Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes

Abstract

The development of distinct regions in the amniote vertebral column results from somite formation and Hox gene expression, with the adult morphology displaying remarkable variation among lineages. Mammalian regionalization is reportedly very conservative or even constrained, but there has been no study investigating vertebral count variation across Amniota as a whole, undermining attempts to understand the phylogenetic, ecological, and developmental factors affecting vertebral column variation. Here, we show that the mammalian (synapsid) and reptilian lineages show early in their evolutionary histories clear divergences in axial developmental plasticity, in terms of both regionalization and meristic change, with basal synapsids sharing the conserved axial configuration of crown mammals, and basal reptiles demonstrating the plasticity of extant taxa. We conducted a comprehensive survey of presacral vertebral counts across 436 recent and extinct amniote taxa. Vertebral counts were mapped onto a generalized amniote phylogeny as well as individual ingroup trees, and ancestral states were reconstructed by using squared-change parsimony. We also calculated the relationship between presacral and cervical numbers to infer the relative influence of homeotic effects and meristic changes and found no correlation between somitogenesis and Hox-mediated regionalization. Although conservatism in presacral numbers characterized early synapsid lineages, in some cases reptiles and synapsids exhibit the same developmental innovations in response to similar selective pressures. Conversely, increases in body mass are not coupled with meristic or homeotic changes, but mostly occur in concert with postembryonic somatic growth. Our study highlights the importance of fossils in large-scale investigations of evolutionary developmental processes.

Fig. 1.

Phylogeny of the major amniote groups treated in this article, based on a compilation from several sources (23, 53, 54). The position of turtles follows current hypotheses (50, 51). See SI Appendix for a detailed phylogeny of all taxa treated in this article. Circles at major nodes illustrate ancestral states for cervical (gray) and dorsal (white) vertebrae, based on rounded numbers (in italics) derived from the ancestral reconstructions. The skeletal reconstructions of taxa in bold are modified from several sources (SI Appendix) and serve to illustrate the diversity of skeletal structures and the associated vertebral numbers. The figure is not to scale.

Fig. 2.

Diagram showing the cervical/presacral ratio (y axis) vs. presacral number (x axis) for the major amniote clades. Mammals, extinct synapsids, and stem amniotes (light green, green, and black circles) show much less variability than extinct and extant reptiles (light blue and blue circles). See section 7 of SI Appendix for taxa and values.