Unveiling the evolutionary history of European vipers and their venoms from a multi-omic approach

Talavera, A.; Palmada-Flores, M.; Martinez-Freiria, F.; Mochales-Riano, G.; Burriel-Carranza, B.; Estarellas, M.; Fernandez-Guiberteau, D.; Camina, A.; Ursenbacher, S.; Vörös, J.; Halpern, B.; Pla, D.; Calvete, J. J.; Mikheyev, A. S.; Marques-Bonet, T.; Carranza, S.

doi:10.1101/2024.12.10.627732

bioRxiv · 10.1101/2024.12.10.627732

Unveiling the evolutionary history of European vipers and their venoms from a multi-omic approach

Talavera, A.·Palmada-Flores, M.·Martinez-Freiria, F.·Mochales-Riano, G.·Burriel-Carranza, B.·Estarellas, M.·Fernandez-Guiberteau, D.·Camina, A.·Ursenbacher, S.·Vörös, J.·Halpern, B.·Pla, D.·Calvete, J. J.·Mikheyev, A. S.·Marques-Bonet, T.·Carranza, S.

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Abstract

Snake genomes attract significant attention from multiple disciplines, including medicine, drug bioprospection, and evolutionary biology, due to the unique features found in snakes, especially, the evolution of venom. However, genomic research within the family Viperidae has mostly focused to date on the subfamily Crotalinae, while overlooking Viperinae, the Old World vipers. Among Viperinae, European vipers (Vipera) have been the subject of extensive research because of their venoms, phylogeographic, and ecological diversification. Nevertheless, venom research in this group has been conducted using mostly proteomes alone, while phylogeography and systematics in the genus have relied on biased information from mitochondrial phylogenies. Here, we generated chromosome-level genome assemblies for three Vipera species and whole-genome sequencing data for 94 samples representing 15 Vipera taxa. This comprehensive dataset has enabled us to disentangle the phylogenomic relationships of this genus, affected by mito-nuclear discordance and pervaded by ancestral introgression. Population-level analyses in the Iberian Peninsula, where the three oldest lineages within Vipera meet, revealed signals of recent adaptive introgression between ecologically dissimilar species, whereas chromosomal rearrangements isolate species occupying similar niches. Finally, using transcriptomic and proteomic data, we characterized the Vipera toxin-encoding genes, in which opposing selective forces were unveiled as common drivers of the evolution of venom as an integrated phenotype.

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Talavera, A., Palmada-Flores, M., Martinez-Freiria, F., Mochales-Riano, G., Burriel-Carranza, B., Estarellas, M., Fernandez-Guiberteau, D., Camina, A., Ursenbacher, S., Vörös, J., Halpern, B., Pla, D., Calvete, J. J., Mikheyev, A. S., Marques-Bonet, T., Carranza, S.. 2024-12-13. Unveiling the evolutionary history of European vipers and their venoms from a multi-omic approach. https://doi.org/10.1101/2024.12.10.627732

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