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

Wei Yin,Bing-Zheng Lu,Peng-Xin Qiu,Qi Zhou,Guang-Mei Yan,Jin-Ming Lian,Yang Zhou,Wen-Bo Zhu,Zhi-Long Lin,Xing-Wen Su,Guo-Jie Zhang,Li-Jun Jin,Qi-Ye Li,Huan-Ming Yang,Yi-Jun Huang,Pei Zhang,Bo Wen,Bi-Tao Qiu,Zong-Ji Wang

doi:10.1038/ncomms13107

Abstract

Snakes have numerous features distinctive from other tetrapods and a rich history of genome evolution that is still obscure. Here, we report the high-quality genome of the five-pacer viper, Deinagkistrodon acutus, and comparative analyses with other representative snake and lizard genomes. We map the evolutionary trajectories of transposable elements (TEs), developmental genes and sex chromosomes onto the snake phylogeny. TEs exhibit dynamic lineage-specific expansion, and many viper TEs show brain-specific gene expression along with their nearby genes. We detect signatures of adaptive evolution in olfactory, venom and thermal-sensing genes and also functional degeneration of genes associated with vision and hearing. Lineage-specific relaxation of functional constraints on respective Hox and Tbx limb-patterning genes supports fossil evidence for a successive loss of forelimbs then hindlimbs during snake evolution. Finally, we infer that the ZW sex chromosome pair had undergone at least three recombination suppression events in the ancestor of advanced snakes. These results altogether forge a framework for our deep understanding into snakes' history of molecular evolution.

Highlights

Snakes have numerous features distinctive from other tetrapods and a rich history of genome evolution that is still obscure
On the basis of 5,353 one-to-one orthologous gene groups of four snake species, the green anole lizard[23] and several other sequenced vertebrate genomes (Methods), we constructed a phylogenomic tree with high bootstrapping values at all nodes (Fig. 1b)
We estimated that advanced snakes diverged from boa and python about 66.9 (47.2–84.4) million years ago (MYA), and five-pacer viper and king cobra diverged 44.9 (27.5–65.0) MYA assuming a molecular clock

Summary

Introduction

Snakes have numerous features distinctive from other tetrapods and a rich history of genome evolution that is still obscure. We infer that the ZW sex chromosome pair had undergone at least three recombination suppression events in the ancestor of advanced snakes These results altogether forge a framework for our deep understanding into snakes’ history of molecular evolution. Snakes have undergone a massive adaptive radiation with B3,400 extant species successfully inhabiting almost all continents except for the polar regions[1] This process has culminated in ‘advanced snakes’ (Caenophidia, B3,000 species), involved numerous evolutionary changes in body form, chemo and thermo-perception, venom and sexual reproductive systems, which altogether distinguish snakes from the majority of other squamates (lizards and worm lizards). This deficiency hampers our comprehensive understanding into the molecular basis of stepwise or independent acquisition of snake-specific traits We bridge this gap here by deep-sequencing the genomes and transcriptomes of the five-pacer viper, Deinagkistrodon acutus (Fig. 1a), a member of the Viperidae family. With the inferred recombination suppression events between the ZW sex chromosomes, we have reconstructed the major genomic changes during the snake evolution in this work

Methods

Results

Conclusion