A shared pattern of midfacial bone modelling in hominids suggests deep evolutionary roots for human facial morphogenesis.

Midfacial morphology varies between hominoids, in particular between great apes and humans for which the face is small and retracted. The underlying developmental processes for these morphological differences are still largely unknown. Here, we investigate the cellular mechanism of maxillary development (bone modelling, BM), and how potential changes in this process may have shaped facial evolution. We analysed cross-sectional developmental series of gibbons, orangutans, gorillas, chimpanzees and present-day humans (n = 183). Individuals were organized into five age groups according to their dental development. To visualize each species's BM pattern and corresponding morphology during ontogeny, maps based on microscopic data were mapped onto species-specific age group average shapes obtained using geometric morphometrics. The amount of bone resorption was quantified and compared between species. Great apes share a highly similar BM pattern, whereas gibbons have a distinctive resorption pattern. This suggests a change in cellular activity on the hominid branch. Humans possess most of the great ape pattern, but bone resorption is high in the canine area from birth on, suggesting a key role of canine reduction in facial evolution. We also observed that humans have high levels of bone resorption during childhood, a feature not shared with other apes.

Dental morphology in Homo habilis and its implications for the evolution of early Homo.

The phylogenetic position of Homo habilis is central to debates over the origin and early evolution of the genus Homo. A large portion of the species hypodigm consists of dental remains, but they have only been studied at the often worn enamel surface. We investigate the morphology of the H. habilis enamel-dentine junction (EDJ), which is preserved in cases of moderate tooth wear and known to carry a strong taxonomic signal. Geometric morphometrics is used to characterise dentine crown shape and size across the entire mandibular and maxillary tooth rows, compared with a broad comparative sample (n = 712). We find that EDJ morphology in H. habilis is for the most part remarkably primitive, supporting the hypothesis that the H. habilis hypodigm has more in common with Australopithecus than later Homo. Additionally, the chronologically younger specimen OH 16 displays a suite of derived features; its inclusion in H. habilis leads to excessive levels of variation.

Anatomically modern human in the Châtelperronian hominin collection from the Grotte du Renne (Arcy-sur-Cure, Northeast France).

Around 42,000 years ago, anatomically modern humans appeared in Western Europe to the detriment of indigenous Neanderthal groups. It is during this period that new techno-cultural complexes appear, such as the Châtelperronian that extends from northern Spain to the Paris Basin. The Grotte du Renne (Arcy-sur-Cure) is a key site for discussing the biological identity of its makers. This deposit has yielded several Neanderthal human remains in its Châtelperronian levels. However, the last inventory of the paleoanthropological collection attributed to this techno-complex allowed the identification of an ilium belonging to a neonate (AR-63) whose morphology required a thorough analysis to assess its taxonomic attribution. Using geometric morphometrics, we quantified its morphology and compared it to that of 2 Neanderthals and 32 recent individuals deceased during the perinatal period to explore their morphological variation. Our results indicate a morphological distinction between the ilia of Neanderthals and anatomically modern neonates. Although AR-63 is slightly outside recent variability, it clearly differs from the Neanderthals. We propose that this is due to its belonging to an early modern human lineage whose morphology differs slightly from present-day humans. We also explore different hypotheses about the presence of this anatomically modern neonate ilium among Neanderthal remains.

Mousterian human fossils from El Castillo cave (Puente Viesgo, Cantabria, Spain).

El Castillo cave is a well-known site because of its Paleolithic archaeology and parietal rock art. This paper is focused on the human remains found by V. Cabrera in the Mousterian Unit XX assigned to MIS 4 and early MIS 3. The fossils consist of one upper left second premolar (ULP4), one incomplete proximal hand phalanx, and one partial femoral head. The tooth and the phalanx were assigned to adults, whereas the femoral head belonged to an immature individual due to the absence of fusion traces to the metaphyseal surface. The external morphology and metrical characterization of the Castillo-1466 (ULP4) tooth crown was quantified and compared to the variability of other Neanderthal dental remains and a sample of modern human populations. We also quantified its 3D enamel thickness distribution, its roots morphology, as well as the presence of chipping, and their possible relation to masticatory or paramasticatory activities. Castillo-1466 shows crown dimensions compatible with middle-sized Neanderthal teeth, but with a remarkably thicker enamel than other Neanderthal premolars, such as Marillac 13. The femoral head and the hand phalanx fragment are compared to published values for Neanderthals, although both partial fossils lack diagnostic features precluding any clear taxonomic diagnostic. Therefore, their attribution to Neanderthals is assumed based on the dating of the layers in which they were discovered. El Castillo cave Mousterian fossils represent another contribution to the knowledge of the Middle Paleolithic populations of Northern Spain, where different sites along the Cantabrian mountains yielded several human remains assigned to MIS 4 and early MIS 3.

Early presence of Homo sapiens in Southeast Asia by 86-68 kyr at Tam Pà Ling, Northern Laos.

The timing of the first arrival of Homo sapiens in East Asia from Africa and the degree to which they interbred with or replaced local archaic populations is controversial. Previous discoveries from Tam Pà Ling cave (Laos) identified H. sapiens in Southeast Asia by at least 46 kyr. We report on a recently discovered frontal bone (TPL 6) and tibial fragment (TPL 7) found in the deepest layers of TPL. Bayesian modeling of luminescence dating of sediments and U-series and combined U-series-ESR dating of mammalian teeth reveals a depositional sequence spanning ~86 kyr. TPL 6 confirms the presence of H. sapiens by 70 ± 3 kyr, and TPL 7 extends this range to 77 ± 9 kyr, supporting an early dispersal of H. sapiens into Southeast Asia. Geometric morphometric analyses of TPL 6 suggest descent from a gracile immigrant population rather than evolution from or admixture with local archaic populations.

From fossils to mind.

Fossil endocasts record features of brains from the past: size, shape, vasculature, and gyrification. These data, alongside experimental and comparative evidence, are needed to resolve questions about brain energetics, cognitive specializations, and developmental plasticity. Through the application of interdisciplinary techniques to the fossil record, paleoneurology has been leading major innovations. Neuroimaging is shedding light on fossil brain organization and behaviors. Inferences about the development and physiology of the brains of extinct species can be experimentally investigated through brain organoids and transgenic models based on ancient DNA. Phylogenetic comparative methods integrate data across species and associate genotypes to phenotypes, and brains to behaviors. Meanwhile, fossil and archeological discoveries continuously contribute new knowledge. Through cooperation, the scientific community can accelerate knowledge acquisition. Sharing digitized museum collections improves the availability of rare fossils and artifacts. Comparative neuroanatomical data are available through online databases, along with tools for their measurement and analysis. In the context of these advances, the paleoneurological record provides ample opportunity for future research. Biomedical and ecological sciences can benefit from paleoneurology's approach to understanding the mind as well as its novel research pipelines that establish connections between neuroanatomy, genes and behavior.

Insights into brain evolution through the genotype-phenotype connection.

It has recently become possible to start exploring how the genotype translates into human brain morphology and behavior by combining detailed genomic and phenotypic data from thousands of present-day people with archaic genomes of extinct humans, and gene expression data. As a starting point into this emerging interdisciplinary domain, we highlight current debates about which aspects of the modern human brain are unique. We review recent developments from (1) comparative primate neuroscience-a fast-growing field offering an invaluable framework for understanding general mechanisms and the evolution of human-specific traits. (2) paleoanthropology-based on evidence from endocranial imprints in fossil skulls, we trace the evolution from the ape-like brain phenotype of early hominins more than 3 million years ago to the unusual globular brain shape of present-day people. (3) Genomics of present-day and extinct humans. The morphological and genetic differences between modern humans and our closest extinct cousins, the Neandertals, offer important clues about the genetic underpinnings of brain morphology and behavior. The functional consequences of these genetic differences can be tested in animal models, and brain organoids.

Brain structure and function: a multidisciplinary pipeline to study hominoid brain evolution.

To decipher the evolution of the hominoid brain and its functions, it is essential to conduct comparative studies in primates, including our closest living relatives. However, strong ethical concerns preclude in vivo neuroimaging of great apes. We propose a responsible and multidisciplinary alternative approach that links behavior to brain anatomy in non-human primates from diverse ecological backgrounds. The brains of primates observed in the wild or in captivity are extracted and fixed shortly after natural death, and then studied using advanced MRI neuroimaging and histology to reveal macro- and microstructures. By linking detailed neuroanatomy with observed behavior within and across primate species, our approach provides new perspectives on brain evolution. Combined with endocranial brain imprints extracted from computed tomographic scans of the skulls these data provide a framework for decoding evolutionary changes in hominin fossils. This approach is poised to become a key resource for investigating the evolution and functional differentiation of hominoid brains.

The relevance of late MSA mandibles on the emergence of modern morphology in Northern Africa.

North Africa is a key area for understanding hominin population movements and the expansion of our species. It is home to the earliest currently known Homo sapiens (Jebel Irhoud) and several late Middle Stone Age (MSA) fossils, notably Kébibat, Contrebandiers 1, Dar-es-Soltane II H5 and El Harhoura. Mostly referred to as "Aterian" they fill a gap in the North African fossil record between Jebel Irhoud and Iberomaurusians. We explore morphological continuity in this region by quantifying mandibular shape using 3D (semi)landmark geometric morphometric methods in a comparative framework of late Early and Middle Pleistocene hominins (n = 15), Neanderthals (n = 27) and H. sapiens (n = 145). We discovered a set of mixed features among late MSA fossils that is in line with an accretion of modern traits through time and an ongoing masticatory gracilization process. In Northern Africa, Aterians display similarities to Iberomaurusians and recent humans in the area as well as to the Tighenif and Thomas Quarry hominins, suggesting a greater time depth for regional continuity than previously assumed. The evidence we lay out for a long-term succession of hominins and humans emphasizes North Africa's role as source area of the earliest H. sapiens.

How did modern morphology evolve in the human mandible? The relationship between static adult allometry and mandibular variability in Homo sapiens.

Key to understanding human origins are early Homo sapiens fossils from Jebel Irhoud, as well as from the early Late Pleistocene sites Tabun, Border Cave, Klasies River Mouth, Skhul, and Qafzeh. While their upper facial shape falls within the recent human range of variation, their mandibles display a mosaic morphology. Here we quantify how mandibular shape covaries with mandible size and how static allometry differs between Neanderthals, early H. sapiens, and modern humans from the Upper Paleolithic/Later Stone Age and Holocene (= later H. sapiens). We use 3D (semi)landmark geometric morphometric methods to visualize allometric trends and to explore how gracilization affects the expression of diagnostic shape features. Early H. sapiens were highly variable in mandible size, exhibiting a unique allometric trajectory that explains aspects of their 'archaic' appearance. At the same time, early H. sapiens share a suite of diagnostic features with later H. sapiens that are not related to mandibular sizes, such as an incipient chin and an anteroposteriorly decreasing corpus height. The mandibular morphology, often referred to as 'modern', can partly be explained by gracilization owing to size reduction. Despite distinct static allometric shape changes in each group studied, bicondylar and bigonial breadth represent important structural constraints for the expression of shape features in most Middle to Late Pleistocene hominin mandibles.

Quantifying maxillary development in chimpanzees and humans: An analysis of prognathism and orthognathism at the morphological and microscopic scales.

Facial orientation (projection and degree of prognathism) and form in hominins is highly variable, likely related to evolutionary modifications of the microscopic process of bone modeling (the simultaneous cellular activities of bone formation and resorption) during ontogeny. However, in anteriorly projected faces such as those of early hominins, little is known about the link between bone modeling and facial developmental patterns. Similarly, these aspects have been infrequently investigated in extant great apes. In this study, quantitative methods were applied to a cross-sectional ontogenetic sample of 33 chimpanzees (Pan troglodytes verus) and 59 modern humans (Homo sapiens) to compare the development of maxillary prognathism to orthognathism at both microscopic and macroscopic (or morphological) scales using surface histology and geometric morphometric techniques. Chimpanzees express on average lower amounts of bone resorption than humans on the maxillary periosteum throughout ontogeny; however, the premaxilla is consistently resorbed from early stages on. The presence of bone resorption in the chimpanzee premaxilla, such as that seen in some early hominins, suggests a more ape-like pattern of maxillary bone modeling in these specimens. However, this shows that similarities in bone modeling patterns can lead to variations in shape, suggesting that other aspects of facial growth (such as modifications of rates and timings of development, as well as sutural growth) also played a crucial role in facial evolution.

Intraspecific variability in human maxillary bone modeling patterns during ontogeny.

OBJECTIVES: This study compares the ontogenetic bone modeling patterns of the maxilla to the related morphological changes in three human populations to better understand how morphological variability within a species is established during ontogeny at both micro- and macroscopic levels. MATERIALS AND METHODS: The maxillary bones of an ontogenetic sample of 145 subadult and adult individuals from Greenland (Inuit), Western Europe (France, Germany, and Portugal), and South Africa (Khoekhoe and San) were analyzed. Bone formation and resorption were quantified using histological methods to visualize the bone modeling patterns. In parallel, semilandmark geometric morphometric techniques were used on 3D models of the same individuals to capture the morphological changes. Multivariate statistics were applied and shape differences between age groups were visualized through heat maps. RESULTS: The three populations show differences in the degree of shape change acquired during ontogeny, leading to divergences in the developmental trajectories. Only subtle population differences in the bone modeling patterns were found, which were maintained throughout ontogeny. Bone resorption in adults mirrors the pattern found in subadults, but is expressed at lower intensities. DISCUSSION: Our data demonstrate that maxillary morphological differences observed in three geographically distinct human populations are also reflected at the microscopic scale. However, we suggest that these differences are mostly driven by changes in rates and timings of the cellular activities, as only slight discrepancies in the location of bone resorption could be observed. The shared general bone modeling pattern is likely characteristic of all Homo sapiens, and can be observed throughout ontogeny.

Distinct mandibular premolar crown morphology in Homo naledi and its implications for the evolution of Homo species in southern Africa.

Homo naledi displays a combination of features across the skeleton not found in any other hominin taxon, which has hindered attempts to determine its placement within the hominin clade. Using geometric morphometrics, we assess the morphology of the mandibular premolars of the species at the enamel-dentine junction (EDJ). Comparing with specimens of Paranthropus, Australopithecus and Homo (n = 97), we find that the H. naledi premolars from the Dinaledi chamber consistently display a suite of traits (e.g., tall crown, well-developed P3 and P4 metaconid, strongly developed P3 mesial marginal ridge, and a P3 > P4 size relationship) that distinguish them from known hominin groups. Premolars from a second locality, the Lesedi Chamber, are consistent with this morphology. We also find that two specimens from South Africa, SK 96 (usually attributed to Paranthropus) and Stw 80 (Homo sp.), show similarities to the species, and we discuss a potential evolutionary link between H. naledi and hominins from Sterkfontein and Swartkrans.

Ontogenetic changes of diploic channels in modern humans.

OBJECTIVES: The diploic channels are bony passages of veins, running within frontal, parietal, and occipital bones. In this study, we investigate ontogenetic changes of these channels in a sample of nonadult and adult modern humans. MATERIALS AND METHODS: Using computed tomography scans of dried crania, we provide quantitative comparisons of lumen size, branch length, volume, and vascular asymmetries, and correlations with age, cranial size, and bone thickness. RESULTS: The vascular system displays progressive but nonlinear changes throughout ontogeny, becoming even more complex with adulthood. Vascular variables are significantly different in frontal, parietal, and occipital bones for most of the postnatal ontogeny. Diploic channels of the left and right sides are developed similarly. Vascular variables display a nonlinear association with age and cranial size in modern humans. Cranial bone thickness is shown to be a major determinant of lumen size, branch length, and volume. CONCLUSIONS: A previous radiographic survey suggested that diploic channels are more developed in adult modern humans than in nonadults. Recent advances in digital anatomy have been used in this study to investigate this craniovascular structure. The complexity of the channels increases during development, with a noticeable boost in adults. Taking into account the potential metabolic differences and constraints associated with modern human brain size and shape, the vascular differences found might be related to endocranial thermoregulation.

Australopithecus afarensis endocasts suggest ape-like brain organization and prolonged brain growth.

Human brains are three times larger, are organized differently, and mature for a longer period of time than those of our closest living relatives, the chimpanzees. Together, these characteristics are important for human cognition and social behavior, but their evolutionary origins remain unclear. To study brain growth and organization in the hominin species Australopithecus afarensis more than 3 million years ago, we scanned eight fossil crania using conventional and synchrotron computed tomography. We inferred key features of brain organization from endocranial imprints and explored the pattern of brain growth by combining new endocranial volume estimates with narrow age at death estimates for two infants. Contrary to previous claims, sulcal imprints reveal an ape-like brain organization and no features derived toward humans. A comparison of infant to adult endocranial volumes indicates protracted brain growth in A. afarensis, likely critical for the evolution of a long period of childhood learning in hominins.

A morphometric comparison of the parietal lobe in modern humans and Neanderthals.

The modern human brain and braincase have a characteristic globular shape including parietal and cerebellar bulging. In contrast, Neanderthals, although having similar endocranial volume, displayed more elongated endocrania with flatter parietal and cerebellar regions. Based on endocranial imprints, we compare the parietal lobe morphology of modern humans and Neanderthals, as this brain region is central to several cognitive functions including tool use and visual imaging. In paleoneurology, shape analyses of endocasts are based either on anatomical landmarks that represent endocranial surface features homologous to cortical convolutions (impressions of brain gyri and sulci) or on dense meshes of semilandmarks that capture overall endocranial shape. Previous analyses using the former suggested that modern humans have relatively longer and taller parietal lobes than extinct human species, while the latter emphasized parietal bulging without a significant size difference of parietal regions. In the present study, we combine both anatomical landmarks and surface semilandmarks to investigate the morphological differences of the parietal lobes between modern humans and Neanderthals. Despite limitations by landmark uncertainty, our analyses were able to detect and confirm average different parietal shapes, with modern humans displaying taller and anteroposteriorly extended parietal lobes. We also show mean size differences, with modern humans displaying slightly larger surface areas on the dorsal posterior parietal region, and on a lateral region comprising the supramarginal gyrus, angular gyrus, and intraparietal sulcus. While we observed average differences in the parietal form between the two species, their ranges of distribution overlap, indicating the differences could be a matter of degree. Thus, further analyses on intraspecific variation in parietal lobe morphology within modern human brains should help understand the differences between globular and elongated endocrania. This is crucial because changes to the parietal cortex might affect associative and integrative functions between somatic and visual primary inputs.

Evolution of brain lateralization: A shared hominid pattern of endocranial asymmetry is much more variable in humans than in great apes.

Brain lateralization is commonly interpreted as crucial for human brain function and cognition. However, as comparative studies among primates are rare, it is not known which aspects of lateralization are really uniquely human. Here, we quantify both pattern and magnitude of brain shape asymmetry based on endocranial imprints of the braincase in humans, chimpanzees, gorillas, and orangutans. Like previous studies, we found that humans were more asymmetric than chimpanzees, however so were gorillas and orangutans, highlighting the need to broaden the comparative framework for interpretation. We found that the average spatial asymmetry pattern, previously considered to be uniquely human, was shared among humans and apes. In humans, however, it was less directed, and different local asymmetries were less correlated. We, thus, found human asymmetry to be much more variable compared with that of apes. These findings likely reflect increased functional and developmental modularization of the human brain.

Skull reconstruction of the late Miocene ape Rudapithecus hungaricus from Rudabánya, Hungary.

We report on a computer-based reconstruction of a well-preserved ape skull from late Miocene deposits in Rudabánya, Hungary. Based on micro-computed tomographic scans of the original Rudapithecus hungaricus partial cranium RUD 200 and the associated mandible RUD 212 we realign displaced bone fragments, and reconstruct the shape of the upper and lower jaws guided by occlusal fingerprint analysis of dental wear patterns. We apply geometric morphometric methods based on several hundred landmarks and sliding semilandmarks to estimate missing data, and create multiple reconstructions of the specimen. We then compare the reconstructed overall cranial shape, as well as the volume and shape of the endocast, with extant primates. Multiple reconstructions of RUD 200 yield an average endocranial volume of 234 cc (S.D.: 9 cc; range: 221-247 cc). RUD 200 is most similar to African apes in overall cranial shape, but in a statistical analysis of endocranial shape the specimen falls closest to extant hylobatids. Our data suggest that R. hungaricus from the late Miocene in Europe displays aspects of the overall cranial geometry typical of extant African great apes, but it does not show an evolutionary reorganization of the brain evident in Pan, Gorilla, and Pongo.

Endostructural morphology in hominoid mandibular third premolars: Discrete traits at the enamel-dentine junction.

The mandibular third premolar (P3) exhibits substantial differences in size and shape among hominoid taxa, and displays a number of discrete traits that have proven to be useful in studies of hominin taxonomy and phylogeny. Discrete traits at the enamel-dentine junction (EDJ) can be accurately assessed on moderately worn specimens, and often appear sharper than at the outer-enamel surface (OES). Here we use microtomography to image the P3 EDJ of a broad sample of extant apes, extinct hominins and modern humans (n = 100). We present typologies for three important premolar discrete traits at the EDJ (transverse crest, marginal ridge and buccal grooves), and score trait frequencies within our sample. We find that the transverse crest is variable in extant apes, while the majority of hominins display a transverse crest which runs directly between the two major premolar cusps. Some Neanderthals display a unique form in which the transverse crest fails to reach the protoconid. We find that mesial marginal ridge discontinuity is common in Australopithecus anamensis and Australopithecus afarensis while continuous marginal ridges largely characterize Australopithecus africanus and Paranthropus. Interrupted mesial and distal marginal ridges are again seen in Homo sapiens and Neanderthals. Premolar buccal grooves, previously identified at the OES as important for hominin systematics, are again found to show a number of taxon-specific patterns at the EDJ, including a clear difference between Australopithecus and Paranthropus specimens. However, their appearance may be dependent on the morphology of other parts of the crown such as the protoconid crest, and the presence of accessory dentine horns. Finally, we discuss rare variations in the form of dentine horns that underlie premolar cusps, and their potential homology to similar morphologies in other tooth positions.