Testing Thirty Years of Hypotheses: Ancient Trout-Salmon Introgression and Limited Pre-Colonial Gene Flow Between Rainbow and Cutthroat Trout Shaped Pacific Salmonid Evolution

Abstract

Introgression is the transfer of genetic material between species or populations through hybridization and backcrossing. While often deleterious or neutral in nature, introgression can also have beneficial consequences for the recipient lineage. Oncorhynchus is a genus of ray-finned fish (family Salmonidae) composed of nine species of Pacific trout and eight species of Pacific salmon, in which deep introgression has long been proposed to explain patterns of gene-tree-species-tree discordance, and in which hybridization is extensively observed between introduced and endemic species. In this study, we identified well-supported introgression between the ancestral lineage of Pacific trout and the ancestor of Chinook and coho salmon, a long-posited but previously untested hypothesis. While other salmon lineages (pink, chum, sockeye, and masu salmon) have been sympatric with trout for extended periods, providing an opportunity for hybridization to occur, we found no evidence of introgression between trout and these other salmon lineages. Our findings suggest mito-nuclear incompatibilities serve as a possible barrier to gene flow between the clade comprised of pink, chum, and sockeye salmon and all other lineages in Oncorhynchus. Within Pacific trout, we detected no historical introgression between cutthroat and rainbow trout lineages, suggesting that the extensive hybridization observed between them today reflects recent, primarily human-mediated contact rather than long-term gene flow. These findings show that ancestral introgression has shaped the evolutionary history of Oncorhynchus and should be accounted for in future comparative phylogenetic studies of the genus.