Endocranial ontogeny and evolution in early Homo sapiens: The evidence from Herto, Ethiopia.

Fossils and artifacts from Herto, Ethiopia, include the most complete child and adult crania of early Homo sapiens. The endocranial cavities of the Herto individuals show that by 160,000 y ago, brain size, inferred from endocranial size, was similar to that seen in modern human populations. However, endocranial shape differed from ours. This gave rise to the hypothesis that the brain itself evolved substantially during the past ∼200,000 y, possibly in tandem with the transition from Middle to Upper Paleolithic techno-cultures. However, it remains unclear whether evolutionary changes in endocranial shape mostly reflect changes in brain morphology rather than changes related to interaction with maxillofacial morphology. To discriminate between these effects, we make use of the ontogenetic fact that brain growth nearly ceases by the time the first permanent molars fully erupt, but the face and cranial base continue to grow until adulthood. Here we use morphometric data derived from digitally restored immature and adult H. sapiens fossils from Herto, Qafzeh, and Skhul (HQS) to track endocranial development in early H. sapiens. Until the completion of brain growth, endocasts of HQS children were similar in shape to those of modern human children. The similarly shaped endocasts of fossil and modern children indicate that our brains did not evolve substantially over the past 200,000 y. Differences between the endocranial shapes of modern and fossil H. sapiens adults developed only with continuing facial and basicranial growth, possibly reflecting substantial differences in masticatory and/or respiratory function.

Human shoulder development is adapted to obstetrical constraints.

In humans, obstetrical difficulties arise from the large head and broad shoulders of the neonate relative to the maternal birth canal. Various characteristics of human cranial development, such as the relatively small head of neonates compared with adults and the delayed fusion of the metopic suture, have been suggested to reflect developmental adaptations to obstetrical constraints. On the other hand, it remains unknown whether the shoulders of humans also exhibit developmental features reflecting obstetrical adaptation. Here we address this question by tracking the development of shoulder width from fetal to adult stages in humans, chimpanzees, and Japanese macaques. Compared with nonhuman primates, shoulder development in humans follows a different trajectory, exhibiting reduced growth relative to trunk length before birth and enhanced growth after birth. This indicates that the perinatal developmental characteristics of the shoulders likely evolved to ease obstetrical difficulties such as shoulder dystocia in humans.

The primitive brain of early Homo.

The brains of modern humans differ from those of great apes in size, shape, and cortical organization, notably in frontal lobe areas involved in complex cognitive tasks, such as social cognition, tool use, and language. When these differences arose during human evolution is a question of ongoing debate. Here, we show that the brains of early Homo from Africa and Western Asia (Dmanisi) retained a primitive, great ape-like organization of the frontal lobe. By contrast, African Homo younger than 1.5 million years ago, as well as all Southeast Asian Homo erectus, exhibited a more derived, humanlike brain organization. Frontal lobe reorganization, once considered a hallmark of earliest Homo in Africa, thus evolved comparatively late, and long after Homo first dispersed from Africa.

Early development of the Neanderthal ribcage reveals a different body shape at birth compared to modern humans.

Ontogenetic studies provide clues for understanding important paleobiological aspects of extinct species. When compared to that of modern humans, the adult Neanderthal thorax was shorter, deeper, and wider. This is related to the wide Neanderthal body and is consistent with their hypothetical large requirements for energy and oxygen. Whether these differences were already established at birth or appeared later during development is unknown. To delve into this question, we use virtual reconstruction tools and geometric morphometrics to recover the 3D morphology of the ribcages of four Neanderthal individuals from birth to around 3 years old: Mezmaiskaya 1, Le Moustier 2, Dederiyeh 1, and Roc de Marsal. Our results indicate that the comparatively deep and short ribcage of the Neanderthals was already present at birth, as were other skeletal species-specific traits. This morphology possibly represents the plesiomorphic condition shared with Homo erectus, and it is likely linked to large energetic requirements.

Variation of bony labyrinthine morphology in Mio-Plio-Pleistocene and modern anthropoids.

OBJECTIVES: The bony labyrinth of the inner ear has special relevance when tracking phenotypic evolution because it is often well preserved in fossil and modern primates. Here we track the evolution of the bony labyrinth of anthropoid primates during the Mio-Plio-Pleistocene-the time period that gave rise to the extant great apes and humans. MATERIALS AND METHODS: We use geometric morphometrics to analyze labyrinthine morphology in a wide range of extant and fossil anthropoids, including New World and Old World monkeys, apes, and humans; fossil taxa are represented by Aegyptopithecus, Microcolobus, Epipliopithecus, Nacholapithecus, Oreopithecus, Ardipithecus, Australopithecus, and Homo. RESULTS: Our results show that the morphology of the anthropoid bony labyrinth conveys a statistically significant phylogenetic signal especially at the family level. The bony labyrinthine morphology of anthropoids is also in part associated with size, but does not cluster by locomotor adaptations. The Miocene apes examined here, regardless of inferred locomotor behaviors, show labyrinthine morphologies distinct from modern great apes. DISCUSSION: Our results suggest that labyrinthine variation contains mixed signals and alternative explanations need to be explored, such as random genetic drift and neutral phenotypic evolution, as well as developmental constraints. The observed pattern in fossil and extant hominoids also suggests that an additional factor, for example, prenatal brain development, could have potentially had a larger role in the evolutionary modification of the bony labyrinth than hitherto recognized.

Evidence for independent brain and neurocranial reorganization during hominin evolution.

Throughout hominin evolution, the brain of our ancestors underwent a 3-fold increase in size and substantial structural reorganization. However, inferring brain reorganization from fossil hominin neurocrania (=braincases) remains a challenge, above all because comparative data relating brain to neurocranial structures in living humans and great apes are still scarce. Here we use MRI and same-subject spatially aligned computed tomography (CT) and MRI data of humans and chimpanzees to quantify the spatial relationships between these structures, both within and across species. Results indicate that evolutionary changes in brain and neurocranial structures are largely independent of each other. The brains of humans compared to chimpanzees exhibit a characteristic posterior shift of the inferior pre- and postcentral gyri, indicative of reorganization of the frontal opercular region. Changes in human neurocranial structure do not reflect cortical reorganization. Rather, they reflect constraints related to increased encephalization and obligate bipedalism, resulting in relative enlargement of the parietal bones and anterior displacement of the cerebellar fossa. This implies that the relative position and size of neurocranial bones, as well as overall endocranial shape (e.g., globularity), should not be used to make inferences about evolutionary changes in the relative size or reorganization of adjacent cortical regions of fossil hominins.

Human bony labyrinth is an indicator of population history and dispersal from Africa.

The dispersal of modern humans from Africa is now well documented with genetic data that track population history, as well as gene flow between populations. Phenetic skeletal data, such as cranial and pelvic morphologies, also exhibit a dispersal-from-Africa signal, which, however, tends to be blurred by the effects of local adaptation and in vivo phenotypic plasticity, and that is often deteriorated by postmortem damage to skeletal remains. These complexities raise the question of which skeletal structures most effectively track neutral population history. The cavity system of the inner ear (the so-called bony labyrinth) is a good candidate structure for such analyses. It is already fully formed by birth, which minimizes postnatal phenotypic plasticity, and it is generally well preserved in archaeological samples. Here we use morphometric data of the bony labyrinth to show that it is a surprisingly good marker of the global dispersal of modern humans from Africa. Labyrinthine morphology tracks genetic distances and geography in accordance with an isolation-by-distance model with dispersal from Africa. Our data further indicate that the neutral-like pattern of variation is compatible with stabilizing selection on labyrinth morphology. Given the increasingly important role of the petrous bone for ancient DNA recovery from archaeological specimens, we encourage researchers to acquire 3D morphological data of the inner ear structures before any invasive sampling. Such data will constitute an important archive of phenotypic variation in present and past populations, and will permit individual-based genotype-phenotype comparisons.

Reconstructing the Neanderthal brain using computational anatomy.

The present study attempted to reconstruct 3D brain shape of Neanderthals and early Homo sapiens based on computational neuroanatomy. We found that early Homo sapiens had relatively larger cerebellar hemispheres but a smaller occipital region in the cerebrum than Neanderthals long before the time that Neanderthals disappeared. Further, using behavioural and structural imaging data of living humans, the abilities such as cognitive flexibility, attention, the language processing, episodic and working memory capacity were positively correlated with size-adjusted cerebellar volume. As the cerebellar hemispheres are structured as a large array of uniform neural modules, a larger cerebellum may possess a larger capacity for cognitive information processing. Such a neuroanatomical difference in the cerebellum may have caused important differences in cognitive and social abilities between the two species and might have contributed to the replacement of Neanderthals by early Homo sapiens.

Identification of in vivo Sulci on the External Surface of Eight Adult Chimpanzee Brains: Implications for Interpreting Early Hominin Endocasts.

The only direct source of information about hominin brain evolution comes from the fossil record of endocranial casts (endocasts) that reproduce details of the external morphology of the brain imprinted on the walls of the braincase during life. Surface traces of sulci that separate the brain's convolutions (gyri) are reproduced sporadically on early hominin endocasts. Paleoneurologists rely heavily on published descriptions of sulci on brains of great apes, especially chimpanzees (humans' phylogenetically closest living relatives), to guide their identifications of sulci on ape-sized hominin endocasts. However, the few comprehensive descriptions of cortical sulci published for chimpanzees usually relied on post mortem brains, (now) antiquated terminology for some sulci, and photographs or line drawings from limited perspectives (typically right or left lateral views). The shortage of adequate descriptions of chimpanzee sulcal patterns partly explains why the identities of certain sulci on australopithecine endocasts (e.g., the inferior frontal and middle frontal sulci) have been controversial. Here, we provide images of lateral and dorsal surfaces of 16 hemispheres from 4 male and 4 female adult chimpanzee brains that were obtained using in vivo magnetic resonance imaging. Sulci on the exposed surfaces of the frontal, parietal, temporal, and occipital lobes are identified on the images based on their locations, positions relative to each other, and homologies known from comparative studies of cytoarchitecture in primates. These images and sulcal identifications exceed the quantity and quality of previously published illustrations of chimpanzee brains with comprehensively labeled sulci and, thus, provide a larger number of examples for identifying sulci on hominin endocasts than hitherto available. Our findings, even in a small sample like the present one, overturn published claims that australopithecine endocasts reproduce derived configurations of certain sulci in their frontal lobes that never appear on chimpanzee brains. The sulcal patterns in these new images also suggest that changes in two gyri that bridge between the parietal and occipital lobes may have contributed to cortical reorganization in early hominins. It is our hope that these labeled in vivo chimpanzee brains will assist future researchers in identifying sulci on hominin endocasts, which is a necessary first step in the quest to learn how and when the external morphology of the human cerebral cortex evolved from apelike precursors.

Femoral ontogeny in humans and great apes and its implications for their last common ancestor.

Inferring the morphology of the last common ancestor of humans, chimpanzees and gorillas is a matter of ongoing debate. Recent findings and reassessment of fossil hominins leads to the hypothesis that the last common ancestor was not extant African ape-like. However, an African great-ape-like ancestor with knuckle walking features still remains plausible and the most parsimonious scenario. Here we address this question via an evolutionary developmental approach, comparing taxon-specific patterns of shape change of the femoral diaphysis from birth to adulthood in great apes, humans, and macaques. While chimpanzees and gorillas exhibit similar locomotor behaviors, our data provide evidence for distinct ontogenetic trajectories, indicating independent evolutionary histories of femoral ontogeny. Our data further indicate that anthropoid primates share a basic pattern of femoral diaphyseal ontogeny that reflects shared developmental constraints. Humans escaped from these constraints via differential elongation of femur.

Neomorphosis and heterochrony of skull shape in dog domestication.

The overall similarity of the skull shape of some dog breeds with that of juvenile wolves begs the question if and how ontogenetic changes such as paedomorphosis (evolutionary juvenilisation) played a role in domestication. Here we test for changes in patterns of development and growth during dog domestication. We present the first geometric morphometric study using ontogenetic series of dog and wolf crania, and samples of dogs with relatively ancestral morphology and from different time periods. We show that patterns of juvenile-to-adult morphological change are largely similar in wolves and domestic dogs, but differ in two ways. First, dog skulls show unique (neomorphic) features already shortly after birth, and these features persist throughout postnatal ontogeny. Second, at any given age, juvenile dogs exhibit skull shapes that resemble those of consistently younger wolves, even in dog breeds that do not exhibit a 'juvenilized' morphology as adults. These patterns exemplify the complex nature of evolutionary changes during dog domestication: the cranial morphology of adult dogs cannot simply be explained as either neomorphic or paedomorphic. The key to our understanding of dog domestication may lie in a closer comparative examination of developmental phases.

Individual-based modelling of population growth and diffusion in discrete time.

Individual-based models (IBMs) of human populations capture spatio-temporal dynamics using rules that govern the birth, behavior, and death of individuals. We explore a stochastic IBM of logistic growth-diffusion with constant time steps and independent, simultaneous actions of birth, death, and movement that approaches the Fisher-Kolmogorov model in the continuum limit. This model is well-suited to parallelization on high-performance computers. We explore its emergent properties with analytical approximations and numerical simulations in parameter ranges relevant to human population dynamics and ecology, and reproduce continuous-time results in the limit of small transition probabilities. Our model prediction indicates that the population density and dispersal speed are affected by fluctuations in the number of individuals. The discrete-time model displays novel properties owing to the binomial character of the fluctuations: in certain regimes of the growth model, a decrease in time step size drives the system away from the continuum limit. These effects are especially important at local population sizes of <50 individuals, which largely correspond to group sizes of hunter-gatherers. As an application scenario, we model the late Pleistocene dispersal of Homo sapiens into the Americas, and discuss the agreement of model-based estimates of first-arrival dates with archaeological dates in dependence of IBM model parameter settings.

Development of Pelvic Sexual Dimorphism in Hylobatids: Testing the Obstetric Constraints Hypothesis.

Pelvic sexual dimorphism in primates is typically seen as the result of female-specific adaptations to obstetric constraints, which arise from the tight fit between the neonate head and the maternal pelvis. However, it remains debated to which extent pelvic dimorphism is a correlate of obstetric constraints, of body size dimorphism, and/or of other factors. Also, little is known on how pelvic dimorphism develops. Here we use methods of biomedical imaging and geometric morphometrics to address these questions in two hylobatid species, Hylobates lar and Symphalangus syndactylus. These species differ markedly in body size, but within each species, there is only little body size dimorphism. Results show that the neonates of H. lar are large compared to the maternal pelvis, resulting in high cephalopelvic proportions and substantial obstetric constraints. Pelvic sexual dimorphism is moderate but significant: During puberty, females develop a more capacious pelvic inlet than males, while overall pelvic size is similar in both sexes. S. syndactylus has substantially larger pelves than H. lar, but neonates are similar in size to those of H. lar. Cephalopelvic proportions are thus low, and there are no obstetric constraints. Pelvic sexual dimorphism is absent. Overall, these data indicate that pelvic sexual dimorphism in hylobatids reflects obstetric constraints. Anat Rec, 300:859-869, 2017. © 2017 Wiley Periodicals, Inc.

Skull 5 from Dmanisi: Descriptive anatomy, comparative studies, and evolutionary significance.

A fifth hominin skull (cranium D4500 and mandible D2600) from Dmanisi is massively constructed, with a large face and a very small brain. Traits documented for the first time in a basal member of the Homo clade include the uniquely low ratio of endocranial volume to basicranial width, reduced vertex height, angular vault profile, smooth nasal sill coupled with a long and sloping maxillary clivus, elongated palate, and tall mandibular corpus. The convex clivus and receding symphysis of skull 5 produce a muzzle-like form similar to that of Australopithecus afarensis. While the Dmanisi cranium is very robust, differing from OH 13, OH 24, and KNM-ER 1813, it resembles Homo habilis specimens in the "squared off" outline of its maxilla in facial view, maxillary sulcus, rounded and receding zygomatic arch, and flexed zygomaticoalveolar pillar. These characters distinguish early Homo from species of Australopithecus and Paranthropus. Skull 5 is unlike Homo rudolfensis cranium KNM-ER 1470. Although it appears generally primitive, skull 5 possesses a bar-like supraorbital torus, elongated temporal squama, occipital transverse torus, and petrotympanic traits considered to be derived for Homo erectus. As a group, the Dmanisi crania and mandibles display substantial anatomical and metric variation. A key question is whether the fossils document age-related growth and sex dimorphism within a single population, or whether two (or more) distinct taxa may be present at the site. We use the coefficient of variation to compare Dmanisi with Paranthropus boisei, H. erectus, and recent Homo sapiens, finding few signals that the Dmanisi sample is excessively variable in comparison to these reference taxa. Using cranial measurements and principal components analysis, we explore the proposal that the Dmanisi skulls can be grouped within a regionally diverse hypodigm for H. erectus. Our results provide only weak support for this hypothesis. Finally, we consider all available morphological and paleobiological evidence in an attempt to clarify the phyletic relationship of Dmanisi to Homo species evolving >2.0 to 1.0 Ma.

Development of Modular Organization in the Chimpanzee Pelvis.

The bony pelvis of primates is a composite structure serving a variety of functions, and exhibiting a complex pattern of modularity and integration. Still little is known, however, about how patterns of modularity and integration arise, and how they change throughout ontogeny. Here we study the ontogeny of modularity and integration in developmental and functional units of the pelvis of our closest living relatives, the chimpanzees. We use methods of biomedical imaging and geometric morphometrics to quantify pelvic shape change from late fetal stages to adulthood, and to track changes in patterns of covariation within and among pelvic regions. Our results show that both developmental and functional units of the pelvis exhibit significant levels of modularity throughout ontogeny. Modularity of developmental units (ilium, ischium, and pubis) decreases with increasing age, whereas modularity of functional units tends to increase. We suggest that the decreasing modularity and increasing integration of developmental units reflects their gradual fusion. In contrast, increasing modularity of functional pelvic units likely reflects changing functional demands during an individual's lifetime. Overall, ontogenetic changes in patterns of modularity and integration imply that natural selection could act differently on each module, either developmental or functional, at different stages of ontogeny. This further implies that adult patterns of covariation in the pelvis provide only limited information about its evolvability. Anat Rec, 300:675-686, 2017. © 2017 Wiley Periodicals, Inc.

Effects of cranial integration on hominid endocranial shape.

Because brains do not fossilize, the internal surface of the braincase (endocast) serves as an important source of information about brain growth, development, and evolution. Recent studies of endocranial morphology and development in great apes, fossil hominins, and modern humans have revealed taxon-specific differences. However, it remains to be investigated to which extent differences in endocranial morphology reflect differences in actual brain morphology and development, and to which extent they reflect different interactions of the brain and its case with the cranial base and face. Here we address this question by analyzing the effects of cranial integration on endocranial morphology. We test the 'spatial packing' and 'facial orientation' hypotheses, which propose that size and orientation of the neurocranium relative to the viscerocranium influence endocranial shape. Results show that a substantial proportion of endocranial shape variation along and across ontogenetic trajectories is due to cranial integration. Specifically, the uniquely globular shape of the human endocast mainly results from the combination of an exceptionally large brain with a comparatively small face. Overall, thus, cranial integration has pervasive effects on endocranial morphology, and only a comparatively small proportion of inter- and intra-taxon variation can directly be associated with variation in brain morphology.

Brain development is similar in Neanderthals and modern humans.

While the braincase of adult Neanderthals had a similar volume to that of modern humans from the same period, differences in endocranial shape suggest that brain morphology differed between modern humans and Neanderthals. When and how these differences arose during evolution and development is a topic of ongoing research, with potential implications for species-specific differences in brain and cognitive development, and in life history [1,2]. Earlier research suggested that Neanderthals followed an ancestral mode of brain development, similar to that of our closest living relatives, the chimpanzees [2-4]. Modern humans, by contrast, were suggested to follow a uniquely derived mode of brain development just after birth, giving rise to the characteristically globular shape of the adult human brain case [2,4,5]. Here, we re-examine this hypothesis using an extended sample of Neanderthal infants. We document endocranial development during the decisive first two years of postnatal life. The new data indicate that Neanderthals followed largely similar modes of endocranial development to modern humans. These findings challenge the notion that human brain and cognitive development after birth is uniquely derived [2,4].

Developmental evidence for obstetric adaptation of the human female pelvis.

The bony pelvis of adult humans exhibits marked sexual dimorphism, which is traditionally interpreted in the framework of the "obstetrical dilemma" hypothesis: Giving birth to large-brained/large-bodied babies requires a wide pelvis, whereas efficient bipedal locomotion requires a narrow pelvis. This hypothesis has been challenged recently on biomechanical, metabolic, and biocultural grounds, so that it remains unclear which factors are responsible for sex-specific differences in adult pelvic morphology. Here we address this issue from a developmental perspective. We use methods of biomedical imaging and geometric morphometrics to analyze changes in pelvic morphology from late fetal stages to adulthood in a known-age/known-sex forensic/clinical sample. Results show that, until puberty, female and male pelves exhibit only moderate sexual dimorphism and follow largely similar developmental trajectories. With the onset of puberty, however, the female trajectory diverges substantially from the common course, resulting in rapid expansion of obstetrically relevant pelvic dimensions up to the age of 25-30 y. From 40 y onward females resume a mode of pelvic development similar to males, resulting in significant reduction of obstetric dimensions. This complex developmental trajectory is likely linked to the pubertal rise and premenopausal fall of estradiol levels and results in the obstetrically most adequate pelvic morphology during the time of maximum female fertility. The evidence that hormones mediate female pelvic development and morphology supports the view that solutions of the obstetrical dilemma depend not only on selection and adaptation but also on developmental plasticity as a response to ecological/nutritional factors during a female's lifetime.

Comparative analysis of dentognathic pathologies in the Dmanisi mandibles.

OBJECTIVES: Due to the scarcity of the fossil record, in vivo changes in the dentognathic system of early Homo are typically documented at the level of individual fossil specimens, and it remains difficult to draw population-level inferences about dietary habits, diet-related activities and lifestyle from individual patterns of dentognathic alterations. The Plio-Pleistocene hominin sample from Dmanisi (Georgia), dated to 1.77 million years ago, offers a unique opportunity to study in vivo changes in the dentognathic system of individuals belonging to a single paleodeme of early Homo. MATERIALS AND METHODS: We analyze dentognathic pathologies in the Dmanisi sample, and in comparative samples of modern Australian and Greenlander hunter-gatherer populations, applying clinical protocols of dentognathic diagnostics. RESULTS: The Dmanisi hominins exhibit a similarly wide diversity and similar incidence of dentognathic pathologies as the modern human hunter-gatherer population samples investigated here. Dmanisi differs from the modern population samples in several respects: At young age tooth wear is already advanced, and pathologies are more prevalent. At old age, hypercementosis is substantial. CONCLUSIONS: Results indicate that dentognathic pathologies and disease trajectories are largely similar in early Homo and modern humans, but that the disease load was higher in early Homo, probably as an effect of higher overall stress on the dentognathic system. Am J Phys Anthropol 160:229-253, 2016. © 2016 Wiley Periodicals, Inc.