Morphological integration affects the evolution of midline cranial base, lateral basicranium, and face across primates

Abstract

Objectives: The basicranium and face are two integrated bony structures displaying great morphological diversity across primates. Previous studies in hominids determined that the basicranium is composed of two independent modules: the midline basicranium, mostly influenced by brain size, and the lateral basicranium, predominantly associated with facial shape. To better assess how morphological integration impacts the evolution of primate cranial shape diversity, we test to determine whether the relationships found in hominids are retained across the order.Materials and methods: Three-dimensional landmarks (29) were placed on 143 computed tomography scans of six major clades of extant primate crania. We assessed the covariation between midline basicranium, lateral basicranium, face, and endocranial volume using phylogenetically informed partial least squares analyses and phylogenetic generalized least squares models.Results: We found significant integration between lateral basicranium and face and between midline basicranium and face. We also described a significant correlation between midline basicranium and endocranial volume but not between lateral basicranium and endocranial volume.Discussion: Our findings demonstrate a significant and pervasive integration in the craniofacial structures across primates, differing from previous results in hominids.The uniqueness of module organization in hominids may explain this distinction. We found that endocranial volume is significantly integrated to the midline basicranium but not to the lateral basicranium. This finding underlines the significant effect of brain size on the shape of the midline structures of the cranial base in primates. With the covariations linking the studied features defined here, we suggest that future studies should focus on determining the causal links between them.K E Y W O R D S endocranium, geometric morphometrics, modularity, skull

Ontogenetic changes in magnitudes of integration in the macaque skull

“…However, the results in the present study only partially corresponded to these previous studies, as the magnitude of integration in the chondrocranium/face complex was significantly higher than for the skull as a whole in juvenile groups (p < .001), but not in adults (U = 500,530, p = .9675; Table S1). One possible reason for the discrepancy between the present and previous investigations is that some studies were performed on endocranial morphology of the basicranium/face complex (Gkantidis & Halazonetis, 2011;Lieberman, Pearson, et al, 2000;Lieberman, Ross, et al, 2000;Neaux, 2017;Neaux et al, 2018;Neaux, Guy, Gilissen, Coudyzer, & Ducrocq, 2013;Neaux, Wroe, Ledogar, Heins Ledogar, & Sansalone, 2019;Scott et al, 2018). Nevertheless, our results likely indicate that the chondrocranium/face complex is not as tightly integrated in adults as it is in juveniles.…”

“…However, our results for adults differ from those of Shirai and Marroig (2010), as the magnitude of integration in the chondrocranium was similar in magnitude to the vault/chondrocranium complex, and higher in magnitude than the chondrocranium/face complex (Figure 3). These results indicate that the chondrocranium module of juveniles (but not adults) requires a lower magnitude of integration for more coordination with adjacent soft tissue (i.e., brain) or other cranial regions in early ontogenetic stages because the chondrocranium serves as a platform for development and growth of the brain (Lieberman, 2011; Neaux et al, 2018; Neaux et al, 2019; Neubauer et al, 2009). For instance, Neaux et al (2019) reported that there was significant morphological integration between the midline basicranium and endocranial volume across primates, which may indicate a significant effect of brain size on the shape of midline morphology in the cranial base.…”

Selection for increased tibia length in mice alters skull shape through parallel changes in developmental mechanisms

“…The exact ontogenetic mechanism by which the observed cranial base changes may lead to shape change across the entire cranium in Longshanks remains to be elucidated. There is extensive evidence for strong phenotypic covariation among cranial traits (i.e., morphological integration) causing indirect change throughout the cranium (Bookstein et al, 2003;Goswami, 2006;Goswami et al, 2012;Singh et al, 2012;Bastir and Rosas, 2016;Neaux, 2016;Neaux et al, 2019). For example, direct basicranium perturbations by genetic mutations in mice generated predictable shape changes throughout the cranium (Parsons et al, 2015).…”

Morphological consequences of artificial cranial deformation: Modularity and integration

“…Based on a similar criterion [32], the latter has been also divided in two additional regions: i.e. the basicranium with endochondral ossification from a cartilaginous mesodermic precursor (chondrocranium) [3, [33][34][35][36][37], and the calvaria whose bones derive from the desmocranium, which has an intramembranous ossification from paraxial mesoderm and neural crests cells [38]. In fact, different studies have shown that the patterns of covariation and correlation between different parts of the cranium are partially independent, thus suggesting that they behave as partially independent units [15,[39][40][41][42].…”