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.

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.

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.

Ontogeny of the human maxilla: a study of intra-population variability combining surface bone histology and geometric morphometrics.

Bone modeling is the process by which bone grows in size and models its shape via the cellular activities of the osteoblasts and osteoclasts that respectively form and remove bone. The patterns of expression of these two activities, visible on bone surfaces, are poorly understood during facial ontogeny in Homo sapiens; this is due mainly to small sample sizes and a lack of quantitative data. Furthermore, how microscopic activities are related to the development of morphological features, like the uniquely human-canine fossa, has been rarely explored. We developed novel techniques for quantifying and visualizing variability in bone modeling patterns and applied these methods to the human maxilla to better understand its development at the micro- and macroscopic levels. We used a cross-sectional ontogenetic series of 47 skulls of known calendar age, ranging from birth to 12 years, from a population of European ancestry. Surface histology was employed to record and quantify formation and resorption on the maxilla, and digital maps representing each individual's bone modeling patterns were created. Semilandmark geometric morphometric (GM) methods and multivariate statistics were used to analyze facial growth. Our results demonstrate that surface histology and GM methods give complementary results, and can be used as an integrative approach in ontogenetic studies. The bone modeling patterns specific to our sample are expressed early in ontogeny, and fairly constant through time. Bone resorption varies in the size of its fields, but not in location. Consequently, absence of bone resorption in extinct species with small sample sizes should be interpreted with caution. At the macroscopic level, maxillary growth is predominant in the top half of the bone where bone formation is mostly present. Our results suggest that maxillary growth in humans is highly constrained from early stages in ontogeny, and morphological changes are likely driven by changes in osteoblastic and osteoclastic rates of expression rather than differences in the bone modeling patterns (i.e. changes in location of formation and resorption). Finally, the results of the micro- and macroscopic analyses suggest that the development of the canine fossa results from a combination of bone resorption and bone growth in the surrounding region.