Morphometric Variation at Different Spatial Scales: Coordination and Compensation in the Emergence of Organismal Form

Abstract

It is a classic aim of quantitative and evolutionary biology to infer genetic architecture and potential evolutionary responses to selection from the variance–covariance structure of measured traits. But a meaningful genetic or developmental interpretation of raw covariances is difficult, and classic concepts of morphological integration do not directly apply to modern morphometric data. Here, we present a new morphometric strategy based on the comparison of morphological variation across different spatial scales. If anatomical elements vary completely independently, then their variance accumulates at larger scales or for structures composed of multiple elements: morphological variance would be a power function of spatial scale. Deviations from this pattern of “variational self-similarity” (serving as a null model of completely uncoordinated growth) indicate genetic or developmental coregulation of anatomical components. We present biometric strategies and R scripts for identifying patterns of coordination and compensation in the size and shape of composite anatomical structures. In an application to human cranial variation, we found that coordinated variation and positive correlations are prevalent for the size of cranial components, whereas their shape was dominated by compensatory variation, leading to strong canalization of cranial shape at larger scales. We propose that mechanically induced bone formation and remodeling are key mechanisms underlying compensatory variation in cranial shape. Such epigenetic coordination and compensation of growth are indispensable for stable, canalized development and may also foster the evolvability of complex anatomical structures by preserving spatial and functional integrity during genetic responses to selection.[Cranial shape; developmental canalization; evolvability; morphological integration; morphometrics; phenotypic variation; self-similarity.]

Intraspecific variability in human maxillary bone modeling patterns during ontogeny

“…Western Europeans and South Africans. We thus propose that the location of bone resorption on the bone may be a response to largerscale ontogenetic patterns (such as integration patterns within the skull), and result from compensatory mechanisms as proposed by other authors (Mitteroecker et al, 2020;O'Higgins, Bromage, Johnson, Moore, & McPhie, 1991). Finally, the analysis of covariation between the shape residuals and the bone modeling patterns again highlighted subtle population differences (Figure 8, Supporting Information S3 and S4), while overall, a similar general pattern is found (Figure 9).…”

On the use of the coefficient of variation to quantify and compare trait variation

“…Additionally, for complex traits composed of multiple parts that covary, the increase of the standard deviation with the mean depends on the sign of the covariance, a positive covariance (i.e., coordinated variation ) leads to a steeper increase of the variation (Taylor power >2), whereas a negative covariance ( compensatory variation ) leads to a shallower increase (Taylor power < 2; Mitteroecker et al. 2020). When computing the phenotypic CV for length and mass measurements of the data gathered by Hansen et al.…”

A model of developmental canalization, applied to human cranial form

“…The coefficient of variation for sinus size just decreased because the mean size increased faster during development than the standard deviation [cf. 47,83]. Several earlier studies on targeted growth relied on the comparison of coefficients of variation across age groups, but these results should be interpreted with care.…”

“…Developing soft tissue, such as the brain, eyes, and tongue, provide a matrix that affects and integrates the growth of the surrounding cranial elements. Likewise, sutural growth mechanically induced by stunted or overshooting growth of the adjacent bones canalizes overall cranial shape despite ample variation in the relative dimensions of the constituting bones [47]. Apparently, the lack of epigenetic growth induction in the upper airways accounts for the hyper-variability of nasopharyngeal dimensions in infancy and early childhood.…”

“…However, alleles that destabilize development not necessarily indicate an evolved basis of genetic canalization [e.g., 12,30]. The second line of research explains canalization as an inherent property of the developmental-genetic architecture, such as nonlinear developmental processes, redundancies among pathways, epistatic interactions, averaging effects of independent sources of variation, and epigenetic effects of tissue interactions [30,[37][38][39][40][41][42][43][44][45][46][47].…”