Abstract
The ecological origin of snakes remains amongst the most controversial topics in evolution, with three competing hypotheses: fossorial; marine; or terrestrial. Here we use a geometric morphometric approach integrating ecological, phylogenetic, paleontological, and developmental data for building models of skull shape and size evolution and developmental rate changes in squamates. Our large-scale data reveal that whereas the most recent common ancestor of crown snakes had a small skull with a shape undeniably adapted for fossoriality, all snakes plus their sister group derive from a surface-terrestrial form with non-fossorial behavior, thus redirecting the debate toward an underexplored evolutionary scenario. Our comprehensive heterochrony analyses further indicate that snakes later evolved novel craniofacial specializations through global acceleration of skull development. These results highlight the importance of the interplay between natural selection and developmental processes in snake origin and diversification, leading first to invasion of a new habitat and then to subsequent ecological radiations.
Highlights
The ecological origin of snakes remains amongst the most controversial topics in evolution, with three competing hypotheses: fossorial; marine; or terrestrial
Our data reveal that while the most recent common ancestor (MRCA) of crown snakes had a small skull with a shape fully adapted to a fossorial lifestyle, all snakes plus their sister group evolved from a terrestrial form with non-fossorial or non-leaf-litter behaviors, indicating a surface-terrestrial-to-fossorial scenario at the origin of snakes
Our principal component analysis (PCA) performed on Procrustes coordinates of skulls from a large data set of adult squamate species (302 and 91 species for two-dimensional (2D) and three-dimensional (3D) data, respectively; Fig. 1, Supplementary Fig. 1, and Supplementary Note 1) generated a morphospace defined by two principal components, PC1 and PC2, which together account for more than 60% of the total shape variation in both 2D and 3D analyses (Fig. 2a and Supplementary Figs 3 and 4)
Summary
The ecological origin of snakes remains amongst the most controversial topics in evolution, with three competing hypotheses: fossorial; marine; or terrestrial. Our comprehensive heterochrony analyses further indicate that snakes later evolved novel craniofacial specializations through global acceleration of skull development These results highlight the importance of the interplay between natural selection and developmental processes in snake origin and diversification, leading first to invasion of a new habitat and to subsequent ecological radiations. We demonstrate that the unique skull features of modern snakes later evolved by peramorphosis through global acceleration in the rate of craniofacial development during embryogenesis This set of results demonstrates the importance of the relationships between skull form, function, and development in the major ecological radiations of snakes to different habitats, and provides a new framework to understand the origin and evolutionary history of snakes
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