Caucasian treasure: Genomics sheds light on the evolution of half-extinct Sevan trout, Salmo ischchan, species flock

[Display omitted] •Half-extinct species flock of brown trout (5 forms) was studied using aDNA and WGS.•mtDNA and nuclear data confirm the monophyly and recent origin of Sevan trouts.•Stepwise evolution from riverine to lacustrine mode of life was revealed.•Climatic oscillations were the likely trigger for speciation of lacustrine forms.•A few SNPs under selection may be responsible for assortative mating. Five ecologically and phenotypically divergent ecomorphs of the genus Salmo are known from a landlocked alpine lake in the Caucasus, Lake Sevan. It is an example of sympatric diversification within a species-rich lineage with predominate mode of speciation being allopatric. The diversification of Sevan trouts was accompanied by spawning resource partitioning. Four lacustrine ecomorphs with different temporal-spatial spawning strategies and divergent morphology and coloration evolved along with a fifth ecomorph, brook trout, inhabiting the tributaries. Unfortunately, the Sevan trout diversity was almost destroyed by human activity, with two ecomorphs becoming extinct in the 1980s. We performed reconstruction of the evolutionary history of Sevan trouts based on high-throughput sequencing of both contemporary and historical DNA (∼ 50 y.o.) of all Sevan trout ecomorphs. Our study of complete mitogenomes along with genome-wide SNP data revealed the monophyly of four lacustrine ecomorphs and local brook trout, all derived from the anadromous form Caspian salmon, S. caspius. The species tree suggests a scenario of stepwise evolution from riverine to lacustrine spawning. Three genomic clusters were revealed, of which two refer to the riverine and lacustrine spawners within the flock of Sevan trouts (with FST value = 0.069). A few SNP outliers under selection were discovered that could be responsible for assortative mating based on visual recognition. The Holocene climatic oscillations and the desiccation of tributaries could have played an important role in the origin of lacustrine spawning. The relationships between lacustrine ecomorphs were not yet fully resolved. This radiation warrants further investigation.