Macaca Nasalis Pan Papio (a) 0.07 0.03 0.01 0.02 0.02 0.01 0.85 (b) 0.05 0.05 0.21 0.60 0.02 0.05 0.05 H. georgicus H. sapiens (a) 0.99 (b) 0.99 H. ergaster H. sapiens 1 H. floresiensis Cebus Colobus H. sapiens Nasalis Papio Procolobus Trachypithecus 0.02 0.02 0.02 0.13 0.63 0.14 0.05

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Table 3.2. Published fossil sample TABLE 3.1. Published fossil sample Specimen Humerus Radius Femur Tibia ARA-VP-6/50015 261.5 250 312 262 235,14 236.8,1 (235.9), 280,14 280.5,4 A.L. 288-1 238,9 2392 (238.5) 174,3 2158 28118 (280.5) 2415 BOU-VP-12/18 226, 236 231 335, 348 - OH 624 264 210, 246 280 - Dmanisi14 295 - 382,18 386 306 KNM-WT 150006 319 255 429,18 432 380 LB 110 243 210 280 235 Published fossil long bone length measurements and estimates. Multiple values for a given long bone length indicate varying published values. Values in parentheses are averages of preceding values within 10 mm of one another used in these analyses. Bold values are published length estimates of unavailable or incomplete long bones. Dashes are unavailable and unpublished lengths. Bold values will be re-estimates, and dashes will be predicted with CART-selected model taxa. 1) Johanson et al., 1982; 2) Jungers et al., 1982; 3) Schmid, 1983; 4) Hartwig-Scherer & Martin, 1991; 5) McHenry, 1992; 6) Walker & Leakey 1993; 8) Asfaw et al., 1999; 9) Richmond et al., 2002 ; 10) Brown, et al., 2004; 11) Steudel-Numbers & Tilkens, 2004; 12) Moorwood et al., 2005; 13) Vančata, 2005; 14) Lordkipanidze et al., 2007; 15) Lovejoy et al., 2009; 18) Pontzer et al., 2010.

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Table 3.3. Fossil regression estimates results TABLE 3.4. Reconstructed fossils limb proportions Specimen Num Grade Class Model Fem Tib Hum Rad Error IMI HFI BRI CRI PI- PI+ ARA-VP-6/500 arr.0 Au. regression Papio 312 262 245.5 250 4.5 86.3 78.7 101.8 84.0 238 256 A.L. 288-1 auaf.01 Au. regression Papio 281 241 235.9 251.2 4.7 93.3 84.0 106.5 85.8 249 255 A.L. 288-1 auaf.02 Au. regression Papio 281 241 238.5 252.7 4.7 94.1 84.9 106.0 85.8 253 256 BOU-VP-12/1 aug.01 Au. regression Colobus 335 279.7 226 231 2.6 74.3 67.5 102.2 83.5 258 303 BOU-VP-12/1 aug.02 Au. regression Saguinus 348 266.8 236 231 2.2 76.0 67.8 97.9 76.7 115 419 BOU-VP-12/1 aug.03 Au. regression Presbytis 348 312.1 226 231 2.6 69.2 64.9 102.2 89.7 253 358 BOU-VP-12/1 aug.04 Au. regression Colobus 335 280.6 236 231 2.9 75.9 70.4 97.9 83.8 260 303 OH 62 hha.01 Au. regression Pan 280 217.1 264 210 6 95.4 94.3 79.5 77.5 211 223 OH 62 hha.02 Au. regression Pan 280 229.4 264 246 1.7 100.1 94.3 93.2 81.9 226 232 KNM-WT 15000 her.0 Ho. regression Homo 448.8 380 319 255 10.3 69.3 71.1 79.9 84.7 448 450 Dmanisi hge.01 Ho. regression Homo 384 306 295 212.6 7.5 73.6 76.8 72.1 79.7 212 214 Dmanisi hge.02 Ho. regression Homo 384 306 282 208.4 7.5 71.1 73.4 73.9 79.7 208 209 LB 1 hfl.01 regression Papio 280 235 243 253.56 4.7 96.4 86.8 104.3 83.9 250 258 ARA-VP-6/500 arr.1 Au. publication 312 262 261.5 250 89.1 83.8 95.6 84.0 A.L. 288-1 auaf.1 Au. publication 281 241 235.9 174 78.5 84.0 73.8 85.8 A.L. 288-1 auaf.2 Au. publication 281 241 238.5 215 86.9 84.9 90.1 85.8 KNM-WT 15000 her.1 Ho. publication 432 380 319 255 70.7 73.8 79.9 88.0 KNM-WT 15000 her.2 Ho. publication 429 380 319 255 71.0 74.4 79.9 88.6 LB 1 hfl.1 publication 280 235 243 210 88.0 86.8 86.4 83.9 Unadjusted maximum lengths and estimates of femur (Fem), tibia (Tib), humerus (Hum), and radius (Rad). Traditional limb indices: intermembral (IMI), humerofemoral (HFI), brachial (BRI), and crural (CRI). Emphasized values are regression estimates based on model taxa indicated in the Model column. OH 62 and BOU-VP-12/1 are included for comparative purposes only, as their poor preservation has reduced the reliability of any published long bone maximum length estimates. Prediction intervals (PI) calculated in R.

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Table 3.4a. Regression formulae TABLE 3.4a. Regression formulae Ar. ramidus Papio Humerus Radius Femur Tibia 250 312 262

Residuals: Min 1Q Median 3Q Max -6.2879 -2.4884 0.1205 1.3032 12.3030

Coefficients: Estimate Std. Error t value P (Intercept) 10.3827 5.9741 1.738 0.0915 rad 0.3296 0.1259 2.618 0.0133 tib -0.1511 0.1275 -1.185 0.2446 fem 0.6422 0.1368 4.695 0.0000452 --- Residual standard error: 3.851 on 33 degrees of freedom Multiple R-squared: 0.9732, Adjusted R-squared: 0.9707 F-statistic: 399.3 on 3 and 33 DF, p-value: < 2.2e-16

A. afarensis Papio Humerus Radius Femur Tibia 237.2 281 241

Residuals: Min 1Q Median 3Q Max -8.3184 -2.6398 -0.1986 2.2705 9.7350

Coefficients: Estimate Std. Error t value Pr(>|t|) (Intercept) 0.4382 7.8523 0.056 0.9558 tib 0.2545 0.1577 1.614 0.1161 fem 0.2392 0.2183 1.096 0.2811 hum 0.5217 0.1993 2.618 0.0133 * --- Residual standard error: 4.845 on 33 degrees of freedom Multiple R-squared: 0.9641, Adjusted R-squared: 0.9608 F-statistic: 295.3 on 3 and 33 DF, p-value: < 2.2e-16

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Table 3.4b. Regression formulae TABLE 3.4b. Regression formulae A. garhi Humerus Radius Femur Tibia Colobus (a) 226 231 335 Colobus (b) 236 231 335

Residuals: Min 1Q Median 3Q Max -4.6054 -1.7091 -0.2555 1.6482 5.6845

Coefficients: Estimate Std. Error t value Pr(>|t|) (Intercept) 12.98378 14.08489 0.922 0.3703 fem 0.36732 0.14717 2.496 0.0239 * hum 0.09366 0.17428 0.537 0.5984 rad 0.53444 0.13983 3.822 0.0015 ** --- Residual standard error: 2.583 on 16 degrees of freedom Multiple R-squared: 0.908, Adjusted R-squared: 0.8908 F-statistic: 52.64 on 3 and 16 DF, p-value: 0.00000001641

H. georgicus H. sapiens Humerus Radius Femur Tibia (a) 295 386 306 (b) 282 386 306

Residuals: Min 1Q Median 3Q Max -25.5183 -4.7121 0.0724 4.7632 25.0818

Coefficients: Estimate Std. Error t value Pr(>|t|) (Intercept) 7.12624 2.98514 2.387 0.0171 * tib 0.40000 0.01854 21.577 <2e-16 *** fem -0.03299 0.02161 -1.527 0.1271 hum 0.32357 0.02384 13.574 <2e-16 *** --- Residual standard error: 7.428 on 1178 degrees of freedom Multiple R-squared: 0.8433, Adjusted R-squared: 0.8429 F-statistic: 2113 on 3 and 1178 DF, p-value: < 2.2e-16

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Table 3.4c. Regression formulae TABLE 3.4c. Regression formulae H. sapiens Humerus Radius Femur Tibia (a) 295 386 306 (b) 282 386 306

Residuals: Min 1Q Median 3Q Max -25.5183 -4.7121 0.0724 4.7632 25.0818

H. ergaster H. sapiens Humerus Radius Femur Tibia 319 255 380

Residuals: Min 1Q Median 3Q Max -31.402 -6.716 -0.034 6.406 33.493

Coefficients: Estimate Std. Error t value Pr(>|t|) (Intercept) 22.67197 3.90234 5.810 0.00000000805 *** rad -0.03584 0.03859 -0.929 0.353 tib 0.52860 0.02459 21.500 < 2e-16 *** hum 0.73370 0.02692 27.258 < 2e-16 *** --- Residual standard error: 9.79 on 1172 degrees of freedom Multiple R-squared: 0.9048, Adjusted R-squared: 0.9046 F-statistic: 3715 on 3 and 1172 DF, p-value: < 2.2e-16

Table 3.4d. Regression formulae TABLE 3.4d. Regression formulae

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H. floresiensis Papio Humerus Radius Femur Tibia 243 280 235

Residuals: Min 1Q Median 3Q Max -6.2879 -2.4884 0.1205 1.3032 12.3030

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Chapter 4: Evaluating hominin locomotor grades

ABSTRACT

Whether hominin diversity is characterized by more or fewer taxa is a widely discussed topic, with many researchers now (e.g., Asfaw et al., 1999; Leakey et al., 2001;

Spoor et al., 2015) supporting a more speciose view than was suggested in earlier hypotheses (Mayr, 1950; Wolpoff, 1971). The speciose interpretation has been challenged, however, because proposals for new species have not always accounted for phenotypic variation among extant taxa (see also Mayr, 1950; Wolpoff, 1968; White et al., 2003; Lordkipanidze et al., 2013). Likewise, the preservation bias in favor of craniodental elements has directed the focus of discussions about functional variation away from the postcranium, and especially from the scarce data about traditional limb proportions that may be informative about locomotor adaptations (but see Richmond et al., 2002, Young et al., 2010). Here, we use resampling methods to compare the variation in limb proportions among fossil hominins to the variation in large samples of extant hominoids. Statistical tests are performed to assess whether the differences among the fossils is evidence of the sort of functional distinctions between groups of specimens that is implied by the locomotor grade hypotheses (e.g., Collard and Wood, 1999).

Overall the results are consistent with the locomotor grade hypothesis. The exception is that LB 1 (Homo floresiensis) is more similar to the skeleton of A.L. 288-1

(Australopithecus afarensis) than is ARA-VP-6/500 (Ardipithecus ramidus).

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INTRODUCTION

There is still uncertainty about hominin alpha taxonomy (i.e., how many taxa are represented in the hominin fossil record) because there is no universally applied way of assessing how much variation should be accepted within a single hominin species (see

Ackermann & Smith, 2007; see also Villmoare, 2018 for a review of discussions on the genus concept in paleoanthropology). For paleoanthropologists, this is a potential source of error that may account for the tendency to allocate newly discovered hominin fossils to a new taxon (e.g., Tattersall, 1986; White, 2003). Assigning species to genera is also a vexed issue because there are no established criteria for assessing what ‘grade’ or

‘adaptive type’ (i.e., groups of species sharing consistent functional adaptations) a species belongs to (Huxley, 1958). Most prior attempts have tended to focus on craniodental evidence with little attention paid to evidence from the postcranial skeleton (e.g.,

Lordkipanidze et al., 2013; Rightmire et al., 2017). Richmond et al., (2002) and

Lordkipanidze et al., (2007), on the other hand, did look at fossil variation in postcranial variables (e.g., humerofemoral proportions) and compared them to the variation observed in extant hominoids, but these were univariate studies that did not explore whether combinations of variables increased discriminatory power.

Defining the grade concept

When considering what functional criteria could be extracted from the hominin fossil record to evaluate the hypothesis that the origin of Homo coincided with a grade shift (i.e., a major shift in adaptive strategies and associated phenotypes), Collard and

Wood (1999) suggested that limb proportions might be a reasonable proxy for locomotor mode. Huxley (1958) introduced the grade concept. He suggested that a grade, also

114 known as an adaptive type, comprises a taxon, or group of taxa, that share a distinctive combination of functional adaptations. When they considered how to distinguish hominin genera, Collard and Wood (1999) (see also Collard, 2002) suggested that in addition to being a clade, a genus should also be a grade. One of several characteristics that Collard and Wood (1999) considered (e.g., diet, cognition, rate of development, etc.) as a grade criterion was locomotion, and they suggested that limb proportions could be used to discriminate obligate (i.e., those taxa whose locomotor behaviors are nearly entirely bipedal) from facultative (i.e., those taxa that typically use arboreal climbing behaviors, but opportunistically use bipedalism, especially on the ground) bipeds (see Prost, 1980;

Collard and Wood, 1999).

Recognizing grades

Unlike clades, grades are not necessarily monophyletic, so a grade may include polyphyletic groups of organisms that have converged upon functionally equivalent ways of dealing with similar ecological challenges (Huxley, 1958). Collard and Wood (1999) suggested that any grade divisions within the hominin clade should be based on variables available from the fossil record that can be linked to important adaptive functions such as diet, locomotion, and cognition. Among the variables they considered was information about limb proportions, which they wrote would be indicative of locomotor mode, and therefore limb proportions were likely to have been different in facultative and obligate bipeds. However, comparative quantitative data about the way limb proportions vary within and among extant primate species was not provided until later (see Richmond et al., 2002, but this study did not examine overall traditional limb proportions). On the basis of evidence about the limb proportions of Homo habilis Collard and Wood inferred

115 that it was a facultative biped, and allocated it to the grade (referred to as the australopith grade from here forward) that included Orrorin tugenensis, Ardipithecus ramidus,

Australopithecus afarensis, Australopithecus africanus, Australopithecus anamensis, A. garhi, Homo habilis, Homo rudolfensis, Kenyanthropus platyops, Paranthropus (or

Australopithecus) aethiopicus, Paranthropus boisei, and Paranthropus robustus, rather than the grade characterized by obligate bipedalism, which includes Homo ergaster,

Homo erectus, Homo neanderthalensis and Homo sapiens (referred to as the Homo grade from here forward). Taxa discovered more recently, such as Australopithecus sediba

(Berger et al., 2010), Homo naledi (Berger et al., 2015), Homo georgicus, (Lordkipanidze et al., 2007), and Homo floresiensis (Brown et al., 2004), were not evaluated for grade affinities on the basis of locomotor behavior (but see Dembo et al., 2016). Sufficient appendicular anatomy is available for the latter two (H. georgicus and H. floresiensis) to reconstruct their limb proportions (see Chapter 3), and these data are used to assess their grade affinities in the present analyses. This study uses observed variation in extant hominoid limb proportions as criteria for assessing whether differences among individual fossil hominins (see Materials below, and Table 2) are consistent with them sampling two locomotor modes – obligate and facultative – bipedalism.

Evaluating grades

Any hypothesis that uses differences in limb proportions to suggest more than one locomotor grade within the hominin clade is contingent on there being a close relationship between limb proportions and locomotor behavior in anthropoids and especially hominoids (Napier, 1967; Napier & Napier, 1967; Fleagle, 1988; see also

Chapter 2) and there being comparable differences between the limb proportions of

116 members of the australopith grade (Ar. ramidus and Au. afarensis) and those of the

Homo-grade (H. ergaster, H. georgicus (i.e., Dmanisi), and extant H. sapiens). For the purposes of this analysis A.L. 288-1 is assumed to represent the australopith grade, and

KNM-WT 15000 is assumed to represent the Homo grade, so results will be reported for comparisons between pairs of fossils, one of which will be either A.L. 288-1 or KNM-

WT 15000.

MATERIALS AND METHODS

Fossil specimens

Traditional indices (in this case, intermembral and humerofemoral indices) are calculated from the lengths of four major long bones: humerus, radius, femur, and tibia

(Mollison, 1911; Schultz, 1937; Napier & Napier, 1967). The total available fossil specimens (n=5) include Ar. ramidus (ARA-VP 6/500), Au. afarensis (A.L. 288-1), and

H. ergaster (KMN-WT 15000 and the adult Dmanisi hominin, also called H. georgicus).

To maximize the sample and better understand the possible variation in Homo, the grade affinities of H. floresiensis (LB 1) will also be assessed in the context of other hominins, even though its small overall size may complicate attempts to understand the significance of the results (Holliday & Franciscus, 2009; Jungers, 2009; see also Bromham &

Cardillo, 2007; Henneberg et al., 2014). See Table 4.2 for a list of hominin taxa and limb proportions used herein.

Comparative sample

The comparative hominoid dataset (n=1,575) comprises the same long bone maximum length data that was described in Chapter 2 and Table 4.1 below, but focusing

117 only on hominoids. It includes modern humans (n = 1,270) (789 males, 481 females) and non-human hominoids (n = 305). Where possible, each taxon has approximately balanced numbers of adult males and females.

Measurements

This study uses the same measurements described in Chapter 2: Table 2.1 and

Figure 2.1. Four maximum length measurements (i.e., humerus, radius, femur, and tibia) were collected from museum specimens and 3D surface scans following the protocols set out in the Goldman Osteometric Dataset methodology (Auerbach & Ruff, 2004, 2006).

Intermembral and humerofemoral indices (i.e., IMI and HFI) were also used because of their close covariance with locomotor behavior in extant anthropoids (Mollison, 1911;

Napier & Napier; 1967; Fleagle, 1988; Chapter 2).

Analytical Methods Resampling extant distributions A significance test was performed in which the differences between the limb indices of pairs of fossils are used to determine a) whether it is possible to find differences among fossils consistent with variation observed within extant hominoids, and b) the probabilities of observing fossil differences within a given extant hominoid group. Exact randomization resampling (Richmond & Jungers, 1995; Richmond et al.,

2005) is used to generate distributions of differences in IMI and HFI for all possible pairs of individuals belonging to all major extant hominoid genera, respectively (i.e., Homo,

Pan, Gorilla, Pongo, and Hylobates genera). The likelihood of drawing from extant genera two individuals as different as the fossil pairs is then quantified.

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To further quantify grade-like variation and place soft upper limits on the amount of variation that should be expected within closely related groups beyond the genus level, more taxonomically inclusive extant distributions that include multiple genera (referred to as ‘putative grades’ to distinguish them from genera) are also generated. The family

Hylobatidae (i.e., Hylobates and Symphalangus) is included because it is the only hominoid family that contains multiple extant genera, and will provide a test of the family level containing genera with similar phenotypes (see Tables 2.5-2.6).

African (i.e., Pan and Gorilla) and Asian apes (i.e., Pongo and the Hylobatidae) are also grouped to provide tests of regional-scale grades that share functional similarity due to convergence rather than ancestry. The results of two-block partial least squares analyses in Chapter 2 of this thesis demonstrated that African and Asian apes cluster into two groups that have more within than between group similarity in terms of limb proportions and behavioral repertoires. In other words, the Asian and African apes, respectively, share similar limb proportions (i.e., long forelimbs and humeri) and frequencies of arboreal forelimb dominated behaviors (e.g., ‘arm hanging’ and

‘brachiation and forelimb swinging’). These putative grades are, thus, distinct from the genus-grade equivalence suggested by Collard and Wood (1999).

In order to reduce the possibility that differences in sample size mean that any one taxon biases interpretations of genus or putative grade distributions, H. sapiens and Pan samples are restricted to 73 randomly selected individuals (matching the total Gorilla sample of 73), 39 Hylobates (matching the Pongo sample size), and seven Hylobates

(matching the Symphalangus sample) from the larger samples described above. The same

119 individuals were used to generate pairwise difference distributions for both intermembral and humerofemoral index iterations for each sample.

The differences between individuals were calculated as the arithmetic differences in IMI and HFI for the pair of fossils in question. Arithmetic differences were used because as ratios, indices reflect shape using a single percentage value that concisely indicates how different two specimens are. This method is adapted from the exact randomization method used by previous researchers (Grine et al., 1993; Richmond &

Jungers, 1995; Lockwood et al., 1996, Richmond et al., 2002). Richmond et al. (2002) were the first among these researchers to use these methods exclusively on postcrania to evaluate taxonomic hypotheses, as opposed to previous studies that focused on cranial elements, and to evaluate hypotheses of sexual dimorphism. Here, these methods are used to evaluate grade hypotheses within the hominin clade, recognizing that the extant ape genera themselves may represent adaptive types that have expanded to fill their respective functional niches (see Schultz, 1937; Lovejoy et al., 2009). Thus, the hominoid comparative genera deliberately comprise more than one species, and putative grades deliberately comprise more than one genus.

The procedure is repeated for every possible pair of extant individuals. The samples of 73 individuals belonging to Homo, Pan and Gorilla resulted in 2,628 unique pairwise comparisons each, and the 39 individuals belonging to Pongo and Hylobates generated 741 unique comparisons. In combined samples, African apes, Asian apes, and the Hylobatidae generated 10,585, 3,003, and 91 unique comparisons, respectively. See

Table 1.

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Significance testing

To test the likelihood of a single genus or grade hypothesis for fossils, frequency distributions were produced representing the complete pairwise differences in IMI and

HFI for each extant reference group. The 95th percentiles of each distribution are then used as critical values to test fossil grade similarity. A percentile value was then calculated for the arithmetic difference of each fossil pair relative to each extant reference group. The arithmetic difference for fossil pairs is used as a test statistic. Thus, fossil pairs whose IMI or HFI differences fall below the 95th percentiles of extant distributions cannot be rejected as sharing a single genus or putative grade, whereas those that fall beyond the 95th percentile can be confidently rejected as likely to be sampled from within a single genus or grade.

RESULTS

The results of resampling tests indicate that extant hominoid genera and putative grades can be defined on the basis of overall limb proportions. At each grade level, groups share remarkably consistent IMI and HFI variation, providing support for the proposition that genus-level and region-level grades are characterized by different levels of functional consistency. Ninety-five percent of individual pairs within extant genera do not differ by more than 6-10% in terms of IMI. The HFI 95th percentiles of extant genera are similar, but have a wider range between 6-13%. Extant putative grades (see

Resampling Significance Tests in the Methods section, above), on the other hand, have

IMI 95th percentiles between 14-15%. That the closely related African apes (Pan and

Gorilla) are similar may be expected, but that Pongo and Hylobates are nearly as similar

121 as the African apes is either due to retained primitive phenotypes in the Asian apes, or to convergence on limb proportions due to both using relatively greater amounts of forelimb-dominated locomotor behaviors (Chapter 2). The Hylobatidae putative grade

(i.e., Hylobates and Symphalangus) is the exception, with an IMI 95th percentile value of

22%. The HFI 95th percentiles are consistent across all putative grades, with values between 22-21%. The large IMI 95th percentile of the Hylobatidae grade (which markedly exceeds the IMI 95th percentile of even the overall Asian apes) may be due to the small number of pairs in the distribution.

The IMI differences for the pairs of fossils are consistently greater than their HFI differences, but generally adhere to the grade pattern proposed by Collard and Wood

(1999; see also Collard, 2002). In general, hominins are most similar to those specimens within their inferred grade than they are to others, except that H. floresiensis is more similar to Au. afarensis than the latter is to Ar. ramidus. Fossil pair IMI and HFI differences have different values, but nearly identical patterns: predictably approaching or exceeding the 95th percentile limits of some extant genera, but HFI differences never exceed the 95th percentiles of grade-level distributions. Fossil pairs whose IMI differences exceeded the 95th percentiles of genus-level reference distributions also closely approach or exceed the 95th percentiles for putative grade-like reference distributions. However, this is not true for fossil HFI differences of putative grades.

Results are detailed in Table 1 and graphically represented in Figures 1 and 2.

A.L. 288-1 vs. ARA-VP 6/500

Intermembral index differences matching or exceeding the arithmetic differences between A.L. 288-1 and ARA-VP 6/500 (7.4%) are rare in extant non-Homo hominoid

122 genera, and almost entirely absent in extant Homo. This fossil pair exceeds 87% of extant

Pongo pairs, 95-96% of Pan, Gorilla, and Hylobates pairs, and 98% of Homo sapiens pairs. The 7.4% IMI difference between Au. afarensis and Ar. ramidus falls at the 58th,

66th, and 45rd percentiles for African apes, Asian apes, and the Hylobatidae, respectively.

A similar pattern exists for the HFI, but the fossil difference (5.5%) falls between the 70th and 94th genus-level percentiles, but between 34th and 38th percentiles at the grade level.

A.L. 288-1 vs. Dmanisi

The IMI difference between the Au. afarensis-H. georgicus fossil pair (21%) exceeds the entire range of pairwise differences of all extant hominoid genera and grade distributions, and approaches the 95th percentile of the Hylobatidae.

For the HFI, the fossil difference (9%) exceeds the 95th percentiles of Pan and H. sapiens reference distributions, approaches the 95th percentile of the Hylobates distribution, and falls at approximately the 90th percentile for Gorilla and Pongo distributions. However, the A.L. 288-1-Dmanisi HFI difference falls at approximately the

50th percentiles of all extant grades.

A.L. 288-1 vs. LB 1

The IMI and HFI differences (both 3%) for the A.L. 288-1-LB 1 pair are the smallest of all fossil pair differences. The IMI difference falls comfortably below the 95th percentiles (between the 27th and 71st) of all extant genera and grade distributions.

Similarly, their HFI difference falls between the 18th and 64th percentiles of all extant genera and grade distributions.

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KNM-WT 15000 vs. A.L. 288-1

The H. ergaster-Au. afarensis pair IMI difference (24%) exceeds the entire range of values for all extant genus and grade-level reference samples. Their HFI difference

(13%) also meets (i.e., Pongo) or exceeds the 95th percentiles for all extant genus distributions, but this 13% difference falls between the 63rd and 66th percentiles of extant grades.

KNM-WT 15000 vs. Dmanisi

Neither the IMI (3%) nor the HFI (4%) differences of the H. ergaster-H. georgicus pair approaches the 95th percentiles of any extant genus or grade reference distribution. The value most closely approaches significance against the H. sapiens reference distribution, in which the fossil difference falls at the 77th percentile for the

IMI, and the 84th percentile for the HFI.

KNM-WT 15000 vs. LB 1

The IMI difference (27%) for the H. ergaster-H. floresiensis pair is the largest of all of the fossil pairs, and exceeds the entire range of difference values for all extant genus and grade distributions. The HFI difference (16%) is also the largest of all fossil pairs, exceeding the 95th percentiles, and approaching the 100th percentiles, for all extant genus reference distributions.

DISCUSSION

This study examined distributions of variation in the limb proportions of extant hominoid reference samples, and used those distributions to test the functional consistency among the hominin locomotor grades suggested by Collard and Wood (1999; see also Collard, 2002). The results for extant reference samples show consistent levels of

124 variation for intermembral (IMI) and humerofemoral (HFI) indices, however larger samples of Symphalangus are necessary to refine results for the Hylobatidae. According to the grade classification of Collard and Wood (1999), both Ar. ramidus and Au. afarensis are facultative bipeds within a single australopith grade, whereas H. ergaster, and by inference H. georgicus, are in the obligate biped grade that also includes H. sapiens. A third member of genus Homo, H. floresiensis, was only published after the most recent review of hominin grades (Collard, 2002), and thus was not allocated to a grade. Fossil pairs that are less similar than 95 percent of extant references can be confidently rejected as belonging to the same genus or ‘putative grade’.

The results of this study show that the two larger-bodied Homo individuals (i.e.,

KNM-WT 15000 vs. Dmanisi) cannot be rejected as belonging to the same grade. The differences in their limb proportions do not exceed the 95th percentiles of any extant hominoid genera or putative grades. This is consistent with expectations, as both individuals fall within the H. sapiens cluster in shape space (Lordkipanidze et al., 2007; see also Chapter 3: Principal Components Analysis). On the other hand, the differences in limb proportions between the two hominins proposed within the australopith grade (i.e.,

A.L. 288-1 vs. ARA-VP 6/500) do not consistently exceed the 95th percentile differences of extant groups. The exceptions are the IMI distributions of Hylobates (96%), Pan

(96.5%) and Homo sapiens (97.9%). The IMI difference also closely approaches the 95th percentile of the Gorilla distribution. The mixed results for the Au. afarensis-Ar. ramidus pair are consistent with suggestions that these taxa may have different locomotor adaptations (see Lovejoy et al., 2009; Harcourt-Smith et al., 2016). However, a single

125 genus hypothesis cannot be confidently rejected, as the pair neither consistently exceeds

95th percentiles for genus-level IMI nor ever exceeds genus-level HFI.

The A.L. 288-1-LB 1 pair is more similar for IMI and HFI than are either the A.L.

288-1-ARA-VP 6/500 or the KNM-WT 15000-LB 1 pairs. If H. floresiensis is retained in the genus Homo, it suggests that Homo subsumes more than just obligate bipeds, and thus the inclusion of H. floresiensis would reduce the functional consistency within Homo (see

Jungers, 2009; but Bromham & Cardillo, 2009; Henneberg et al., 2014 for alternative interpretations). If LB 1 is not a member of the Homo grade, then it may be more appropriate to allocate it to a different genus. It could also be the case that early hominins were opening new behavioral niches such that limb proportions alone are not as good indicators of locomotor mode as they are in extant non-human anthropoids. However, even if H. floresiensis did not share behavioral locomotor repertoires similar to those of the australopith grade, its limb proportions and diminutive size make it unlikely that it behaved much like most other known members of genus Homo.

The results may also help inform interpretations of the limb proportions of fossil skeletons that have been referred to Homo habilis (OH 62) (Johanson, 1987) and to Au. garhi (BOU-VP-12/1) (Asfaw, et al., 1999). It has been suggested that these fossils are evidence of evolutionary reversals, and hominin behavioral diversity within Homo, respectively (see Richmond et al., 2002). Although other authors have included them in analyses (e.g., Richmond et al., 2002), their long bone length estimates are too uncertain

(see Reno et al., 2005) to include in the present analyses. However, if estimates of the limb proportions of OH 62 (c. IMI- 97.8%, HFI- 94%) and BOU-VP-12/1 (ca. IMI- 75%,

HFI- 69%) are close to being correct (see Chapter 3), then their IMI difference (22.8%) is

126 comparable to that of the Au. afarensis-H. georgicus and A. afarensis-H. ergaster pairs, and their HFI difference (25%) exceeds that of all other fossil pairs. In this scenario, the

OH 62-A.L. 288-1 IMI difference is minimal (c. 4%) and intermediate between the differences between Au. afarensis-H. floresiensis (2.7%) and Au. afarensis-Ar. ramidus

(7.4%). However, their HFI difference (c.10%) is comparable to the Au. afarensis-H. georgicus pair. On the other hand, BOU-VP-12/1 is most similar to early fossil Homo specimens, such that its IMI differs from Dmanisi and its HFI differs from KNM-WT

15000 roughly 2%. Thus, in terms of those limb proportions most closely associated with behavior in hominoids, BOU-VP-12/1 is most similar to the Homo grade, whereas OH 62 is similar to the australopith grade for IMI.

If the limb proportions, taxonomic allocations, and phylogenetic positions of OH

62 and BOU-VP 12/1 are correct, then a) OH 62 is evidence of either lineage diversity, or an Australopith-like reversal within Homo; and b) BOU-VP-12/1 implies that

Australopithecus exhibited diversity in limb proportions and, by inference, behavior.

Alternatively, these results could indicate that the taxonomic allocations for both specimens should be reconsidered. Better preserved associated skeletons from the period of the Australopithecus-Homo transition will provide more reliable conclusions, but because the younger H. floresiensis is much better preserved than either OH 62 or BOU-

VP-12/1, it provides more reliable evidence that its limb proportions are outside the range of other larger-bodied members of genus Homo. Thus, if OH 62 and LB 1 are both correctly allocated to genus Homo, then they may belong to a separate grade that either retained, or secondarily re-acquired, primitive limb proportions (i.e., ‘reversal’).

127

Future directions

This paper presents a comparative means of assessing claims that differences in locomotor mode are consistent with grade differences within the hominin clade.

Elsewhere (Chapter 2) it was suggested that, of all the traditional indices, IMI is the best discriminator among extant genera, and we showed here that IMI best reflects obvious fossil genus and grade differences even when compared to the broadly defined extant

‘putative grades’ (e.g., Asian apes). However, it should be emphasized that the HFI is also an effective indicator of inter-generic differences. Therefore, future work should more closely examine the HFI alone, which will allow the analysis of many more fossil specimens to refine these conclusions.

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CHAPTER 4 FIGURES Figure 4.1a. Genus distributions

Figure 4.1a. Genus distributions

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Figure 4.1b. Genus distributions, continued Figure 4.1b. Genus distributions, continued

Pairwise difference distributions for extant genus intermembral and humerofemoral indices. Shaded areas are beyond the 95th percentiles of respective distributions. Dashed lines represent where fossils fall in relation to extant distributions. A) Au. afarensis-Ar. ramidus; (B) Au. afarensis-H. georgicus; (C) Au. afarensis-H. floresiensis; (D) H. ergaster-Au. afarensis; (E) H. ergaster-H. georgicus; (F) H. ergaster- H. floresiensis. IMI and HFI differences for small bodied hominins (i.e., Au. afarensis, Ar. ramidus, and H. floresiensis) do not exceed the differences observed in extant distributions, with the exception of the H. sapiens distribution. HFI distinguishes fossils with nearly the same pattern as IMI, but does not exceed the 95th percentiles for Gorilla, Pongo, or Hylobates for Au. afarensis-H. georgicus.

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Figure 4.2. Putative “grade” distributions Figure 4.2. Putative “grade” distributions

Pairwise difference distributions for extant putative grades’ (see Methods, above) intermembral and humerofemoral indices. Shaded areas are beyond the 95th percentiles of respective distributions. Dashed lines represent where fossils fall in relation to extant distributions. A) Au. afarensis-Ar. ramidus; (B) Au. afarensis-H. georgicus; (C) Au. afarensis-H. floresiensis; (D) H. ergaster-Au. afarensis; (E) H. ergaster-H. georgicus; (F) H. ergaster-H. floresiensis. IMI captures differences between smaller and larger-bodied hominins against ‘grade’ distributions, with the exception of the Hylobatidae. HFI does not exceed the 95th percentile for any extant ‘grades’.

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CHAPTER 4 TABLES Table 4.1. Extant sample TABLE 4.1. Extant sample Genus Species Males Females Unknown Total Homo sapiens 789 481 1270 Pan troglodytes 53 28 14 95 paniscus 9 9 18 Gorilla gorilla 37 27 2 66 beringei 3 4 7 Pongo pygmaeus 14 15 5 34 abelii 3 2 5 Hylobates lar 39 34 7 80 Symphalangus syndactylus 3 3 1 7 Total=1582 Reference Num. of Num. of grade individuals comparisons Homo 73 2,628 Pan 73 2,628 Gorilla 73 2,628 Pongo 39 741 Hylobates 39 741 African apes 146 10,585 Asian apes 78 3,003 Hylobatidae 14 91

Extant sample and grade Reference sample sizes. African apes comprise Pan and Gorilla. Asian apes comprise Pongo and Hylobates. The Hylobatidae comprises Hylobates and Symphalangus.

132

Table 4.2. Fossil specimens TABLE 4.2. Fossil limb proportions Intermembral index Humerofemoral index ARA-VP-6/500 86.3% 78.7% A.L. 288-1 93.7% 84.2% Dmanisi 72.4% 75.1% KNM-WT 15000 69.3% 71.1% LB 1 96.4% 86.8% Chapter 3 estimated the limb proportions of for the five hominins listed above. Intermembral (IMI) and humerofemoral (HFI) indices were determined to best correlate with locomotor behavior in extant taxa (Chapter 2). Here are provided the mean IMI and HFI for the two versions of A.L. 288-1 and Dmanisi (see Chapter 3).

133

Table 4.3. Arithmetic index differences and percentile values TABLE 4.3. Arithmetic index differences and percentile values IMI H. Pan Gorilla Pongo Hylobates African Asian Hylobatidae difference sapiens (6.9) (7.5) (9.6) (6.6) apes apes (21.9) (5.5) (15.2) (13.6) Au. afarensis (93.7) vs. A) Ar. ramidus 7.4 97.9 96.5 94.7 86.7 96.0 58.0 65.6 45.1 (86.3) B) H. 21.3 100.0 100.0 100.0 100.0 100.0 100.0 99.6 92.3 georgicus (72.4) C) H. 2.7 71.2 52.2 51.8 41.3 59.0 26.6 29.1 30.8 floresiensis (96.4) H. ergaster (69.3) vs. D) Au. 24.4 100.0 100.0 100.0 100.0 100.0 100.0 100.0 100.0 afarensis (93.7) E) H. 3.10 77.3 59.0 58.1 46.4 66.3 30.1 33.0 33.0 georgicus (72.4) F) H. 27 100.0 100.0 100.0 100.0 100.0 100.0 100.0 100.0 floresiensis (96.4)

HFI H. Pan Gorilla Pongo Hylobates African Asian Hylobatidae difference sapiens (8.3) (10.6) (12.9) (9.9) apes apes (21.2) (5.9) (21.9) (21.9) Au. afarensis (84.2) vs. A) Ar. ramidus 5.5 93.8 80.9 69.0 72.1 74.5 37.8 37.4 34.1 (78.7) B) H. 9.1 99.4 96.9 90.7 90 93.5 50.6 50.9 47.3 georgicus (75.1) C) H. 2.6 63.9 46.4 36.5 38.1 41 20.6 19.6 17.6 floresiensis (86.8) H. ergaster (71.1) vs. D) Au. 13.1 100 99.8 97.9 95 99 64.3 65.7 62.6 afarensis (84.2) E) H. 4 84 66 53 57.2 59.9 29.8 29.4 25.3 georgicus (75.1) F) H. 15.7 100 100 99.1 96.8 99.9 74.9 76.9 74.7 floresiensis (86.8) Provided are fossil intermembral (IMI) and humerofemoral (HFI) index differences and percentile values as compared to extant groups. The 95th percentiles of extant groups are given in parentheses below their group titles. IMI reflects the greatest differences between fossils compared to both extant genus and ‘grade’ distributions. HFI also reflects significant fossil differences compared to extant genera, but no significant differences are relative to extant ‘grade’ distributions.

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Chapter 5: Conclusion

The goals of this thesis were to develop quantitative methods for using comparative evidence to interpret variation in the limb proportions of fossil hominins. Because hominin skeletons are typically incomplete and their limb proportions (e.g., intermembral, humerofemoral, brachial, and crural indices) are often reconstructed using regression estimates based on extant taxa, another goal was to determine which extant anthropoids in the available sample had limb proportions most like those fossil hominin skeletons, and may thus be an appropriate model for reconstructing hominin limb proportions. Multivariate methods were used to characterize large samples of extant anthropoid genera according to their overall traditional limb proportions, and to gauge the degree of association between their limb proportions and behavioral repertoires.

Resampling approaches were then used on extant hominoid samples to estimate the amount of intrageneric and within-grade variation present in selected limb indices (i.e., intermembral and humerofemoral indices). Machine-learning methods selected optimal extant anthropoid models for fossil hominin skeletons, and multivariate regression estimates for unavailable long bone lengths were modeled on the selected extant genera.

Finally, the arithmetic differences between relevant pairs of fossil hominins’ reconstructed limb proportions were compared to the amount of variation within extant hominoid samples to test the locomotor grade affinities hypothesized by Collard and

Wood (1999). These approaches 1) quantitatively link limb proportions and behavioral repertoires; 2) support that extant hominoid genera may be considered both clades and locomotor grades, but that they may also demonstrate higher-level (e.g., regional) grade- like differences; 3) contradict the common presupposition that hominin overall limb

135 proportions should be reconstructed using extant hominoid models; and 4) demonstrate that hominin functional diversity, as captured by reconstructed limb proportions, sometimes exceeds expectations based on grade hypotheses (as Wood and Collard, 1997 concluded regarding functional consistency in Homo craniodental variables). The results of Chapter 4 imply that the taxonomic, and perhaps the phylogenetic, affinities of LB 1,

OH 62, and BOU-VP-12/1 should be reevaluated, as limb proportion reconstructions of

LB 1 and OH 62 are significantly more like A.L. 288-1 than they are like modern Homo sapiens, H. ergaster, or H. georgicus, while BOU-VP-12/1 has far more traditionally

Homo-like limb proportions than either LB 1 or OH 62 (see also Richmond et al., 2002;

Jungers, 2013).

Schultz (1930, 1937) and Napier and Napier (1967) suggested that the extant hominoids had evolved more diverse body plans and behaviors than extant monkeys, and this has been corroborated by other researchers (see also Straus, 1963; Moyà-Solà and

Köhler., 1996; Lovejoy, et al., 2009; Moyà-Solà et al., 2004; Young et al., 2010). The data presented here accord with this claim, demonstrating that hominoids (including H. sapiens) have greater intergeneric disparities in overall limb proportions than monkeys, even though hominoids are represented by far fewer genera. Thus, the strong covariance between overall limb proportions and behavioral repertoires, and the considerable extant hominoid intrageneric variation in overall limb proportions and behavioral repertoires

(especially regarding the intermembral index or relative forelimb length, and ‘brachiation and forelimb swinging’ or ‘arm hanging’, respectively) supports hominoid genera being locomotor grades as well as clades. At a greater (i.e., regional or continental) scale, however, the association between limb proportions and forelimb-dominated behaviors

136 also clusters the Asian apes (i.e., Pongo and the Hylobatidae) and the African apes (i.e.,

Pan and Gorilla) to the exclusion of the other. At both scales, inter-group differences in limb proportions and behavioral repertoires demonstrably exceed intra-group differences.

This suggests regional levels of hominoid grade organization, even though phylogenetic comparative methods found strong phylogenetic signals in all non-human hominoid limb proportions.

Debate persists about whether the Pan-Homo last common ancestor (PHLCA) was like extant apes, but Lovejoy et al., (2009) predicted on the basis of Ar. ramidus-- which has been interpreted as an arboreal quadruped-- that the PHLCA shared phenotypic and behavioral similarities with generalized monkeys and Ekembo (i.e., the revised genus of some Proconsul specimens) (see McNulty et al., 2015). The phylomorphospace of extant anthropoid mean overall limb proportions in Chapter 2 reconstructed the PHLCA as falling in the range of extant monkeys (although more similar to Pan than H. sapiens).

However, overall traditional limb proportions for the fossil sample were not then available to calibrate primitive and derived phenotypes, so ancestral state reconstructions

(ASRs) hypotheses must be interpreted cautiously. Machine-learning analyses also indicate that extant generalized monkeys have more similar overall limb proportions to hominin fossils than do apes (Chapter 2). This is consistent with expectations regarding the hypothesis that the long forelimbs of the great apes are derived from an ancestral generalized monkey-like phenotype such as that inferred for Ekembo (see Ward et al.,

1993; Lovejoy et al., 2009). Conversely, Young et al., (2010) wrote that an evolutionary trajectory from an ape-like PHLCA would also necessarily “cross” through a phase of quadrupedal limb proportions as they approached the modern H. sapiens condition. They

137 also wrote that a PHLCA with monkey-like limb proportions would require multiple instances of convergence on ape-like limb proportions to reach the conditions seen in extant apes - a hypothesis accepted by other researchers (see Lovejoy et al., 2009). In a bivariate plot of hindlimb-to-forelimb length, however, no fossil hominin falls with extant apes below the quadrupedal monkey line of allometry where the apes are, but instead all fall between the monkey line and extant H. sapiens (Young et al., 2010, figure

1). Thus, while the precursor of the PHLCA may have been ape-like, there is no evidence that even the earliest available fossil hominin skeletons had ape-like limb proportions.

The reconstructed hominin fossil limb proportions presented in this thesis can be used to calibrate ancestral state reconstructions and refine expectations about the Pan-Homo last common ancestor under various phylogenetic hypotheses.

Of those hominins discussed in this thesis, Collard (2002) suggested that an australopith grade would comprise Ar. ramidus, Au. afarensis, Au. garhi, and H. habilis, while the subsequent Homo grade would comprise H. ergaster, H. sapiens, and by inference, H. georgicus and H. floresiensis. The taxa in each grade should, therefore, have functionally consistent locomotor habits, which Collard and Wood (1999) suggested may be reflected by similar limb proportions. However, the analyses of fossil hominin limb proportions herein imply locomotor diversity sometimes inconsistent with these grade hypotheses (see below).

The H. georgicus-H. ergaster pair is consistent with a single Homo grade hypothesis and the Ar. ramidus-Au. afarensis pair does not consistently exceed expected genus-level variation. The limb proportions of H. floresiensis (LB 1), however, are far beyond any H. sapiens in the comparative sample (n= 1,270), but are very similar to Ar. ramidus and Au.

138 afarensis (see also Jungers, 2013). Considering the close association of limb proportions and behavior among extant anthropoids from three superfamilies, the limb proportions of

LB 1 likely have implications for the behavioral repertoire of H. floresiensis, if the skeleton is representative of its species (but see Bromham & Cardillo, 2007; Henneberg, et al., 2014). Its limb proportions imply that it behaved significantly differently from other Homo post-dating H. habilis, which adds complexity to the notion of functional consistency within the Homo grade (see Jungers et al., 2009a; Jungers et al., 2009b;

Larson et al., 2009a; Larson et al., 2009b; Holliday et al., 2012; see also Wood and

Collard, 1997 which recognizes craniodental functional variation in Homo).

The relatively poor preservation of the skeletons OH 62 (assigned to H. habilis;

Johanson, 1987) and BOU-VP-12/1 (assigned to Au. garhi; Asfaw et al., 1999) prevents confident assessments of their overall limb proportions, but preliminary reconstructions for OH 62 are consistent with its inclusion in an australopith grade. On the other hand, the BOU-VP-12/1 reconstruction is more similar to members of the Homo grade, and if its estimates are correct, then they are inconsistent with the skeleton’s placement in the australopith grade. Further investigation should reconsider the taxonomy of OH 62 and

BOU-VP-12/1.

The monkey-like (or australopith-like) inferred limb proportions of OH 62 are consistent with the hypothesis that H. floresiensis and H. ergaster share a common australopith-like ancestor (see Argue et al., 2017). If correct, H. floresiensis’ craniofacial similarities with H. erectus would have been due either to their early and unrecorded emergence in an unknown common ancestor, or convergence (i.e., ‘homoplasy’) (see

Baab et al., 2016; Jungers et al., 2016). If hominin limb proportions are indicative of

139 generic affinities as they are in extant hominoids, then OH 62 and H. floresiensis may be best placed among the australopiths, whereas BOU-VP-12/1 may belong within Homo or another as-yet-unknown grade. Thus, using limb proportions as evidence partially supports proposed hominin locomotor grades, but implies that locomotor grade hypotheses and some taxic allocations should be reevaluated.

The methods presented in this thesis are another step in efforts to decipher the behavioral and taxic implications of fossil hominin variation. They provide quantitative means of defining hominin functional groupings, which should have implications for taxonomy. Multivariate analyses of limb proportions in extant anthropoids support the hypothesis that they are closely associated with behavioral repertoires at the genus level, and thus supports their potential utility for evaluating functional and taxic affinities. The results of these analyses demonstrate that reconstructions of hominin limbs proportions suggest more intra-generic variation than seen in any extant anthropoid. Either the extreme fossil intrageneric variation is real and the result of temporal and geographic variation, or the taxic affinities of some of the skeletons in question (i.e., LB 1 and potentially OH 62 and BOU-VP-12/1) require re-evaluation. This thesis supports the hypothesis that reconstructions of well-enough preserved hominin fossil associated skeletons fall into two groups: one most similar to H. sapiens, and another remarkably similar to A.L. 288-1 and extant monkeys. The author hopes that this work will encourage future researchers to evaluate the significance of differences in hominin phenotypic variation in limb proportions.

140

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Appendix

CHAPTER 2 CODE

Box plots

Packages: ggplot2 qplot(x=genus, y=index, geom="boxplot", fill=dataframe$superfamily, data=dataframe)

Creates a box plot from the dataframe at the genus level for one of four index variables

(i.e., intermembral, humerofemoral, brachial, or crural indices), and color codes boxes by superfamily.

Principal Components Analysis

Packages: ggplot2 princomp((Dataframe[,16:19])) ggplot(Dataframe,aes(x=PC1,y=PC2,color=color))+geom_point(size=2)+ scale_y_continuous(breaks = c(-50,-25,0,25,50))

Calculates PCs for Dataframe using continuous variables in columns 16-19, then plots observations according to their first two PCs, color codes points according to a Color factor, and forces the Y to plot with the same variance as the X axis. Convex hulls and labels were added manually in Photoshop CS 6

Tukey’s Honestly Significant Difference

Packages: N/A

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TukeyHSD(aov(Ghum+Grad+Gfem+Gtib~genus,data=dataframe))

2-BPLS

Packages: geomorph

PLS <- two.b.pls(LocomotorData, ExtantAnthData, iter = 1000, seed = "random", print.progress = TRUE) summary( PLS) plot(PLS)

Quantifies covariance between a matrix of locomotor values (i.e., LocomotorData) and a matrix of species mean limb proportions (i.e., ExtantAnthData). Results are then summarized and plotted.

Phylomorphospace

Packages: ape, phytools phylomorphospace(MyTree, ExtantAnthData,control=list(col.node=cols))

Creates a phylomorphospace plot mapping a phylogenetic tree (i.e., MyTree) on to a

PCA of species mean limb proportions (i.e., ExtantAnthData). Colors and labels were added manually in Photoshop CS 6.

Blomberg’s K

Packages: geomorph physignal (dataframe[,6:9], MyTree, iter = 1000, seed = NULL, print.progress =

TRUE)

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Calculates the phylogenetic signal present in dataframe among multiple continuous variables (i.e., columns 6-9, which in this case are Mosimann ratios) using the phylogenetic tree MyTree.

CHAPTER 3 CODE Classification and Regression Trees

# Required packages: rpart, rpart.plot

# Trains model (i.e., ExtantModel) at the genus level using three size-adjusted variables

(i.e., var1-var3) and saves to ExtantModel

ExtantModel<-rpart(genus~var1,var2,var3, data=ExtantAnthData)

# Prunes ExtantModel to the tree with the lowest complexity parameter (cp) and saves to

PrunedModel.

PrunedModel<-prune(ExtantModel,cp=0.010000) prp(PrunedModel)

# Predicts how new FossilData fits to PrunedModel, or which extant genera in the sample have limb proportions most like fossil specimens.

FossilPrediction<-predict(PrunedModel, FossilData,na.action = "na.omit")

Multiple regressions

# Fits a linear model to ExtantData at the genus level (e.g., Papio) to perform a multiple regression, and saves results in ExtantRegressionModel.

ExtantRegressionModel<-lm(formula = var1 ~ var2 + var3 + var4, data = subset(ExtantData, ExtantData$genus == "Papio"))

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# Estimates a given missing variable (e.g., var1) and prediction intervals for a new dataset (i.e., FossilData) using the multiple regression equations in

ExtantRegressionModel and fossil data columns 4-6 (i.e., var2, var3, and var4). predict(ExtantRegressionModel, newdata=FossilData[,4:6], interval="prediction", level=.95)

CHAPTER 4 CODE Resampling and distributions

# Saves var1 as VariableName

VariableName <- "var1"

# Saves the column titled var1 from the dataset ReferenceGrade into CurrentVariable

CurrentVariable <-ReferenceGrade[,VariableName]

# Computes the absolute differences in var1 between all possible pairs of observations in

CurrentVariable and saves them as Distances.

Distances <- dist(CurrentVariable,method = "maximum",upper=FALSE)

# Displays the frequency distribution of values in Distances. hist(Distances)

# Converts Distances to a matrix and saves it as DistanceMatrix.

DistanceMatrix <-as.matrix(Distances)

#Reorganizes DistanceMatrix column names as a list named MatrixNames.

MatrixNames <- t(combn(colnames(DistanceMatrix), 2))

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#Combines MatrixNames and the distance values in DistanceMatrix (now in a vector, diff) into a data frame named var1DM. var1DM<-data.frame(MatrixNames, diff= DistanceMatrix [MatrixNames])

Percentiles and testing quantile(var1DM $diff,c(.25,.50,.75,.95)) #computes and returns the percentiles indicated in bold (i.e., 25th, 50th, 75th, and 95th) for the vector diff in var1DM.

Data<-ecdf(var1DM$diff) #computes the empirical cumulative distribution function

(ecdf) using the vector diff in var1DM and saves it as the function Data.

Data(#) #computes and returns the percentile for any value (#) given the reference distribution saved in Data.

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