A weakly structured stem for human origins in Africa.

Despite broad agreement that Homo sapiens originated in Africa, considerable uncertainty surrounds specific models of divergence and migration across the continent1. Progress is hampered by a shortage of fossil and genomic data, as well as variability in previous estimates of divergence times1. Here we seek to discriminate among such models by considering linkage disequilibrium and diversity-based statistics, optimized for rapid, complex demographic inference2. We infer detailed demographic models for populations across Africa, including eastern and western representatives, and newly sequenced whole genomes from 44 Nama (Khoe-San) individuals from southern Africa. We infer a reticulated African population history in which present-day population structure dates back to Marine Isotope Stage 5. The earliest population divergence among contemporary populations occurred 120,000 to 135,000 years ago and was preceded by links between two or more weakly differentiated ancestral Homo populations connected by gene flow over hundreds of thousands of years. Such weakly structured stem models explain patterns of polymorphism that had previously been attributed to contributions from archaic hominins in Africa2-7. In contrast to models with archaic introgression, we predict that fossil remains from coexisting ancestral populations should be genetically and morphologically similar, and that only an inferred 1-4% of genetic differentiation among contemporary human populations can be attributed to genetic drift between stem populations. We show that model misspecification explains the variation in previous estimates of divergence times, and argue that studying a range of models is key to making robust inferences about deep history.

Virtual reconstruction of the Kebara 2 Neanderthal pelvis.

The paucity of well-preserved pelvises in the hominin fossil record has hindered robust analyses of shifts in critical biological processes throughout human evolution. The Kebara 2 pelvis remains one of the best preserved hominin pelvises, providing a rare opportunity to assess Neanderthal pelvic morphology and function. Here, we present two new reconstructions of the Kebara 2 pelvis created from CT scans of the right hip bone and sacrum. For both reconstructions, we proceeded as follows. First, we virtually reconstructed the right hip bone and the sacrum by repositioning the fragments of the hip bone and sacrum. Then, we created a mirrored copy of the right hip bone to act as the left hip bone. Next, we 3D printed the three bones and physically articulated them. Finally, we used fiducial points collected from the physically articulated models to articulate the hip bones and sacrum in virtual space. Our objectives were to (1) reposition misaligned fragments, particularly the ischiopubic ramus; (2) create a 3D model of a complete pelvis; and (3) assess interobserver reconstruction variation. These new reconstructions show that, in comparison with previous measurements, Kebara 2 possessed a higher shape index (maximum anteroposterior length/maximum mediolateral width) for the pelvic inlet and perhaps the outlet and a more anteriorly positioned sacral promontory and pubic symphysis relative to the acetabula. The latter differences result in a lower ratio between the distances anterior and posterior to the anterior margins of the acetabula. Generally, the new reconstructions tend to accentuate features of the Kebara 2 pelvis--the long superior pubic ramus and anteriorly positioned pelvic inlet--that have already been discussed for Kebara 2 and other Neanderthals.

Effects of hybridization on pelvic morphology: A macaque model.

Ancient DNA analyses have shown that interbreeding between hominin taxa occurred multiple times. Although admixture is often reflected in skeletal phenotype, the relationship between the two remains poorly understood, hampering interpretation of the hominin fossil record. Direct study of this relationship is often impossible due to the paucity of hominin fossils and difficulties retrieving ancient genetic material. Here, we use a sample of known ancestry hybrids between two closely related nonhuman primate taxa (Indian and Chinese Macaca mulatta) to investigate the effect of admixture on skeletal morphology. We focus on pelvic shape, which has potential fitness implications in hybrids, as mismatches between maternal pelvic and fetal cranial morphology are often fatal to mother and offspring. As the pelvis is also one of the skeletal regions that differs most between Homo sapiens and Neanderthals, investigating the pelvic consequences of interbreeding could be informative regarding the viability of their hybrids. We find that the effect of admixture in M. mulatta is small and proportional to the relatively small morphological difference between the parent taxa. Sexual dimorphism appears to be the main determinant of pelvic shape in M. mulatta. The lack of difference in pelvic shape between Chinese and Indian M. mulatta is in contrast to that between Neanderthals and H. sapiens, despite a similar split time (in generations) between the hybridizing pairs. Greater phenotypic divergence between hominins may relate to adaptations to disparate environments but may also highlight how the unique degree of cultural buffering in hominins allowed for greater neutral divergence. In contrast to some previous work identifying extreme morphologies in first- and second-generation hybrids, here the relationship between pelvic shape and admixture is linear. This linearity may be because most sampled animals have a multigenerational admixture history or because of relatively high constraints on the pelvis compared with other skeletal regions.

Inferring archaic introgression from hominin genetic data.

Questions surrounding the timing, extent, and evolutionary consequences of archaic admixture into human populations have a long history in evolutionary anthropology. More recently, advances in human genetics, particularly in the field of ancient DNA, have shed new light on the question of whether or not Homo sapiens interbred with other hominin groups. By the late 1990s, published genetic work had largely concluded that archaic groups made no lasting genetic contribution to modern humans; less than a decade later, this conclusion was reversed following the successful DNA sequencing of an ancient Neanderthal. This reversal of consensus is noteworthy, but the reasoning behind it is not widely understood across all academic communities. There remains a communication gap between population geneticists and paleoanthropologists. In this review, we endeavor to bridge this gap by outlining how technological advancements, new statistical methods, and notable controversies ultimately led to the current consensus.

Ontogeny of the distal femoral metaphyseal surface and its relationship to locomotor behavior in hominoids.

OBJECTIVE: Distal femoral metaphyseal surface morphology is highly variable in extant mammals. This variation has previously been linked to differences in locomotor behavior. We perform the first systematic survey and description of the development of this morphology in extant hominoids. MATERIALS AND METHODS: We collected 3D surface laser scans of the femora of 179 human and great ape individuals throughout all subadult stages of development. We qualitatively and quantitatively describe metaphyseal surface morphology. RESULTS: We find that the metaphysis is topographically simple in all hominoids during the fetal and infant periods relative to later developmental periods, and in apes it develops significant complexity throughout development. Humans, by contrast, retain relatively flat metaphyseal surfaces throughout ontogeny. DISCUSSION: Major shifts in morphology appear to coincide with major shifts in locomotor behavior, suggesting that metaphyseal morphology is developmentally plastic and highly dependent on the biomechanical loadings at the knee joint. This is consistent with a large body of biomedical research, which demonstrates the primacy of mechanical forces in determining growth plate ossification patterns. Additionally, specific metaphyseal morphology appears highly correlated with specific locomotor modes, suggesting that metaphyseal surface morphology will be useful for reconstructing the locomotor behavior of fossil primate taxa.

Changes in human skull morphology across the agricultural transition are consistent with softer diets in preindustrial farming groups.

Agricultural foods and technologies are thought to have eased the mechanical demands of diet-how often or how hard one had to chew-in human populations worldwide. Some evidence suggests correspondingly worldwide changes in skull shape and form across the agricultural transition, although these changes have proved difficult to characterize at a global scale. Here, adapting a quantitative genetics mixed model for complex phenotypes, we quantify the influence of diet on global human skull shape and form. We detect modest directional differences between foragers and farmers. The effects are consistent with softer diets in preindustrial farming groups and are most pronounced and reliably directional when the farming class is limited to dairying populations. Diet effect magnitudes are relatively small, affirming the primary role of neutral evolutionary processes-genetic drift, mutation, and gene flow structured by population history and migrations-in shaping diversity in the human skull. The results also bring an additional perspective to the paradox of why Homo sapiens, particularly agriculturalists, appear to be relatively well suited to efficient (high-leverage) chewing.

Neonatal postcrania from Mezmaiskaya, Russia, and Le Moustier, France, and the development of Neandertal body form.

Neandertal and modern human adults differ in skeletal features of the cranium and postcranium, and it is clear that many of the cranial differences-although not all of them-are already present at the time of birth. We know less, however, about the developmental origins of the postcranial differences. Here, we address this deficiency with morphometric analyses of the postcrania of the two most complete Neandertal neonates-Mezmaiskaya 1 (from Russia) and Le Moustier 2 (from France)-and a recent human sample. We find that neonatal Neandertals already appear to possess the wide body, long pubis, and robust long bones of adult Neandertals. Taken together, current evidence indicates that skeletal differences between Neandertals and modern humans are largely established by the time of birth.

Comparative perspective on antemortem tooth loss in Neandertals.

Neandertal specimens with severe antemortem (before death) tooth loss (AMTL) are sometimes interpreted as evidence for human-like behaviors in Neandertals, such as conspecific care or cooking, although it is uncertain whether AMTL frequencies in Neandertals are similar to those in modern humans and exceed those in non-human primates. This study characterizes AMTL (all tooth types) in Neandertals relative to recent human hunter-gatherers and several non-human primate taxa using binomial-normal regression models fit in a Bayesian framework to a sample of 25 Neandertals, 310 recent human hunter-gatherers, 61 chimpanzees, 38 orangutans, and 75 baboons. The probability that a tooth is lost antemortem is modeled to depend on tooth class, taxon, and estimated age at death. Neandertals have odds of AMTL above orangutans and baboons, similar to or somewhat lower than chimpanzees, and below recent humans, if we assume a human-like rate of senescence; or intermediate between chimpanzees and recent humans, if we assume a faster rate of senescence. These findings suggest that Neandertals can only be considered to have frequencies of AMTL above non-human primates if they had more rapid life histories than modern humans. Either Neandertals are not human-like in their life history or their frequency of AMTL. These interpretations are complicated, however, by the substantial inter-population variation in AMTL among recent humans, with some populations having odds of AMTL as low as in non-human primates. These results, together with theoretical considerations, suggest that only high frequencies of AMTL are diagnostic of behavior. Consequently, the behavioral implications of low frequencies of AMTL, such as those found in Neandertals, are ambiguous. Low frequencies in Neandertals could be because they had a low risk of AMTL rather than because they had high mortality from AMTL relative to an average modern human of similar age.

A mixed model for the relationship between climate and human cranial form.

OBJECTIVES: We expand upon a multivariate mixed model from quantitative genetics in order to estimate the magnitude of climate effects in a global sample of recent human crania. In humans, genetic distances are correlated with distances based on cranial form, suggesting that population structure influences both genetic and quantitative trait variation. Studies controlling for this structure have demonstrated significant underlying associations of cranial distances with ecological distances derived from climate variables. However, to assess the biological importance of an ecological predictor, estimates of effect size and uncertainty in the original units of measurement are clearly preferable to significance claims based on units of distance. Unfortunately, the magnitudes of ecological effects are difficult to obtain with distance-based methods, while models that produce estimates of effect size generally do not scale to high-dimensional data like cranial shape and form. METHODS: Using recent innovations that extend quantitative genetics mixed models to highly multivariate observations, we estimate morphological effects associated with a climate predictor for a subset of the Howells craniometric dataset. RESULTS: Several measurements, particularly those associated with cranial vault breadth, show a substantial linear association with climate, and the multivariate model incorporating a climate predictor is preferred in model comparison. CONCLUSIONS: Previous studies demonstrated the existence of a relationship between climate and cranial form. The mixed model quantifies this relationship concretely. Evolutionary questions that require population structure and phylogeny to be disentangled from potential drivers of selection may be particularly well addressed by mixed models. Am J Phys Anthropol 160:593-603, 2016. © 2015 Wiley Periodicals, Inc.

Unconstrained cranial evolution in Neandertals and modern humans compared to common chimpanzees.

A variety of lines of evidence support the idea that neutral evolutionary processes (genetic drift, mutation) have been important in generating cranial differences between Neandertals and modern humans. But how do Neandertals and modern humans compare with other species? And how do these comparisons illuminate the evolutionary processes underlying cranial diversification? To address these questions, we used 27 standard cranial measurements collected on 2524 recent modern humans, 20 Neandertals and 237 common chimpanzees to estimate split times between Neandertals and modern humans, and between Pan troglodytes verus and two other subspecies of common chimpanzee. Consistent with a neutral divergence, the Neandertal versus modern human split-time estimates based on cranial measurements are similar to those based on DNA sequences. By contrast, the common chimpanzee cranial estimates are much lower than DNA-sequence estimates. Apparently, cranial evolution has been unconstrained in Neandertals and modern humans compared with common chimpanzees. Based on these and additional analyses, it appears that cranial differentiation in common chimpanzees has been restricted by stabilizing natural selection. Alternatively, this restriction could be due to genetic and/or developmental constraints on the amount of within-group variance (relative to effective population size) available for genetic drift to act on.

Variation and signatures of selection on the human face.

There has been much debate about why humans throughout the world differ in facial form. Previous studies of human skull morphology found levels of among-population differentiation that were comparable to those of neutral genetic markers, suggesting that genetic drift (neutral processes) played an important role in influencing facial differentiation. However, variation in soft-tissue morphology has not been studied in detail. In this study, we analyzed high-resolution 3D images of soft-tissue facial form in four Eurasian populations: Han Chinese, Tibetans, Uyghur and Europeans. A novel method was used to establish a high-density alignment across all of the faces, allowing facial diversity to be examined at an unprecedented resolution. These data exhibit signatures of population structure and history. However, among-population differentiation was higher for soft-tissue facial form than for genome-wide genetic loci, and high-resolution analyses reveal that the nose, brow area and cheekbones exhibit particularly strong signals of differentiation (Qst estimates: 0.3-0.8) between Europeans and Han Chinese. Our results suggest that local adaptation and/or sexual selection have been important in shaping human soft-tissue facial morphology.

Brief Communication: Quantitative- and molecular-genetic differentiation in humans and chimpanzees: implications for the evolutionary processes underlying cranial diversification.

Estimates of the amount of genetic differentiation in humans among major geographic regions (e.g., Eastern Asia vs. Europe) from quantitative-genetic analyses of cranial measurements closely match those from classical- and molecular-genetic markers. Typically, among-region differences account for ∼10% of the total variation. This correspondence is generally interpreted as evidence for the importance of neutral evolutionary processes (e.g., genetic drift) in generating among-region differences in human cranial form, but it was initially surprising because human cranial diversity was frequently assumed to show a strong signature of natural selection. Is the human degree of similarity of cranial and DNA-sequence estimates of among-region genetic differentiation unusual? How do comparisons with other taxa illuminate the evolutionary processes underlying cranial diversification? Chimpanzees provide a useful starting point for placing the human results in a broader comparative context, because common chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) are the extant species most closely related to humans. To address these questions, I used 27 cranial measurements collected on a sample of 861 humans and 263 chimpanzees to estimate the amount of genetic differentiation between pairs of groups (between regions for humans and between species or subspecies for chimpanzees). Consistent with previous results, the human cranial estimates are quite similar to published DNA-sequence estimates. In contrast, the chimpanzee cranial estimates are much smaller than published DNA-sequence estimates. It appears that cranial differentiation has been limited in chimpanzees relative to humans.

Predicting the shape, size, and placement of adult human pubic symphyses.

OBJECTIVES: When reconstructing fossil pelves, the articulation of the pelvic bones largely relies on subjective decisions by researchers. Different positionings at the pubic symphysis can affect the overall morphology of the pelvis and the subsequent biological interpretation associated with that individual or species. This study aims to reduce this subjectivity using quantitative models to predict pubic symphysis morphology. METHODS: We collected 3D landmarks and semilandmarks on the pubic symphysis and adjacent aspects on the CT scans of 103 adults. Using geometric morphometrics we, (1) quantified pubic symphysis morphology, (2) trained simple and two-stage least-squares linear regression models to predict pubic symphysis shape, and (3) assessed the shape variation in the sample. The model with the lowest prediction error was identified as the best model. Principal components analysis was used to explore the effects of each variable on shape and hypothetical shapes were generated from the model to illustrate these effects. RESULTS: The best model is a two-stage least-squares model that predicts pubic symphysis size at the first stage using additive effects of sex and age, then subsequently interacts pubic symphysis size with sex and age at the second stage to predict pubic symphysis shape. Other models with low prediction errors included variables reflecting pelvic size and breadth. CONCLUSION: Linear regression modeling can be used to systematically predict pubic symphysis morphology. This method can be used in addition to other techniques to improve fossil reconstructions by more accurately estimating the morphology of this region of the pelvis.

Developing an automated skeletal phenotyping pipeline to leverage biobank-level medical imaging databases.

OBJECTIVES: Collecting skeletal measurements from medical imaging databases remains a tedious task, limiting the research utility of biobank-level data. Here we present an automated phenotyping pipeline for obtaining skeletal measurements from DXA scans and compare its performance to manually collected measurements. MATERIALS AND METHODS: A pipeline that extends the Advanced Normalization Tools (ANTs) framework was developed on 341 whole-body DXA scans of UK Biobank South Asian participants. A set of 10 measurements throughout the skeleton was automatically obtained via this process, and the performance of the method was tested on 20 additional DXA images by calculating percent error and concordance correlation coefficients (CCC) for manual and automated measurements. Stature was then regressed on the automated femoral and tibia lengths and compared to published stature regressions to further assess the reliability of the automated measurements. RESULTS: Based on percent error and CCC, the performance of the automated measurements falls into three categories: poor (sacral and acetabular breadths), variable (trunk length, upper thoracic breadth, and innominate height), and high (maximum pelvic aperture breadth, bi-iliac breadth, femoral maximum length, and tibia length). Stature regression plots indicate that the automated measurements reflect realistic body proportions and appear consistent with published data reflecting these relationships in South Asian populations. DISCUSSION: Based on the performance of this pipeline, a subset of measurements can be reliably extracted from DXA scans, greatly expanding the utility of biobank-level data for biological anthropologists and medical researchers.

Did a discrete event 200,000-100,000 years ago produce modern humans?

Scenarios for modern human origins are often predicated on the assumption that modern humans arose 200,000-100,000 years ago in Africa. This assumption implies that something 'special' happened at this point in time in Africa, such as the speciation that produced Homo sapiens, a severe bottleneck in human population size, or a combination of the two. The common thread is that after the divergence of the modern human and Neandertal evolutionary lineages ∼400,000 years ago, there was another discrete event near in time to the Middle-Late Pleistocene boundary that produced modern humans. Alternatively, modern human origins could have been a lengthy process that lasted from the divergence of the modern human and Neandertal evolutionary lineages to the expansion of modern humans out of Africa, and nothing out of the ordinary happened 200,000-100,000 years ago in Africa. Three pieces of biological (fossil morphology and DNA sequences) evidence are typically cited in support of discrete event models. First, living human mitochondrial DNA haplotypes coalesce ∼200,000 years ago. Second, fossil specimens that are usually classified as 'anatomically modern' seem to appear shortly afterward in the African fossil record. Third, it is argued that these anatomically modern fossils are morphologically quite different from the fossils that preceded them. Here I use theory from population and quantitative genetics to show that lengthy process models are also consistent with current biological evidence. That this class of models is a viable option has implications for how modern human origins is conceptualized.

Out of Africa: modern human origins special feature: the meaning of neandertal skeletal morphology.

A procedure is outlined for distinguishing among competing hypotheses for fossil morphology and then used to evaluate current views on the meaning of Neandertal skeletal morphology. Three explanations have dominated debates about the meaning of Neandertal cranial features: climatic adaptation, anterior dental loading, and genetic drift. Neither climatic adaptation nor anterior dental loading are well supported, but genetic drift is consistent with the available evidence. Climatic adaptation and activity patterns are the most discussed explanations for Neandertal postcranial features. Robust empirical relationships between climate and body form in extant humans and other endotherms currently make climatic adaptation the most plausible explanation for the wide bodies and relatively short limbs of Neandertals, and many additional postcranial features are likely secondary consequences of these overall skeletal proportions. Activity patterns may explain certain Neandertal postcranial features, but unlike the situation for climate, relationships in extant humans between morphology and activities are typically not well established. For both the cranium and the postcranium, changes in diet or activity patterns may underlie why Neandertals and Pleistocene modern humans tend to be more robust than Holocene humans.

Neandertal birth canal shape and the evolution of human childbirth.

Childbirth is complicated in humans relative to other primates. Unlike the situation in great apes, human neonates are about the same size as the birth canal, making passage difficult. The birth mechanism (the series of rotations that the neonate must undergo to successfully negotiate its mother's birth canal) distinguishes humans not only from great apes, but also from lesser apes and monkeys. Tracing the evolution of human childbirth is difficult, because the pelvic skeleton, which forms the margins of the birth canal, tends to survive poorly in the fossil record. Only 3 female individuals preserve fairly complete birth canals, and they all date to earlier phases of human evolution. Here we present a virtual reconstruction of a female Neandertal pelvis from Tabun, Israel. The size of Tabun's reconstructed birth canal indicates that childbirth was about as difficult in Neandertals as in present-day humans, but the canal's shape indicates that Neandertals had a more primitive birth mechanism. A significant shift in childbirth apparently occurred quite late in human evolution, during the last few hundred thousand years. Such a late shift underscores the uniqueness of human childbirth and the divergent evolutionary trajectories of Neandertals and the lineage leading to present-day humans.

Do modern humans and Neandertals have different patterns of cranial integration?

Studies of cranial differences between modern humans and Neandertals have identified several characteristics for which the two groups differ in their mean values, the proportional relationships with other traits, or both. However, the limited number of fairly complete Neandertals has hindered investigations into patterns of integration - covariance and correlation among traits - in this fossil group. Here, we use multiple approaches specifically designed to deal with fragmentary fossils to test if metric cranial traits in Neandertals fit modern human patterns of integration. Based on 37 traits collected from a sample of 2524 modern humans from Howells' data set and 20 Neandertals, we show that overall patterns of cranial integration are significantly different between Neandertals and modern humans. However, at the same time, Neandertals are consistent with a modern human pattern of integration for more than three-quarters of the traits. Additionally, the differences between the predicted and actual values for the deviating traits are rather small, indicating that the differences in integration are subtle. Traits for which Neandertals deviate from modern human integration patterns tend to be found in regions where Neandertals and modern humans are known to also differ in their mean values. We conclude that the evolution of patterns of cranial integration is a cause for caution but also presents an opportunity for understanding cranial differences between modern humans and Neandertals.