Morphological integration and serial homology: A case study of the cranium and anterior vertebrae in salamanders

Abstract

Serial homology or the repetition of equivalent developmental units and their derivatives is a phenomenon encountered in a variety of organisms, with the vertebrate axial skeleton as one of the most notable examples. Serially homologous structures can be viewed as an appropriate model system for studying morphological integration and modularity, due to the strong impact of development on their covariation. Here, we explored the pattern of morphological integration of the cranium and the first three serially homologous structures (atlas, first, and second trunk vertebrae) in salamandrid salamanders, using micro‐CT scanning and three‐dimensional geometric morphometrics. We explored the integration between structures at static and evolutionary levels. Effects of allometry on patterns of modularity were also taken into account. At the static level (within species), we analyzed inter‐individual variation in shape to detect functional modules and intra‐individual variation to detect developmental modules. Significant integration (based on inter‐individual variation) among all structures was detected and allometry is shown to be an important integrating factor. The pattern of intra‐individual, asymmetric variation indicates statistically significant developmental integration between the cranium and the atlas and between the first two trunk vertebrae. At the evolutionary level (among species), the cranium, atlas, and trunk vertebrae separate as different modules. Our results show that morphological integration at the evolutionary level coincides with morphological and functional differentiation of the axial skeleton, allowing the more or less independent evolutionary changes of the cranial skeleton and the vertebral column, regardless of the relatively strong integration at the static level. The observed patterns of morphological integration differ across levels, indicating different impacts of developmental and phylogenetic constraints and functional demands.

Regionalization and morphological integration in the vertebral column of Eurasian small‐bodied newts (Salamandridae: Lissotriton)

“…To estimate the strength of covariation between vertebrae, we employed a two-block PLS analysis, based on a singular value decomposition of the matrix of covariances between the two sets of variables (Bookstein, 1991;Rohlf & Corti, 2000;Young & Hallgrímsson, 2005). This approach is suitable for testing covariation between the two separate sets of landmarks, with separate Procrustes superimpositions (Bastir & Rosas, 2005;Klingenberg, 2009;McCane & Kean, 2011;Neaux et al, 2013;Urošević et al, 2020). The measures of covariation between the vertebrae were the RV coefficient (Klingenberg, 2009(Klingenberg, , 2011 and z scores (Adams & Collyer, 2016).…”

“…Serially homologous structures such as vertebrae, teeth, and ribs provide worthwhile model systems for the study of regionalization, modularity, and morphological integration, because they share a common structural plan with variation throughout the series (Gómez-Robles & Polly, 2012;Jones et al, 2018;Urošević et al, 2020). Elements within serially homologous structures tend to be developmentally constrained and strongly integrated (Asher et al, 2011;Carroll, 2001;Cowley & Atchley, 1990;Jones et al, 2018Jones et al, , 2020Young & Hallgrímsson, 2005).…”

Shape asymmetry — what's new?

“…This measure can be followed over different growth stages [22,39] or related to a variety of factors such as genetic, environmental, performance or socioeconomic measures [8,9,[40][41][42][43][44][45]. Patterns of covariation in fluctuating asymmetry of shape have been used to investigate the developmental origins of integration in morphological structures [46][47][48], based on reasoning that covariation of fluctuating asymmetry between traits indicates direct developmental interactions between them [4,49].…”