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), 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’ bone modelling 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 bone modelling 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.

Methods
Microscopic data on bone modeling patterns are collected from the maxillary bones of each species. Geometric morphometric techniques are used to obtain species-specific average shapes for each age group. Maps based on microscopic data are overlaid onto the species-specific average shapes to visualize bone modeling patterns and corresponding morphological changes during ontogeny. The amount of bone resorption is quantified and compared between species.