Candidate Genes Associated with Parity Mode Evolution are Under Selection in Oviparous and Viviparous Snakes

Abstract

Over 100 divergent lineages of squamates are viviparous (live-bearing) while others are oviparous (egg-laying). Estimated origins of oviparity and viviparity across the squamate phylogeny are a subject of scientific debate. Identifying genomic changes that influence parity mode evolution can provide insights on the adaptive nature of both parity modes. Using BUSTED in the HyPhy suite and whole genomes of 27 species of snakes, I test for gene-wide episodic diversifying selection (EDS) in 1,587 candidate genes. The genomes represent 14 viviparous and 13 oviparous species across four families (Viperidae, Elapidae, Natricidae, and Pythonidae), including eight new genomes from Lachesis muta, Lachesis stenophrys, Agkistrodon contortrix, Trimeresurus albolabris, Gloydius halys, Ophryacus undulatus, Ovophis monticola, and Calloselasma rhodostoma. Candidate genes were chosen based on evidence for their involvement of seven physiological processes expected to change during evolutionary transitions between parity modes. EDS was measured across candidate gene trees under different foreground branch tests: 1) all viviparous branches, 2) viviparous Viperidae branches, 3) viviparous Elapidae and Natricidae branches, 4) all oviparous branches, and 5) oviparous Viperidae branches (estimated reversals). Over 16% of tests found evidence for EDS, translating to 533 genes with EDS associated with parity mode. Some genes had significant EDS in multiple tests. However, the all oviparous test identified a 2.8 to 5.9-fold increase in the number of unique genes with EDS compared to other foreground tests. These results suggest that EDS may influence the evolution of both oviparity and viviparity. Future research using population-level data from snakes may further elucidate the role of selection in parity mode evolution.