Covariation of the endocranium and splanchnocranium during great ape ontogeny

Abstract

That great ape endocranial shape development persists into adolescence indicates that the splanchnocranium succeeds brain growth in driving endocranial development. However, the extent of this splanchnocranial influence is unknown. We applied two-block partial least squares analyses of Procrustes shape variables on an ontogenetic series of great ape crania to explore the covariation of the endocranium (the internal braincase) and splanchnocranium (face, or viscerocranium). We hypothesized that a transition between brain growth and splanchnocranial development in the establishment of final endocranial form would be manifest as a change in the pattern of shape covariation between early and adolescent ontogeny. Our results revealed a strong pattern of covariation between endocranium and splanchnocranium, indicating that chimpanzees, gorillas, and orangutans share a common tempo and mode of morphological integration from the eruption of the deciduous dentition onwards to adulthood: a reflection of elongating endocranial shape and continuing splanchnocranial prognathism. Within this overarching pattern, we noted that species variation exists in magnitude and direction, and that the covariation between the splanchnocranium and endocranium is somewhat weaker in early infancy compared to successive age groups. When correcting our covariation analyses for allometry, we found that an ontogenetic signal remains, signifying that allometric variation alone is insufficient to account for all endocranial-splanchnocranial developmental integration. Finally, we assessed the influence of the cranial base, which acts as the interface between the face and endocranium, on the shape of the vault using thin-plate spline warping. We found that not all splanchnocranial shape changes during development are tightly integrated with endocranial shape. This suggests that while the developmental expansion of the brain is the main driver of endocranial shape during early ontogeny, endocranial development from infancy onwards is moulded by the splanchnocranium in conjunction with the neurocranium.

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.…”

“…Previous investigations have reported high magnitudes of integration between the basicranium and face throughout ontogeny in humans (Gkantidis & Halazonetis, 2011) and other great apes (Scott, Strauss, Hublin, Gunz, & Neubauer, 2018). Moreover, these previous studies also reported that degrees of integration between the basicranium and face increased throughout ontogeny (Gkantidis & Halazonetis, 2011;Scott et al, 2018). 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).…”

Assessing thoraco‐pelvic covariation in Homo sapiens and Pan troglodytes: A 3D geometric morphometric approach

“…The vast majority of the research on patterns of integration and covariation in hominoids are focused on the skull (e.g., Ackermann, 2002; Bastir, 2008; Bastir et al, 2005; Bookstein et al, 2003; Bruner, Pereira‐Pedro, & Bastir, 2017; Mitteroecker & Bookstein, 2008; Neaux et al, 2018; Profico et al, 2017; Püschel, Friess, & Manríquez, 2020; Scott et al, 2018; Singh, Harvati, Hublin, & Klingenberg, 2012; Stelzer, Gunz, Neubauer, & Spoor, 2018), but studies investigating integration and covariation within and between elements of the torso are scarce (Arlegi et al, 2020; Grabowski et al, 2011; Huseynov et al, 2017; Lewton, 2012; Middleton, 2015; Torres‐Tamayo et al, 2018; C. V. Ward et al, 2015). Among those, Middleton (2015) quantified and compared for the first time trunk relationships between H. sapiens and Pan collecting linear metrics and 3D coordinates on disarticulated trunk skeletal elements.…”

“…Two‐block Partial Least Squares (2B‐PLS) analysis has been revealed as a useful method to statistically assess the covariation between two different sets of original variables, for example, between two sets of shape data (2D or 3D) (Adams & Collyer, 2016; Arlegi et al, 2018; Bastir, Rosas, & Sheets, 2005; Bookstein et al, 2003; Klingenberg & Marugán‐Lobón, 2013; Mitteroecker & Bookstein, 2007; Mitteroecker, Gunz, Neubauer, & Müller, 2012; Neaux et al, 2018; Rohlf & Corti, 2000; Scott, Strauss, Hublin, Gunz, & Neubauer, 2018; Torres‐Tamayo et al, 2018).…”

“…For this purpose, after performing a GPA of the entire landmark configurations, the torso dataset was subdivided into two a priori assumed modules: thorax (block 1) and pelvis (block 2). As 2B‐PLS results depend on the covariance matrix on which the analysis is based (Mitteroecker & Bookstein, 2008), 2B‐PLS analyses were performed based on two approaches in line with Objective 1 and Objective 2 and following Scott et al (2018).…”