Intraspecific variability in human maxillary bone modeling patterns during ontogeny

Abstract

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.

Association between shape changes and bone remodeling patterns in the middle face during ontogeny in South American populations

“…The bone remodeling maps correspond to the extreme individuals along the first PLS axis et al, 1980). In general, the anterior maxilla has a prevalence of resorption at early ages with an increase in deposition among adults (Brachetta-Aporta et al, 2019a, 2019bEnlow & Bang, 1965;Kurihara et al, 1980;Martinez-Maza et al, 2013;Schuh et al, 2020). We found that in the Chubut sample, the extension of resorption across the alveolar process persists into adulthood, which could be related to the high load demands among hunter-gatherers (Brachetta-Aporta et al, 2019a).…”

“…The gray lines represent the consensus and the black lines represent the shapes at the extremes of the first PLS axis. The bone remodeling maps correspond to the extreme individuals along the first PLS axis origin, suggesting that there is a common sequence of bone remodeling changes associated with facial growth in human populations (Enlow & Bang, 1965;McCollum, 2008;Schuh et al, 2020).…”

“…Therefore, the distribution of remodeling activity observed on surfaces is considered to be an important indicator of the growth pattern of craniofacial structures (Bromage, 1982;Enlow & Hans, 1996;O'Higgins & Jones, 1998). Spatial and temporal changes in the activity of osteoclasts and osteoblasts shape cranial growth and development during the ontogeny, resulting in size, and shape differences among individuals and populations (Brachetta-Aporta, Gonzalez, & Bernal, 2019a, 2019bBrachetta-Aporta, Martinez-Maza, Gonzalez, & Bernal, 2014;Freidline, Martinez-Maza, Gunz, & Hublin, 2017;Martínez-Vargas, Muñoz-Muñoz, Martinez-Maza, Molinero, & Ventura, 2017;Schuh et al, 2020).…”

“…The few studies on the maxilla and the zygomatic in adults indicate a higher proportion of formation, with more limited areas of resorption around the insertion of the masseter in the zygomatic and in the canine fossa and the alveolar process of the maxilla (Brachetta-Aporta et al, 2014, 2019aMartinez-Maza et al, 2013). Such differences in the bone remodeling patterns suggest that there are changes in the morphological configuration of the middle face during growth trajectory (Brachetta-Aporta et al, 2019b;Schuh et al, 2020), which in turn would have a key role in population differentiation (Freidline, Gunz, & Hublin, 2015;Gonzalez et al, 2011;Strand Viðarsd ottir et al, 2002).…”

“…To which extent the changes in the remodeling patterns of the middle face are related with morphological changes within and among populations has been scarcely explored (Brachetta-Aporta et al, 2014;Freidline et al, 2017;Martinez-Maza et al, 2013;McCollum, 2008). Recent studies have assessed the association between bone remodeling maps and morphometric variation, although they are limited to the maxilla (Brachetta-Aporta et al, 2019b;Schuh et al, 2020;Schuh, Kupczik, Gunz, Hublin, & Freidline, 2019). In a sample from South America the presence of bone formation was found to be associated with the increase in size throughout ontogeny, and with a greater inferior projection of the maxilla in adults; while bone resorption was associated with an inferior displacement of the bone in subadults (Brachetta-Aporta et al, 2019b).…”