The functional genetic architecture of egg-laying and live-bearing reproduction in common lizards

All amniotes reproduce either by egg-laying (oviparity), which is ancestral to vertebrates, or by live-bearing (viviparity), which has evolved many times independently. However, the genetic basis of these parity modes has never been resolved and consequently the homology across evolutionary scales is currently unknown. Here we describe the functional genes and genetic architecture of parity mode and its key traits, eggshell and gestation length, by leveraging natural hybridisations between oviparous and viviparous lizards, and comparing our findings across vertebrates. In lizards, parity trait genes were associated with progesterone-binding functions and enriched for tissue remodelling and immune system pathways. Viviparity involved more genes and complex gene networks than did oviparity. Angiogenesis, vascular endothelial growth, and adrenoreceptor pathways were enriched in the viviparous female reproductive tissue, while pathways for transforming growth factor were enriched in the oviparous. Natural selection on these parity mode genes was evident genome-wide. Our analysis of seven independent origins of viviparity in mammals, squamates and fish, showed that genes active in pregnancy related to immunity, tissue remodelling, and blood vessel generation. Therefore, our results demonstrate that pre36 established regulatory networks are repeatedly recruited for viviparity and that these are shared at deep evolutionary scales.