Genomic and mitochondrial evidence of ancient isolations and extreme introgression in the four-lined snake.

ABSTRACT

Comparing mitochondrial and genomic phylogenies is an essential tool for investigating speciation processes, because each genome carries different inheritance properties and evolutionary characteristics. Furthermore, mitonuclear discordance may arise from ecological adaptation, historic isolation, population size changes, and sex-biased dispersal. Closely related taxa are expected to experience gene flow; however, this may not be true for insular populations or populations isolated in refugia. The four-lined snake Elaphe quatuorlineata has a fragmented distribution, separating populations of the Italian and Balkan Peninsulas, whereas several insular Aegean populations of significantly smaller body size (Cyclades island group and Skyros Island, Greece) are currently considered distinct subspecies. We constructed the species-tree phylogeny of this species utilizing genome-wide single nucleotide polymorphisms and a gene-tree based on complete cytochrome b sequences, aiming to detect convergence and discrepancies between biparentally and maternally inherited genomes. Population structuring, phylogenetic patterns and migration events among geographically defined lineages supported our hypothesis of isolation in multiple sub-refugia. Where biogeographical barriers did not restrict subsequent dispersal, extensive genetic exchange occurred between mainland Balkan populations. This process has led to the mitochondrial sweep of an ancestral mitolineage that survived only in peripheral (East Greece) and insular populations (North Cyclades and Skyros). The Central Cyclades represent an ancient lineage for both molecular markers that emerged almost 3.3 Mya. Considering their distinct morphology, insular E. quatuorlineata populations should be the future focus of an extensive sampling, especially since the mitonuclear discordance observed in this species could be related to ecological adaptations, such as the island-dwarfism phenomenon.