Convergent molecular evolution of viviparity across squamate reptiles

Abstract

The molecular mechanisms underlying convergent phenotypic innovations across the tree of life are largely unknown. Viviparity (live-bearing) is a complex reproductive mode transition having more than 100 independent origins in squamate reptiles, making it an ideal model to understand the molecular basis of evolutionary innovations. Here we used 141 squamate genomes, including 42 viviparous species and representing more than 18 independent evolutionary transitions to viviparity, to search for convergent molecular signals in 14,096 protein coding genes. We show that convergent positive selection associated with viviparity at the gene-level and amino acid substitutions at the site-level are widespread in squamates, but there is no universal convergence across all viviparous clades. The chance of molecular convergence associated with viviparity is negatively correlated with genetic distance between species. Nevertheless, convergent genes are shared across independent origins of viviparity even spanning deep divergence times, and these genes are enriched in viviparity-related biological processes, including placental development, nutrient transport, and immune response to external organisms. Our result demonstrates that molecular convergence in the evolution of complex traits decreases in likelihood with evolutionary time, but when it occurs is more likely through changes in different genes of similar functional pathway rather than changes in the same genes.