Phylogenomics of Vipers and the Role of Competition on Venom Evolution

Abstract

Competition is a critical selective force for diversification; however, empirical studies on its role promoting differentiation of adaptive phenotypes have largely been limited to small spatial and taxonomic scales. Here, we test the effect of competition on the evolution of pitviper venoms – a cross-continental radiation of venomous snakes each with tens to hundreds of individual toxins varying in expression, composition, and overall complexity among species. By inferring a novel phylogenomic tree and reconstructing the biogeography of the Viperidae, we demonstrate a rapid radiation occurred upon invasion of the New World. Using \u3e500 venom gland transcriptomes and phylogenetic comparative modeling, we reveal that venom phenotypes diverge when multiple species coexist in a given area through time via positive diversity dependence. Furthermore, we find that pitviper communities have evolved to maximize functional diversity despite comparatively low phylogenetic diversity, suggesting an evolutionary response of venom rather than communities accumulating phylogenetically diverse species. Together, these findings support competition as a likely selective pressure driving venom diversification in pitvipers