Independent origins of vertebral complexity in tetrapods

Abstract The axial skeleton is the central anatomical structure uniting vertebrates, varying across the clade in the total number of constituent elements and morphological complexity, associated with changes in regulatory genetic mechanisms, respiratory efficiency, and locomotory adaptation. The evolution of this morphological complexity has historically been interpreted as a linear increase from relatively simple, homogeneous anatomies in tetrapods and stem mammals to uniquely high complexity in crown mammals. However, axial skeletal complexity remains poorly understood in stem taxa beyond Pan-Mammalia, restricting the ability to infer the evolutionary history of the vertebral column outside of this clade. Here we combine 3D geometric morphometrics with maximum likelihood model testing in a comprehensive phylogenetic framework of tetrapods, including crown and stem taxa, to reveal the independent acquisition of equally high degrees of regionalization across Pan-Mammalia and every major reptile clade. We reject the traditional view of linear increases in vertebral complexity leading to mammals. We demonstrate divergent evolutionary histories across amniote clades, associated with the differential presence or absence of functional constraint on the axial skeleton. In most reptiles, morphological heterogeneity within the column is associated with body size and segment count, unlike Pan-Mammalia, across which heterogeneity is a component of functional regionalization associated with the evolution of endothermy. Intracolumnar heterogeneity is constrained in mammals and birds by anatomical complexity required for respiratory and locomotory function regardless of body size. The absence of such physiological or metabolic constraints on axial skeletal evolution across non-avian reptiles has facilitated the morphological plasticity that has contributed to their remarkable diversity of function and form.