MORPHOLOGICAL CHARACTERIZATION OF FOSSIL

GWM10/P1, A PHALANX OF ARDIPITHECUS RAMIDUS

by

YVONNE P. McDERMOTT

Submitted in partial fulfillment of the requirements for

the degree of Master of Science

Department of Biology

CASE WESTERN RESERVE UNIVERSITY

January 2019

CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES

We hereby approve the thesis of Yvonne McDermott

candidate for the degree of Master of Science

Committee Chair Karen Abbott, Ph.D

Committee Member/Research Advisor Scott Simpson, Ph.D.

Committee Member Michael Benard, Ph.D.

Committee Member Bruce Latimer, Ph.D.

Date of Defense August 31, 2018

We also certify that written approval has been obtained for any proprietary material contained therein.

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Dedication

This thesis is dedicated to Quinn, Shay, Tristane and Brian for all their love, support and encouragement.

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Table of Contents

List of Tables, 6 List of Figures, 7 Acknowledgements, 11

Abstract, 12

Introduction, 13 General features and functions of primate hands, 13 Modes of locomotion, 15 Bipedalism, 15 Knuckle walking, 17 Plantigrade, digitigrade, and suspensory locomotion, 20 Hands as predictors of locomotion, 24 Phalangeal curvature, 25 The hand and the emergence of tool use, 27 The fossil record with an emphasis on the hand, 28 Orrorin tugenensis, 28 Ardipithecus ramidus, 28 Australopithecus anamensis, 32 Australopithecus afarensis, 33 Australopithecus sediba, 34 OH 86, 36

Methods and materials, 38 Measurements, 39 Phalangeal curvature, 41 Articular surface area, 44 Torsion, 44 Graphical plots and statistics, 44

Results, 46 The morphology of proximal phalanges, 47 Proximal phalanx 1 of humans, gorillas, and chimpanzees, 47 Proximal phalanx 2 of humans, gorillas, and chimpanzees, 54 Proximal phalanx 3 of humans, gorillas, and chimpanzees, 59 Proximal phalanx 4 of humans, gorillas, and chimpanzees, 61 Proximal phalanx 5 of humans, gorillas, and chimpanzees, 62

GWM10/P1, 65

Metrical comparisons of proximal phalanges, 71 Lengths of proximal phalanges of humans, gorillas, and chimpanzees, 71 Proximal articular surface area (PAS) of phalanges as a proxy for body mass and its relation to phalangeal length, 75

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Axial torsion, 82 Comparison of phalangeal shapes, 89 Phalangeal curvature, 97

Discussion, 101 The morphology of proximal phalanges, 101 Torsion as a tool for manual proximal phalanx ray assignment, 101 Morphology and metrical descriptions of manual proximal phalanges of humans, gorillas, and chimpanzees, 102 GWM10/P1 hand side and ray, 104 GWM10/P1 is long and curved, 105 Ar. ramidus had a hand similar to a Miocene ape, a pelvis for arboreality and bipedal terrestriality and a phalanx suited for arboreality, 107 The relation of phalangeal length and the transition between arboreality and bipedality, 109

Appendix, 112

References, 116

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List of Tables

Table R1.Distinguishing features of the proximal phalanges, 64

Table R2. Measurements of GWM10/P1 and other 4th proximal phalanges, 73

Table R3. Mean lengths of proximal phalanges of chimpanzees, gorillas and humans, 74

Table R4. Median torsion values, 87

Appendix Table 1, Gorilla specimen information, 112

Appendix Table 2, Chimpanzee specimen information, 113

Appendix Table 3, Human specimen information, 114

Appendix Table 4, Fossil specimen information, 115

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List of Figures

Figure 1. Bones of the hands of extant and extinct hominins and their predecessors, 15

Figure 2. Hand bone positions of knuckle walker, 19

Figure 3. Modes of locomotion by primates, 21

Figure 4. Orangutan engaging in quadrumanous clambering, above-branch

quadrupedalism with a gripping hand, suspensory locomotion, and hand-assisted

arboreal bipedalism, 23

Figure 5. Lateral view illustrating varying degrees of curvature of the manual proximal

phalanges of extant anthropoids and early fossil hominins, 26

Figure 6. Dorsal and palmar view of the hand of Ar. ramidus, 31

Figure 7: Four views of proximal phalanx KNM-KP 30503, 33

Figure 8. Images of palmar and dorsal aspects of Au. sediba MH2 right hand, 35

Figure 9. Images of OH 86, a manual proximal phalanx, 36

Figure M1. Eleven linear measurements acquired from manual proximal phalanges, 40

Figure M2. Determination of included angle of a proximal phalanx, 42

Figure R1. Right hand proximal phalanges of rays 1 to 5 of a human, 48

Figure R2. View of the articular surfaces of the 1st proximal phalanges from a human,

gorilla and chimpanzee from left to right, 48

Figure R3. Left hand proximal phalanges of rays 5 to 1 of a female gorilla and a female

chimpanzee, 49

Figure R4. Human proximal phalanx 1 of the right hand, palmar surface, displays the

distal ulnar condyle extending in the palmar direction and the distal direction, 51

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Figure R5. Palmar surfaces of chimpanzee and gorilla proximal phalanges 1 of the right

hand display the distal ulnar condyles extending in the palmar direction and distal

direction, 52

Figure R6. Comparison of side views of proximal phalanges 1 of gorillas, chimpanzees,

and humans, 53

Figure R7. Gorilla distal articular surface does not extend to the dorsal aspect for

proximal phalanx 1, 53

Figure R8. Gorilla proximal phalanx 2 and 4 of right hand displaying proximal surfaces,

55

Figure R9 – Proximal articular surfaces of human proximal phalanges 2 and 4 of the

right hand, 56

Figure R10. Chimpanzee proximal phalanges 2 (left) and 4 (right) of the right hand

display proximal surfaces, 56

Figure R11. Human proximal phalanx 2 of the right hand shows that the ulnar side distal

condyle extends further in the palmar direction than the radial condyle, 57

Figure R12. Gorilla proximal phalanx 2 of the right hand, 57

Figure R13. An oblique view of the palmar aspects of gorilla proximal phalanges, 2-5,

left to right, 58

Figure R14. Palmar surface view of proximal phalanx 3 of humans, gorillas, and

chimpanzees from left to right of the right hand, 60

Figure R15. Articular surfaces of proximal phalanx 5 of humans, chimpanzees and

gorillas from left to right of the right hand, 62

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Figure R16. Palmar sides of the 5th proximal phalanges of humans, gorillas and

chimpanzees of the right hand, 63

Figure R17. GWM10/P1 in dorsal, palmar and side view, 66

Figure R18. Side view of GWM10/P1 and a human 4th proximal phalanx (bottom)

comparing longitudinal curvature, 69

Figure R19. Proximal articular surface of GWM10/P1 cast, 69

Figure R20. Dorsal view of GWM10/P1 and A. L. 333-63 (Au. afarensis), 70

Figure R21. GWM10/P1 condyles at the distal surface, 70

Figure R22. Comparisons of PAS areas of proximal phalanges of ray 2 of chimpanzees,

gorillas, and humans, 78

Figure R23. Evaluations of PAS areas of proximal phalanges of ray 3 of chimpanzees,

gorillas, and humans, 78

Figure R24. Assessments of PAS areas of proximal phalanges of ray 4 of chimpanzees,

gorillas, humans, Hadar, and GWM10/P1, 79

Figure R25. Plots of the square root of the PAS area of each proximal phalanx from ray

2, 3, and 4 against total length of each cognate bone from chimpanzees, gorillas,

humans, Au. afarensis, and GWM10/P1, 80

Figure R26. Ratios of the means of the square root of the PAS of proximal phalanx/TL

± SEM for each species, 81

Figure R27. Image of axial torsion for proximal phalanx of Au. afarensis AL 333-62, a

likely fourth proximal phalanx of the left hand, 83

Figure R28. Images of distal and proximal articular surfaces of proximal phalanges of

gorillas, chimpanzees, and humans, 84

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Figure R29. Torsion values in degrees, 86

Figure R30. Comparison of proximal phalanges 2 and 4 mean torsion values ± SEM of

humans, gorillas, and chimpanzees, 88

Figure R31. Base shape comparisons, 90

Figure R32. Midshaft shape comparisons, 91

Figure R33. Head shape comparisons, 92

Figure R34. Proximal shaft shape comparisons, 94

Figure R35. Distal Shaft Shape ratio comparisons, 95

Figure R36. Linear regression performed on all distal shaft shape ratios demonstrate a

correlation between distal shaft shapes and length, 96

Figure R37. Representative phalangeal curvature analyses performed on digital photos

with ImageJ, 98

Figure R38. Curvature of the 4th proximal phalanges from fossil GWM10/P1 and those

of extant and extinct hominoids, 100

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Acknowledgments

First and foremost, I would like to thank my advisor, Dr. Scott Simpson, for his constant support along this process. I thank him for giving so much of his time in guiding me through this fascinating and complicated field. For me, it was worth all the work.

I am very grateful to Dr. Bruce Latimer for being so generous with his time, knowledge and guidance.

I would like to thank Dr. Michael Benard for agreeing to be a committee member and for his advice and guidance.

I would like to thank Dr. Karen Abbott for being my DGS representative.

I would like to thank Dr. Yohannes Haile-Selassie for allowing me to have access to the Physical Anthropology Laboratory at the Cleveland Museum of Natural History and the research collection kept there.

I am so grateful to Lyman Jellema for always being so accommodating and helpful at the Physical Anthropology lab.

I would like to thank Dr. Linda Spurlock for her encouragement and friendship and all our wonderful conversations about this crazy field we love so well.

I am very grateful to Dr. Mark Hans for making my dream come true and making me part of an incredible Archaeological Excavation.

I would like to thank the wonderful scientists in Israel that I have had the extreme good fortune to get to know as part of the Manot Cave Project, such as Dr. Ofer Marder and Dr. Israel Hershkovitz. I thank them for their support and many thoughtful and inspiring conversations.

I would like to especially thank my guardian angel, Julia Brown. I can’t imagine having been able to navigate this journey without her.

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Morphological Characterization of Fossil GWM10/P1, a

Proximal Manual Phalanx of Ardipthecus ramidus

Abstract

YVONNE P. McDERMOTT

Pliocene hominin Ardipithecus ramidus represents an early human ancestor proficient at quadrupedalism and bipedalism. Its anatomically mosaic pelvis and lower limbs reveal adaptations for both modes of locomotion. The Ar. ramidus hand is one of a generalist, lacking the derived features of knuckle-walking modern African apes or of the suspensory orangutans. Here, we characterize GWM10/P1, an Ar. ramidus manual proximal phalanx from Gona, Ethiopia. By comparisons of morphologies and metrics of manual proximal phalanges of modern human and non-human primates, we assign

GWM10/P1 to the 4th proximal phalanx of the left hand. Moreover, relating the 4th proximal phalanges of humans, African great apes, and Au. afarensis, to GWM10/P1 demonstrates that this phalanx is long, curved, and with many shape similarities to the 4th manual proximal phalanx of chimpanzees. These features show that the Ar. ramidus hand had arboreal function and support the hypothesis that this species was a careful climber.

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Introduction

Primate hands exhibit extensive anatomical variation that enables them to exploit many ecological niches (Jones, 1942). Ateles has elongated medial fingers and a substantially reduced thumb, which has created a hook-like hand that permits deft swinging through the forest canopy (Jones, 1942). Papio has comparatively short fingers and a thumb that is fairly robust and capable of oppositional manipulation (Jones, 1942). In contrast, callitrichids do not have opposable thumbs with flat nails but instead have sharp claws, which enable them to run up trees, hold on to tree limbs, and forage for insects and tree sap (Jones, 1942). By comparison, human hands have subtle specializations that enable remarkable abilities. The major difference in function of the human hand as compared to those of many primates is that it is not encumbered with any role in locomotion or in weight bearing. Bipedality in the human lineage has freed the hands and forelimbs from the pressure that natural selection imposes on mobility (Darwin, 1871; Tuttle, 2014).

Therefore, comparative analyses of the hands of extinct species of human ancestors and modern-day primates can yield information on the way these human precursors locomoted and ultimately how the human lineage may have transitioned to bipedality.

General features and functions of primate hands

Generally speaking, the hands of extant hominoids (primate group that includes humans their extinct ancestors and anthropoid apes) are distinguishable (Fig. 5). Chimpanzees and orangutans have the longest phalanges and metacarpals. Because of finger length, chimpanzees often handle small objects with the thumb pushed up against the side of the index finger (Christel, 1993; Marzke, 1996; Marzke, 1997; Kivell et al., 2016). Humans

13 in contrast have long thumbs relative to their medial finger lengths and a well-developed distal phalanx of the pollex, which is broad shaped with clear attachment sites for the flexor pollicis longus (FPL) muscle (Tuttle, 2014). The robusticity of the pollex is unique to the human hand, and it enables humans to use their fingers differently than apes, with pad-to-pad precision grip to firmly pinch, hold and manipulate objects (Kivell, 2015).

This type of manual dexterity is not possible for chimpanzees and gorillas because of the relative lengths of the longer medial phalanges to the much shorter thumb. Similarly, Ar. ramidus (Lovejoy et al., 2009b) has a shorter thumb than humans, longer than large bodied apes and similar to OWM (except colobines). Phalanges 2-5 of Ar. ramidus are longer than gorillas and shorter than chimpanzees (Almecija et al., 2015). Therefore, the grip of Ar. ramidus is likely to have been not as dexterous as humans.

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Figure 1. Bones of the hands of extant and extinct hominins and their predecessors. Adapted from (Kivell et al., 2016).

Modes of locomotion

Bipedalism

Bipedalism is a form of locomotion where an organism moves primarily by its two rear legs. Humans are the only obligate bipedal primates among the extant primates. This form of locomotion preceded the expansion of the brain (Johanson et al., 1978; Kimbel &

Delezene, 2009). Human bipedalism may have arisen from a quadrupedal terrestrial ancestor, or it may have evolved from arboreal antecedents. This distinctive form of

15 locomotion is characterized by derived anatomical adaptations, primarily occurring in the lower limbs but also throughout the postcranial skeleton and skull (Latimer, 1991b;

Leakey et al., 1995; Senut, 2001; Ward, 2002; Galik et al., 2004; White et al., 2006;

Lovejoy et al., 2009b; Lovejoy et al., 2009c; Lovejoy et al., 2009d).

Early signs of bipedal specialization in hominin (the taxonomic group that includes humans and their fossil ancestors) anatomy first appear in Orrorin tugenensis (Or. tugenensis) approximately 6 million years ago (Ma) (Senut, 2001; Galik et al., 2004).

Ardipithecus ramidus which came later, 4.4 Ma, had a unique form of locomotion that integrated “arboreal palmigrade clambering and careful climbing with a form of terrestrial bipedality” (White et al., 2009; White et al., 2015). Australopithecus anamensis (Au. anamensis), a biped, from sites in Ethiopia and Kenya (Leakey et al.,

1995; Leakey et al., 1998; White et al., 2006) dates (3.9 – 4.2 Ma) to after Ar. ramidus but before Australopithecus afarensis.

Au. afarensis (Johanson et al., 1978), dated to between 3.4 – 2.95 Ma from the Hadar formation in central Afar Ethiopia, is thought to have been bipedal and represents among the earliest times many anatomical adaptations for bipedalism were observed, derived features include the pelvis (Johanson et al., 1982; Tague & Lovejoy, 1986; Lovejoy et al., 1999), femoral neck structure (Johanson et al., 1982), valgus angle of the knee

(Tardieu & Trinkaus, 1994), and arched foot (Latimer et al., 1987; Latimer & Lovejoy,

1989, 1990b, a; Ward et al., 2011). These derived features of the lower body are paired with a high humero-femoral index (Jungers, 1982). Perhaps the best evidence for

16 bipedalism for Au. afarensis are the footprints at Laetoli, Tanzania (Leakey & Hay, 1979;

White, 1980).

Knuckle walking

Knuckle walking is a specialized form of quadrupedal locomotion where the African apes

(Gorilla gorilla, Gorilla beringei, Pan troglodytes, Pan paniscus) support their upper body weight on the dorsal aspect of their flexed middle phalanges (Fig. 2)(Tuttle, 1967;

Simpson et al., 2018). Since the African apes, particularly the chimpanzees, were shown by genetic means to be our closest living relatives, it was concluded that the last ancestor humans and chimpanzees shared must have knuckle walked (Richmond & Strait, 2000;

Corruccini & McHenry, 2001; Richmond, 2006). It wasn’t until the discovery of Ar. ramidus (White et al., 1994; White et al., 2009) that it was understood that early hominins did not have knuckle walking specializations in their anatomy (Lovejoy et al.,

2009b; White et al., 2015). On the contrary, Ar. ramidus had features in the forelimbs and torso that are adapted for arboreality (Lovejoy et al., 2009b; Selby et al., 2016). Ar. ramidus did not have rigid, non-flexible wrists like the chimpanzees and gorillas

(Richmond, 2006; Kivell & Schmitt, 2009; Lovejoy et al., 2009b; Selby et al., 2016;

Simpson et al., 2018). It has been compellingly argued that chimpanzees and gorillas have evolved the knuckle-walking behavior independently (Dainton & Macho, 1999;

Kivell & Schmitt, 2009; Simpson et al., 2018). There are salient differences in the anatomy of chimpanzees and gorillas (Dainton & Macho, 1999; Crompton et al., 2008), including dissimilarities in the exact digits that bear the majority of the weight between the species. Furthermore, disparities exist in the orientation of the forelimbs amongst

17 chimpanzees and gorillas (Doran, 1997). Therefore, although both chimpanzees and gorillas knuckle walk, they are using their anatomy differently to perform this task.

Since Ar. ramidus shed light on the anatomy of an early human ancestor, researchers were now free to accept certain conclusions that anatomical and behavioral studies had been intimating (Doran, 1997; Kivell & Schmitt, 2009): the last common ancestor (LCA) of humans and African apes possessed a generalized, arboreal body-plan, indicating that knuckle walking is a derived behavior (Lovejoy et al., 2009b). These findings raise and important question: why do modern African apes knuckle walk? Simpson et al. explained that knuckle walking is an adaptation using muscles isometrically and eccentrically to remedy the detrimental impacts that continual loading of the upper body has on soft tissue, bones, and joints (Simpson et al., 2018). By studying the directions of muscles, the quality of the muscle fibers, and how these relate to the joints and skeleton, it was demonstrated how knuckle walking works as a “shock absorber” of sorts, the same way muscles in the arch of the foot and other muscles of the leg work. The wrist of African apes exhibit limited extension with little capacity for dorsiflexion or for open hand palmigrady (Kivell & Schmitt, 2009). The metacarpophalangeal joints for rays 2-5 have the ability to hyperextend thus allowing the flexion of the intermediate phalanges to make contact with the substrate on the dorsum of that bone (Matarazzo, 2013).

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Figure 2. Hand bone positions of knuckle walker. Adapted from (Kivell et al., 2011).

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Plantigrade, digitigrade, and suspensory locomotion

Palmigrady/plantigrady are types of locomotion where the entire metacarpal/metatarsal pads, respectively, are in contact with the substrate (Ankel-Simons, 2007). Terrestrial quadrupedal walkers, such as baboons and macaques, place the volar aspects of manual/pedal phalanges 2 through 5 on the ground (Figs.3 c,d). Arboreal above-branch quadrupedal walkers have the same positions in the trees. This type of locomotion is thought to be the primitive mammalian condition (Jones, 1946).

Digitigrade locomotion is a type of movement where the podials (bones of the carpus and tarsus) are off the ground. Phalanges (distal, middle, and proximal) are in direct contact with the substrate (Ankel-Simons, 2007). Only phalanges (of the hands or feet) support the body weight (Figs. 3a,b). Heels and wrists are permanently raised.

Animals that employ this type of locomotion are able to run faster. Baboons are classified as semi-digitigrade terrestrial quadrupeds.

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Figure 3. Modes of locomotion by primates. (A, B) Baboons demonstrate digitigrady, wherein only the phalanges are in contact with the substrate. (C, D) Non-baboon monkeys exhibiting plantigrady, where all phalanges and the entire palms (including metacarpals) are juxtaposition to the substrate. Adapted from (Patel, 2010). Note, baboons can, and do often, place their calcaneus on the substrate—hence the term semi-digitigrade.

Brachiation is a highly specialized method of swinging hand over hand with a suspensory grip under branches (Tuttle, 1967; Ankel-Simons, 2007). True suspensory brachiation is a very fast paced movement that is only performed by smaller bodied primates, such as

Ateles (spider monkeys) and lesser apes (hylobatids & siamangs). Orangutans move fairly slowly and deliberately through the forest in what is called “orthograde clamber” (Thorpe et al., 2007) (Fig. 4). In this movement, the trunk is orthograde and the body weight is supported partially by the forelimbs as they suspend from supports above the head, and

21 are also supported by their legs and feet as they climb. This unique form of locomotion has been proposed as a precursor to bipedality in hominins, most probably because of the skeletal changes that must be present in order to move this way (Thorpe et al., 2007). The thoraxes of apes and atelines are broad, and in each the scapula is dorsally positioned, changing the orientation of the glenoid fossa to a more lateral and cranial position.

Redirection of the glenoid sockets increases the span of the arms and their range of circumduction (Ankel-Simons, 2007). All of the great apes employ this method of orthograde clamber, but orangutans do it most frequently (Thorpe et al., 2007). Hand- assisted bipedalism or slow brachiation allows apes to move on flexible branches that would seem too thin to support their body weight (Fig. 4) (Thorpe et al., 2007).

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Figure 4. (A) Orangutan engaging in quadrumanous clambering, (B) above-branch quadrupedalism with a gripping hand, (C) suspensory locomotion, and (D) hand-assisted arboreal bipedalism. Adapted from Thorpe et al., (2007).

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Hands as predictors of locomotion

Studies of the hand have been used to reveal modes of primate and hominin locomotion

(Kivell et al., 2016). These studies include the analysis of the manual phalanges, which provide essential information on locomotor modalities because the hand directly interacts with terrestrial and arboreal substrates, providing support during movement (Rein et al.,

2011). There are significant differences in the proportions and shapes of the bones, and these differences have been analyzed for what they can tell us about the natural history of the animal in question. Beginning with a clear understanding of how skeletal anatomy shapes function and movement in extant animals, we infer how extinct animals, whose anatomy is available in the fossil record, lived in their various environments.

Morphological patterns in manual phalanges can correlate to substrate use and habitat preference (Rein et al., 2011). Some parameters of the hand skeleton that can reveal potential modes of locomotion include joint orientation, surface area of joint articulations, relative phalangeal lengths among digits, phalangeal length in relation to metacarpal lengths, phalangeal curvature, orientation of proximal articular surface of proximal phalanges, and relative robusticity of basal palmar tubercles on the base of the proximal end of proximal phalanges (Rein et al., 2011). Using these anatomical parameters, possible modes of primate locomotion in the prehistoric environment can be deduced.

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Phalangeal curvature

Phalangeal curvature is a characteristic of intense interest because it, along with elongated phalanges, are well correlated with arboreal behaviors in living primates

(Tuttle, 1969; Marzke, 1971; Susman, 1979; Hunt, 1991; Stern et al., 1995; Richmond,

2007). Therefore, it follows that these characters in fossils could also be used to determine if arboreal behaviors were present in the associated extinct primates. Curvature of a primate’s phalanges are thought to be reflective of the position of its hands and feet on substrate, so this measurable value can be a trait in determining the posture and locomotion in fossil primates. But this measurement alone is not enough; it requires information about an animal’s postcranial anatomy to conclude a mode of locomotion

(Ward, 2002). Nonetheless, long and curved phalanges have often been cited as evidence of arboreal adaptation. Depending on the species, phalangeal curvature can vary widely among African apes, humans, and extinct hominins (Fig. 5). It has been argued that during ontogeny, phalangeal curvature is greatly impacted by a primate’s behavior.

(Richmond, 1998; Jungers & Rakotosamimanana, 2001; Congdon, 2012). In more recent years, studies have lent support to the idea that phalangeal lengths are under genetic control (Indjeian et al., 2016).

Prior to 1983, phalangeal curvature was assessed by descriptions (Stern & Susman,

1983). However, using geometry and measurements of the proximal phalanx, it is possible to generate a quantitative analysis of this trait. The radius of curvature (R = radius of curvature) of a fossil is often not discussed because it does not allow comparison of fossils with different lengths (i.e. different species or different digits of the

25 same species). Therefore, what is used for comparison is included angle (Theta = 2*Arc-

Sin (L/2R)), which is independent of length. (See methods for more details).

Figure 5. Lateral view illustrating varying degrees of curvature of the manual proximal phalanges of extant anthropoids in the left column and early fossil hominins in the right column. Proximal phalanges are ordered from straighter at the top to those with greater curvature toward the bottom,. Proximal phalanges of extant taxa include (a) modern human, (b) baboon, (c) gorilla, (d) chimpanzee, (e) gibbon, and (f) orangutan. Fossil proximal phalanges include (g) Hominini gen. et sp. indet. (OH 86; adapted from (Dominguez-Rodrigo et al., 2015), (h) Au. africanus (StW 293; adapted from (Kivell et al., 2011)), ( i )Au. sediba (UW 88-120 of MH2; adapted from (Kivell et al., 2011), (j) H habilis (OH 7, cast), (k) H. naledi (UW 101-1327; adapted from (Kivell et al., 2015), and (l) Au. afarensis (A.L. 333- 57). Adapted from Kivell et al., (2016).

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The hand and the emergence of tool use

Humans have specialized morphological characters that are unique among great apes; this makes it possible to produce two types of grips (Napier & Tuttle, 1993; Kivell et al.,

2016). One is the precision grip, which is achieved by contact of the broad distal phalanges of second to fifth fingers with the robust pollex, enabling grasping of small objects. The second is called the power grip and is produced by the pollex wrapping around an object in a secure manner. Both these grips are made possible because of the robustness of the pollex and its relative length, when compared to the medial digits. Also, the carpometacarpal joint in the pollex has a saddle shape, which enables a wide range of motion of the pollex, including turning and facing in opposition to digits 2-5 and pad-to- pad opposition for precision gripping. These grips allow the remarkable use of tools that modern humans are capable of. The African apes and orangutans have short thumbs, as compared to their medial digits, such that they generally perform a thumb-to-the-side-of- second-digit touch when attempting to hold small objects (Tuttle, 2014).

For many decades, the connection between the emergence of our genus Homo and the appearance of the earliest stone tool technology, was believed to be fundamentally linked.

Lithic tools from Gona, Ethiopia date to 2.6 Ma (Semaw et al., 2003). The current evidence suggests that hominins earlier than members of the Homo genus made these tools. Recently, stone artifacts from West Turkana, Kenya dated to ~3.3 Ma were excavated (Harmand et al., 2015). These artifacts are an assemblage of 149 cores, flakes and cobbles, broken and whole. Therefore, the earliest evidence of tool use is outside of the known age range for even the earliest of the Homo genus.

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The fossil record with an emphasis on the hand

Orrorin tugenensis

Or. tugenensis is an early putative hominin that has signs of bipedal specialization. It is dated to approximately 6 Ma (Senut, 2001; Galik et al., 2004; Almecija et al., 2013).

Little is known about the hand of Or. tugenensis. However, a manual proximal phalanx was identified with a preserved length of 33.8 mm and phalangeal curvature that is similar to Au. afarensis and climbing living primates (Senut, 2001).

Ardipithecus ramidus

The discovery and analysis of Ar. ramidus has transformed our knowledge of the course of human evolution (Lovejoy et al., 2009b; White et al., 2009). Up to and until 2009, when the hand and other anatomy of Ar. ramidus was published (Lovejoy et al., 2009a;

Lovejoy et al., 2009b; Lovejoy et al., 2009d), it was generally thought that the last common ancestor humans shared with the African great apes closely resembled the extant

African apes in morphology and who had predicted behaviors, such as suspensory locomotion, vertical climbing, and knuckle walking (Lovejoy et al., 2009a; Lovejoy et al., 2009b; Lovejoy et al., 2009d). Ar. ramidus dates to approximately 4.4 Ma in the

Pliocene. However, it lacks the derived, forelimb features of African great apes, such as for chimpanzees there are elongated metacarpals from rays 2-5, metacarpal heads are expanded in a fashion that is indicative of knuckle walking, and carpometacarpal joints are rigid (Simpson et al., 2018). This strongly suggests that hominins had not evolved through ancestors that depended on suspensory locomotion, vertical climbing, and

28 knuckle walking (Lovejoy et al., 2009b; White et al., 2009).

Key features of the Ar. ramidus hand and wrist

The wrist of Ar. ramidus has many similarities to those of the Miocene apes (Proconsul), and, therefore, lacks the specialized features of extant African apes that provide rigidity and restrict motion (Lovejoy et al., 2009b). Differences in the central joint complex

(CJC) of Ar. ramidus and extant African great apes are telling. Constituted by the trapezoid, capitate, metacarpal (Mc) 2, and Mc3, this structure of extant African great apes has two key features that reduce hand mobility: one, Mc2 functions as a structure to support and restrict rotation of the CJC because the capitate extends distally to create a capitate-Mc2 facet. Two, a partial screw effect has been created by the lateral portion of the capitate’s dorsodistal surface, which has been withdrawn proximally. The partial screw effect enables energy dissipation in a way that preserves cartilage during loading for knuckle walking, an advantage because cartilage does not regenerate (Lovejoy et al.,

2009b; Selby et al., 2016). Mc3 has external axial rotation relative to the capitate, which enables extensive flexion of the joint. More extensive carpometacarpal ligaments can constrain this rotation by tension. This novel capitate position restricts motion of Mc2 and Mc3 from a neutral position, which makes their movement in the opposite direction impermissible. A consequence of the angle formed by the Mc3-capitate is that it transforms dorsopalmar shear into tension. The carpometacarpal ligaments limit this shear and the torsion formed in the CJC with the overall effect of increasing rigidity and enabling more even distribution of energy. This may facilitate suspension, vertical climbing, and knuckle-walking in the African great apes.

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The structural differences between the Ar. ramidus’ CJC and those of the great apes are distinctive and consequential. Ar. ramidus has a planar CJC like those of Miocene apes, old world monkeys and humans. In addition, the head of the capitate of Ar. ramidus, being set in a more palmar direction than the other hominoids, allows hyper dorsiflexion of the hand and clambering arboreal behavior (Fig. 6) (Lovejoy et al., 2009b). Also, different than the extant apes are the relative sizes of the metacarpals in rays 2-5

(Lovejoy et al., 2009b). The metacarpals of extant apes are relatively long compared to those of Ar. ramidus. Also, the heads of the metatarsals of Ar. ramidus lack expansion, which is thought to be a feature of knuckle walking.

The phalanges of Ar. ramidus are shorter than those of chimpanzees but longer than those of gorillas, relative to body size (Lovejoy et al., 2009b). The proximal phalanx of ray 1 has a relatively human looking head that is larger dorsally and shows attachments for sesamoid bones, as seen in members of the genus Homo (Napier, 1962; Leakey et al.,

1964). The terminal phalanx of ray 1 exhibits significant attachment site for the flexor pollicis longus tendon, differing from extant great apes that often lack a separate FPL

(Kivell, 2015). However, the proximal phalanges of Ar. ramidus have not been studied in great detail, and the interpretation of these features may broaden our understanding of the function of the hand and ultimately the behaviors of this important hominin. In Ar. ramidus, we see a unique coupling of ancestral characteristics that reflect adaptations for arboreality (long arms, grasping, opposable hallux) and derived characters primarily in the hip and lower limbs, which we associate with adaptations for bipedality (Lovejoy et al., 2009a; Lovejoy et al., 2009d).

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Figure 6. Dorsal and palmar view of the hand of Ar. ramidus. Also displayed in inset are three capitate bones used for comparison. Letters A – H are used to indicate features that are considered primitive or generalized and found in arboreal primates. A. Short metacarpals; B. No knuckle walking grooves; C. Elongated joint surface for digit 5; D. Larger thumb as compared to apes; E. Insertion point on distal phalanx of thumb; F. Hamate which allows palm into flexion; G. Non-specialized wrist joints; H. The head of the capitate allows significant palmar flexion. Inset: Lateral views of the capitate from (left to right) chimpanzee, Ar. ramidus and human. The dashed lines are used to highlight the orientation of the head of the capitate, which is orientated towards the palm in Ar. ramidus and humans. This bend in the capitate’s head is responsible for hominids having a more flexible wrist. Adapted from Lovejoy et al., (2009b).

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The most extensively studied Ar. ramidus fossils are from Aramis, Ethiopia (White et al.,

1994). Therefore, information regarding the locomotion of this species mainly comes from fossils from this locality (Lovejoy et al., 2009a; Lovejoy et al., 2009b; Lovejoy et al., 2009d). Other Ar. ramidus skeletal remains have been identified in Gona Western

Margin (GWM), Afar, Ethiopia (Semaw et al., 2005). Collected from locality GWM10 was a relatively well-preserved Ar. ramidus manual proximal phalanx termed

GWM10/P1. Further investigations into fossils such as this one may add to our knowledge of Ar. ramidus locomotion.

Australopithecus anamensis

Assemblages of Australopithecus anamensis fossils were identified in Kanapoi and Allia

Bay, Kenya (Leakey et al., 1995; Leakey et al., 1998) and Asa Issie, Aramis, Ethiopia

(White et al., 2006). They were dated to 3.9 - 4.2 Ma. These dating studies indicate that

Au. anamensis is temporally situated between Ar. ramidus and Au. afarensis in the fossil record.

A single proximal manual phalanx fragment of Au. anamensis has been described in the literature: KNM-KP 30503 (Fig.7) (Ward et al., 2001). This specimen is 39.2 mm in length and has three-quarters of the phalanx preserved. This phalanx is estimated to have been 40 - 42 mm long when fully intact (Ward et al., 2001). The palmar aspect though flattens distally. Its left and right flexor ridges are estimated at 14 mm and 17 mm in length, respectively. The shaft, when viewed from the side, is longitudinally curved. The shaft pinches in mediolaterally just before it flares towards the base.

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Figure 7. Four views of proximal phalanx KNM-KP 30503. Adapted from Ward et al., (2001).

Au. afarensis

Au. afarensis remnants from the Hadar formation in Ethiopia are estimated at 3.2 Ma

(Johanson et al., 1978). The collection includes 15 proximal phalanges (Johanson et al.,

1978; Bush et al., 1982). Digits 2-5 have proximal phalanges that are curved and thinner than those of chimpanzees (Stern & Susman, 1983). They are shorter in total length than those of humans and chimpanzees (Bush et al., 1982). The shaft of each of these bones has a bilateral expansion. The manual proximal phalanx trochlea has a large surface area and is deeply trenched. These characteristics are reminiscent of the phalanges of chimpanzees. However, since Au. afarensis lacks a transverse dorsal ridge and a dorsally

33 expanded articular surface on the metacarpal head, there is no evidence of knuckle walking or terrestrial digitigrady (Simpson et al., 2018). Ward and colleagues (2012) published extensive findings of Au. afarensis from 1990 – 2007 from Ethiopia. Among the specimens described were 5 differentially preserved manual proximal phalanges. The morphology of the medial digits are similar to the specimens from Hadar Ethiopia described by Bush et al., 1982. Specimen AL 438-4 is the distal end of a pollex. The asymmetry between the tubercles for the flexor pollicis brevis muscle and the abductor pollicis brevis muscle indicates that the musculature of the thenar muscles in Au. afarensis was very similar that found in humans. Ward et al., infers this to mean that the movement and capabilities of the hand in Au. afarensis could have been human-like.

The curved proximal phalanges of Au. afarensis have been indicative to some that these primates used suspensory and climbing modes in locomotion (Richmond & Strait, 2000).

But, it seems improbable that Au. afarensis, with all the changes in the pelvis and hind limbs and loss of an abductable hallux (Latimer et al., 1987; Latimer & Lovejoy, 1989,

1990a, b; Latimer, 1991a), could have relied heavily on suspensory and climbing locomotion (see above).

Australopithecus sediba (MH2)

A 1.977 Ma hand fossil, MH2, from Malapa, South Africa, represents a near complete

Australopithecus sediba hand (Fig. 8) (Kivell et al., 2011). This sample exhibits a mixture of traits that both infers arboreal capabilities and Homo-like finger proportions.

The thumb is relatively long and robust compared to rays 2-5, which is similar to both

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humans and other non-suspensory primates. The total lengths of the proximal phalanges

of MH2 are shorter than Au. afarensis and Homo. Some characters that are similar to

African apes are the curved and robust phalanges, well-developed flexor sheath ridges,

and the poorly developed FPL. The mean included angle of the proximal phalanges is

less than that of Au. afarensis and OH7 but still greater than that found in Homo. Taken

together, this mixture of traits seems to indicate a retention of phalangeal curvature

coupled with derived relative finger length proportions.

Figure 8. Images of palmar and dorsal aspects of Au. sediba MH2 right hand. The australopithecine-like (primitive) qualities are denoted on the palmar view. In the dorsal view, are aspects of the fossil that are derived and also seen in later hominins. Adapted from Kivell et al., (2011).

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OH 86

The Olduvai hominin fossil, OH 86, was found in Olduvai Gorge, Tanzania, and dates to

1.84 Ma (Dominguez-Rodrigo et al., 2015). It is a manual proximal phalanx of the fifth ray and the sole fossil remnant of this assemblage (Fig. 9). It is thought to be an early

Homo species, possibly Homo habilis; although, the morphology is different enough from

OH 7 to cast doubt on the potential designation of OH 86 to the Homo habilis species group (Dominguez-Rodrigo et al., 2015). The length of the fossil is short and within the range of modern humans.

Figure 9. Images of OH 86, a manual proximal phalanx. Scale bar = 1 cm. Adapted from Dominguez-

Rodrigo et al., (2015).

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Phalangeal curvature measurements place OH 86 close to measurements taken for humans (Dominguez-Rodrigo et al., 2015). OH 86 is more human-like and less australopithecine-like in most measurements taken at the trochlea, midshaft, and base of this phalanx. Without knowledge of other bones of the hand, analyses of this fossil indicate this 5th proximal phalanx is short, has the same amount of longitudinal curvature as humans, and is metrically similar to humans. At 1.8 Ma. this phalanx is almost completely modern looking in these respects. This fossil demonstrates that by 1.8 Ma. this hominin most probably functioned like later species of Homo, without any trace of its arboreal antecedents.

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Methods and Materials

Materials

Measurements were acquired for the second, third, fourth, and fifth proximal phalanges of 20 common chimpanzees (Pan troglodytes), 20 lowland gorillas (Gorilla gorilla), and

20 modern humans (Homo sapiens) from specimens housed in the Laboratory of Physical

Anthropology, Cleveland Museum of Natural History, Cleveland, OH (Appendix Tables

M1-M4). As the GWM10/P1 fossil is from a lateral ray, no measurements of the pollical proximal phalanx were made.

The chimpanzees and gorillas used in this study were adult, wild-shot, non-pathological individuals. For the human samples, age and sex were taken from the museum archives.

The gorilla and chimpanzee specimens were considered adult status on the basis of third molar eruption and epiphyseal synostosis. Gender of the African apes was taken from museum archival records. Research grade casts of Au. afarensis from Hadar, Ethiopia

(Johanson et al., 1978; Bush et al., 1982) were used for comparative analyses and are housed in the Physical Anthropology Laboratory, Cleveland Museum of Natural History.

A cast of GWM10/P1 (Semaw et al., 2005) was provided by Dr. S. Simpson.

Measurements of Ar. ramidus specimens ARA-VP-6/500-022 and ARA-VP-6/500-069 from Aramis, Ethiopia, were obtained from published literature (Lovejoy et al., 2009b).

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Measurements

Standard anthropometric techniques and instruments (digital calipers; Mitutoyo Inc and digital outside point calipers; Insize Inc.) were used to measure 11 linear variables to the nearest 0.01 mm (Fig. M1): total length, TL; proximal base width, PBW; proximal base height, PBH; head width, HW; head height, HH; midshaft width, MSW; midshaft height,

MSH; proximal shaft width, PSW (mediolateral measurement at TL x .25 from base); proximal shaft height, PSH (dorsopalmar measurement at TL x .25 from base); distal shaft width, DSW (mediolateral measurement at TL x .75 from base); and distal shaft height, DSH (dorsopalmar measurement at TL x .75 from base). The PSW, PSH, DSW, and DSH measurements were taken to reveal the shapes of the shafts near the ends of each bone. Similar measurements have been used to characterize the phalanges of numerous species (Almecija et al., 2009; Rein et al., 2011) . All measurements are maximal length measurements. DSH at midshaft does not include flexor sheath ridges because when taking this measurement a digital outside point caliper was used.

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Figure M1. Eleven linear measurements acquired from manual proximal phalanges. A. Distal shaft width (DSW), midshaft width (MSW), proximal shaft width (PSW), total length (TL). B. Distal shaft height (DSH), midshaft height (MSH), proximal shaft height (PSH). C. Head height (HH), head width (HW). D. Proximal base height (PBH), proximal base width (PBW).

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Phalangeal curvature

The included angle of proximal phalanges is a measure of curvature, and it has been used to infer an animal’s arboreality and terrestriality (Susman et al., 1984; Susman et al., 2001; Dominguez-Rodrigo et al., 2015; Lorenzo et al., 2015). Three measurements were used to calculate the radius of curvature (R), which were then used to calculate the included angle (ϴ) (Fig. M2). The three measurements required for this calculation are maximum length (L), dorsopalmar midshaft diameter (D), and the height of the dorsal surface of the bone (at the midshaft) from a line connecting the center of the proximal and distal articular surfaces (H). The three measurements L, H, D, and R were all calculated on the program ImageJ

(https://imagej.nih.gov/ij/). This software program was used to draw these lines

(shown in Fig. M2) onto the digital photographs and measurements were obtained.

Photographs were obtained with a digital camera (Cannon 5D; Cannon Inc.) The camera was on a tripod and not moved from a mark on the ground in order to ensure that the measurements would not vary and were duplicable.

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Figure M2. Determination of included angle of a proximal phalanx. Left, Measurements required to determine included angle: maximum length (L), dorsopalmar midshaft diameter (D), height of the dorsal surface of the bone (at the midshaft) from a line connecting the center of the proximal and distal articular surfaces (H). Right, points required for the calculation of the radius of curvature and included angle (ϴ). Images modified from Susman, (1984).

Instead of using coordinate calipers, values for L, D, H and R were obtained by taking digital pictures of the proximal phalanges and then using ImageJ software. Since L was also obtained manually using digital calipers, the values were checked for consistency. More specifically, in order to ensure that measurements obtained by

ImageJ using digital pictures were approximately equivalent to measurements taken by hand using digital calipers, the scale on ImageJ was set several times in order to take the same measurement multiple times. Each time the measurement obtained by ImageJ was compared, the difference was less than 0.1 mm.

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Protocol to obtain the radius of curvature (R) and included angle (ϴ) using

ImageJ:

1- Import image of proximal phalanx to ImageJ and set the scale from pixels to

millimeters (mm).

2- Determine the midpoint of each articular surface for the proximal phalanx (Fig.

M2).

3- Draw a line connecting the midpoints of each articular surface. This is L (Fig.

M2).

4- Find the midpoint of the length measurement and then determine and measure

values for H and D (Fig. M2).

5- Determine line segment PB using H and D values: Line segment PB = (H-D/2)

6- Determine where B will be starting from the length measurement AC. B will

serve as the midpoint line for the three-point tool in the next step (Fig. M2).

7- Use the Three-Point Tool in ImageJ to find the value of radius of curvature (R)

by inputting points A, B, and C (Fig. M2).

8- R is given in pixels and then converted to mm.

9- Once R was obtained by ImageJ, ϴ was calculated by using an Arc-sin

calculator on a personal computer (MacBook Pro; Apple).

ϴ = 2*Arc-sin[L/2R]

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Articular surface area

The surface area of the articular surface of a long bone can be used as a proxy for body size because as body mass increases, joints also expand in order to distribute that force placed on the joint (Ruff & Niskanen, 2018). In this study, the surface area of the proximal articular surface of a proximal phalanx was calculated by taking a picture of the proximal articular surface. That image was imported into ImageJ and then a line was drawn tracing the perimeter of the articular surface. The surface area tool was used on

ImageJ to obtain a value for surface area.

Torsion

Images of the distal view of the trochlea of all proximal phalanges were taken. Every image was imported onto ImageJ and an angle was drawn with one side of the angle tracing along the palmar edge of the distal condyles and the other side of the angle tracing the edge of the surface that the phalanx was resting on. This is done while palmar tubercles on proximal end of phalanx are both resting on surface. Each angle was given as a read-out from ImageJ.

Graphical plots and Statistics

Statistical analyses were performed with SAS JMP software. Plots were executed using a software program (GraphPad Prism; GraphPad Software Inc.). In box-and-whisker plots, each box represents the 25th and 75th percentile, with whiskers that denote the range or

44 the 10th and 90th percentiles, as specified in graphs; outliers are plotted. Pairwise means comparisons of groups were performed by Tukey-Kramer test. Statistically significant differences are defined as a P value < 0.0001.

45

Results

Goals of this thesis

Ar. ramidus is an interesting and important early hominin because its skeletal remains reflect both arboreal and terrestrial locomotive capabilities. Most of what is known about

Ar. ramidus comes from fossil remains identified at Aramis, Ethiopia. One aspect of the

Ar. ramidus manus that remains to be investigated are the manual proximal phalanges.

GWM10/P1 is a Ar. ramidus manual proximal phalanx from Gona, Ethiopia. The first goal of this thesis was to determine hand side and ray number of GWM10/P1 by comparisons of morphologies and metrics to those of manual proximal phalanges of humans and African great apes. The second goal was to compare the 4th proximal phalanges of humans, African great apes, and Au. afarensis to GWM10/P1 to identify likenesses and dissimilarities and yield insight into the associated animal’s mode of locomotion.

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The morphology of proximal phalanges

Proximal phalanx 1 of humans, gorillas, and chimpanzees

In order to address the above goals, including to describe the Ar. ramidus manual proximal phalanx (GWM10/P1) and assign it to a side and a ray number, it was first necessary to extensively characterize the morphology of proximal phalanges of humans, lowland gorillas (Gorilla gorilla), and common chimpanzees (Pan troglodytes). Initially, proximal phalanx 1 was inspected for salient features that may serve as characteristics that could be used to distinguish it from the proximal phalanges of the other rays. This information could also potentially be used to establish features to distinguish ray 1 between these three species.

In humans, there is a large radial side basal tubercle on the pollical proximal phalanx, which is the insertion point for the abductor pollicis brevis muscle, and this gives the phalanx an asymmetric appearance on the radial side when viewed from the dorsal aspect

(Fig. R1, Table R1). The proximal articular surface of the base of a human proximal phalanx 1 is elongated medio-laterally, giving the surface an oval shape which is different from the shapes of the articular surfaces for either chimpanzees or gorillas— both of which have more rounded articular surfaces (Fig. R2, Table R1). There is a tubercle for the chimpanzee proximal phalanx 1 (Fig. R3), whereas gorillas exhibit a radial tubercle that is best seen from the palmar aspect.

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Figure R1. Right hand proximal phalanges of rays 1 to 5 (left to right) of a human. Circle indicates radial side tubercle of proximal phalanx 1. Scale bar = 10 mm.

Figure R2. View of the articular surfaces of the 1st proximal phalanges from a human, gorilla and chimpanzee from left to right. Specimens are all from right hands. Scale bar = 10 mm.

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Figure R3. Left hand proximal phalanges of rays 5 to 1 (left to right) of a female gorilla (top) and a female chimpanzee (bottom). Scale bar = 10 mm.

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In humans, gorillas, and chimpanzees, when viewing the 1st proximal phalangeal condyles from the palmer vantage, the ulnar (medial) condyle projects further in the palmar and distal directions (Figs. R4 and R5). The distal articular surface of proximal phalanx 1 in chimpanzees and gorillas does not extend onto the dorsal aspect (Fig. R6,

Table R1) as it does in humans. This different feature is most evident in the side view

(Fig. R6) because for the African great apes, the distal phalanx is very flat on the dorsal aspect, with no rounded dorsal articular surface (Fig. R7). The palmar surface of the 1st

proximal phalanges of the shafts of humans and gorillas are flat (with no flexor sheath ridges); in contrast, the chimpanzee shaft of the same bone is convex longitudinally (with no flexor sheath ridges) (Fig. R4, bottom; Fig. R5, bottom).

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Figure R4. Human proximal phalanx 1 of the right hand, palmar surface, displays the distal ulnar condyle extending in the palmar direction (top) and the distal direction (bottom). Distal region of the phalanx is towards the tops of the photos. Scale bar = 10 mm. 51

Figure R5. Palmar surfaces of chimpanzee (left) and gorilla (right) proximal phalanges 1 of the right hand display the distal ulnar condyles (encircled) extending in the palmar (top) direction and distal direction (bottom). Scale bar = 10 mm. 52

Figure R6. Comparison of side views of proximal phalanges 1 of gorillas (top), chimpanzees (middle), and humans (base). Only the human distal articular surface is rounded and its articular surface extends to the dorsal aspect (white arrow). The distal articular surfaces of gorilla and chimpanzee are flat. Scale bar = 10 mm.

Figure R7 - Gorilla distal articular surface does not extend to the dorsal aspect for proximal phalanx 1 (circle).

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Proximal phalanx 2 of humans, gorillas, and chimpanzees

The second proximal phalanx of humans, gorillas, and chimpanzees can be distinguished from the other proximal phalanges when viewed from the proximal articular surface because of the presence of a radial tubercle, which is the insertion point for the first dorsal interosseous muscle that gives the base an asymmetric shape (Figs. R8, R9,R10 and Table R1). This asymmetry of the proximal palmar tubercle can also be seen when viewed from the palmar aspect. At the distal end, the ulnar condyle projects further in the palmar direction (Figs. R11 and R12). The palmar aspect of proximal phalanx 2 of all three species have flexor sheath ridges in the mid-shaft region. The flexor sheath ridges are the attachment points for the flexor retinacula. The sheaths are strong transverse fibrous bands that restrain the tendons of the digital flexor muscles (flexor digitorum profundus and flexor digitorum superficialis). Humans exhibit the smallest flexor sheath ridges. Chimpanzees display moderate flexor sheath ridges in the mid-shaft region, and the shaft surface is very flat in that area. Gorillas have the most prominent flexor sheath ridges, and the palmar surface of the proximal phalanx 2 shaft is also flat as opposed to being concave or convex (Fig. R13).

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Figure R8. Gorilla proximal phalanx 2 (left) and 4 (right) of right hand displaying proximal surfaces. The radial side tubercle (black arrowhead) on the left image identifies bone as proximal phalanx 2 from a right hand. Scale bar = 10 mm.

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Figure R9. Proximal articular surfaces of human proximal phalanges 2 (left) and 4 (right) of the right hand. The tubercle (arrowhead) is a salient distinguishing feature found on the radial side of proximal phalanx 2. The bones are oriented so that the dorsal sides of the phalanges are up. Scale bar = 10 mm.

Figure R10. Chimpanzee proximal phalanges 2 (left) and 4 (right) of the right hand display proximal surfaces. The radial side of proximal phalanx 2 on the base has a tubercle (black arrow head) that identifies it as proximal phalanx 2. Scale bar = 10 mm.

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Figure R11. Human proximal phalanx 2 of the right hand shows that the ulnar side distal condyle extends further in the palmar direction (white arrowhead) than the radial condyle. Radial side basal tubercle (white arrow). Scale bar = 10 mm.

Figure R12. Gorilla proximal phalanx 2 of the right hand. Arrowhead marks the ulnar side distal condyle that extends further in the palmar direction) than the radial condyle. This is the same morphology as humans for the analogous bone. Scale bar = 10 mm.

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Figure R13. An oblique view of the palmar aspects of gorilla proximal phalanges, 2-5, left to right. The palmar sides of proximal phalanx 2, 3, 4, and 5 shafts are flat, concave mediolaterally, concave mediolaterally, and convex mediolaterally, respectively.

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Proximal phalanx 3 of humans, gorillas, and chimpanzees

The third proximal phalanx of humans, gorillas, and chimpanzees have a radial side basal tubercle that is slightly more developed than the ulnar side basal tubercle when viewed from the palmar aspect. These tubercles are the insertion points of the second and third dorsal interosseous muscles. The asymmetry of the basal tubercles is subtle. At the distal end, the ulnar condyle projects further in the palmar and distal directions than the radial condyle, similar to the morphology of the proximal phalanx of ray 2 (Fig. R14, black arrowhead).

The palmar side of proximal phalanx 3 is substantially different in the three species. Humans and chimpanzees exhibit small flexor ridges and the palmar midshaft is flat (Fig. R14). In chimpanzees, there is a constriction, or ‘waisting’, of the mediolateral width between the midshaft and the base (Fig. R14, white arrowhead). Gorillas have a strikingly concave palmar midshaft, so that a cross-section would look like the letter “U” with a broad bowl. Their flexor ridges are large (Figs. R13 and R14, Table R1).

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Figure R14. Palmar surface view of proximal phalanx 3 of humans, gorillas, and chimpanzees from left to right of the right hand. Shown are the slight flexor ridges in humans and chimpanzees and the prominent flexor ridges of gorillas. White arrowhead marks the wasting effect. Black arrowhead indicates ulnar-side condyle. Scale bar = 10 mm.

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Proximal phalanx 4 of humans, gorillas, and chimpanzees

When viewing the basal tubercles from the palmar aspect, the ulnar tubercle is slightly larger than the radial tubercle (Figs. R8, R9, and R10, Table R1) in the three species.

The ulnar tubercle is the insertion point for the fourth dorsal interosseous muscle. Also, the overall shape or outline of the articular surface of proximal phalanx 4 has a more square-like shape as compared to proximal phalanx 2, whose shape is more mediolaterally rectangular because of the presence of the ulnar-dorsal tubercle (Fig. R9,

Table R1). The ulnar-palmar tubercle also extends further in the palmar direction, relative to the radial-side tubercle. The palmar side of the human proximal phalanx displays a relatively flat surface with small flexor ridges in the mid-shaft region (not shown). In the chimpanzee proximal phalanx 4, the palmar surface is slightly concave.

The flexor ridges, which are more pronounced in chimpanzees than in humans, are located in the mid-shaft region and are slightly larger on the radial side. In gorillas, the palmar surface is deeply concave (Fig. R13), though not as much as in the proximal phalanx of ray 3 of this species. The flexor ridges are prominent and located mid-shaft.

Flexor sheath ridges, in all three species, when present are found in the middle third of the shaft (mid-shaft).

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Proximal phalanx 5 of humans, gorillas, and chimpanzees

The fifth proximal phalanx is the smallest and most gracile of the medial four proximal phalanges. It is asymmetrical on the ulnar side due to the larger ulnar tubercle, which is the insertion point of the abductor digiti minimi and flexor digiti minimi muscles. This marked asymmetry is most notable in humans when viewing the articular surface (Fig.

R15). Gorillas and chimpanzees have a square-like shape of the base of the phalanx and a round outline to the articular face. Humans have a mediolaterally oval outline of the base and of the outline of the articular surface (Fig. R15, Table R1). The distal condyles project more distally on the radial side than the ulnar side for humans, gorillas, and chimpanzees (Fig. R16, white arrows). The palmar surface of the shaft of proximal phalanx 5 of humans and chimpanzees are flat with very small flexor sheath ridges. In the gorilla’s proximal phalanx 5, the palmar surface is markedly mediolaterally convex and has prominent flexor ridges that are higher on the radial side (Fig. R16).

Figure R15. Articular surfaces of proximal phalanx 5 of humans, chimpanzees and gorillas from left to right of the right hand. Image displays the rectangular shape of the base and the round shape of the articular surface of the gorilla and chimpanzee proximal phalanges. This is in contrast to the mediolaterally oval outline of the base and articular surface of the proximal phalanges of humans.. Scale bar = 10 mm.

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Figure R16. Palmar sides of the 5th proximal phalanges of humans, gorillas and chimpanzees of the right hand. Each ulnar side shows a prominent tubercle, which is an effective means to identify the hand to which this phalanx belongs. The radial side of the shaft has a prominent flexor ridge in gorillas. Similarly, the chimpanzees have a small flexor ridge on the radial side of the shaft. Arrows mark radial distal condyles, which extend further in the distal direction than the ulnar condyles. Scale bar = 10 mm.

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Table R1: Distinguishing features of the proximal phalanges Feature PP1 PP2 PP3 PP4 PP5 Large basal radial Present Absent Absent Absent tubercle for the Absent * abductor Pollicis brevis muscle (H) Thickest mediolaterially Present Absent Absent Absent (H) Absent * Basal articular surface Present Absent Absent Absent oval mediolaterally (H) Absent * Shortest and thinnest of Present Absent Absent Absent all PPs (G, C) Absent * Palmar surface very Absent Absent Present Present Absent concave with large flexor sheath ridges (G) Distal articular surface Present Present Present Present rounded and extends to Present * the dorsal surface (H) Distal articular surface Absent Present Present Present rounded and extends to Present * the dorsal surface (G, C) Radial side tubercle of Absent Present Absent Absent first dorsal interosseous Absent * muscle (H, G, C) Proximal articular Absent Present Absent Absent surface is mediolaterally Absent * oval, as opposed to square, because of radial side tubercle (H, G, C) Proximal or basal Absent Present Absent Absent surface is rectangular, Absent * greater in the mediolateral direction (H, G, C) Longitudinally curved Absent Present Present Present dorsal surface (G, C) Present * Flexor sheath ridges Absent Present Present Present present in the middle Present * third of shaft (G, C) Widening of the shaft at Absent Absent Absent Absent Absent mid-shaft (H) Widening of the shaft at Absent Present Present Present mid-shaft (G) Present * Widening of the shaft at Absent Present Present Present Absent mid-shaft (C) * denotes presence or absence of feature found in GWM10/P1 H = Humans G = Gorillas C = Chimpanzees

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GWM10/P1

GWM10/P1 preservation The Ar. ramidus manual proximal phalanx (GWM10/P1) was found in Gona Western

Margin (GWM), Afar, Ethiopia (Semaw et al., 2005). The fossil was recovered from sediments of the Sagantole Formation with an estimated age range of between 4.8-4.3 Ma

(Semaw et al., 2005). The sediments from this location could not be dated directly because it did not contain datable volcanic material. The dates that were established biochronologically by comparison with nearby localities within the same project area that were datable. The GWM10/P1 proximal phalanx is nearly complete, and its dimensions are shown in Table R2. However, the fossil is broken and is missing some material on the medial side. There are several superficial longitudinal surface cracks, which appear to have been filled with some amount of matrix (expanding matrix deformation) and may have produced minimal distortion (Fig. R17).

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*

Figure R17. GWM10/P1 in dorsal, palmar and side view (Simpson). Palmar view of GWM10/P1, which shows the flat morphology of the shaft. White arrowhead marks ulnar side tubercle. Black arrowhead indicates small flexor sheath ridge and transverse widening of bone. Asterisk denotes slightly larger radial condyle. Scale bar = 10 mm.

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GWM10/P1 morphology

To assign a ray number and side to GWM10/P1, we characterized the morphology of this specimen and compared it to key features of humans, gorillas, and chimpanzees

(Chapter 1) and those of relevant fossils. The proximal epiphysis of the bone is fused and therefore this bone is believed to have belonged to an adult (Simpson, et al., in review). GWM10/P1 has a flat palmar surface (Fig. R17) and a longitudinally convex dorsal surface (Fig. R18, Table R1). The region of the bone where the radial side flexor sheath should appear is broken leaving little evidence of any tubercle that might have been present. (Fig. R19). The proximal articular surface is round and concave (does not have an ovoid, or mediolaterally elongated outline (Fig. R20 Table R1). In dorsal view, the base has an ulnar tubercle for the insertion of the fourth dorsal interosseous muscle.

This observation together with the overall square-like outline of the base of the phalanx, in proximal view, makes GWM10/P1 most likely to be from ray 4 of the left hand. See

Figs. R8, R9, R10 for comparisons with humans, gorillas, and chimpanzees. The condyles are approximately symmetrical with the radial condyle slightly larger. The dorsal edge of the same condyle is partially broken (Fig. R19). There is a small flexor sheath ridge present on the ulnar side (Fig. R17). When observed in dorsal view, there is a slight widening of the shaft at mid-shaft, similar to Au. afarensis and gorillas and chimpanzees (Fig. R21), but distinct from humans (Fig. R1, Table R1). Moreover, there is slight axial torsion of the shaft (Fig. R22; see axial torsion section and discussion).

Basal palmar tubercles are present and generally symmetrical with a slightly larger tubercle on the lateral side. However, the taphonomic damage to the bone makes this analysis challenging. With a total length of 50.3 mm (Table R2), GWM10/P1 is slightly

67 longer than the 4th proximal phalanges of Ar. ramidus from Aramis (ARA-VP-6/500-022

= 47.1 mm, ARA-VP-6/500-069 = 47.8 mm) (Lovejoy et al., 2009b). GWM10/P1 is also longer than any of the Hadar Au. afarensis (Fig. R21) (Bush et al., 1982) and human specimens (Table R2; see below). With respect to its total length, the GWM10/P1 phalanx falls within the ranges of the African great apes. In summary, GWM10/P1 is likely a 4th proximal phalanx from the left hand based on morphology.

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Figure R18. Side view of GWM10/P1 (top) and a human 4th proximal phalanx (bottom) comparing longitudinal curvature. Image of GWM10/P1 shows the missing portion of the radial side of the shaft. Scale bars = 10 mm.

Figure R19. Proximal articular surface of GWM10/P1 cast.

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Figure R20. Dorsal view of GWM10/P1 and A. L. 333-63 (Au. afarensis). GWM10/P1 is much larger overall in size. A. L. 333-63 is problably the 3rd proximal phalanx of the right hand. Scale bars = 10 mm.

Figure R21. GWM10/P1 condyles at the distal surface. Axial torsion shown.

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Metrical comparisons of proximal phalanges

Lengths of proximal phalanges of humans, gorillas, and chimpanzees

In order to address the main goals of this thesis, including (1) the detailed anatomical description of the fossil GWM10/P1, (2) the assignment of hand side and ray number to this fossil, and (3) surmise how the associated hominin may have locomoted, it was necessary to extensively characterize the metrics of proximal phalanges of humans, gorillas, and chimpanzees. Once these comparative data were obtained, they could be used in conjunction with other metrics and morphological analyses to examine

GWM10/P1. Up to this point, we have mainly described morphologies, so here we examine manual proximal phalanges quantitatively.

Total length comparisons of phalanges are useful with data sets that contain multiple proximal phalanges of the same individuals. To assist in the assignation of a proximal phalanx to a correct ray position, a comparison of the total lengths (TL) of the bones was conducted (Fig. M1). The total length size order for each finger of humans, from longest to shortest, is generally 3>4>2>5>1 (Jones, 1942). Human digit lengths are sexually dimorphic and, in males, digit 4 is commonly longer than digit 2; however, in human females (Zheng & Cohn, 2011), the 2nd digit is often longer than or equal to the 4th. So for females, the order of total length for each digit can be 3>2>4>5>1 (Zheng & Cohn,

2011).

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The lengths of human manual proximal phalanges were studied to determine if the digit length order was similar to the proximal phalanges length order. For males, the descending order of lengths for the proximal phalanges were 3>4>2>5>1 for 9 of 10 hands and in a single hand the order was 3>4=2>5>1 (Fig. R1; Table R2). For 8 of 10 female hands, the order of lengths for the proximal phalanges were 3>4>2>5>1. For one female hand, the order was 3>4=2>5>1, and for another the digression was 3>2>4>5>1, indicating that females have a slightly greater variation in proximal phalangeal lengths.

The mean lengths of the proximal phalanges are displayed on Table R2. These findings indicate that some other element(s) of the human ray (such as the metacarpals or intermediate phalanges) must contribute to the differential lengths that are affected by hormones while in utero (Zheng & Cohn, 2011).

The lengths of the manual proximal phalanges of chimpanzees and gorillas were analyzed to determine the relative length order (Fig. R3; Table R2). It was found that proximal phalanx 4 is longer than proximal phalanx 2 for chimpanzees and gorillas. For chimpanzees (n=20) and gorillas (n=20), the relative order of proximal phalanx length was universally 3>4>2>5>1 regardless of sex and species. Gorillas exhibit marked sexual dimorphism in size, making the male of the species much larger than the females in overall body size and this is also seen in their hand bones.

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Table R2. Measurements of GWM10/P1* and the 4th proximal phalanges of other extinct and extant primates. *All measurements were taken on a cast of the fossil Measurements GWM10/P1 Au. Humans Chimpanzees Gorillas (mm) (n = 1) afarensis (n = 20) (n = 20) (n = 20) (n = 2)

Total length (mm) 50.13 38.74 42.10 ± 2.5 56.33 ± 3.4 55.09 ± 4.8 Proximal base 12.9 10.17 11.51 ± 0.9 13.67 ± 1.6 17.28 ± 2.3 height (mm) Proximal base 13.11 11.92 14.56 ± 1.2 14.54 ± 1.5 20.21 ± 3.0 breadth (mm) First quarter height 10.28 6.94 8.39 ± 0.8 9.16 ± 1.3 9.92 ± 1.2 (mm) First quarter breadth 11.08 7.90 9.93 ± 1.4 10.74 ± 1.7 15.36 ± 2.2 (mm) Midphalanx height 8.61 5.70 6.59 ± 0.7 7.54 ± 0.5 7.98 ± 1.1 (mm) Midphalanx breadth 11.18 8.46 9.14 ± 1.1 11.42 ± 1.3 16.15 ± 2.2 (mm) Third quarter height 7.92 4.86 5.98 ± 0.6 6.59 ± 0.7 6.74 ± 1.1 (mm) Third quarter 12.09 7.75 9.48 ± 0.9 12.23 ± 1.2 15.78 ± breadth (mm) 2.2 Distal trochlear 9.16 6.28 8.08 ± 0.6 10.05 ± 0.7 11.11 ± 1.6 height (mm) Distal trochlear 10.46 8.74 11.21 ± 1.2 11.44 ± 0.8 14.47 ± 2.0 breadth (mm) Proximal articular 60 58.80 70.92 ± 9.7 95.27 ± 9.3 158.05 ± surface area (mm2) 33.4 Torsion (angle in - 3.69 - 2.65 0.7 ± 2.9 - 2.39 ± 2.3 - 5.01 ± degrees) 3.0 Included angle 50 52 31 56.4 45.6 (degrees)

Sexes combined. Means with standard deviations demonstrated when multiple samples available.

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Table R3: Mean lengths ± SD of proximal phalanges from male and female chimpanzees, gorillas, and humans.

Male Female

PP2 PP3 PP4 PP5 PP 2 PP3 PP4 PP5

Chimpanzees 50.6 ± 60.3 ± 56.7 ± 44.2 ± 50.5 ± 59.6 ± 55.9 ± 42.8 ±

2.8 2.9 2.9 2.2 3.1 4.8 4.2 3.2

Gorillas 55.9 ± 62.5 ± 59.6 ± 49.6 ± 48. 5 ± 53.9 ± 50.8 ± 41.6 ±

2.6 1.7 2.1 2.1 1.9 2.4 2.3 2.4

Humans 41.3 45.6 42.6 34.2 40.9 45.3 41.6 32.8

± 2.2 ± 2.9 ± 2.8 ± 2.1 ± 2.1 ± 2.6 ± 2.4 ± 2.0

Units: millimeters. n = 20 for all samples: 10 males, 10 females. Note: TLs of proximal phalanges (PP) of ray 1 are not shown but are always smaller than all other proximal phalanges within a species. All lengths are maximum lengths.

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Proximal articular surface area (PAS) of phalanges as a proxy for body mass and its relation to phalangeal length

The body size of an animal is related to overall activity level, behavior, and mode of locomotion (Ruff & Niskanen, 2018). Thus, knowing an animal’s mass is important to better understanding its niche and its conduct within. However, if an isolated finger bone fossil is all that is found, how do you know it is long for the size of the animal or is it from a larger animal? This information may yield insight into the animal’s mode of locomotion, as long phalanges relative to body size can be an indicator of its level of arboreality (de Bonis & Koufos, 2014).

In an ideal situation, fossil remains that contain several parts of the animal’s skeleton, will yield the most accurate estimate for body size. However, what can be known about body size from a single proximal phalanx, e.g. GWM10/P1? Certain dimensions of long bones can vary predictably with the mass (Ruff & Niskanen, 2018). The distal femoral articular surface area of primates reflects the level of loading (body mass) and at the same time exhibits relatively little excursion since it is part of a largely uniaxial joint.

Excursion is defined as the lateral movement of bones at a joint. Based on what has been shown for body mass estimation and the femur (Ruff & Niskanen, 2018), we hypothesized that it would be possible to estimate the body mass of GWM10/P1 using the proximal articular surface (PAS) area because it is a proxy for the magnitude of loading due to the functional limitations of hyaline cartilage (Davies et al., 2007). In life, joints are separated only by a very thin and frictionless layer of hyaline cartilage. Cartilage is

75 non-vascularized and therefore vulnerable to injury with virtually no mechanism for repair once injury occurs. In order to minimize the stress placed on the cartilaginous layer with increasing body size, joints have expanded. Ultimately, PAS area information could be used to decide if the GWM10/P1 phalanx is long for the animal’s body mass or not.

The first goal was to determine whether the PAS areas of proximal phalanges were appropriate indicators of body mass of extant species. If this were the case, then we would use the PAS area of the proximal phalanx to estimate the relative size of the Gona hominin. The body mass of gorilla males > gorilla females > human ≥ chimpanzees. For proximal phalanges 2, 3, and 4, the order of the mean values for the square roots of the

PAS areas is gorilla males > gorilla females > chimpanzees > humans (Figs. 22, 23, 24).

The order of the mean values of square roots of the PAS area of these species is correct to validate this method for estimating relative body mass. For humans and chimpanzees, the mean values of the square root of the PAS areas of proximal phalanx 2 were not significantly different (Fig. 22). However, for proximal phalanx 3 and 4, the mean values of the square roots of the PAS areas were slightly larger for chimpanzees (Figs 23, 24), indicating that for smaller mass differences between species this method may not be sensitive enough to discern. For instance, the method to determine the PAS areas does not consider that the PAS areas may have appreciable depths, which may contribute to PAS areas. Nonetheless, a clear relationship is observed: as a primate’s body mass increases, so do the PAS areas of its proximal phalanges.

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Next, we attempted to determine what constitutes a long phalanx versus what seems to be a long phalanx but is actually a bone from a larger sized animal. To establish this, four specimen types were used: gorilla males, gorilla females, humans, and chimpanzees.

Plots of the mean values of the square roots of the PAS of proximal phalanges 2, 3, and 4 against their total lengths (TL) explored this relationship (Fig. 25) as did a plot of the mean of the ratio of the square root of the PAS of proximal phalanx/TL (Fig. 26). Figure

R26 demonstrates that in general the ratios within each group (gorilla males, gorilla females, humans, and chimpanzees) are similar. However, between groups, chimpanzees stand apart (with statistically significant lower ratios), indicating that these proximal phalanges are longer when normalized against a proxy for body mass.

These analyses validated our method which aimed to determine what constitutes a long phalanx versus what seems to be a long phalanx but is actually a bone from a larger sized animal. Next, we evaluated how the lengths of fossil proximal phalanges of Au. afarensis and GWM10/P1 scaled with body size. Au. afarensis grouped with male and female gorillas and humans (Figs. 25, 26). However, GWM10/P1 had long phalanges relative to its body size as demonstrated by a low ratio for the square root of the PAS of proximal phalanx/TL (~0.15). Our analyses of GWM10/P1 support a degree of arboreality for this hominin. These data buttress the analysis of Ar. ramidus from Aramis by distinct methods, which described Ar. ramidus as arboreally capable.

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Figure R22. Comparisons of PAS areas of proximal phalanges of ray 2 of chimpanzees, gorillas, and humans. Plotted is the square root of the mean PAS area ± SEM for each species. * P < 0.0001; ns = no significance.

Figure R23. Evaluations of PAS areas of proximal phalanges of ray 3 of chimpanzees, gorillas, and humans. Plotted is the square root of the mean PAS area ± SEM for each species. * P < 0.0001.

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Figure R24. Assessments of PAS areas of proximal phalanges of ray 4 of chimpanzees, gorillas and humans. Plotted is the square root of the mean PAS area ± SEM for each species. * P < 0.0001.

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A

B

C

Figure R25. Plots of the square root of the PAS area of each proximal phalanx from ray 2 (A), 3 (B), and 4 (C) against total length of each cognate bone from chimpanzees, gorillas, humans, Au. afarensis, and GWM10/P1.

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Figure R26. Ratios of the means of the square root of the PAS of proximal phalanx/TL ± SEM for chimpanzees, gorillas and humans and individual ratios of Au. afarensis and GWM10/P1. P-Value < .0001 for the comparison of chimpanzees to male gorillas, female gorillas and humans.

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Axial torsion

To further characterize manual proximal phalanges, we examined the axial torsion of each of the manual phalanges. Axial torsion of the pedal distal phalanges and the manual distal phalanges are related to locomotor pattern in hominins and the African great apes

(Day & Napier, 1966; Almecija et al., 2010). Whether torsion may assist in the characterization of GWM10/P1 is a relevant question. Finally, how torsion may contribute in the assignment of a ray to any manual proximal phalanx from an extant or extinct specimen maybe a potent potential tool.

The axial torsion of manual proximal phalanges 2-5 of humans, gorillas, chimpanzees, the Hadar specimens of Au. afarensis, and GWM10/P1 was measured (Figs. R21, R27, and R28). The 2nd and 3rd proximal phalanges are described as having positive torsion because the bone twists so that the trochlea is oriented towards the pollex. This can also be called lateral torsion. In the 4th and 5th proximal phalanges the opposite is true. The phalanges twist in such a way that the trochlea is oriented away from the pollex. This can also be described as having medial torsion. The absence of axial torsion is presented as zero. The results for analyzing torsion can be found in figure R29 and table R4. For the

2nd and 3rd proximal phalanges, torsion is usually positive.

The 4th proximal phalanx usually has negative values for all specimen groups (Fig. R29 and Table R4). For chimpanzees, gorillas, Au. afarensis, and GWM10/P1, the torsion values were exclusively negative (Fig. R29 and Table R4). Torsion for the 5th proximal phalanx tends to twist in the same direction as the 4th proximal phalanx, i.e., medially.

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Figure R27. Image of axial torsion for proximal phalanx of Au. afarensis AL 333-62, a likely fourth proximal phalanx of the left hand.

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Figure R28. Images of distal and proximal articular surfaces of proximal phalanges of gorillas (A, distal; A1, articular), chimpanzees (B, distal; B1, articular), and humans (C, distal; C1, articular). They are ordered 2-5 from left to right, respectively. The three specimens are right hands. All bones similarly display, at most, a modicum of asymmetry in the heights of the basal tubercles. Therefore, when torsion does occur it begins somewhere along the shaft of the phalanx. All phalanges are oriented with the dorsal aspect at the top of the picture. Scale bars = 10 mm.

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In addition to box-and-whisker plots, statistical analyses were conducted in order to determine whether the mean torsion values of the 2nd proximal phalanx were significantly different from mean torsion values of the 4th proximal phalanx. If this was the case, then torsion would be useful in determination of ray number and side (Fig. R30). For humans, the mean torsion value ± SEM (standard error of the mean) was 4.53° ± 0.87 for the 2nd proximal phalanx and 0.7° ± 0.64 for the 4th proximal phalanx, with a p = 0.0011 via a

Students t-test. In the comparison of gorillas, the mean torsion value was 12.3° ± 1.18 for the 2nd proximal phalanx and -5.0° ± 0.662 for the 4th proximal phalanx, with a p <

0.0001. For chimpanzees, the mean torsion value was 6.36° ± 1.54 for the 2nd proximal phalanx and -2.39° ± 0.5 for the 4th proximal phalanx, with a p < 0.0001. These findings demonstrate that torsion values are statistically different between the 2nd proximal phalanx and 4th proximal phalanx for humans, gorillas, and chimpanzees. These results support a role for torsion being used to distinguish between the 2nd and 4th phalanges that would otherwise be challenging to distinguish based on morphology or other metrics. The torsion value of GWM10/P1 is -3.7°. This value in addition to the morphological observations supports a conclusion that GWM10/P1 is the fourth proximal phalanx of the left hand of Ar. ramidus.

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Figure R29. Torsion values in degrees. Each box represents the 25th and 75th percentile, with whiskers that denote 10th and 90th percentiles. A positive value signifies torsion towards the pollex or lateral side. A negative value signifies torsion away from the pollex or towards the medial side. The centerline is the median. Sample sizes for humans, chimpanzees, and gorillas were 20 each. Sample size for Au. afarensis is 2.

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Table R4 - Median torsion values (degrees) Chimpanzees Gorillas Humans Au. afarensis GWM10/P1 Proximal 5.1 11.85 5.3 10.9 phalanx 2 Proximal 0 4.05 2.1 0 phalanx 3 Proximal -2.4 -4.5 0 -2.65 -3.7 phalanx 4 Proximal -8.2 -7.15 0 phalanx 5

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Figure R30. Comparison of proximal phalanges 2 and 4 mean torsion values ± SEM of humans, gorillas, and chimpanzees. In all cases, the mean torsion of proximal phalanx 2 is greater than proximal phalanx 4, with statistical significance. **** p < 0.0001 and **p = 0.0011 by Students t-test, unpaired.

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Comparison of phalangeal shapes

Establishing the side and ray of GWM10/P1 as proximal phalanx 4 of the left hand enabled metrical comparisons with analogous manual positions with those of other extinct and extant species. The purposes of these numerical comparisons were to quantitatively characterize the size and shape of the specimen in order to gain insight into

GWM10/P1’s mode of locomotion, use of its hand, and phylogenetic relationships. For a quantitative comparison of the shape of GWM10/P1 to the 4th proximal phalanges of extinct and extant hominoids, the shape of the phalanges at five different points along the bone is described (Fig. M1). The measurements to describe shape were mediolateral breadth vs. dorsopalmar height at the proximal end (the base), half way between the base and the mid-shaft, the mid-shaft, half way between the mid-shaft and the distal end, and the distal end (the head). A ratio that is more than 1.0 describes a shape that is broader, and a ratio less than 1.0 describes a shape that is relatively taller. A ratio of 1.0 could mean the shape is square-like or circle-like, which can be discerned by visual inspection.

At the proximal or basal end (Fig. M1, D) of proximal phalanx 4, humans and gorillas overlap and have a base shape (proximal base width (PBW)/proximal base height (PBH)) range from ~1.2 – ~1.5. Au. afarensis specimens base shape ratios are ~1.2, so they occupy a domain that is most like the lower range of humans. The base shape ratios of chimpanzees are ~1.0 – ~1.2, making them square like (Figs. R31; R10; R28). This contrasts with the base shape ratios of humans and gorillas, which reveal bones that are relatively longer mediolaterally. The GWM10/P1 base shape ratio falls within the range of chimpanzees and has a shape ratio of ~1.0, which is square like (Figs. R31; R28). As

89 noted previously, GWM10/P1 has damage on is radial side, which influences these measurements. GWM10/P1’s length is at the lower end of chimpanzees. Therefore, with respect to base shape, GWM10/P1 is more similar to chimpanzees.

Figure R31. Base shape comparisons. ML – mediolateral (width); AP- anteroposterior (height). See Fig M1, D.

Next, we examined the midshaft (Fig. M1, A,B) of the 4th proximal phalanges. At the midshaft, there is separation between the gorillas and chimpanzees shape ratios (midshaft width (MSW)/ midshaft height (MSH)) (Fig. R32). Chimpanzees and humans occupy a shape ratio range ~1.2 – 1.7, which indicates a shape that is slightly mediolaterally flat.

These two groups are only separated by the lengths of the phalanges. Gorillas shape ratios occupy a larger range that begins where chimpanzees end, at approximately 1.7, and end at 2.4, making these the most mediolaterally flat of the samples. This morphology in gorillas is coincidental with the region on the shaft where there is extreme

90 concavity of the ventral surface produced by the projecting retinacular ridges. These retinacular ridges are not included in the height measurements of the phalanx because digital outside point calipers were used. GWM10/P1 has a shape ratio at midshaft that is

~1.2, so square-like (Fig. R32). The shape ratio and length measurement of GWM10/P1 on the midshaft shape graph is situated between humans and chimpanzees, whereas Au. afarensis points fall near the human distribution.

Figure R32. Midshaft shape comparisons. See Fig. M1, A,B.

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The distal end or the head of the proximal phalanx was next examined (Fig. M1, C).

Humans head shape ratios (head width/ head height) ranged from ~1.3 – ~1.5, making them relatively flat mediolaterally (Figs. R33, R28). Au. afarensis head shape ratios were ~1.4, and these fall within the human range (Fig. R33). The chimpanzees shape ratios range between ~1.0 - ~1.3, and gorillas shape ratios range between ~1.2 - ~1.4, which indicates that gorillas have a slightly flatter shape mediolaterally at the head of the phalanx and the chimpanzees are slightly more square-like. GWM10/P1 falls within the range of chimpanzees with a head shape ratio ~1.1. This finding indicates that the head shapes are most similar between chimpanzees and GWM10/P1.

Figure R33. Head shape comparisons. See Fig. M1, C.

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We examined the shape ratio at the point midway between the base and the midshaft termed the proximal shaft shape (proximal shaft width (PSW)/ proximal shaft height

(PSH) (Figs. M1, A, B and R34). At this point along the shaft, the great ape groups exhibit a significant amount of separation, when plotted against maximum length.

Gorillas shape ratios for the proximal shaft occupy a range between ~1.9 - ~3.1, which indicates that they are significantly flatter mediolaterally than the other groups. The shape ratios of humans and chimpanzees overlap, only showing separation on the graph by their different lengths (Fig. R34). The range they occupy begins at just under 1.0 indicating that they are slightly taller than they are wide at that point, and ending their range at 1.8

(Fig. R34). The proximal shaft shapes for humans tend to be flatter mediolaterally than those of chimpanzees. Both Au. afarensis and GWM10/P1 have similar shape ratios of approximately 1.5. Their shapes at the proximal shaft are separated on the graph mainly by the longer length of GWM10/P1. Overall, these results indicate that most hominoids, with the exception of gorillas, have similar shapes at this point along the proximal phalanx. Importantly, at this point along the proximal phalanx, GWM10/P1 is situated between chimpanzees and humans in terms of shape and length.

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Figure R34. Proximal shaft shape comparisons. See Fig. M1 A,B.

The last sets of breadth and height measurements were taken at the point midway between the midshaft and head of the phalanx to yield the distal shaft shape ratio (Distal shaft width (DSW)/ Distal shaft height (DSH)) (Figs. R35 and M1A,B). The distal shaft shape ratios of humans, gorillas, and chimpanzees tend to group separately. The gorillas range between ~1.3 – ~1.7, and the chimpanzee specimens lie between ~1.6 – ~2.4, indicating that the proximal phalanges 4 of chimpanzees are flatter mediolaterally at this point than those of gorillas (Fig. R35). The low end of the distal shaft shape ratios for humans is ~1.1, and the high end is ~1.4, which is approximately where the chimpanzees begin. The Au. afarensis specimens and GWM10/P1 fall within the range of the human distal shaft shape ratios, which are square like (Fig. R35). In summary, the distal shaft shape ratios draw a distinction between the great apes and humans, Au. afarensis, and

GWM10/P1. Interestingly, linear regression analysis of all of the distal shaft shape ratios

94 plotted against length indicate that short proximal phalanges tend to be more square-like; in contrast, as the bones get longer, they get flatter at this point along the shaft (Fig.

R36).

Figure R35. Distal Shaft Shape ratio comparisons. See Fig. M1 A, B.

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Figure R36. Linear regression performed on all distal shaft shape ratios demonstrate a correlation between distal shaft shapes and length. All species distal shaft shape ratios from Fig. R35 are plotted. Plot demonstrates that shorter bones have a more square-like shape ratio and longer bones tend to be flatter at distal shaft point. R squared value = 0.59, indicating a good fit to the line. Y=0.03178*X-0.1025

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Phalangeal curvature

Phalangeal curvature is a characteristic of great interest because it is thought to reveal a primate’s manual and locomotor patterns (Tuttle, 1969; Marzke, 1971; Susman, 1979;

Hunt, 1991; Stern et al., 1995; Richmond, 2007). We determined the phalangeal curvature for humans, gorillas, chimpanzees, Au. afarensis (Hadar), and . To determine phalangeal curvature, digital images of the profiles of each proximal phalanx were captured (Fig. R37). These photos were analyzed with ImageJ to provide values for the calculation of the included angle. Because GWM10/P1 is the 4th proximal phalanx of the left hand, we limited our comparative sample to the 4th proximal phalanges of humans, gorillas, chimpanzees, and Au. afarensis. By our method of determining included angle, the median values are chimpanzees > Au. afarensis > gorillas > humans (Table R1). The included angle value for GWM10/P1 is 50 (Fig. R38).

97

Figure R37. Representative phalangeal curvature analyses performed on digital photos with ImageJ. 4th proximal phalanges of gorilla, chimpanzee, GWM10/P1, and human, from top to bottom. Scale bar = 10 mm.

98

The included angle values obtained for gorillas are larger than the values obtained for humans and this might, at least partly, be explained by a unique feature of the distal end of the gorilla phalanges. Gorilla phalanges appear ‘bent’ in the palmar orientation of the distal trochlea of the phalanx instead of curved throughout the entirety of the phalanx.

Our measurement and calculations incorporate this “bent” feature in the curvature measurements; this is because there is a palmar orientation of the distal trochlea, which yields a low point for the middle of the articular surface length. This point serves as one of the three points that make up a line segment to determine curvature (Fig. 37).

Importantly, the GWM10/P1 included angle value is distinct from humans, in that it is higher, demonstrating that it is more curved. The included angle value for GWM10/P1 is more similar to those of chimpanzee ray 4 and the Hadar specimens. This GWM10/P1 included angle value, thus, supports the hypothesis that the cognate species locomoted arboreally. This hypothesis is also supported by other postcranial anatomical features (see discussion).

99

Figure R38. Curvature of the 4th proximal phalanges from fossil GWM10/P1 and those of extant and extinct hominoids. Graph of included angle values. GWM10/P1 included angle value is more similar to those of gorillas and chimpanzees than humans. Each box represents the 25th and 75th percentile, with whiskers that denote the range. The centerline and + symbol are the median and mean, respectively. Each blue dot is an individual included angle value. Sample size for humans, chimpanzees and gorillas were 20 individuals each.

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Discussion

The morphology of proximal phalanges

A major effort of this thesis is to determine the key aspects of the proximal phalanges of humans, gorillas, and chimpanzees that allow discernment of these bones, and to use this comparative sample to establish similarities to GWM10/P1, a proximal phalanx of Ar. ramidus. This integrated description of characteristics considers morphology, length versus articular base surface area along a phalanx, phalangeal curvature, and longitudinal torsion. This information was used to address goals 1 and 2.

Torsion as a tool for manual proximal phalanx ray assignment

New to the field, is the use of longitudinal torsion in identifying from which ray a proximal phalanx comes. It has been shown that torsion in the distal manual and pedal phalanges relates to bipedality (Day & Napier, 1966; Almecija et al., 2010). In gorillas and chimpanzees, the torsion is zero for the distal phalanges, but in humans torsion is substantial and correlates with bipedality (Day & Napier, 1966; Almecija et al., 2010).

We found a use for torsion as a tool for assigning a manual proximal phalanx to a ray.

We observed that proximal phalanges exhibit torsion along the longitudinal axis of the phalanx. The torsion appears to begin near the midshaft and continue in a distal direction causing the orientation of the distal end to change. In order to determine how torsion may assist in the assignment of a ray to any manual proximal phalanx from an extant or extinct specimen, we sought to identify a pattern for this morphology. Proximal

101 phalanges 2 and 3 have positive or medial torsion because they twist to face the pollex

(Figs. R28, R29). One possible reason for this torsion direction in these two phalanges is it may enable better grip in combination with the pollex. Proximal phalanges 4 and 5 exhibit negative or lateral torsion: they twist to face away from the pollex (Figs. R28,

R29). For the 2nd, 3rd and 4th proximal phalanges, gorillas had the greatest torsion. For the

5th proximal phalanx, chimpanzees had the greatest amount of torsion (Table R4). There is variation in the torsion values within a phalanx type in the same species, indicating that this trait may not be under strong selective pressure. Intraspecific variation in this trait could be due to bone remodeling from experience during the animal’s life. Nonetheless, the torsional patterns are robust enough to serve as markers to assigning a ray to a phalanx when used in conjunction with other bone characters. As shown below, the torsion feature was used to assign GWM10/P1 to a ray.

Morphological and metrical descriptions of manual proximal phalanges of humans, gorillas, and chimpanzees

Proximal phalanx 1 in gorillas and chimpanzees is a uniquely small phalanx with a rounded articular surface. In humans, proximal phalanx 1 bears a large radial side tubercle, an insertion point for the abductor pollicis brevis muscle. Gorillas and chimpanzees do not have this tubercle, which is informative about the functionality and use of the pollex in the African apes. A long and robust pollex is essential for the dexterous manipulation that the human hand is capable of (Marzke, 1997; Susman, 1998;

Almecija et al., 2010).

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Proximal phalanx 2 is generally the third longest phalanx in humans, gorillas, and chimpanzees (Table R2). Morphologically, proximal phalanx 2 is asymmetric because of the large radial-side tubercle for the attachment of the first interosseous muscle that is apparent in humans, gorillas, and chimpanzees (Figs. R8 - R10). For humans, gorillas, and chimpanzees the torsion is usually positive, specifically, in gorillas, proximal phalanx

2 is the most torqued (Figs. R28, R29; Table R4).

Proximal phalanx 3 is the longest phalanx of all the five phalanges in the species studied

(Table R2). This phalanx is unique in its symmetry along the longitudinal axis at the base

(Fig. R14). This symmetry is present in humans, gorillas, and chimpanzees. Humans and chimpanzees have no apparent flexor sheath ridges (Fig. R14) which is in contrast to gorillas that have deep concavity of the palmar side of the shaft due to the large and projecting flexor sheath ridges. For all species, proximal phalanx 3 usually has positive torsion or is neutral (Figs. R28, R29).

Proximal phalanx 4 is usually the second longest phalanx in the hands of humans, gorillas, and chimpanzees (Table R2). The dorsal interosseous muscle insertion points are a useful landmark in identification between proximal phalanges 2 and 4. The tubercle on proximal phalanx 2 (insertion point for dorsal interosseous muscle 1) is larger than the tubercle on proximal phalanx 4 (insertion point for dorsal interosseous muscle 4). When viewing the proximal end of these two phalanges, the larger tubercle on proximal phalanx

2 gives the perimeter outline a mediolaterally oval shape, whereas the perimeter outline for proximal phalanx 4 does not have that shape (Figs. R8, R9, R10). The torsion values

103 for proximal phalanx 4 are usually negative for gorillas and chimpanzees, but the median value for the human bone is 0 (Figs. R28, R29).

In all species, proximal phalanx 5 has asymmetry between the ulnar and radial sides due to the larger ulnar tubercle (Fig. R15). In addition, proximal phalanx 5 has pronounced negative torsion in chimpanzees and gorillas. For chimpanzees and gorillas, this is the most torqued phalanx. In humans, the median torsion value is 0° (Figs. R28, R29).

GWM10/P1 hand side and ray

The proximal phalanx GWM10/P1 was examined for how well it aligned with these aforementioned morphological traits in order to assign ray and hand side Despite the fossil sustaining postmortem damage to the radial side the identifying morphology is nevertheless present (Fig. R18). When viewing the proximal articular side, it is evident that the perimeter outline of the base is more square-like and not mediolaterally oval

(Fig. R19). Were the base to appear more oval, that would signify the presence of a radial tubercle for the insertion of the first dorsal interosseous muscle, which would identify the phalanx as a 2nd proximal phalanx. The proximal articular surface of GWM10/P1 is round and concave (Fig. R19), reminiscent of the round articular surfaces of the chimpanzee’s phalanges (Fig. 28 b1). The basal tubercles of the Gona specimen are moderately pronounced, most similar to the basal tubercle shapes of chimpanzees (Fig. R28).

When viewing the distal condyles of GWM10/P1 from the palmar aspect, the radial condyle is slightly larger. There is a distinct pattern that emerges in the morphology of condyles and basal tubercles. In all proximal phalanges, when the radial distal condyle protrudes, the ulnar basal tubercle is also enlarged. Conversely, if the ulnar distal condyle

104 protrudes, the radial tubercle is enlarged. GWM10/P1 exhibits negative torsion (Figs.

R22, R29; see axial torsion sections), which supports the notion that this fossil is a proximal phalanx 4 of the left hand.

GWM10/P1 is long and curved

Knowledge of the hand side and ray position of GWM10/P1 enabled comparisons with other species’ 4th proximal phalanges to infer function of GWM10/P1 and the associated animal’s behavior. Five specific comparisons of shapes (shape ratios) at different points along the phalanx (base shape, midshaft shape, head shape, proximal shaft shape, and distal shaft shape) yielded morphological similarities or dissimilarities between

GWM10/P1 and those of humans, gorillas, chimpanzees, and Au. afarensis (Figs. R31 –

R35). The shape ratios were most informative when examined in conjunction with the total length of each phalanx (Figs. R31 – R35). In plots of base shape, midshaft shape, head shape, and proximal shaft shape verses total length, GWM10/P1 falls at the lower end of the range of chimpanzees (Figs. R31 – R34). In fact, the only shape plot, where

GWM10/P1 distinguishes itself from chimpanzees is distal shaft shape. Here, the Gona phalanx is undamaged, and so it serves as a reliable feature to identify this species (Fig.

R35).

The distribution of Au. afarensis in shape plots contrasts starkly with GWM10/P1, as the former groups with humans in all graphs (Figs. R31 – R35). Finger elongation is an adaptation for arboreal behaviors because it enables grasping of branches for quadrupedalism and below branch movement (Susman, 1979; Patel et al., 2009). Short

105 fingers relative to hand length or metacarpal length are seen as adaptations for terrestrial behaviors in primates (Susman, 1979; Patel et al., 2009). Finger bone lengths when normalized to body size are the most effective means to compare lengths between different species (Lovejoy et al., 2009b). To estimate body mass from the manual proximal phalanx, we used a novel method, PAS area. Generally, our methods yielded relative body mass estimates for gorilla males > gorilla females > chimpanzees > humans

(Fig. R22 – R24). Human and chimpanzee estimates are very similar but reversed compared to actual published body masses: mean body masses of gorillas, chimpanzees, and humans are 113.9 kg, 46.0 kg and 57.0 kg, respectively (Smith & Jungers, 1997;

Grabowski et al., 2018). Interestingly, a similar order (gorillas > chimpanzees > humans) of body masses is seen when maximum midshaft dorsopalmar length of manual proximal phalanges or mediolateral breadth of humeral distal articular surface are used as proxies for body mass, lending strength to our method (Rein, 2011). In further support of this

PAS area method, we found that GWM10/P1 and Au. afarensis have similar areas, thus implying comparable body sizes. This finding agrees with earlier estimates of the Ar. ramidus skeleton with a body mass of ~50 kg, a mass that is similar to the heaviest Au. afarensis individuals (Reno & Lovejoy, 2015).

Since relative PAS body mass estimates and actual measurements yield similar relative body mass orders (Rein, 2011), we used the PAS measurements in normalization of phalangeal lengths. PAS areas were thought to be a proxy for body mass because joints bear the weight of an animal’s body (Perry et al., 2018). GWM10/P1 is relatively the longest and groups with the manual proximal phalanges of chimpanzees (Fig. R26). In

106 contrast, Au. afarensis 4th proximal phalanges are among the shortest and group with the proximal phalanges of humans and gorillas.

Finally, we examined the level of curvature of GWM10/P1. Phalangeal curvature is one parameter that indicates if the animal may have been arboreal (Stern et al., 1995;

Almecija et al., 2009; Rein, 2011). GWM10/P1 is highly curved, indicating arboreal behavior and a hand that was used for grasping branches for locomotion. The hindlimbs and pelvis of Ar. ramidus supports that hypothesis (Lovejoy et al., 2009), as does the long length of GWM10/P1. There has been debate as to whether Au. afarensis was arboreal, since the manual proximal phalanges of that hominin were also curved (Fig. R38) (Stern

& Susman, 1983). Examination of the lower limbs of Au. afarensis however reveal that

Au. afarensis was a committed biped (Johanson et al., 1982; Tague & Lovejoy, 1986;

Ward et al., 2011). In summary, these studies describe GWM10/P1 as being a long, curved 4th proximal phalanx.

Ar. ramidus had a hand similar to a Miocene ape, a pelvis for arboreality and bipedal terrestriality, and a phalanx suited for arboreality.

Ardipithecus ramidus was proficient at locomotion both as a terrestrial biped and through the trees with arboreal capabilities (Lovejoy et al., 2009b). The hand of Ar. ramidus indicates that the human lineage did not evolve from a knuckle-walking ancestor. When comparing the hand and wrist of Ar. ramidus to those of the chimpanzees and gorillas,

Ar. ramidus lacks the specializations that the African apes possess in order to support their large body size while they locomote (Lovejoy et al., 2009b; Simpson et al., 2018).

107

Some of these derived specializations that are seen in the anatomy of chimpanzees and gorillas include stiffened wrist and metacarpophalangeal joints (Simpson et al., 2018), and importantly those highly derived adaptations are not present in Ar. ramidus.

The GWM10/P1 phalanx of Gona is longer (50.13 mm) than the 4th proximal phalanges of Ar. ramidus (47.1 and 47.8 mm) of Aramis (Lovejoy et al., 2009b). When corrected for body mass (using the geometric mean of several dimensions of the talus and capitate) the order of lengths of Ar. ramidus of Aramis is chimpanzees > Ar. ramidus of Aramis >

Proconsul = gorillas > humans ((Lovejoy et al., 2009b); This is different from the relative length order of the 4th proximal phalanges when corrected for body mass of the

GWM10/P1 phalanx Ar. ramidus from Gona using proximal articular surface area square root (Fig. R26): GWM10/P1 > chimpanzees > male gorillas > female gorillas > humans

> Au afarensis of Hadar. With a relative length of GWM10/P1 that is similar to that of chimpanzees (very long) both greater than Ar. ramidus of Aramis, our finding further strengthens the hypothesis, by Lovejoy et al. (Lovejoy et al., 2009b), that Ar. ramidus was “arboreally capable”, perhaps even more so than previously thought, as long phalanges are indicators of arboreality. This hypothesis is further supported by our data, which shows that GWM10/P1 is shaped most like a chimpanzee phalanx (4/5 shape ratios

(Figs. R32 - R36), with similar degrees of curvature (Fig. R39). It is important to emphasize that we are not suggesting that this animal locomoted or had hands like chimpanzees, but it did have at least one phalanx similar to this African ape. In fact, it should be noted that our comparison of phalanges in humans, gorillas, chimpanzees, Au.

108 afarensis, and Ar. ramidus was not able to detect a character indicative of knuckle walking.

The anatomy of the pelvis of Ar. ramidus shows a unique set of adaptations that allow the animal to be both bipedal and arboreal (Lovejoy et al., 2009d). The upper pelvis exhibits a morphology with repositioned gluteal muscles, which allow the animal to balance on one foot while walking. The lower pelvis has morphology that aids in climbing. In addition, Ar. ramidus had a foot anatomy with a fully opposable hallux for grasping branches while navigating in trees. We reinforce the notion that this animal had a mosaic anatomical repertoire by demonstrating that Ar. ramidus had long, curved phalanges to aid in arboreal locomotion.

The relation of phalangeal length and the transition between arboreality and bipedality

The anatomy of the hand can yield information about evolutionary relationships.

GWM10/P1 is no exception. Ar. ramidus (4.8 - 4.3 Ma) is considered a predecessor to

Au. afarensis (3.6 Ma) (Lovejoy et al., 2009d; Kivell et al., 2016). Au. anamensis was a temporal (3.9 – 4.2 Ma) and morphological intermediate between Ar. ramidus and Au. afarensis (White et al, 2006; Leakey et al., 1995; Leakey et al., 1998) however it must be noted that the timespan between Ar. ramidus and Au. anamensis is relatively short, approximately 100,000 years. GWM10/P1 is the 4th phalanx of the left hand of Ar. ramidus, and its length (Fig. R26) reflects arboreality. The Ar. ramidus pelvis anatomy infers locomotion by arboreality and terrestrial bipedality (Lovejoy et al., 2009d). In

109 contrast, Au. afarensis lower limbs and pelvis enabled upright walking and running; however, these anatomies were no longer arboreally capable (Latimer & Lovejoy, 1989,

1990b, a; Lovejoy et al., 2009c; Ward et al., 2011; White et al., 2015). We show by our methods that Au. afarensis has shorter phalanges relative to body size, supporting the established hypothesis that this animal was habitually bipedal (Fig. R26). Nevertheless, this animal’s phalanx maintains significant curvature (Fig R38), but it was not arboreal.

The curvature trait in this case could be a feature trait that is under little or no directional adaptive pressure, and thus did not vanish with the elimination of arboreal selective pressures. This argument implies that finger length is under genetic, not ontogenetic, control (Indjeian et al., 2016). Moreover, dental remains of Au. anamensis show primitive characters, such as a large canine (White et al., 2006), which are more archaic than those of Au. afarensis. In contrast, an Au. anamensis femur that was recovered from

Ethiopia (White et al., 2006) and a tibia that was recovered from Kenya (Leakey et al.,

1995) reveal adaptations for bipedality, similar to those found in Au. afarensis. This bipedal animal’s size and phalangeal length is similar to Au. afarensis, indicating that the transition from long to short phalanges happened before Au. anamensis.

The progression of the shortening of phalangeal lengths in conjunction with changes in the hips and lower limbs reflects a shift from arboreality to bipedality before the appearance of Au. anamensis (4.4 - 4.2 Ma). It indicates a directional vector to this evolutionary change (Latimer, 1991a). There seems to have been a de-coupling of phalangeal length and phalangeal curvature, which are universally linked traits observed in modern arboreal primates. It would appear that phalangeal elongation fell away from

110 the suite of manual characters at around the time of Au. afarensis, but curvature persisted until well into the appearance of the Homo lineage, when curvature was no longer present

(Dominguez-Rodrigo et al., 2015).

111

Appendix

Table Appendix 1: Gorilla specimen information. Specimen # Genus Species Sex Collection site HTB1709 Gorilla gorilla M Cameroon HTB 1409 Gorilla gorilla M Cameroon HTB 1431 Gorilla gorilla M No data HTB 1430 Gorilla gorilla M No data HTB 1729 Gorilla gorilla M Cameroon HTB 1730 Gorilla gorilla M Cameroon HTB 1732 Gorilla gorilla M Cameroon HTB 1754 Gorilla gorilla M Cameroon HTB 1857 Gorilla gorilla M Cameroon HTB 1859 Gorilla gorilla M Cameroon HTB 1710 Gorilla gorilla F Cameroon HTB 1725 Gorilla gorilla F Cameroon HTB 1752 Gorilla gorilla F Cameroon HTB 1798 Gorilla gorilla F Cameroon HTB 1806 Gorilla gorilla F Cameroon HTB 1794 Gorilla gorilla F Cameroon HTB 1846 Gorilla gorilla F Cameroon HTB 1764 Gorilla gorilla F Cameroon HTB 1851 Gorilla gorilla F Cameroon HTB 1801 Gorilla gorilla F Cameroon

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Table Appendix 2: Chimpanzee specimen information. Specimen # Genus Species Sex Collection site HTB 1745 Pan troglodytes M Cameroon HTB 2027 Pan troglodytes M Cameroon HTB 1739 Pan troglodytes M Cameroon HTB 1708 Pan troglodytes M No data HTB 1056 Pan troglodytes M Cameroon

HTB 1718 Pan troglodytes M Cameroon HTB 1726 Pan troglodytes M Cameroon HTB 2747 Pan troglodytes M French Cameroon HTB 1882 Pan troglodytes M Cameroon HTB 1758 Pan troglodytes M Cameroon HTB 1744 Pan troglodytes F Cameroon HTB 1434 Pan troglodytes F No Data HTB 1748 Pan troglodytes F Cameroon HTB 1755 Pan troglodytes F Cameroon HTB 1713 Pan troglodytes F Cameroon HTB 1723 Pan troglodytes F Cameroon HTB 1721 Pan troglodytes F Cameroon HTB 1720 Pan troglodytes F Cameroon HTB 1749 Pan troglodytes F Cameroon HTB 2730 Pan troglodytes F No data

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Table Appendix 3: Human specimen information. Specimen # Genus Species Sex Collection site HTH 1182 Homo sapiens Male European HTH 1185 Homo sapiens Male African HTH 1223 Homo sapiens Male European HTH 1189 Homo sapiens Male African HTH 1202 Homo sapiens Male European HTH 464 Homo sapiens Male European HTH 467 Homo sapiens Male European HTH 486 Homo sapiens Male African HTH 487 Homo sapiens Male European HTH 489 Homo sapiens Male European HTH 2561 Homo sapiens Female African HTH 2478 Homo sapiens Female Asian HTH 2515 Homo sapiens Female European HTH 2516 Homo sapiens Female African HTH 2494 Homo sapiens Female African HTH 442 Homo sapiens Female African HTH 461 Homo sapiens Female African HTH 466 Homo sapiens Female European HTH 529 Homo sapiens Female African HTH 530 Homo sapiens Female African

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Table Appendix 4: Fossil specimen information. Specimen # Genus Species Sex Collection site Hadar, AL333-62 Australopithecus afarensis Unknown Ethiopia Hadar, AL333-19 Australopithecus afarensis Unknown Ethiopia Aramis, 6/500-022 Ardipithecus ramidus Unknown Ethiopia Aramis, 6/500-069 Ardipithecus ramidus Unknown Ethiopia

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