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.

The brains of living humans are about three times larger than those of our closest living relatives, the great apes, and human brains exhibit marked structural differences, notably in areas involved in complex cognitive tasks such as language (1). When and how the characteristic features of the human brain evolved, however, is a matter of ongoing discussion because fossil endocasts—the shapes and sizes of natural or virtual fillings of braincases—can only partially inform about brain anatomy (2, 3). Brain size can be estimated from endocranial size, brain shape from endocranial shape, and external brain structures such as sulci and gyri from their imprints on the endocranial surfaces. Fossil evidence suggests that key features of the brains of living humans, such as expanded cerebral association areas of the inferior frontal and posterior parietal lobes, evolved relatively late (<1.7–1.5 million years ago [Ma]), rather than at the beginnings of our genus Homo at approximately 2.5 Ma (4). The brains of fossil Homo younger than 1.5 Ma therefore were likely structurally similar to those of present-day humans (4). However, our brains and their surrounding braincases are now more rounded in shape (5). Indeed, endocranial globularity in combination with facial retraction is characteristic of Late Pleistocene-to-recent Homo sapiens, but rarely present in earlier fossils (4).Various hypotheses have been proposed to explain how the modern human endocranial morphology evolved and developed after the split from the last common ancestor with our close fossil relatives, the Neanderthals (5–8). Endocranial ontogeny is relatively well documented in Neanderthals, permitting inferences about brain ontogeny. Compared to present-day humans, Neanderthals had similar endocranial sizes at birth, indicating similar neonatal brain sizes. However, Neanderthals had higher postnatal endocranial (and brain) growth rates, resulting, on average, in larger adult brain sizes [but not in earlier completion of brain growth (9)]. Furthermore, tracking Neanderthal endocranial development (i.e., change in shape) from birth to adulthood suggests marked differences in brain development compared to present-day humans, either in utero (10), or during early postnatal life (11).When and how the modern human mode of endocranial and brain ontogeny evolved, however, remains an open question. This is because, on the one hand, the adult endocranial shape of recent humans is markedly different from that of Pleistocene fossil H. sapiens (5, 8); and on the other, because only few immature fossil specimens have been available with which to document endocranial ontogeny in fossil H. sapiens. The difference between fossil and recent adult H. sapiens endocranial shapes has been interpreted as evidence for developmental and structural novelties of the brain that evolved gradually over the past 200 ka (thousand years ago) probably in concert with techno-cultural innovations during the Middle to Upper Paleolithic transition (8).This hypothesis assumes that evolutionary changes in endocranial shape reflect changes in brain shape that were ultimately caused by structural changes in the brain. Endocranial shape does largely represent brain shape (12). However, this does not signify that the brain alone influences endocranial shape. Other external constraints also influence endocranial shape. Overall, evolutionary and developmental changes in endocranial shape are due not only to intrinsic changes in the brain but also to extrinsic factors such as the changing proportions of the neurocranium (the skull region enclosing the brain) relative to the viscerocranium (the face and cranial base) (7, 13). Facial size in members of the H. sapiens species lineage gradually reduced during the past 200–300 ka (14), a period during which techno-cultural changes and changes in subsistence strategy had impacts on facial size and shape as well as on masticatory function (15).Consequently, it is necessary to assess the effects of both viscerocranial and cerebral factors on changes in endocranial size and shape during both ontogeny of fossil H. sapiens and also during the past 200 ka of our evolution. Fortunately, there is now a growing sample of immature and adult fossil H. sapiens with which to investigate these relations. Key among them are the crania of a child (age at death estimated to 6–7 y, based on dental maturation patterns) and an adult from Herto, Ethiopia (14), recovered in archaeological (16) and chronostratigraphic (∼160 ka) contexts that have rendered them crucial referents in discussions about the biological evolution and behavior of early H. sapiens (17, 18). Although well-preserved, both the child (BOU-VP-16/5) and adult (BOU-VP-16/1) from Herto suffered slight but significant prerecovery taphonomic distortion that limited their initial metric characterization. To accurately compare and illuminate the evolutionary and developmental biology of fossil and recent H. sapiens, we employ newly rendered digital restorations of these two crania.We apply an evolutionary developmental approach to compare endocranial and viscerocranial growth and development between fossil and recent H. sapiens and to examine how facial size reduction affected endocranial shape in evolving H. sapiens. The human brain nearly ceases its growth around the age of 5–6 y (19) whereas the face and cranial base continue to grow. This rate transition occurs around the time when the first permanent molars (M1s) fully erupt into functional occlusion. This allows us to test the hypothesis that adult endocranial shape is influenced by viscerocranial (i.e., facial and basicranial) development.Here, we describe and illustrate our stepwise field and laboratory recovery and physical restorations of the two original Herto fossil crania (Fig. 1 and SI Appendix, Figs. S1–S14), as well as the methods used to digitally render and accurately restore them (Fig. 2 and SI Appendix, Figs. S15–S22). We then generate comprehensive metric datasets for comparative uses and apply geometric morphometric methods to quantify endocranial and viscerocranial size and shape of these key specimens. Finally, we compare them with similarly processed child and adult fossils from Skhul and Qafzeh (∼120–100 ka) and a large comparative sample spanning the evolutionary time from early Homo to recent humans.Open in a separate windowFig. 1.Discovery and restoration of the Herto adult (BOU-VP-16/1) and child (BOU-VP-16/5) crania. Adult cranium (A–F). (A) D. DeGusta examines scatter of surface cranial vault fragments of (yellow flags); (then) seasonally abandoned Herto Afar village in background. When occupied, hundreds of domestic ungulates (camels, cows, sheep, goats) cross this surface each day. View is to the west. (B) Tight concentration of cranial vault pieces indicated relatively limited scatter after recent erosional exposure. (C) Indurated sandstone cemented to the right side of the cranium obscures most bone. (D) Removal of sand and sandstone reveals the intact right side of the cranium. (E) The frontal sinus is large, with thin anterior and posterior walls. Even more fragile maxillary, ethmoidal and sphenoid bone is left encased in the hardened sandstone because it cannot be safely cleaned. (F) Right lateral view of the cranium after physical restoration. Child cranium (G–K). (G) B. Asfaw points to fragments of cranial vault. View is to the north, Central Awash Complex in background. (H) Larger cranial vault pieces indicated by yellow arrows. Other surface lag comprises indurated sandstone fragments and artifacts. Wet sieving recovered smaller pieces. (I) Recovered pieces. (J) Refitting. (K) Three-quarter view of the restored specimen. An extended set of photographs documenting the recovery and restoration procedures is provided in SI Appendix, Figs. S1–S14.Open in a separate windowFig. 2.Digital restoration of the Herto crania and their endocasts. Left: Herto adult BOU-VP-16/1. Right: Herto child BOU-VP-16/5. Crania are shown in anterior and lateral views; endocasts in posterior and lateral views. (Scale bar: 5 cm.) Details of the restoration procedure and full sets of the six standard views are provided in SI Appendix, Figs. S15–S22.