Oral processing, sexual selection, and size variation in the circumorbital region of Colobus and Piliocolobus.

OBJECTIVES: The function of the browridge in primates is a subject of enduring debate. Early studies argued for a role in resisting masticatory stresses, but recent studies have suggested sexual signaling as a biological role. We tested associations between circumorbital form, diet, oral processing, and social behavior in two species of colobus monkey-the king colobus (Colobus polykomos) and western red or bay colobus (Piliocolobus badius). MATERIALS AND METHODS: We quantified circumorbital size and dimorphism in a sample of 98 crania. Controlling for age and facial size, we tested whether variation in circumorbital morphology can be explained by variation in diet, oral processing behavior, masticatory muscle size, and mating system. To contextualize our results, we included a broader sample of facial dimorphism for 67 anthropoid species. RESULTS: Greater circumorbital thickness is unrelated to the stresses of food processing. King colobus engages in longer bouts of anterior tooth use, chews more per ingestive event, and processes a tougher diet, yet circumorbital thickness of C. polykomos is reduced compared to P. badius. Differences in circumorbital development do not vary with wear or facial size. Greater sexual dimorphism is present in P. badius; comparisons across anthropoids indicated patterns of circumorbital dimorphism were decoupled from overall size dimorphism. CONCLUSIONS: The expanded circumorbits of male red colobus monkeys evolved in response to intense male-male competition. This hypothesis is consistent with the pattern across anthropoid primates and highlights the underappreciated role of sexual selection in shaping the primate face.

Introduction to special issue Kanapoi: Paleobiology of a Pliocene site in Kenya.

This paper introduces this Special Issue of the Journal of Human Evolution entitled "Kanapoi: Paleobiology of a Pliocene site in Kenya." Kanapoi, West Turkana, Kenya, is part of the Omo-Turkana Basin and is the type site of the earliest known genus of Australopithecus, A. anamensis. Kanapoi preserves among the earliest earliest evidence of Australopithecus in deposits dated between 4.195 to 4.108 million years old. Explored by several teams since the 1960s, the Kanapoi sediments have yielded a rich and abundant fauna, providing important information about the paleoenvironments and the context surrounding the earliest evolution of the genus Australopithecus, as well as about the evolution and biogeography of African Pliocene vertebrate faunas.

Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007-2015).

Recent fieldwork at Kanapoi has expanded the sample of fossil cercopithecids, facilitating a re-appraisal of their taxonomy. The assemblage now includes at least one species of cercopithecin, two papionins, and two colobines. The guenon Nanopithecus browni is similar in dental size to extant Miopithecus. We tentatively re-affirm the identification of Parapapio cf. ado and confirm the presence of Theropithecus. The colobines include a small form tentatively attributed to Kuseracolobus and a second larger species. The Kanapoi fossils represent the oldest occurrences of guenons in Africa and of the important genus Theropithecus, the most abundant and widespread primate in the Neogene of Africa. In the assemblage, Parapapio cf. ado is the most abundant form, comprising the majority of specimens. All of the other taxa are comparatively rare. Colobines make up a small part of the Kanapoi fossil assemblage compared to most other contemporary sites, including Allia Bay, Kenya, where, like Kanapoi, Australopithecus anamensis has been found. The presence of Theropithecus is consistent with the presence of some relatively open habitat at Kanapoi. While the ecological preferences of the small cercopithecin are unknown, most guenons are associated with relatively wooded habitats, as are most colobines, suggesting the availability of at least some wooded areas.

The ecology of Australopithecus anamensis in the early Pliocene of Kanapoi, Kenya.

Australopithecus anamensis is a pivotal species in human evolution. It is likely to be the direct ancestor of Australopithecus afarensis and the species that may have given rise to the Homo and Paranthropus lineages. It had a suite of adaptations for habitual bipedalism and a diet that differed from that of earlier hominin species. Under what environmental and ecological conditions did this suite of adaptations arise? The early Pliocene site of Kanapoi in the Lake Turkana Basin of Kenya has the largest sample of A. anamensis in eastern Africa and a rich record of fossil vertebrates. Most Kanapoi fossils are chronologically well constrained by radiometrically dated tephras between the ages of 4.2 and 4.1 million years ago. Sedimentological, isotopic, and faunal data indicate that the environments of Kanapoi during the early Pliocene had a complex range of vegetation types that included closed woodlands, shrubs, and grasslands near a river (for most of the sequence) or lake. These were dynamic landscapes that could shift rapidly from fluvial to lacustrine conditions, and then back. Australopithecus anamensis shared its environments with at least 10 species of very large herbivores, which undoubtedly played a major role in modifying the landscape by opening wooded areas and providing pathways for bipedal hominins. Hominins may have competed for terrestrial resources with abundant suids (Nyanzachoerus and Notochoerus) and for arboreal resources with monkeys (Parapapio being the most common cercopithecid). Kanapoi had a formidable group of predators that included a very abundant species of hyena (Parahyaena howelli), two sabre-tooth felids (Dinofelis and Homotherium), a giant otter (Enhydriodon cf. dikikae), and three species of crocodiles. Various measures of abundance indicate that A. anamensis was an important component of the Kanapoi early Pliocene ecosystems, and that its key adaptations allowed this species to thrive in complex and dynamic landscapes.

Dental microwear and Pliocene paleocommunity ecology of bovids, primates, rodents, and suids at Kanapoi.

Reconstructions of habitat at sites like Kanapoi are key to understanding the environmental circumstances in which hominins evolved during the early Pliocene. While Australopithecus anamensis shows evidence of terrestrial bipedality traditionally associated with a more open setting, its enamel has low δ13C values consistent with consumption of C3 foods, which predominate in wooded areas of tropical Africa. Habitat proxies, ranging from paleosols and their carbonates to associated herbivore fauna and their carbon isotope ratios, suggest a heterogeneous setting with both grass and woody plant components, though the proportions of each have been difficult to pin down. Here we bring dental microwear texture analysis of herbivorous fauna to bear on the issue. We present texture data for fossil bovids, primates, rodents, and suids (n = 107 individuals in total) from the hominin bearing deposits at Kanapoi, and interpret these in the light of closely related extant mammals with known differences in diet. The Kanapoi bovid results, for example, are similar to those for extant variable grazers or graze-browse intermediate taxa. The Kanapoi suid data vary by taxon, with one similar to the pattern of extant grazers and the other more closely resembling mixed feeders. The Kanapoi primates and rodents are more difficult to associate with a specific environment, though it seems that grass was likely a component in the diets of both. All taxa evince microwear texture patterns consistent with a mosaic of discrete microhabitats or a heterogeneous setting including both tree and grass components.

A late Miocene hominid partial pelvis from Hungary.

Substantial differences among the pelves of anthropoids have been central to interpretations of the selection pressures that shaped extant hominoids, yet the evolution of the hominoid pelvis has been poorly understood due to the scarcity of fossil material. A recently discovered partial hipbone attributed to the 10 million-year-old fossil ape Rudapithecus hungaricus from Rudabánya, Hungary, differs from the hipbones of cercopithecids and earlier apes in functionally significant ways. Comparisons were made to extant and other fossil anthropoids using combination of non-landmark-based and linear metrics. Measurements were taken on 3D polygonal models of hipbones collected using laser scans. These metrics capture functionally relevant morphology given the incomplete preservation of the Rudapithecus specimen. This fossil displays features that reflect changes in spinal musculature and torso structure found only in extant great and lesser apes among hominoids. Rudapithecus has an expanded cranial acetabular lunate surface related to orthograde positional behaviors, a shallow acetabulum and relatively short ischium like orangutans and hylobatids. It displays evidence of moderately coronally-oriented iliac blades as in all extant apes and Ateles, and flaring iliac blade shape of siamangs and great apes, associated with some level of spinal stiffness. However, this fossil lacks the long lower ilium that characterizes chimpanzees, gorillas and orangutans, associated with their reduction of the number of lumbar vertebrae. The R. hungaricus pelvis demonstrates that the extreme elongation of the lower ilium seen in extant great apes does not necessarily accompany adaptation to orthograde posture and forelimb-dominated arboreal locomotion in hominoid evolution. Lower iliac elongation appears to have occurred independently in each lineage of extant great apes, supporting the hypothesis that the last common ancestor of Pan and Homo may have been unlike extant great apes in pelvic length and lower back morphology.

A diminutive Pliocene guenon from Kanapoi, West Turkana, Kenya.

Although modern guenons are diverse and abundant in Africa, the fossil record of this group is surprisingly sparse. In 2012 the West Turkana Paleo Project team recovered two associated molar teeth of a small primate from the Pliocene site of Kanapoi, West Turkana, Kenya. The teeth are bilophodont and the third molar lacks a hypoconulid, which is diagnostic for Cercopithecini. The teeth are the same size as those of extant Miopithecus, which is thought to be a dwarfed guenon, as well as a partial mandible preserving two worn teeth, previously recovered from Koobi Fora, Kenya, which was also tentatively identified as a guenon possibly allied with Miopithecus. Tooth size and proportions, as well as analysis of relative cusp size and shearing crest development clearly separate the fossil from all known guenons. Based on the Kanapoi material, we erect a new genus and species, Nanopithecus browni gen. et sp. nov. The small size of the specimen suggests either that dwarfing occurred early in the lineage, or at least twice independently, depending on the relationship of the new species with extant Miopithecus. Further, the distinctive habitat and geographic separation from Miopithecus suggests that the origin of small body size is not uniquely linked to the current habitat of Miopithecus, and possibly that relatives of extant Miopithecus were much more widely distributed in the past. This in turn argues caution in using extant biogeography in models of the origins of at least some guenons.

Early Pleistocene third metacarpal from Kenya and the evolution of modern human-like hand morphology.

Despite discoveries of relatively complete hands from two early hominin species (Ardipithecus ramidus and Australopithecus sediba) and partial hands from another (Australopithecus afarensis), fundamental questions remain about the evolution of human-like hand anatomy and function. These questions are driven by the paucity of hand fossils in the hominin fossil record between 800,000 and 1.8 My old, a time interval well documented for the emergence and subsequent proliferation of Acheulian technology (shaped bifacial stone tools). Modern and Middle to Late Pleistocene humans share a suite of derived features in the thumb, wrist, and radial carpometacarpal joints that is noticeably absent in early hominins. Here we show that one of the most distinctive features of this suite in the Middle Pleistocene to recent human hand, the third metacarpal styloid process, was present ∼1.42 Mya in an East African hominin from Kaitio, West Turkana, Kenya. This fossil thus provides the earliest unambiguous evidence for the evolution of a key shared derived characteristic of modern human and Neandertal hand morphology and suggests that the distinctive complex of radial carpometacarpal joint features in the human hand arose early in the evolution of the genus Homo and probably in Homo erectus sensu lato.

A validated method for modeling anthropoid hip abduction in silico.

OBJECTIVES: The ability to reconstruct hip joint mobility from femora and pelves could provide insight into the locomotion and paleobiology of fossil primates. This study presents a method for modeling hip abduction in anthropoids validated with in vivo data. METHODS: Hip abduction simulations were performed on a large sample of anthropoids. The modeling approach integrates three-dimensional (3D) polygonal models created from laser surface scans of bones, 3D landmark data, and shape analysis software to digitally articulate and manipulate the hip joint. Range of femoral abduction (degrees) and the abducted knee position (distance spanned at the knee during abduction) were compared with published live animal data. RESULTS: The models accurately estimate knee position and (to a lesser extent) angular abduction across broad locomotor groups. They tend to underestimate abduction for acrobatic or suspensory taxa, but overestimate it in more stereotyped taxa. Correspondence between in vivo and in silico data varies at the specific and generic level. CONCLUSIONS: Our models broadly correspond to in vivo data on hip abduction, although the relationship between the models and live animal data is less straightforward than hypothesized. The models can predict acrobatic or stereotyped locomotor adaptation for taxa with values near the extremes of the range of abduction ability. Our findings underscore the difficulties associated with modeling complex systems and the importance of validating in silico models. They suggest that models of joint mobility can offer additional insight into the functional abilities of extinct primates when done in consideration of how joints move and function in vivo. Am J Phys Anthropol 160:529-548, 2016. © 2016 Wiley Periodicals, Inc.

Associated ilium and femur from Koobi Fora, Kenya, and postcranial diversity in early Homo.

During the evolution of hominins, it is generally accepted that there was a shift in postcranial morphology between Australopithecus and the genus Homo. Given the scarcity of associated remains of early Homo, however, relatively little is known about early Homo postcranial morphology. There are hints of postcranial diversity among species, but our knowledge of the nature and extent of potential differences is limited. Here we present a new associated partial ilium and femur from Koobi Fora, Kenya, dating to 1.9 Ma (millions of years ago) that is clearly attributable to the genus Homo but documents a pattern of morphology not seen in eastern African early Homo erectus. The ilium and proximal femur share distinctive anatomy found only in Homo. However, the geometry of the femoral midshaft and contour of the pelvic inlet do not resemble that of any specimens attributed to H. erectus from eastern Africa. This new fossil confirms the presence of at least two postcranial morphotypes within early Homo, and documents diversity in postcranial morphology among early Homo species that may reflect underlying body form and/or adaptive differences.

Calculating hominin and nonhuman anthropoid femoral head diameter from acetabular size.

Femoral head size provides important information on body size in extinct species. Although it is well-known that femoral head size is correlated with acetabular size, the precision with which femoral head size can be estimated from acetabular size has not been quantified. The availability of accurate 3D surface models of fossil acetabular remains opens the possibility of obtaining accurate estimates of femoral head size from even fragmentary fossil remains [Hammond et al.,: Am J Phys Anthropol 150 (2013) 565-578]. Here we evaluate the relationship between spheres fit to surface models of the femoral head and acetabulum of a large sample of extant anthropoid primates. Sphere diameters are tightly correlated and scale isometrically. In spite of significant taxonomic and possibly functional differences in the relationship between femoral head size and acetabulum size, percent prediction errors of estimated femoral head size remain low regardless of the taxonomic composition of the reference sample. We provide estimates of femoral head size for a series of fossil hominins and monkeys.

Precision and accuracy of acetabular size measures in fragmentary hominin pelves obtained using sphere-fitting techniques.

Hip joint diameter is highly correlated with body size in primates and so can potentially provide important information about the biology of fossil hominins. However, quantifying hip joint size has been difficult or impossible for many important but fragmentary specimens. New three-dimensional technologies can be used to digitally fit spheres to the acetabular lunate surface, potentially allowing hip joint diameter estimates for incomplete joint surfaces. Here we evaluate the reliability of sphere-fitting to incomplete lunate surfaces in silico using three-dimensional polygonal models of extant anthropoid hipbones. Measurement error in lunate sphere-fitting was assessed at the individual observer level, as well as between observers. Prediction error was also established for acetabular sphere size estimates for smaller divisions of the lunate surface. Sphere-fitting techniques were then applied to undistorted regions of lunate surface in Plio-Pleistocene hominin pelves, with a range of diameters constructed from extant error estimates. The results of this study indicate that digital sphere-fitting techniques are precise and that the lunate does not need to be completely preserved to accurately infer hip dimensions, although some aspects of joint size and morphology can influence sphere size estimates. Joint diameter is strongly predicted by spheres fit to the cranial and caudal halves of the lunate in all anthropoids. We present new hip joint size estimates for a number of fossil hominins, and outline additional applications for digital sphere-fitting as a morphometric technique.

Sex at Sterkfontein: 'Mrs. Ples' is still an adult female.

The important question of whether the Australopithecus africanus hypodigm is taxonomically heterogeneous revolves largely around the interpretation of the morphological variation exhibited by the fossils from Sterkfontein. The sex assignment of these specimens is a critical component in the evaluation of their morphological variability. The Sts 5 cranium is pivotal in this regard because it is the most complete and undistorted specimen attributed to A. africanus. Although it has traditionally been regarded as an adult female, this view has been challenged. In particular, it has been argued recently that Sts 5 is a juvenile and that this, together with alveolar bone loss that has supposedly reduced the size of the canine socket, has led to its misinterpretation as a female. Virtual reconstruction of the M(3) roots (and/or alveoli) contradicts arguments that these teeth were erupting at the time of death. Regardless, canine emergence and root completion are well ahead of M(3) development in juvenile australopiths from Sterkfontein. Thus, even if the M(3) root of Sts 5 was incomplete, its canine root would have been fully formed. Measurements of palate depth indicate that the alveolar margins of Sts 5 have not suffered from much (if any) bone loss in the region of the C/P(3); any additional bone would result in a palate of truly exceptional depth. Therefore, the dimensions of the canine alveolus of Sts 5 can be regarded as proxies for those of the canine root. The canine root of Sts 5 is among the smallest recorded for any Sterkfontein australopith, which provides strong support for Robert Broom's initial attribution of sex to this specimen. There is no evidence to contradict the assertion that 'Mrs. Ples' is an adult female.

The enigmatic molar from Gondolin, South Africa: implications for Paranthropus paleobiology.

The specific attribution of the large hominin M(2) (GDA-2) from Gondolin has significant implications for the paleobiology of Paranthropus. If it is a specimen of Paranthropus robustus it impacts that species' size range, and if it belongs to Paranthropus boisei it has important biogeographic implications. We evaluate crown size, cusp proportions and the likelihood of encountering a large-bodied mammal species in both East and South Africa in the Early Pleistocene. The tooth falls well outside the P. robustus sample range, and comfortably within that for penecontemporaneous P. boisei. Analyses of sample range, distribution and variability suggest that it is possible, albeit unlikely to find a M(2) of this size in the current P. robustus sample. However, taphonomic agents - carnivore (particularly leopard) feeding behaviors - have likely skewed the size distribution of the Swartkrans and Drimolen P. robustus assemblage. In particular, assemblages of large-bodied mammals accumulated by leopards typically display high proportions of juveniles and smaller adults. The skew in the P. robustus sample is consistent with this type of assemblage. Morphological evidence in the form of cusp proportions is congruent with GDA-2 representing P. robustus rather than P. boisei. The comparatively small number of large-bodied mammal species common to both South and East Africa in the Early Pleistocene suggests a low probability of encountering an herbivorous australopith in both. Our results are most consistent with the interpretation of the Gondolin molar as a very large specimen of P. robustus. This, in turn, suggests that large, presumptive male, specimens are rare, and that the levels of size variation (sexual dimorphism) previously ascribed to this species are likely to be gross underestimates.

Understanding dimorphism as a function of changes in male and female traits.

I once received a review of a manuscript that took exception to the analysis of sexual dimorphism because the phenomenon is reified from independent changes in male and female characters. The reviewer was both right and wrong. Sexual dimorphism, a difference between males and females of a species in any anatomical, physiological, or behavioral character, is real in the sense that it reflects some underlying difference between the sexes. The fact that the magnitude of these differences varies among species in a measurable and constant way suggests that the phenomenon has a biological basis. But it is also true that dimorphism is a product of independent changes in male and female traits. It is becoming more and more apparent that a complete understanding of the phenomenon of sexual dimorphism can be achieved only by understanding variation in the factors that affect both male and female traits, and the potentially different responses to those factors in each sex.

Estimating canine tooth crown height in early Australopithecus.

Canine tooth size reduction and the associated reduction in canine dimorphism is a basal hominin character that also provides important evidence for models of behavioral evolution. Two specimens of Australopithecus anamensis (KNM-KP 29287 and KNM-KP 29283) that do not preserve the canine crown, but do preserve the root or alveolus, appear to suggest that canine size variation and canine dimorphism in this species may have been greater than in other hominins. We evaluate canine root and crown dimensions in a series of extant hominoids, and estimate canine crown height in Australopithecus afarensis and A. anamensis. Our results demonstrate that it is possible to generate estimates of canine crown height from basal canine crown and root dimensions with a moderate degree of accuracy. Estimates of maxillary canine crown size for A. anamensis are slightly larger than those of A. afarensis, and are approximately the same size as canines of modern female chimpanzees. Estimated mandibular canine crown height is very similar in the two species. Variation within the A. anamensis sample of estimated canine crown heights is similar to that of modern humans, suggesting a low degree of sexual dimorphism. Inclusion of estimates for KNM-KP 29287 and KNM-KP 29283 does not substantially increase either the estimate of overall canine size or variation for A. anamensis.

Canine size, shape, and bending strength in primates and carnivores.

Anthropoid primates are well known for their highly sexually dimorphic canine teeth, with males possessing canines that are up to 400% taller than those of females. Primate canine dimorphism has been extensively documented, with a consensus that large male primate canines serve as weapons for intrasexual competition, and some evidence that large female canines in some species may likewise function as weapons. However, apart from speculation that very tall male canines may be relatively weak and that seed predators have strong canines, the functional significance of primate canine shape has not been explored. Because carnivore canine shape and size are associated with killing style, this group provides a useful comparative baseline for primates. We evaluate primate maxillary canine tooth size, shape and relative bending strength against body size, skull size, and behavioral and demographic measures of male competition and sexual selection, and compare them to those of carnivores. We demonstrate that, relative to skull length and body mass, primate male canines are on average as large as or larger than those of similar sized carnivores. The range of primate female canine sizes embraces that of carnivores. Male and female primate canines are generally as strong as or stronger than those of carnivores. Although we find that seed-eating primates have relatively strong canines, we find no clear relationship between male primate canine strength and demographic or behavioral estimates of male competition or sexual selection, in spite of a strong relationship between these measures and canine crown height. This suggests either that most primate canines are selected to be very strong regardless of variation in behavior, or that primate canine shape is inherently strong enough to accommodate changes in crown height without compromising canine function.