Serial disparity in the carnivoran backbone unveil a complex adaptive role in metameric evolution

Multi-element systems such as the vertebral column of vertebrates represent a major challenge to phenotypic quantification and macroevolutionary analyses. The vertebral column is a metameric structure, composed of serially repeated subunits, and much of what is known so far has been inferred from sparse anatomical samples, providing little insight into local-scale (i.e. vertebra-to-vertebra) variation and its macroevolutionary importance. This limits understanding of how evolutionary constraints and functional adaptation interact during the evolution of multi-element phenotypes. Here, we quantify morphological disparity across all subunits (vertebrae) of the pre-sacral column in the mammalian order Carnivora. We address how vertebral morphology varies among elements, and the extent to which these patterns have been structured by constraints and/or evolutionary adaptation to locomotory capabilities, using 3D geometric morphometrics and multivariate analyses for high-dimensional phenotypes. We find that lumbars and posterior thoracics exhibit high individual disparity but low serial differentiation. These vertebrae are pervasively recruited into locomotory functions, exhibiting high-dimensional ecomorphological signals and patterns of evolution indicative of relaxed constraints. Cervical and anterior thoracic vertebrae have low individual disparity and greater serial differentiation. Individual vertebrae in these regions unexpectedly also show signals of locomotory adaptation that were not generally recognized by previous studies. These are characterized by low-dimensional ecomorphological signals and overall constrained patterns of evolution. Our findings support the hypothesis that the lumbar region is a key innovation that increases ecological versatility of mammalian locomotion. Nevertheless, locomotory adaptation is more widely distributed along the mammalian axial skeleton. This has been masked by local-scale variation and low phenotypic variability in comparison with other skeletal structures such as the skull or limbs. Our analyses demonstrate that the strength of ecomorphological signal does not have a predictable influence on macroevolutionary outcomes even within the same structure, and undermine the traditional view that highly constrained skeletal units are strongly limited in their potential to adapt to new ecological avenues. Our findings emphasize the importance of quantifying local-scale variation in functionally versatile, multi-element phe