Genome-wide single nucleotide polymorphisms reveal recurrent waves of speciation in niche-pockets, in Europe's most venomous snake

Within the Balkan Peninsula, topographic and climatic agents have promoted biodiversity and shaped the speciation history of many ectotherms. Here, we targeted an iconic European reptile, the nose-horned viper species-complex (Vipera ammodytes), and explored its spatial and temporal evolution. We (i) utilized genome-wide single nucleotide polymorphisms to infer genetic structure and build a time-calibrated species-tree, and (ii) applied species distribution modelling with niche-divergence tests among major phylogenomic clades. Geographically structured genetic diversity was found. Cycles of recurrent isolation and expansion during glacial-interglacial periods led to allopatric speciation and to secondary contacts and formation of multiple hybrid zones throughout the Balkan Peninsula. Deep divergence is still detected among populations separated by old and imminent biogeographical barriers (Pindos Mountain Range, the Cyclades islands, etc.), but in most cases speciation is incomplete. At the other end of the speciation continuum, we recognize two well-differentiated lineages, currently lacking any evidence of gene flow; one is distributed in the Northwestern Balkans and the other in the Southeastern Balkans, further expanding into Asia. Despite their split 5 million years ago, there is no evidence of ecological divergence, as speciation probably occurred in niche-pockets of analogous environments. These two lineages probably represent different species, while V. transcaucasiana does not merit species status. By comparing the genomic phylogenies to an updated mitochondrial one, we propose an evolutionary scenario that resolves all mitonuclear conflicts, according to which the history of the V. ammodytes species-complex was shaped by complex processes, including a major event of introgressive hybridization with asymmetric mitochondrial capture.

Automated summary

Within the Balkan Peninsula, topographic and climatic factors have played a significant role in shaping the biodiversity and speciation history of ectotherms like the nose-horned viper species-complex. The study reveals that cycles of isolation and expansion during glacial-interglacial periods have led to allopatric speciation and the formation of hybrid zones in different parts of the Balkan Peninsula. Furthermore, the study proposes an evolutionary scenario that resolves conflicts between genomic and mitochondrial phylogenies.