Evolution trajectories of snake genes and genomes revealed by comparative analyses of five-pacer viper

Abstract

Snakes numerous fascinating features distinctive from other tetrapods necessitate a rich history of genome evolution that is still obscure. To address this, we report the first high-quality genome of a viper, Deinagkistrodon acutus and comparative analyses using other species from major snake and lizard lineages. We map the evolution trajectories of transposable elements (TEs), developmental genes and sex chromosomes onto the snake phylogeny. TEs exhibit dynamic lineage-specific expansion. And in the viper many TEs may have been rewired into the regulatory network of brain genes, as shown by their associated expression with nearby genes in the brain but not in other tissues. We detect signatures of adaptive evolution in olfactory, venom and thermal-sensing genes, and also functional degeneration of genes associated with vision and hearing. Many Hox and Tbx limb-patterning genes show evidence of relaxed selective constraints, and such genes phylogenetic distribution supports fossil evidence for a successive loss of forelimbs then hindlimbs during the snake evolution. Finally, we infer that the Z and W sex chromosomes had undergone at least three recombination suppression events at the ancestor of advanced snakes, with the W chromosomes showing a gradient of degeneration from basal to advanced snakes. These results, together with all the genes identified as undergoing adaptive or degenerative evolution episodes at respective snake lineages forge a framework for our deep understanding into snakes molecular evolution history.