Genome-wide barriers to gene flow reveal the genetic basis of viviparity evolution in a lizard

Viviparity (live-bearing) is a major evolutionary transition repeatedly linked with ecological and evolutionary diversification throughout vertebrates. Live-bearing reproduction entails a novel suite of phenotypes and life history traits, but the genetic processes by which such a reproductive innovation evolves are unknown. Remarkable among amniotes, the common lizard (Zootoca vivipara) has extant oviparous (egg-laying) and viviparous lineages and a to-date unresolved history of parity mode emergence. This species represents an ideal model to reconstruct the evolutionary and genetic mechanisms of how viviparity arises. By analyzing whole genomes of individuals from across the species' distribution, we robustly show that viviparity evolved once. However, gene flow from oviparous to viviparous populations is found to be long-term and extensive, causing pronounced gene tree discordance. We inferred signals of selection for viviparity in many independent regions across the genome, and these were recruited over considerable time. Genomic barriers to gene flow between oviparity and viviparity were found genome wide. These are enriched for regions under selection for parity mode and for genes known to be involved in pregnancy and parturition in squamates and mammals. Further implicating their functional role in viviparity, we show that genes in genomic regions under selection and resisting gene flow are more highly expressed in the uterus of viviparous lizards during pregnancy. Our study demonstrates that viviparity in an amniote evolved by selection in the face of gene flow and primarily by the genome-wide accumulation of functional regulatory variants. These results reveal how complex adaptive innovations can arise and be maintained.