Genomic Insights Into Diversity, Phylogeny, Hybridization and Evolutionary History of Palearctic Fish Genus <i>Rutilus</i> (Leuciscidae)

ABSTRACT Aim Using a widely distributed and frequently hybridising fish (genus Rutilus ) in the Palearctic as a model system, we re‐evaluated a series of hypotheses on phylogeny, taxonomy, phylogeography and the role of hybridization in evolutionary history based on the first large‐scale analyses of nuclear SNPs together with mtDNA data obtained from all Rutilus species. Location Water systems in Northern Eurasia. Methods Based on nuclear (ddRADseq) data, we applied phylogenomic, population genomic and introgression analyses to assess the diversity of lineages, their distribution and hybridization in the context of the hypotheses tested. Results We identified 22 lineages in three major clades— Rutilus s. str., Leucos and Pararutilus . High diversity of lineages was discovered, with three revived species and three novel lineages of undescribed species in Europe. Evidence for extensive mito‐nuclear discordance and ongoing and past inter‐ and intrageneric introgressive hybridization was found in many lineages. A Caucasian relic lineage and the endangered narrow endemic species ‘ Rutilus ’ atropatenus were found to represent an independent lineage ( Orthroleucos ) with a high level of past introgression with Rutilus . Main Conclusions The genetic structure of Rutilus revealed by nuclear SNPs contrasts markedly with that supported by mtDNA. Numerous mito‐nuclear discordances are evidence of the past secondary contacts and highlight the weakness of taxonomy based on mtDNA alone. A super‐lineage of mtDNA covering the range of many European, Siberian, Caucasian, and Central Asian Rutilus species (5000 km long) is a result of introgression of mtDNA from a widespread Ponto‐Caspian lineage whose distribution likely pulsed with Pleistocene glaciation cycles. Anadromous life histories may have evolved in parallel in different clades and been facilitated by hybridization. The high plasticity, adaptiveness and species diversity of the genus Rutilus may be underlined by their heterogeneous genomes resulting from extensive interspecific hybridization. However, narrow‐range endemic species may be threatened by introgressive hybridization.