Simon Neubauer

Brain development after birth differs between Neanderthals and modern humans

Summary Neanderthals had brain sizes comparable to modern humans, but their brain cases were elongated and not globular as in Homo sapiens [1,2]. It has, therefore, been suggested that modern humans and Neanderthals reached large brain sizes along different evolutionary pathways [2]. Here, we assess when during development these adult differences emerge. This is critical for understanding whether differences in the pattern of brain development might underlie potential cognitive differences between these two closely related groups. Previous comparisons of Neanderthal and modern human cranial development have shown that many morphological characteristics separating these two groups are already established at the time of birth [3–5], and that the subsequent developmental patterns of the face are similar, though not identical [6]. Here, we show that a globularization phase seen in the neurocranial development of modern humans after birth is absent from Neanderthals.

The pattern of endocranial ontogenetic shape changes in humans

Humans show a unique pattern of brain growth that differentiates us from all other primates. In this study, we use virtual endocasts to provide a detailed description of shape changes during human postnatal ontogeny with geometric morphometric methods. Using CT scans of 108 dried human crania ranging in age from newborns to adults and several hundred landmarks and semi‐landmarks, we find that the endocranial ontogenetic trajectory is curvilinear with two bends, separating three distinct phases of shape change. We test to what extent endocranial shape change is driven by size increase and whether the curved ontogenetic trajectory can be explained by a simple model of modular development of the endocranial base and the endocranial vault. The hypothesis that endocranial shape change is driven exclusively by brain growth is not supported; we find changes in endocranial shape after adult size has been attained and that the transition from high rates to low rates of size increase does not correspond to one of the shape trajectory bends. The ontogenetic trajectory of the endocranial vault analyzed separately is nearly linear; the trajectory of the endocranial base, in contrast, is curved. The endocranial vault therefore acts as one developmental module during human postnatal ontogeny. Our data suggest that the cranial base comprises several submodules that follow their own temporally and/or spatially disjunct growth trajectories.

The Structural Rigidity of the Cranium of Australopithecus africanus: Implications for Diet, Dietary Adaptations, and the Allometry of Feeding Biomechanics

Australopithecus africanus is an early hominin (i.e., human relative) believed to exhibit stress‐reducing adaptations in its craniofacial skeleton that may be related to the consumption of resistant food items using its premolar teeth. Finite element analyses simulating molar and premolar biting were used to test the hypothesis that the cranium of A. africanus is structurally more rigid than that of Macaca fascicularis, an Old World monkey that lacks derived australopith facial features. Previously generated finite element models of crania of these species were subjected to isometrically scaled loads, permitting a direct comparison of strain magnitudes. Moreover, strain energy (SE) in the models was compared after results were scaled to account for differences in bone volume and muscle forces. Results indicate that strains in certain skeletal regions below the orbits are higher in M. fascicularis than in A. africanus. Moreover, although premolar bites produce von Mises strains in the rostrum that are elevated relative to those produced by molar biting in both species, rostral strains are much higher in the macaque than in the australopith. These data suggest that at least the midface of A. africanus is more rigid than that of M. fascicularis. Comparisons of SE reveal that the A. africanus cranium is, overall, more rigid than that of M. fascicularis during premolar biting. This is consistent with the hypothesis that this hominin may have periodically consumed large, hard food items. However, the SE data suggest that the A. africanus cranium is marginally less rigid than that of the macaque during molar biting. It is hypothesized that the SE results are being influenced by the allometric scaling of cranial cortical bone thickness. Anat Rec, 293:583–593, 2010.

How to Explore Morphological Integration in Human Evolution and Development

Most studies in evolutionary developmental biology focus on large-scale evolutionary processes using experimental or molecular approaches, whereas evolutionary quantitative genetics provides mathematical models of the influence of heritable phenotypic variation on the short-term response to natural selection. Studies of morphological integration typically are situated in-between these two styles of explanation. They are based on the consilience of observed phenotypic covariances with qualitative developmental, functional, or evolutionary models. Here we review different forms of integration along with multiple other sources of phenotypic covariances, such as geometric and spatial dependencies among measurements. We discuss one multivariate method [partial least squares analysis (PLS)] to model phenotypic covariances and demonstrate how it can be applied to study developmental integration using two empirical examples. In the first example we use PLS to study integration between the cranial base and the face in human postnatal development. Because the data are longitudinal, we can model both cross-sectional integration and integration of growth itself, i.e., how cross-sectional variance and covariance is actually generated in the course of ontogeny. We find one factor of developmental integration (connecting facial size and the length of the anterior cranial base) that is highly canalized during postnatal development, leading to decreasing cross-sectional variance and covariance. A second factor (overall cranial length to height ratio) is less canalized and leads to increasing (co)variance. In a second example, we examine the evolutionary significance of these patterns by comparing cranial integration in humans to that in chimpanzees.

Brain ontogeny and life history in Pleistocene hominins

A high level of encephalization is critical to the human adaptive niche and emerged among hominins over the course of the past 2 Myr. Evolving larger brains required important adaptive adjustments, in particular regarding energy allocation and life history. These adaptations included a relatively small brain at birth and a protracted growth of highly dependent offspring within a complex social environment. In turn, the extended period of growth and delayed maturation of the brain structures of humans contribute to their cognitive complexity. The current palaeoanthropological evidence shows that, regarding life history and brain ontogeny, the Pleistocene hominin taxa display different patterns and that one cannot simply contrast an ‘ape-model’ to a ‘human-model’. Large-brained hominins such as Upper Pleistocene Neandertals have evolved along their own evolutionary pathway and can be distinguished from modern humans in terms of growth pattern and brain development. The life-history pattern and brain ontogeny of extant humans emerged only recently in the course of human evolution.

The Evolution of Human Brain Development

The human brain is a large and complex organ, setting us apart from other primates. It allows us to exhibit highly sophisticated cognitive and behavioral abilities. Therefore, our brain’s size and morphology are defining features of our species and our fossil ancestors and relatives. Endocasts, i.e., internal casts of the bony braincase, provide evidence about brain size and morphology in fossils. Based on endocasts, we know that our ancestors’ brains increased overall in size and underwent several reorganizational changes. However, it is difficult to relate evolutionary changes of size and shape of endocasts to evolutionary changes of cognition and behavior. We argue here that an understanding of the tempo and mode of brain development can help to interpret the evolution of our brain and the associated cognitive and behavioral changes. To do so, we review structural brain development, cognitive development, and ontogenetic changes of endocranial size and shape in living individuals on the one hand, and ontogenetic patterns (size increase and shape change) in fossil hominins and their evolutionary change on the other hand. Tightly integrating our knowledge on these different levels will be the key of future work on the evolution of human brain development.

Reconstruction of the late Pleistocene human skull from Hofmeyr, South Africa.

Human skeletal remains from sub-Saharan Africa are virtually non-existent for the period when genetic models indicate the first modern human emigration from this region. The skull from Hofmeyr, South Africa, which has been dated to c. 36ka, is one of the only specimens known from this critical part of the late Pleistocene. The Hofmeyr skull was largely intact at the time of its discovery but has suffered post-recovery mishandling, with the resultant loss of most of the lower facial skeleton, the mandibular angle, the right mastoid process, and much of the occipital. Given the potential significance of this specimen, we have undertaken its restoration and reconstruction so as to provide a more complete picture of the cranial morphology of the late Pleistocene population from which it derived. On the basis of photographs, measurements, and morphological description recorded prior to its having been damaged, we reconstructed some of the missing bone in modeling clay on a high resolution plastic cast of the cranium. The original specimen was CT scanned, as was the cast with the reconstructed maxilla and mastoid; these scans were employed in the final computer reconstruction of the skull. Virtual reconstruction of the remainder of the cranium was accomplished using mirror-imaging and reference-based methods, employing 3D geometric morphometrics from a sample of recent human crania to compute coordinate-based estimates of the missing parts. This reconstruction provides a more complete picture of the Hofmeyr cranium and serves as a basis for more comprehensive morphometric comparisons.

A Shared Pattern of Postnatal Endocranial Development in Extant Hominoids

By comparing species-specific developmental patterns, we can approach the question of how development shapes adult morphology and contributes to the evolution of novel forms. Studies of evolutionary changes to brain development in primates can provide important clues about the emergence of human cognition, but are hindered by the lack of preserved neural tissue in the fossil record. As a proxy, we study the shape of endocasts, virtual imprints of the endocranial cavity, using 3D geometric morphometrics. We have previously demonstrated that the pattern of endocranial shape development is shared by modern humans, chimpanzees and Neanderthals after the first year of life until adulthood. However, whether this represents a common hominoid mode of development is unknown. Here, we present the first characterization and comparison of ontogenetic endocranial shape changes in a cross-sectional sample of modern humans, chimpanzees, gorillas, orangutans and gibbons. Using developmental simulations, we demonstrate that from late infancy to adulthood ontogenetic trajectories are similar among all hominoid species, but differ in the amount of shape change. Furthermore, we show that during early ontogeny gorillas undergo more pronounced shape changes along this shared trajectory than do chimpanzees, indicative of a dissociation of size and shape change. As shape differences between species are apparent in even our youngest samples, our results indicate that the ontogenetic trajectories of extant hominoids diverged at an earlier stage of ontogeny but subsequently converge following the eruption of the deciduous dentition.

Brief communication: Endocranial volumes in an ontogenetic sample of chimpanzees from the taï forest national park, ivory coast

Ontogenetic samples of endocranial volumes (EVs) from great apes and humans are critical for understanding the evolution of the brain growth pattern in the hominin lineage. However, high quality ontogenetic data are scarce, especially for nonhuman primates. Here, we provide original data derived from an osteological collection of a wild population of Pan troglodytes verus from the Taï Forest National Park, Ivory Coast. This sample is unique, because age, sex, and pedigree information are available for many specimens from behavioral observations in the wild. We scanned crania of all 30 immature specimens and 13 adult individuals using high-resolution computed tomography. We then created virtual casts of the bony braincase (endocasts) to measure EVs. We also measured cranial length, width, and height and attempted to relate cranial distances to EV via regression analysis. Our data are consistent with previous studies. The only neonate in the sample has an EV of 127 cm(3) or 34% of the adult mean. EV increases rapidly during early ontogeny. The average adult EV in this sample is 378.7 ± 30.1 cm(3) . We found sexual dimorphism in adults; males seem to be already larger than females before adult EV is attained. Regressions on cranial width and multiple regression provide better estimates for EV than regressions on cranial length or height. Increasing the sample size and compiling more high quality ontogenetic data of EV will help to reconcile ongoing discussions about the evolution of hominin brain growth.

The evolution of modern human brain shape

The evolutionary process leading to human brain globularity was gradual and paralleled the emergence of behavioral modernity. Modern humans have large and globular brains that distinguish them from their extinct Homo relatives. The characteristic globularity develops during a prenatal and early postnatal period of rapid brain growth critical for neural wiring and cognitive development. However, it remains unknown when and how brain globularity evolved and how it relates to evolutionary brain size increase. On the basis of computed tomographic scans and geometric morphometric analyses, we analyzed endocranial casts of Homo sapiens fossils (N = 20) from different time periods. Our data show that, 300,000 years ago, brain size in early H. sapiens already fell within the range of present-day humans. Brain shape, however, evolved gradually within the H. sapiens lineage, reaching present-day human variation between about 100,000 and 35,000 years ago. This process started only after other key features of craniofacial morphology appeared modern and paralleled the emergence of behavioral modernity as seen from the archeological record. Our findings are consistent with important genetic changes affecting early brain development within the H. sapiens lineage since the origin of the species and before the transition to the Later Stone Age and the Upper Paleolithic that mark full behavioral modernity.