Hidden in the sand: phylogenomics unravel an unexpected evolutionary history on the desert-adapted vipers of the genusCerastes

Abstract

The desert vipers of the genusCerastesare a small clade of medically important venomous snakes within the family Viperidae. According to published morphological and molecular studies, the group is comprised by four species: two morphologically similar and phylogenetically sister taxa, the African horned viper (Cerastes cerastes) and the Arabian horned viper (Cerastes gasperettii); a more distantly related species, the Saharan sand viper (Cerastes vipera), and the enigmatic Böhme’s sand viper (Cerastes boehmei), only known from a single specimen in captivity allegedly captured in Central Tunisia. In this study, we analyzed one mitochondrial marker (COI) as well as genome-wide data (ddRAD sequencing) from 28 and 41 samples, respectively, covering the entire distribution range of the genus to explore the population genomics, phylogenomic relationships and introgression patterns within the genusCerastes. Additionally, and to provide insights into the mode of diversification of the group, we carried out niche overlap analyses considering climatic and habitat variables. Both nuclear phylogenomic reconstructions and population structure analyses have unveiled an unexpected evolutionary history for the genusCerastes, which sharply contradicts the morphological similarities and previously published mitochondrial approaches.Cerastes cerastesandC. viperaare recovered as sister taxa whilstC. gasperettiiis a sister taxon to the clade formed by these two species. We found a relatively high niche overlap (OI > 0.7) in both climatic and habitat variables betweenC. cerastesandC. vipera, contradicting a potential scenario of sympatric speciation. These results are in line with the introgression found between the northwestern African populations ofC. cerastesandC. vipera. Finally, our genomic data confirms the existence of a lineage ofC. cerastesin Arabia. All these results highlight the importance of genome-wide data over few genetic markers to study the evolutionary history of species.