The endocast morphology of LES1, Homo naledi.

OBJECTIVES: Homo naledi is near the extreme of small brain size within Homo but is easily recognized as Homo in other aspects of endocast morphology. This study adds new evidence of the endocast morphology of H. naledi by describing the Lesedi Hominin 1 (LES1) endocranium from the Lesedi Chamber and compares it to the previously known H. naledi individual Dinaledi Hominin 3 (DH3) as well as other hominin taxa. MATERIALS AND METHODS: We examined interlandmark distances with both univariate and multivariate methods in multiple hominin taxa and both species of Pan. For each distance, we compared groups using adjusted Z-scores (Azs). Our multivariate analyses included both principal component analyses (PCA) and linear discriminant analyses (LDA). RESULTS: DH3 and LES1 each have absolute third frontal convolution measures that enter the upper half of the variation for Homo sapiens, Homo erectus, and Homo neanderthalensis. Examined relative to the cube root of endocranial volume, H. naledi ranks among the highest values in these samples of Homo. Both absolute and relative values for H. naledi specimens are far above Pan, Australopithecus, and Paranthropus, suggesting an expanded Broca's area. CONCLUSIONS: Both qualitative and quantitative analyses show consistency between LES1 and other H. naledi endocasts and confirm the shared morphology of H. naledi with H. sapiens, H. neanderthalensis, and some specimens of H. erectus.

Co-occurrence of Acheulian and Oldowan artifacts with Homo erectus cranial fossils from Gona, Afar, Ethiopia.

Although stone tools generally co-occur with early members of the genus Homo, they are rarely found in direct association with hominins. We report that both Acheulian and Oldowan artifacts and Homo erectus crania were found in close association at 1.26 million years (Ma) ago at Busidima North (BSN12), and ca. 1.6 to 1.5 Ma ago at Dana Aoule North (DAN5) archaeological sites at Gona, Afar, Ethiopia. The BSN12 partial cranium is robust and large, while the DAN5 cranium is smaller and more gracile, suggesting that H. erectus was probably a sexually dimorphic species. The evidence from Gona shows behavioral diversity and flexibility with a lengthy and concurrent use of both stone technologies by H. erectus, confounding a simple "single species/single technology" view of early Homo.

Endocast morphology of Homo naledi from the Dinaledi Chamber, South Africa.

Hominin cranial remains from the Dinaledi Chamber, South Africa, represent multiple individuals of the species Homo naledi This species exhibits a small endocranial volume comparable to Australopithecus, combined with several aspects of external cranial anatomy similar to larger-brained species of Homo such as Homo habilis and Homo erectus Here, we describe the endocast anatomy of this recently discovered species. Despite the small size of the H. naledi endocasts, they share several aspects of structure in common with other species of Homo, not found in other hominins or great apes, notably in the organization of the inferior frontal and lateral orbital gyri. The presence of such structural innovations in a small-brained hominin may have relevance to behavioral evolution within the genus Homo.

A neurochemical hypothesis for the origin of hominids.

It has always been difficult to account for the evolution of certain human characters such as language, empathy, and altruism via individual reproductive success. However, the striatum, a subcortical region originally thought to be exclusively motor, is now known to contribute to social behaviors and "personality styles" that may link such complexities with natural selection. We here report that the human striatum exhibits a unique neurochemical profile that differs dramatically from those of other primates. The human signature of elevated striatal dopamine, serotonin, and neuropeptide Y, coupled with lowered acetylcholine, systematically favors externally driven behavior and greatly amplifies sensitivity to social cues that promote social conformity, empathy, and altruism. We propose that selection induced an initial form of this profile in early hominids, which increased their affiliative behavior, and that this shift either preceded or accompanied the adoption of bipedality and elimination of the sectorial canine. We further hypothesize that these changes were critical for increased individual fitness and promoted the adoption of social monogamy, which progressively increased cooperation as well as a dependence on tradition-based cultural transmission. These eventually facilitated the acquisition of language by elevating the reproductive advantage afforded those most sensitive to social cues.

Brain enlargement and dental reduction were not linked in hominin evolution.

The large brain and small postcanine teeth of modern humans are among our most distinctive features, and trends in their evolution are well studied within the hominin clade. Classic accounts hypothesize that larger brains and smaller teeth coevolved because behavioral changes associated with increased brain size allowed a subsequent dental reduction. However, recent studies have found mismatches between trends in brain enlargement and posterior tooth size reduction in some hominin species. We use a multiple-variance Brownian motion approach in association with evolutionary simulations to measure the tempo and mode of the evolution of endocranial and dental size and shape within the hominin clade. We show that hominin postcanine teeth have evolved at a relatively consistent neutral rate, whereas brain size evolved at comparatively more heterogeneous rates that cannot be explained by a neutral model, with rapid pulses in the branches leading to later Homo species. Brain reorganization shows evidence of elevated rates only much later in hominin evolution, suggesting that fast-evolving traits such as the acquisition of a globular shape may be the result of direct or indirect selection for functional or structural traits typical of modern humans.

The endocast of the one-million-year-old human cranium from Buia (UA 31), Danakil Eritrea.

OBJECTIVES: The Homo erectus-like cranium from Buia (UA 31) was found in the Eritrean Danakil depression and dated to 1 million years. Its outer morphology displays archaic traits, as well as distinctive and derived characters. The present study provides the description and metric comparison of its endocranial anatomy. MATERIALS AND METHODS: UA 31 was originally filled by a diffuse concretion. Following its removal and cleaning, the endocast (995 cc) was reconstructed after physical molding and digital scan. Its morphology is here compared with specimens belonging to different human taxa, taking into account endocranial metrics, cortical traits, and craniovascular features. RESULTS: The endocast is long and narrow when compared to the H. erectus/ergaster hypodigm, although its proportions are compatible with the morphology displayed by all archaic and medium-brained human species. The occipital areas display a pronounced bulging, the cerebellum is located in a posterior position, and the middle meningeal vessels are more developed in the posterior regions. These features are common among specimens attributed to H. erectus s.l., particularly the Middle Pleistocene endocasts from Zhoukoudian. The parietal lobes are markedly bossed. This lateral bulging is associated with the lower parietal circumvolutions, as in other archaic specimens. This pronounced parietal curvature is apparently due to a narrow cranial base, more than to wider parietal areas. CONCLUSIONS: The endocast of UA 31 shows a general plesiomorphic phenotype, with some individual features (e.g., dolichocephaly and rounded lower parietal areas) which confirm a remarkable degree of morphological variability within the H. erectus/ergaster hypodigm. Am J Phys Anthropol 160:458-468, 2016. © 2016 Wiley Periodicals, Inc.

Levantine cranium from Manot Cave (Israel) foreshadows the first European modern humans.

A key event in human evolution is the expansion of modern humans of African origin across Eurasia between 60 and 40 thousand years (kyr) before present (bp), replacing all other forms of hominins. Owing to the scarcity of human fossils from this period, these ancestors of all present-day non-African modern populations remain largely enigmatic. Here we describe a partial calvaria, recently discovered at Manot Cave (Western Galilee, Israel) and dated to 54.7 ± 5.5 kyr bp (arithmetic mean ± 2 standard deviations) by uranium-thorium dating, that sheds light on this crucial event. The overall shape and discrete morphological features of the Manot 1 calvaria demonstrate that this partial skull is unequivocally modern. It is similar in shape to recent African skulls as well as to European skulls from the Upper Palaeolithic period, but different from most other early anatomically modern humans in the Levant. This suggests that the Manot people could be closely related to the first modern humans who later successfully colonized Europe. Thus, the anatomical features used to support the 'assimilation model' in Europe might not have been inherited from European Neanderthals, but rather from earlier Levantine populations. Moreover, at present, Manot 1 is the only modern human specimen to provide evidence that during the Middle to Upper Palaeolithic interface, both modern humans and Neanderthals contemporaneously inhabited the southern Levant, close in time to the likely interbreeding event with Neanderthals.

New high-resolution computed tomography data of the Taung partial cranium and endocast and their bearing on metopism and hominin brain evolution.

Falk and colleagues [Falk D, Zollikofer CP, Morimoto N, Ponce de León MS (2012) Proc Natl Acad Sci U S A 109(22):8467-8470] hypothesized that selective pressures favored late persistence of a metopic suture and open anterior fontanelle early in hominin evolution, and they put an emphasis on the Taung Child (Australopithecus africanus) as evidence for the antiquity of these adaptive features. They suggested three mutually nonexclusive pressures: an "obstetric dilemma," high early postnatal brain growth rates, and neural reorganization in the frontal cortex. To test this hypothesis, we obtained the first high-resolution computed tomography (CT) data from the Taung hominin. These high-resolution image data and an examination of the hominin fossil record do not support the metopic and fontanelle features proposed by Falk and colleagues. Although a possible remnant of the metopic suture is observed in the nasion-glabella region of the Taung partial cranium (but not along the frontal crest), this character state is incongruent with the zipper model of metopic closure described by Falk and colleagues. Nor do chimpanzee and bonobo endocast data support the assertion that delayed metopic closure in Taung is necessary because of widening (reorganization) of the prefrontal or frontal cortex. These results call into question the adaptive value of delaying metopic closure, and particularly its antiquity in hominin evolution. Further data from hominoids and hominins are required to support the proposed adaptive arguments, particularly an obstetric dilemma placing constraints on neural and cranial development in Australopithecus.

Variations in size, shape and asymmetries of the third frontal convolution in hominids: paleoneurological implications for hominin evolution and the origin of language.

The study of brain structural asymmetries as anatomical substrates of functional asymmetries in extant humans, great apes, and fossil hominins is of major importance in understanding the structural basis of modern human cognition. We propose methods to quantify the variation in size, shape and bilateral asymmetries of the third frontal convolution (or posterior inferior frontal gyrus) among recent modern humans, bonobos and chimpanzees, and fossil hominins using actual and virtual endocasts. These methodological improvements are necessary to extend previous qualitative studies of these features. We demonstrate both an absolute and relative bilateral increase in the size of the third frontal convolution in width and length between Pan species, as well as in hominins. We also observed a global bilateral increase in the size of the third frontal convolution across all species during hominin evolution, but also non-allometric intra-group variations independent of brain size within the fossil samples. Finally, our results show that the commonly accepted leftward asymmetry of Broca's cap is biased by qualitative observation of individual specimens. The trend during hominin evolution seems to be a reduction in size on the left compared with the right side, and also a clearer definition of the area. The third frontal convolution considered as a whole projects more laterally and antero-posteriorly in the right hemisphere. As a result, the left 'Broca's cap' looks more globular and better defined. Our results also suggest that the pattern of brain asymmetries is similar between Pan paniscus and hominins, leaving the gradient of the degree of asymmetry as the only relevant structural parameter. As the anatomical substrate related to brain asymmetry has been present since the appearance of the hominin lineage, it is not possible to prove a direct relationship between the extent of variations in the size, shape, and asymmetries of the third frontal convolution and the origin of language in hominins.

Frontal brain expansion during development using MRI and endocasts: relation to microcephaly and Homo floresiensis.

A major hall of hominid brain evolution is an expansion of the frontal lobes. To determine if a similar trajectory occurs during modern human development, the MRI scans of 118 living infants, children, and adolescents were reviewed and three specific measurements obtained: frontal width (FW), maximal cerebral width (MW), and maximal cerebral length (ML). The infantile brain is uniformly wide but relatively short, with near equal FW and MW. The juvenile brain exhibits a wider MW than FW, while FW of the adolescent brain expands to nearly equal MW, concurrent with an increase in ML. The preferential frontal lobe expansion during modern human development parallels that observed during the evolution of Homo. In 17 microcephalic individuals, only 6 (35%) exhibited preferential frontal lobe hypoplasia, presumably a reflection of multiple etiologies that adversely affect differing brain regions. Compared to 79 modern human adult endocasts and 12 modern microcephalic endocasts, LB1 (Homo floresiensis) clustered more consistently with the microcephalic sample than with the normocephalic sample.

Language and tool making are similar cognitive processes.

Design features for language and stone toolmaking (not tool use) involve similar if not homologous cognitive processes. Both are arbitrary transformations of internal "intrinsic" symbolization, whereas non-human tool using is mostly an iconic transformation. The major discontinuity between humans and non-humans (chimpanzees) is language. The presence of stone tools made to standardized patterns suggests communicative and social control skills that involved language.

Variations and asymmetries in regional brain surface in the genus Homo.

Paleoneurology is an important field of research within human evolution studies. Variations in size and shape of an endocast help to differentiate among fossil hominin species whereas endocranial asymmetries are related to behavior and cognitive function. Here we analyse variations of the surface of the frontal, parieto-temporal and occipital lobes among different species of Homo, including 39 fossil hominins, ten fossil anatomically modern Homo sapiens and 100 endocasts of extant modern humans. We also test for the possible asymmetries of these features in a large sample of modern humans and observe individual particularities in the fossil specimens. This study contributes important new information about the brain evolution in the genus Homo. Our results show that the general pattern of surface asymmetry for the different regional brain surfaces in fossil species of Homo does not seem to be different from the pattern described in a large sample of anatomically modern H. sapiens, i.e., the right hemisphere has a larger surface than the left, as do the right frontal, the right parieto-temporal and the left occipital lobes compared with the contra-lateral side. It also appears that Asian Homo erectus specimens are discriminated from all other samples of Homo, including African and Georgian specimens that are also sometimes included in that taxon. The Asian fossils show a significantly smaller relative size of the parietal and temporal lobes. Neandertals and anatomically modern H. sapiens, who share the largest endocranial volume of all hominins, show differences when considering the relative contribution of the frontal, parieto-temporal and occipital lobes. These results illustrate an original variation in the pattern of brain organization in hominins independent of variations in total size. The globularization of the brain and the enlargement of the parietal lobes could be considered derived features observed uniquely in anatomically modern H. sapiens.

Technical note: the midline and endocranial volume of the Taung endocast.

The Taung endocast is one of the best-preserved and most important known in paleoanthropology. Although the endocast is undistorted and preserves distinctive landmarks, Taung has proved a difficult endocast, because it is only about 60% complete. To reconstruct Taung it is necessary to first use the available anatomical landmarks to define the midline of the endocast. It is only with a proper description of the midline that it is possible to reconstruct the endocast and obtain an accurate measurement of Taung's endocranial volume. Holloway (Science 168 (1970) 966-968) determined a conservative estimate for Taung of 404 ml. More recently this estimate has been revised downward by Falk and Clarke (Am J Phys Anthropol 134 (2007) 529-534) to 382 ml, giving Taung the smallest endocast for A. africanus. Certain challenges exist with the reconstruction of any endocast, particularly a hemi-endocast such as Taung. A virtual reconstruction of Taung must assume perfect symmetry, a feature called into question here in Taung's most recent reconstruction by Falk and Clarke (2007). Holloway's (1970) reconstruction of Taung provides a guidepost for a conservative approach to endocast reconstructions, and the most reliable measurement of Taung's true endocranial volume.

Craniometric ratios of microcephaly and LB1, Homo floresiensis, using MRI and endocasts.

The designation of Homo floresiensis as a new species derived from an ancient population is controversial, because the type specimen, LB1, might represent a pathological microcephalic modern Homo sapiens. Accordingly, two specific craniometric ratios (relative frontal breadth and cerebellar protrusion) were ascertained in 21 microcephalic infants and children by using MRI. Data on 118 age-equivalent control (normocephalic) subjects were collected for comparative purposes. In addition, the same craniometric ratios were determined on the endocasts of 10 microcephalic individuals, 79 normal controls (anatomically modern humans), and 17 Homo erectus specimens. These ratios were then compared with those of two LB1 endocasts. The findings showed that the calculated cerebral/cerebellar ratios of the LB1 endocast [Falk D, et al. (2007) Proc Natl Acad Sci USA 104:2513-2518] fall outside the range of living normocephalic individuals. The ratios derived from two LB1 endocasts also fall largely outside the range of modern normal human and H. erectus endocasts and within the range of microcephalic endocasts. The findings support but do not prove the contention that LB1 represents a pathological microcephalic Homo sapiens rather than a new species, (i.e., H. floresiensis).

A new brain endocast of Homo erectus from Hulu Cave, Nanjing, China.

A new brain endocast of Homo erectus from Hulu Cave, Tangshan, Nanjing is described and compared with a broad sample of endocasts of H. erectus, Neanderthals, and recent modern humans. The Nanjing 1 endocast is reconstructed based on two portions of endocranial casts taken from the original fossil fragments. The fossil was discovered in 1993, near Nanjing, South China and is dated to ∼ 0.58-0.62 Ma. The cranial capacity is ∼ 876 cc, as determined by endocast water displacement. There are some common features of Nanjing 1 and other H. erectus endocasts that differentiate them from the Neanderthals and modern humans in our sample. These include small cranial capacity, low height dimensions, simple middle meningeal vessel patterns, a high degree of cerebral-over-cerebellar lobe overhang, elongated and quite separated cerebellar lobes, and a narrow, low, short and flat frontal region. Some features are found to vary among H. erectus, Neanderthals and modern humans, such as the lateral Sylvian fissure position and the venous sinus and petalial patterns. The Nanjing 1 endocast has unique, large, superior frontal convolutions, and strongly protruding Broca's caps. In contrast to other Chinese H. erectus from Hexian and Zhoukoudian, Nanjing 1 lacks strong posterior projection of the occipital lobes. Bivariate and principal component analyses indicate that the small volume and shape of Nanjing 1 is most similar to KNM-WT 15000, KNM-ER 3883, Sangiran 2 and Hexian, illustrating the combination of narrow, low, and short frontal lobes with wide posterior lobes.

A bivariate approach to the widening of the frontal lobes in the genus Homo.

Within the genus Homo, the most encephalized taxa (Neandertals and modern humans) show relatively wider frontal lobes than either Homo erectus or australopithecines. The present analysis considers whether these changes are associated with a single size-based or allometric pattern (positive allometry of the width of the anterior endocranial fossa) or with a more specific and non-allometric pattern. The relationship between hemispheric length, maximum endocranial width, and frontal width at Broca's area was investigated in extant and extinct humans. Our results do not support positive allometry for the frontal lobe's width in relation to the main endocranial diameters within modern humans (Homo sapiens). Also, the correlation between frontal width and hemispheric length is lower than the correlation between frontal width and parieto-temporal width. When compared with the australopithecines, the genus Homo could have experienced a non-allometric widening of the brain at the temporo-parietal areas, which is most evident in Neandertals. Modern humans and Neandertals also display a non-allometric widening of the anterior endocranial fossa at the Broca's cap when compared with early hominids, again more prominent in the latter group. Taking into account the contrast between the intra-specific patterns and the between-species differences, the relative widening of the anterior fossa can be interpreted as a definite evolutionary character instead of a passive consequence of brain size increase. This expansion is most likely associated with correspondent increments of the underlying neural mass, or at least with a geometrical reallocation of the frontal cortical volumes. Although different structural changes of the cranial architecture can be related to such variations, the widening of the frontal areas is nonetheless particularly interesting when some neural functions (like language or working memory, decision processing, etc.) and related fronto-parietal cortico-cortical connections are taken into account.

Validation of plaster endocast morphology through 3D CT image analysis.

A crucial component of research on brain evolution has been the comparison of fossil endocranial surfaces with modern human and primate endocrania. The latter have generally been obtained by creating endocasts out of rubber latex shells filled with plaster. The extent to which the method of production introduces errors in endocast replicas is unknown. We demonstrate a powerful method of comparing complex shapes in 3-dimensions (3D) that is broadly applicable to a wide range of paleoanthropological questions. Pairs of virtual endocasts (VEs) created from high-resolution CT scans of corresponding latex/plaster endocasts and their associated crania were rigidly registered (aligned) in 3D space for two Homo sapiens and two Pan troglodytes specimens. Distances between each cranial VE and its corresponding latex/plaster VE were then mapped on a voxel-by-voxel basis. The results show that between 79.7% and 91.0% of the voxels in the four latex/plaster VEs are within 2 mm of their corresponding cranial VEs surfaces. The average error is relatively small, and variation in the pattern of error across the surfaces appears to be generally random overall. However, inferior areas around the cranial base and the temporal poles were somewhat overestimated in both human and chimpanzee specimens, and the area overlaying Broca's area in humans was somewhat underestimated. This study gives an idea of the size of possible error inherent in latex/plaster endocasts, indicating the level of confidence we can have with studies relying on comparisons between them and, e.g., hominid fossil endocasts.