Browsing by Subject "Physical anthropology"

Studies of skeletal variation form the basis of our understanding of our species’ history and diversity. This most commonly takes the form of comparative, between- species studies aimed at reconstructing phylogenetic relationships. However, studies of within-species variation can provide insights into relatedness at smaller scales, which can shed light on important microevolutionary processes and be used to identify closely related individuals in the absence of DNA. This dissertation assesses the relationship between genetic and skeletal variation within groups of related and unrelated Homo sapiens and Pan troglodytes, with the aim of better understanding the population sampled by the seemingly homogenous Homo naledi assemblage from the Dinaledi Chamber in Rising Star Cave, South Africa. The hypotheses tested were: 1) closely related individuals exhibit less skeletal variation compared to unrelated individuals, and 2) the Dinaledi assemblage exhibits less morphological variation than H. sapiens and P. troglodytes at the species level, more closely resembling a single population.

Skeletal variation within a subset of H. sapiens from the crypt of Christ Church in Spitalfields, London (17-19th centuries A.D) with documented genealogies and the Gombe population of P. t. schweinfurthii was compared to species-wide baselines and the H. naledi assemblage. The data consisted of 3D models of 556 postcranial elements (first metacarpal (Mc1), proximal femur, talus, calcaneus, and navicular) from 187 individuals that were generated from surface scanners or downloaded from MorphoSource.

This dissertation employed a relatively new 3D geometric morphometric workflow that captures the entire shape of an element through the use of an automated landmarking program and feature-aware registration process. Two hundred pseudolandmarks were automatically and optimally placed on each element. Following alignment, multiple univariate and multivariate statistical analyses were used to quantify shape variation within and between the three species, including distributions of Euclidean distances, Procrustes distances to the mean shapes, Principal Components Analyses (PCA), Between-Group PCA, and Discriminant Function Analyses. The coefficient of relationship was used to represent genetic distance between known genetic relatives within modern humans.

The results of the within-species analyses of skeletal variation support Hypothesis 1 in both modern humans and chimpanzees, though the signal of relatedness is differentially expressed within and across elements. In modern humans, the calcaneus can be used to distinguish known close relatives from distantly related and unrelated individuals. The navicular and femur were also found to be relatively good indicators of relatedness. Within chimpanzees, the talus is the most effective at distinguishing the Gombe population from the species-wide chimpanzee sample, followed by the calcaneus and femur. Within H. naledi, the talus varied the least while the navicular varied the most, though the high levels of variation found in the navicular and Mc1 are likely due to the state of preservation of these elements. The results of the interspecies analyses are more ambiguous. When considering the best preserved elements, the H. naledi talus varies the least within the three species, while the femur varies more than those of either H. sapiens or P. troglodytes at the species level. Hypothesis 2 is thus supported for the talus while rejected in the femur, suggesting that it cannot be rejected as a whole and that the patterns of homogeneity previously observed within H. naledi are more nuanced than previously recognized.

Primates and many other animals that move in an arboreal environment often cling, sometimes for long periods, on vertical supports. Primates, however, face a special challenge in that almost all primates bear nails on the tips of their digits rather than claws. Squirrels and other arboreal animals possess claws and/or adhesive pads on their digits in order to hold their weight on vertical substrates. Assuming the ancestral primate was arboreal and lost claws prior to the radiation of primates this paradox has important implications and raises a significant question about living primates and early primate evolution: how can primates maintain vertical postures without claws and how did early primates meet this challenge? Primate vertically clinging and grasping postures (VCG) have been studied in the wild and theoretical models of VCG postures have been described. This dissertation builds on this work, by studying the biomechanics of VCG postures in primates. Based on mechanical models, it was hypothesized VCG posture in primates will vary in three ways.

Hypothesis 1: Species with different morphological features associated with different locomotor modes will vertically cling and grasp in different ways.

Hypothesis 2: As substrate size increases, primates will place their arms to the side of the support and adjust posture and muscle recruitment in order to maintain a necessary tangential to normal force ratio to resist gravity.

Hypothesis 3: On substrates of the same relative size, larger animals should be less effective at maintaining VCG postures due to scaling relationships between muscle strength and body mass.

The sample consisted of multiple individuals from eight strepsirrhine species at the Duke Lemur Center. The sample varied in locomotor mode--habitual vertical clinging and leaping (VCL) compared to less specialized arboreal quadrupeds--and body mass--100 to 4,000 grams. Subjects were videorecorded while holding VCG postures on substrates of increasing size. Substrate preference data were calculated based on frequency and duration of VCG postures on each substrate. Qualitative kinematic data were recorded for a maximum of thirty trials per individual, per substrate. Angular data were calculated for forelimbs and hindlimbs from these videos for ten trials per individual per substrate. In addition, kinetic data from an imbedded force transducer were collected for two species that vary in locomotor mode, but not body mass.

There are several significant and relevant results from this study that address both primate functional anatomy and locomotor evolution. Hypothesis one was supported by hand and hindlimb joint postures, shown to be highly sensitive to locomotor mode. VCL primates exhibited deeply flexed limbs and more hand grasping (wrapping around the substrate) versus parallel hand postures and use of bowed finger postures compared to less specialized primates. Kinetically, species were shown to bear the majority of their weight in their hindlimbs relative to their forelimbs. The forelimb joints and foot showed little variation by habitual locomotor mode. Hypothesis two found support in that species tend to prefer smaller substrates, clinging less frequently for shorter durations as substrate size increases. Hand posture changed as size increased, as primates (except for the slow lorises) in this study grasped with their pollex on smaller substrates, but the pollex disengaged in grasping on larger substrates. Hypothesis three was not supported; body mass did not influence VCG postures.

Taken together, the finding that the forelimb held a wide range of postures on each substrate size for all species and played a limited role in weight-bearing suggests the forelimb free to move (to adjust posture and or forage). The hindlimb plays a more specific role in weight-bearing and is more sensitive to variations in primate anatomy. Additionally, these findings lead to hypotheses concerning the relatively short pollexes of primates, and that the ancestral primate was smaller than 100g and preferred small substrates as found in a fine-branch niche.

To evaluate alternative hypotheses for the role of mass and muscle-induced forces in joint construction, the allometric scaling relationships of the articular facets of the talus were estimated with phylogenetic regressions. Many articular surfaces scale with significant positive allometry, suggesting that mass-induced forces are an important influence for the bony architecture of synovial joints.

Using a large sample of primates and their nearest living relatives, body mass prediction equations were generated from the articular facet areas of the talus and calcaneus. Those facets that scaled with positive allometry were both accurate and precise. Compared to previously published prediction equations, the novel equations developed for this study were substantially more reliable.

Several methodological debates for body mass prediction were also evaluated. Prediction equations had their highest correlations when species with greater than a 20% difference between sexes are represented by both males and females. Using dental measurements from cercopithecoids housed at the National Museum of Natural History, predictive accuracy was maximized when body mass was predicted using a mean value estimated from a robust sample. Even when only a single individual was represented, tests of predictive accuracy using primates with associated body masses from several localities (Hacienda La Pacifica, Costa Rica; Gombe Stream National Park, Tanzania; Amboseli Reserve, Kenya; and the Duke Lemur Center) demonstrated that prediction equations provide more accurate predictions of species mean values than individual-specific values.

The importance of longitudinal change in body mass was evaluated by comparing coefficients of variation for individual and mean body mass of the populations at La Pacifica, Gombe, and the Duke Lemur Center. Individual coefficients of variation were significantly greater than the population coefficients of variation, which suggests that mean body masses are more stable “targets” of prediction.

Finally, the novel prediction equations were applied to a sample of sympatric primates with associated dental and postcranial elements from the middle Eocene of Wyoming, including Notharctus tenebrosus, Smilodectes gracilis, Omomys carteri, and Hemiacodon gracilis. New body mass predictions suggest two pairs of similarly sized primates: N. tenebrosus and S. gracilis (~2500g), and O. carteri and H. gracilis (~400g). Thus, niche partitioning between closely related taxa was probably achieved through differences in diets, rather than differences in body mass.

In chimpanzees, most females disperse from the community in which they were born to reproduce in a new community, thereby eliminating the risk of inbreeding with close kin. However, across sites, some females breed in their natal community, raising questions about the flexibility of dispersal, the costs and benefits of different strategies and the mitigation of costs associated with dispersal and integration. In this dissertation I address these questions by combining long-term behavioral data and recent field observations on maturing and young adult females in Gombe National Park with an experimental manipulation of relationship formation in captive apes in the Congo.

To assess the risk of inbreeding for females who do and do not disperse, 129 chimpanzees were genotyped and relatedness between each dyad was calculated. Natal females were more closely related to adult community males than were immigrant females. By examining the parentage of 58 surviving offspring, I found that natal females were not more related to the sires of their offspring than were immigrant females, despite three instances of close inbreeding. The sires of all offspring were less related to the mothers than non-sires regardless of the mother’s residence status. These results suggest that chimpanzees are capable of detecting relatedness and that, even when remaining natal, females can largely avoid, though not eliminate, inbreeding.

Next, I examined whether dispersal was associated with energetic, social, physiological and/or reproductive costs by comparing immigrant (n=10) and natal (n=9) females of similar age using 2358 hours of observational data. Natal and immigrant females did not differ in any energetic metric. Immigrant females received aggression from resident females more frequently than natal females. Immigrants spent less time in social grooming and more time self-grooming than natal females. Immigrant females primarily associated with resident males, had more social partners and lacked close social allies. There was no difference in levels of fecal glucocorticoid metabolites in immigrant and natal females. Immigrant females gave birth 2.5 years later than natal females, though the survival of their first offspring did not differ. These results indicate that immigrant females in Gombe National Park do not face energetic deficits upon transfer, but they do enter a hostile social environment and have a delayed first birth.

Next, I examined whether chimpanzees use condition- and phenotype-dependent cues in making dispersal decisions. I examined the effect of social and environmental conditions present at the time females of known age matured (n=25) on the females’ dispersal decisions. Females were more likely to disperse if they had more male maternal relatives and thus, a high risk of inbreeding. Females with a high ranking mother and multiple maternal female kin tended to disperse less frequently, suggesting that a strong female kin network provides benefits to the maturing daughter. Females were also somewhat less likely to disperse when fewer unrelated males were present in the group. Habitat quality and intrasexual competition did not affect dispersal decisions. Using a larger sample of 62 females observed as adults in Gombe, I also detected an effect of phenotypic differences in personality on the female’s dispersal decisions; extraverted, agreeable and open females were less likely to disperse.

Natural observations show that apes use grooming and play as social currency, but no experimental manipulations have been carried out to measure the effects of these behaviors on relationship formation, an essential component of integration. Thirty chimpanzees and 25 bonobos were given a choice between an unfamiliar human who had recently groomed or played with them over one who did not. Both species showed a preference for the human that had interacted with them, though the effect was driven by males. These results support the idea that grooming and play act as social currency in great apes that can rapidly shape social relationships between unfamiliar individuals. Further investigation is needed to elucidate the use of social currency in female apes.

I conclude that dispersal in female chimpanzees is flexible and the balance of costs and benefits varies for each individual. Females likely take into account social cues present at maturity and their own phenotype in choosing a settlement path and are especially sensitive to the presence of maternal male kin. The primary cost associated with philopatry is inbreeding risk and the primary cost associated with dispersal is delay in the age at first birth, presumably resulting from intense social competition. Finally, apes may strategically make use of affiliative behavior in pursuing particular relationships, something that should be useful in the integration process.

The study of culture in wild animals has received wide theoretical and empirical attention, providing preliminary evidence of at least rudimentary culture across a broad range of taxa. However, the majority of previous studies of animal cultural behavior have focused on demonstrating the existence of behavioral variants across study sites, armed only with an assumption that ecological and genetic alternatives are unlikely to sufficiently explain observed geographic variation in behavior. Moreover, previous studies have reported the presence of behavioral variation at the level of the population, without first confirming the presence of such variation in individual repertoires, which could create artificial patterns within or between populations.

Using more rigorous methods than previous studies, I examined rarely tested alternatives to field-based claims of cultural repertoire variation based on ecological heterogeneity and genetic variation. This dissertation relies on a natural experiment to compare two wild orangutan populations. Sungai Lading, a previously unstudied, high-density population of wild Pongo pygmaeus wurmbii, was compared to Tuanan, a P.p.wurmbii population separated from Sungai Lading by an impassable river barrier, but ranging in a broadly similar habitat. Preliminary genetics results indicate that at least some individuals from both sites cluster in the same mitochondrial subclade and that low levels of gene flow must have occurred between the two sites. Even after applying rigorous controls for variation in sampling intensity for individual orangutans, several differences in innovative behaviors exhibited at each site were identified, many of which occurred in the nesting context.

The orangutan is a model taxon for such an investigation, because wild populations exhibit a wide range of sociality, which has been linked to opportunities for social learning. Comparisons between the Tuanan and Sungai Lading populations indicated that cultural variants observed at only one site clustered significantly by population, although only dietary differences were unique at both sites. Orangutans at Sungai Lading maintain significantly lower rates of female-female association and lower individual repertoire sizes of putative cultural variants, a result that is consistent with the possibility that the orangutans of Sungai Lading may have reduced opportunities for social learning as a result of severe population compression, which could constrain opportunities for cultural transmission of key innovative behaviors.

From a broader perspective, the patterns revealed in this study strongly suggest that the last common ancestor of Homo and Pongo shared culturally modified behavior. They further suggest that the extent of cumulative cultural behavior in humans may surpass that of orangutans as a result of lost opportunities for social transmission, owing to varying degrees of limited association among group members.

Fossil taxa are crucial to studies of brain evolution, as they allow us to identify evolutionary trends in relative brain size and brain shape that may not otherwise be identifiable in comparative studies using only extant taxa, owing to multiple events of parallel encephalization among primate clades. This thesis combines indirect and direct approaches to understanding primate evolution, by evaluating variation in the endocranial morphology of extant primates and their fossil representatives. I use a comparative approach to examine the relationships between interspecific adult endocranial volume and shape, and brain evolution and cranial form among extant primate clades and their fossil representatives. The associations are evaluated via phylogenetically informed statistics perfomed on volumetric measurements and three-dimensional geometric morphometric analyses of virtual endocasts constructed from micro-CT scans of primate crania. Fossil taxa included in these analyses are: 1) anthropoids Parapithecus, Aegyptopithecus (Early Oligocene, Egypt), Homunculus and Tremacebus (Early Miocene, Argentina), and 2) Eocene euprimates Adapis and Leptadapis (Eocene adapoids, France), and the Rooneyia (Eocene omomyoid, Texas).

The first part of this work (Chapter 2) explores variation in residual mass of brain components (taken from the literature) among primates, and evaluates the correlated evolution of encephalization and brain proportions with endocast shape, quantified via three-dimensional geometric morphometric techniques. Analyses reveal a broad range of variation in endocast shape among primates. Endocast shape is influenced by a complex array of factors, including phylogeny, body size, encephalization, and brain proportions (residual mass of brain components). The analysis supports previous research, which concludes that anthropoids and tarsiers (Haplorhini) share the enlargement of several key brain regions including the neocortex and visual systems, and a reduction of the olfactory system. Anthropoids further differ from strepsirrhines in endocranial features associated with encephalization--a more flexed brain base, an inferiorly deflected olfactory fossa--and those associated with brain proportions--a small olfactory fossa, and a more caudally extended cerebrum that extends posteriorly past the cerebellar poles. Tarsiers are unique in having a mediolaterally broad and rostro-caudally short endocast with an attenuated anterior and middle cranial fossae. This morphology is likely related to the extreme orbital enlargement in this taxon, which limits anterior expansion of the endocranium. Finally, despite the correlation between residual endocranial volume and endocast shape among modern primates, early anthropoid fossils demonstrate a disconnect between these factors in sharing key features of endocast shape with extant anthropoids at a relatively small brain size.

The second part of this thesis (Chapter 3) explores the relationship between craniofacial organization--cranial base angle, facial size, facial hafting--and encephalization via the lens of the Spatial Constraints and Facial Packing Hypotheses. These hypotheses predict that interspecific adult variation in encephalization correlates with endocranial shape such that a larger brain for a given body size will be more "globular" or spherical in shape. These hypotheses futher predict that basicranial angle covaries with encephalization and that the relative size of the endocranium and facial skeleton will have an antagonistic effect on basicranial angle and facial hafting. Results show that various measures of globularity have inconsistent and weak relationships to phylogeny, encephalization, and basicranial flexion, owing to a diversity of clade-specific scaling patterns between the maximum length, breadth, and width of the endocast. Among extant primates, there is weak but significant evidence to suggest that both facial size and encephalization influence variation in basicranial flexion. Considering the fossil specimens in isolation, their relative ranks in encephalization, basicranial flexion, and midline facial size and shape follow the pattern expected from the Spatial and Facial Packing Hypotheses outlined above; however, relative to modern species, the early fossil anthropoids have more flexed cranial bases and shorter facial skeletons at much smaller level of encephalization than seen in modern anthropoids.

Together, the extant data suggest a moderately conserved pattern of correlated evolution among endocranial size, endocranial shape, brain proportions, and craniofacial organization, which may explain differences in endocranial and facial shape between extant strepsirrhine and anthropoid primates; however, the fossil record for early anthropoid evolution demonstrates that a shift towards key anthropoid-like traits of the endocranium, basicranium, and facial skeleton were initiated early in anthropoid evolution, with subsequent encephalization occurring within and among members of this clade. Thus, these anthropoid cranial traits evolved in tandem with changes in the relative size of brain components, rather than absolute or relative brain size alone. Basicranial flexion, facial length and orientation are influenced by both: 1) shifts in endocranial shape associated with changes in brain proportion--accounting for the initiation of the anthropoid-like craniofacial plan early in the evolution of the clade--and 2) encephalization, which influenced subsequent morphological divergence among extant anthropoid groups.

Humans are more carnivorous than other hominoids. It has been hypothesized that, during the evolution of this increased carnivory, hominins transitioned through a scavenging niche made viable by certain carnivoran taxa (especially sabertooths) that may have lacked the morphology necessary to fully utilize all parts of carcasses (e.g., marrow), therefore leaving an open niche in the form of high-quality scavengable remains available for hominins. In this dissertation, I examine the postcanine dentition of modern carnivorans, using quantifications of occlusal radii of curvature and intercuspid notches, and study the correlation of this morphology with carcass-processing behavior. I use these correlations to deduce the carcass-processing capabilities of the Plio-Pleistocene carnivores of South Africa (a guild for which we have a good appreciation of taxonomic diversity, and that existed at an important time during the evolution of our lineage - possibly the time that we transitioned into that guild), and compare these results with those of previous studies that relied on more conventional morphological measures.

Both radius of curvature and intercuspid notch data do a good job of separating taxa by dietary category, revealing subtle patterns including possible differences in the carcass-processing abilities of fossil and modern members of some extant species. Other strong trends confirm that the "hunting-hyena," Chasmaporthetes, was probably a hypercarnivore, and not a durophage like its modern confamilial taxa. Somewhat surprisingly, results do not support the hypothesis that sabertooth felids were more hypercarnivorous than modern felids. Furthermore, though the sympatric hypercarnivorous taxa were more numerous, so to were the durophageous taxa, with one taxon, Pachycrocuta, probably exceeding the durophageous capabilities of modern durophages.

As such, this dissertation shows no evidence that members of the paleo-carnivore guild were capable of producing higher quality scavengable carcasses than are modern carnivorans, and thus, based on these analyses of fossil carnivorans, it does not appear that high-quality scavengable remains were more available in the Plio-Pleistocene than there are today. Therefore, though there is clear evidence from other sources that hominins did scavenge at least occasionally, this dissertation does not support the hypothesis that there was an open niche consisting of high-quality scavengable remains.

The pace of life history is highly variable across mammals, and several evolutionary biologists have theorized that the tempo of a species' life history is set by external factors. These factors, such as food availability and predation pressure, determine mortality rates. In turn, mortality rate determines the age at maturity. High mortality rate results in early age at maturity; individuals must grow and reproduce quickly because of the high risk of death. Conversely, a low mortality rate is allows individuals to prolong their growth period and reproduce slowly. This theory assumes that growth rates are constant across species, and thus body size is determined by mortality rates.

This project posits that the intrinsic characteristics of species set the pace of life history. Among anthropoids, there is a great deal of variation in growth rates and the pace of life history relative to body size. The hypotheses proposed by this project state that the degree of encephalization in a species determines the growth rates, the length of the growth period, and the adult lifespan. Growing a large brain is costly and requires a prolonged period of development. However, a large brain has the benefit of reducing mortality by facilitating cognitive strategies for food procurement and predator avoidance. This cost/benefit balance results in the pattern of life-history variation in which mortality rates are correlated with the length of the growth period. However, the causal arrows are reversed; instead of the mortality rate determining the age at maturity and consequently the size of the species, the relative brain size of the anthropoid determines the mortality rate and the age maturity.

These hypotheses were tested by determining the body and brain growth trajectories of thirteen anthropoids, and compiling life-history data from long-term studies of these species in the wild. Multi-variate analyses demonstrated that extensive brain growth, whether through prolonged duration or rapid growth rates, results in slow body-growth rates during the juvenile period and delayed age at maturity. In addition, encephalization results in longer adult lifespan. Therefore, this project demonstrated that intrinsic characteristics of anthropoid species determine the pace of their life histories.

Reconstructing locomotor patterns from fossils is crucial for understanding the origins of primates and important transitions in various primate clades. Recent studies suggest that the semicircular canals of the inner ear provide evidence about locomotion. The canals sense rotational head accelerations and drive reflexes essential for normal movement. Because bony aspects of canal morphology influence canal sensitivity, this system can be studied in osteologic specimens and fossils. Variation in canal morphology in living and, by inference, extinct primates has been attributed to interspecific differences in locomotor behavior. However, the manner in which movement selects for canal morphology is debated, alternative scenarios are plausible, and no relevant measurements are available documenting head movements in primates.

To refine proposed links between canal morphology and locomotor function, and to resolve conflicting functional interpretations, this study examines head rotations in lemurs and lorises exhibiting diverse locomotor behaviors. Three-dimensional kinematic analyses were used to characterize angular velocities of the head during locomotion. These data are used to test hypotheses concerning intraspecific, interspecific, and body-size dependent variation in head rotations. Cranial CT scans are used to model canal sensitivity to rotations in different directions. Observed patterns of head rotation are compared to predicted patterns of sensitivity to test hypotheses about the relationship between locomotor behavior and canal design.

Evaluation of existing locomotor inferences reveals that brain size exerts a significant effect on canal size and that the prevailing equations for predicting agility from body and canal size are highly inaccurate. Intraspecific comparisons between maps of observed angular velocity and predicted sensitivity allow identification of map types associated with different general locomotor modes and do not support existing hypotheses about the primary selective forces acting on canal morphology. The new data are used to formulate and test a novel "fast-accurate hypothesis" to explain why all vertebrates are more sensitive to rotations about some axes than others. The fast-accurate hypothesis stipulates that angular velocities presented about axes of mean sensitivity are most accurately interpreted by the brain, and that selection aligns axes of mean sensitivity with axes of habitually fast rotation because accurate perception of rapid rotations confers survival benefit. The fast-accurate hypothesis was used to predict which features of the canals should be correlated with high mean angular velocities of head movement. Novel equations that predict behavior from these newly identified canal morphologies were generated and found to outperform existing equations when tested on the original sample of 11 strepsirrhine species.

Although evolution results from differential reproduction and survival at the level of the individual, most research in evolutionary genetics is concerned with comparisons made at the level of divergent populations or species. This is particularly true in work focused on the evolutionary genetics of natural populations. While this level of inquiry is extremely valuable, in order to develop a complete understanding of the evolutionary process we also need to understand how traits evolve within populations, on the level of differences between individuals, and in the context of natural ecological and environmental variation. A major difficulty confronting such work stems from the difficulty of assessing interindividual phenotypic variation and its sources within natural populations. This level of inquiry is, however, the main focus for many long-term field studies. Here, I take advantage of one such field study, centered on the wild baboon population of the Amboseli basin, Kenya, to investigate the possibilities for integrating functional, population, and evolutionary genetic approaches with behavioral, ecological, and environmental data. First, I describe patterns of hybridization and admixture in the Amboseli population, a potentially important component of population structure. Second, I combine field sampling, laboratory measurements of gene expression, and a computational approach to examine the possibility of using allele-specific gene expression as a tool to study functional regulatory variation in natural populations. Finally, I outline an example of how these and other methods can be used to understand the relationship between genetic variation and naturally occurring infection by a malaria-like parasite, Hepatocystis, also in the Amboseli baboons. The results of this work emphasize that developing genetic approaches for nonmodel genetic systems is becoming increasingly feasible, thus opening the door to pursuing such studies in behavioral and ecological model systems that provide a broader framework for genetic results. Integrating behavioral, ecological, and genetic perspectives will allow us to better appreciate the interplay between these different factors, and thus achieve a better understanding of the raw material upon which selection acts.

During the last six million years, humans shifted from a primarily arboreal lifestyle to a habitually bipedal, terrestrial lifestyle. Australopithecus had a significant bipedal component to its locomotion; whether suspensory and climbing behavior were also important has remained unclear. Morphological features of the forelimb have been linked to locomotor differences among primates, but the interpretation of human fossils has remained problematic.

This dissertation examined the total morphological pattern of the forelimb, specifically the functional integration of the musculature and joint systems. This approach employed both geometric morphometrics and a biomechanical modeling approach to studying how and how well the forelimb morphology of living suspensory and quadrupedal primates, as well as humans and fossil hominins, accommodate climbing and suspensory locomotion. Data collected with a microscribe 3-D digitizer on the scapula, humerus, radius, and ulna of Australopithecus sediba, Australopithecus afarensis, and Homo erectus were compared to a sample of Homo sapiens, Pan troglodytes, Pan paniscus, Gorilla gorilla, Pongo pygmaeus, Hylobates lar, and Macaca fuscicularis.

The hominin upper limb is a rich mosaic of primitive and derived traits. The blade of Australopithecus sediba, although appearing most similar to extant orangutans, is in fact functionally most similar to chimpanzees. The overall morphology of the australopith elbow joint appears most similar to Pan, as does the elbow joint of Homo erectus, suggesting that the modern human configuration happened more recently than 1.5 million years ago.

Au. afarensis and Au. sediba share important similarities, but are clearly distinct species. While their overall elbow joint shape is strikingly similar, the articular surface is not identical. Au. afarensis is more similar in this respect to Pan and Homo, while Au. sediba is more similar to extant taxa that spend substantially more time engaging in vertical climbing and suspensory behavior.

The results from this study support previous interpretations that not all australopiths across time were employing the same locomotor repertoire. While this study does not present unambiguous conclusions regarding early hominin arboreal locomotion, this study suggests that the morphology of the upper limb is varied, and caution must be taken when interpreting single skeletal elements in the hominin fossil record.

The primary aim of this thesis was to quantify the ways Daubentonia uses its specialized feeding apparatus during naturalistic feeding behaviors. This can be divided into two main objectives. The first objective was to better understand how these extreme specializations function in the extractive foraging niche of Daubentonia. The second objective was to use Daubentonia to test for previously unmeasured behavioral modifications of bite forces using the post-cranial musculature. To do this I carried out two experiments measuring the kinetics of wood gnawing and the energetics of feeding behaviors. The main results of these experiments were: 1) Daubentonia does not generate relatively high magnitude bite forces during wood gnawing compared to their maximal voluntary bite force, but wood gnawing is extremely energetically costly compared to other feeding behaviors. 2) Daubentonia recruits post-cranial musculature during wood gnawing, most frequently generating a neck-extending moment that increased the magnitude of bite forces on the mandibular incisor. 3) The energetic costs of feeding were positively correlated with the toughness of foods. 4) The rate of energetic costs (J/s) incurred during the processing and mastication of whole nuts is not significantly greater than the rate of costs to masticate small pieces of nut kernels, but the increased handling time increases the net cost per gram of food consumed (J/g). Taken together, these experiments inform the primary aim of this study. Daubentonia appears to possess a highly specialized toolkit for fracturing stress-limited foods. Their large jaw adducting musculature, rodent-like incisors, and relatively short mandible allow them to produce large bite pressures to rapidly fracture the shells of nuts. Furthermore, it was demonstrated that Daubentonia transfers some forces from the post-cranial musculature to its incisors during wood gnawing and that the energetic costs of this wood gnawing behavior approach what is expected for sustained locomotor costs. This work illuminates a new avenue for investigation in jaw biomechanics: the assistance and modification of bite forces using the post-cranial musculature.

The discovery of hundreds of fossil hominin remains from the Dinaledi Chamber of Rising Star cave in South Africa included dozens of immature elements attributed to multiple individuals. Some of these elements are amongst the most complete in the Dinaledi assemblage, but have not yet been fully studied. Thorough examination of these immature remains is important because they can provide a more complete understanding of the morphology of the Dinaledi hominins, facilitate an assessment of morphological development in the assemblage, and allow for direct comparisons with other immature fossil hominins. This dissertation focuses on the most diagnostic specimens of the immature lower limb (with reference to the immature upper limb and the mature sample) from the site and utilizes a comparative approach examining developmental variation in the proximal femur and limb proportions of extinct and extant ape species to discern the ontogenetic basis of the adult Dinaledi hominin form.

The first portion of this dissertation addresses the development of proximal femoral shape in an ontogenetic series of femora from the Dinaledi hominins, modern humans, chimpanzees, and gorillas. Results indicate that the development of proximal diaphyseal shape and neck-shaft angle are conserved within Homininae, but that neck shape may develop differently in bipeds than non-bipeds. The absolute shape of the femoral neck, however, markedly differs between the Dinaledi sample and modern humans, with greater anteroposterior constriction of the neck in the former, potentially due to increased superioinferior loading of the region associated with differing locomotor kinematics between species.

The second portion of this dissertation investigates the relative proportions of the immature Dinaledi lower limb. To date, the only lower limb long bone preserving the entire diaphysis and an articular surface to be recovered from the chamber, is the immature tibia, U.W. 101-1070. The length of this specimen was evaluated relative to the size of the preserved joint surface in an ontogenetic context and was found to be relatively long compared to other fossil hominins and even modern humans. The humero-tibial proportions of the immature Dinaledi hominins were found to be outside of the range of chimpanzees and gorillas, but comparable to modern humans and the immature Homo erectus specimen KNM-ER 15000. Together, these findings demonstrate that, with respect to relative lower limb length, the Dinaledi hominins are highly derived.

The mixture of primitive (australopith-like) and derived (Homo-like) features of the Dinaledi hominins identified in this dissertation are consistent with other early work on the assemblage and imply that the Dinaledi chamber contains Plio-Pleistocene hominins. Given small brain and predicted body sizes for the Dinaledi hominins, the results presented here suggest that relative limb elongation may have occurred prior to increases in brain and body size during hominin evolution and that bipedal energetic efficiency may have been the primary locus of selection.

There has been a trend toward decreasing skeletal robusticity in the genus Homo throughout the Pleistocene, culminating in the gracile postcrania of living modern humans. This change is typically attributed to changing tool technologies and subsistence patterns among human groups. However, other mammalian groups also experience a similar change in their postcranial strength over the same time period. It is proposed in this dissertation that ecological variables are correlated with measures of postcranial strength and may be a better explanation for Holocene skeletal gracilization in humans, as well as in other mammalian genera. This hypothesis is investigated through a close examination of the scaling patterns in two extant genera, Canis and Ursus, and a comparison of scaling patterns and relative strength of different species of Canis, including a fossil species that provides information about temporal change. Measurements of limb length, joint surface area, bone diameter, and strength measurements derived from radiographic images of long bone midshafts of North American specimens of Canis, (including the fossil Canis dirus) and Ursus were collected. Scaling patterns of the cross-sectional variables on limb length and joint surfaces were analyzed for the interspecific and intraspecific samples.

The first hypothesis tested was that Canis scales with geometric similarity of cross-sectional variables on bone length and body mass, and the Ursus scales with elastic similarity. Larger Canis have relatively stronger postcrania than smaller Canis. The primary way in which this strength is achieved in larger individuals is through a relatively shortening of the bone length. The second hypothesis tested was that postcranial strength is correlated with ecological variables. To investigate this hypothesis, scaling patterns of different species of Canis were compared, including the fossil dire wolf. The results show that the dire wolf is relatively stronger than its living congenerics. There is also a strong relationship between the ratio of prey body mass to predator body mass and relative strength for these species. Carnivores that are hunting animals much larger than themselves must have postcranial skeletons that are strong enough to withstand the loading of the skeleton that occurs during hunting, taking down, and processing large herbivores.

Despite early neglect, recent studies of sexual selection have shown a renewed interest in female reproductive strategies. Clearly the traditional portrayal of female animals as passive participants in mating is incorrect, but much is still unknown about female reproductive strategies, including the extent of female mate choice. The primary goal of this dissertation was to explore the role of female mate choice in mantled howling monkeys (Alouatta palliata), a species in which males have previously been assumed to control mating.

From March 2006 through February 2007, I used continuous focal-animal sampling to record the behavior of adult female mantled howlers at Hacienda La Pacifica, Guanacaste, Costa Rica. The focal animals in the study were nine adult females in a social group that has been regularly monitored since 1984. There were also three capture sessions performed by K. Glander to collect blood samples for genetic paternity analysis. A total of 29 individuals in the study group and eight adult males from surrounding groups were captured.

The genetic paternity analyses were largely inconclusive. Of the eight microsatellite markers used previously in this species, only four were polymorphic in this sample. Additionally, nearly half (7 of 16) of the purported mothers were excluded at one locus. Assuming the mother was unknown allowed determination of genetic paternity in only one case. In terms of behavior, females were largely responsible for soliciting copulations, but female mate choice did not appear to be a major factor. Females almost never rejected copulations (3.3% of copulation attempts) and mated with multiple males in 77.8% of female cycles.

The lack of conclusive genetic paternity data leaves open the possibility of post-copulatory female choice. However, explanations exist for the apparent lack of female mate choice in this species. Because males must attain alpha status to remain in a group, differences in inherent quality may be low among group males. The potential for small differences among males in a social group, combined with the fact that females disperse from their natal group, suggests that female mate choice may occur primarily in choosing a group during dispersal.

The environment dictates many facets of animals’ lives, including how long individuals live and their physiology, fertility, and health along the way. While environment-responsive changes in gene regulation likely play a role in this relationship, we rarely have a clear understanding of the socioenvironmental determinants of gene regulation in natural primate populations. My dissertation addresses this gap by linking longitudinal observations of environmental experiences to measures of gene regulation in wild baboons from a long-term field study in Kenya. By adopting a genome-scale perspective, I investigate (i) whether distinct environmental stressors are reflected in distinct changes in gene regulation, and whether there are sex differences in these relationships, and (ii) what pathways are sensitive to environmental adversity, and whether these pathways overlap across different sources of stress. In chapter one, I test whether environmental stressors accelerate the aging process. I show that, according to a DNA methylation-based “epigenetic clock,” high ranking males experience accelerated aging. In chapter two, I test for links between variation in the adult social environment (social status and social bond strength) and blood-based gene expression. I demonstrate that dominance rank in male and female baboons has directionally opposite links to gene regulation, and that social bonds uniquely predict a more robust response to simulated bacterial threat. In chapter three, I systematically test the hypothesis that biological embedding via DNA methylation translates early life experience into lasting phenotypic effects in adulthood. I find widespread, and often overlapping, associations between major sources or early life adversity and DNA methylation measured in adulthood. Taken together, my work underscores the close ties between fitness-relevant environments and gene regulation in wild primates, including the existence of some pathways that are broadly sensitive to multiple types of environmental stressors. These contributions help fill important gaps in our understanding of the complex mechanisms that connect socioenvironmental variation, phenotype, and evolution in the primate lineage.

Delacour's langurs (Trachypithecus delacouri), one of the six limestone langur taxa of Southeast Asia, inhabit isolated, rugged limestone karst mountains in Northern Vietnam, although the reason for their current restriction to this habitat is unclear. The occupation of karst habitats by limestone langurs has been attributed to the refuge these rocky outcrops provide in a dramatically anthropogenically-altered landscape. Conversely, several ecological explanations have been proposed to account for their distribution, though the ecology of wild Delacour's langurs had yet to be studied. In this dissertation, I quantified the foraging ecology of Delacour's langurs living on Dong Quyen Mountain in Van Long Nature Reserve, Vietnam to address if these langurs show special adaptations to limestone karst or if they are exploiting a refuge habitat into which they have been pushed. I quantified their foraging ecology by systematically investigating their diet and feeding ecology, the chemisty of their eaten leaves, and the locomotions and substrates they utilized.

From August 2007 through July 2008, I used instantaneous focal-animal sampling during all-day follows of Delacour's langurs on Dong Quyen Mountain. I collected data on activity budget, diet, and positional behavior. I also collected samples of soils and eaten and uneaten leaves which were tested for phytochemical content.

With nearly 79% leaves in the diet, 60% of which were young leaves, Delacour's langurs are among the most folivorous of studied colobines, and- along with the closely related T. leucocephalus of southern China- the most folivorous of the Asian langurs. None of the plants that were important in the Delacour's langur diet were endemic limestone plants, and therefore feeding dependence alone cannot explain the current distribution of limestone langurs on karst habitat. Langurs ate leaves with high protein:fiber ratios, and despite a high percentage of carbon in the soil, young leaves were available throughout the year and plant defenses did not seem to have a large impact on eaten leaves. Delacour's langurs spent nearly 80% of their time on rocks. Quadrupedalism was their dominant locomotor style, more than double that of climbing. Terrestrialism, however, does not adequately describe the dangerous locomotion of these langurs; they are cliff-climbers. Delacour's langurs leapt only 6% of the time, much less than other African and Asian colobines, but their morphology (intermembral index) does not suggest terrestrialism or an evolutionary adaptation for limestone karst. Delacour's langurs appear to be a flexible taxon occupying a refuge habitat into which they have pushed. However, this restricted limestone habitat does not appear limiting in resources. The population at Van Long Nature Reserve is increasing which means that- if protected- this local population can rebound. Persistent hunting for traditional medicine and the more recent emergence of quarrying limestone for cement, however, threatens their survival.

The transition from the Pliocene to the Pleistocene appears to be a time of major transition in the hominin lineage with likely adaptive shifts in behavior. Homo erectus is a temporally broad species with apparent behavioral plasticity and potentially related morphological variability. Some H. erectus postcranial material exhibits traits that indicate a general trend of mechanical reinforcement at loadbearing sites across the pelvis and femur. One such fossil, KNM-ER 3228, is a presumed H. erectus os coxae that is representative of this morphological pattern of robusticity, which includes pronounced acetabulosacral and acetabulocristal buttresses and rugose musculoligamentous attachment sites. This femoropelvic complex represents an evolutionarily stable morphological pattern across a significant portion of the Pleistocene, but its biomechanical significance is not well understood. Moderate increases in encephalization combined with an increase in body size seen in H. erectus may be implicated in early Homo pelvic evolution, as the mechanical consequences of a larger body and expansion of the birth canal for parturition may have led to increased loads during locomotion. The retention of ancestral traits in the H. erectus pelvis (such as laterally flared ilia), coupled with derived traits (such as the expanded birth canal), may have necessitated greater robusticity in the pelvis to reduce strain magnitudes in the bone. Alternatively, this robusticity may be serving to reduce strains within the context of behavioral adaptations, such as endurance running or long-distance walking, that may have increased the magnitude or frequency of loads relative to australopiths. This dissertation addresses two objectives relative to the biomechanical significance of the femoropelvic complex of H. erectus. Objective 1 is to investigate the degree to which the patterns we see in some H. erectus pelves are due to body size scaling of bony features resulting from an evolutionary increase in body size. Objective 2 is to determine what, if any, functional significance may be assigned to the femoropelvic complex, beyond that which body size scaling to keep strain magnitudes within physiological limits may explain. A gait analysis study is conducted in which kinematic and kinetic data from modern humans are collected and used as input for a series of finite element models. These models are created from a sample of modern humans, an Australopithecus africanus pelvis (Sts 14), and a novel reconstruction of KNM-ER 3228 (early Homo) created using 3D geometric morphometrics. The results of these finite element models lead to the rejection of the hypothesis that higher magnitude loads in the H. erectus pelvis resulting from increased body size and modest encephalization resulted in the increased robusticity of pelvic features. This mechanical robusticity was hypothesized to maintain strain levels within manageable physiological levels in the context of the retention of ancestral states. Instead, the lower strains incurred during normal bipedal walking in the H. erectus pelvis suggest a pelvis adapted to bipedal walking, beyond that which strain maintenance can explain. Further, the results of finite element analyses of KNM-ER 3228 and modern humans while running provide evidence to support a hypothesis that mechanical buttressing of the H. erectus pelvis is an adaptation to an increased number of loading cycles (relative to australopiths) in the context of long-distance walking and/or endurance running, and/or high magnitude loads in the context of endurance running. This dissertation contributes to the investigation of unanswered questions in Homo pelvic evolution and highlights the value of comparative modeling in paleoanthropology.

Humans are champions of prosociality. Across different cultures and early in life, humans routinely engage in prosocial behaviors that benefit others. Perhaps most strikingly, humans are even prosocial toward strangers (i.e. xenophilic). This is an evolutionary puzzle because it cannot be explained by kinship theory, reciprocal altruism or reputation. The parochialism hypothesis proposes that this extreme prosociality is unique to humans, is motivated by unselfish motivation and evolved through group selection made possible by human culture and warfare. The first impression hypothesis, on the other hand, proposes that xenophilia can evolve to promote the selfish benefits that accrue from extending one's social network. It predicts that 1) nonhuman species can evolve prosociality toward strangers when the benefit of forming new relations is higher than the cost, 2) the motivation for prosociality can be selfish, and 3) encounters with strangers can be a positive social event since strangers represent potential social partners. This dissertation presents three sets of experiments designed to test these predictions with bonobos (Pan paniscus), a species known for reduced xenophobia. These experiments showed, first, that bonobos voluntarily shared monopolizable food with a stranger and helped the stranger to obtain out-of-reach food. Second, the observed prosociality was driven by a selfish motivation to initiate an interaction with the stranger in close proximity and an other-regarding motivation to benefit the stranger. Third, an involuntary yawning task and a voluntary choice task show converging results that bonobos attribute positive valence to completely unknown strangers by default. These experiments support the three core predictions of the first impression hypothesis and challenge the view that intergroup competition is crucial to the origin of prosociality toward strangers in our species. Instead, the first impression hypothesis proposes that xenophilia in bonobos is probably an adaptation to initiating non-kin cooperation. Because female bonobos are highly cooperative even though they are the dispersing sex, xenophilia might function to quickly establish cooperative relationships with new immigrants. This suggests that xenophilia and reciprocity are likely two complementary aspects of non-kin cooperation: the former explains its initiation while the latter explains its maintenance. Similarly, xenophilia in humans is likely a result of the increasing need for cooperation among non-kin due to enhanced fission-fusion dynamics, population expansion, obligate cooperative foraging and greater dependence on cultural knowledge.