Convergent genomic signatures of adaptation to an extreme environment in cyprinoid fishes

Cyprinoids are a worldwide distributed and diverse group of freshwater fish with more than 3,000 species. Although primarily freshwater, some cyprinoid species had convergently evolved to thrive in extreme environments and underlying genetic mechanisms remain unclear. Here, we leveraged 32 cyprinoid fish genomes to identify common genomic changes associated with convergent adaptation to highly saline and alkaline water in two East Asian cyprinoid fish species, Gymnocypris przwalskii and Leuciscus waleckii, representing two independent extremophile fish lineages. We found that genome-wide rate of nonsynonymous substitution and signal of intensified selection is higher in extremophile relative to non-extremophile fish taxa. We further tested gene-wide molecular convergence and found hundreds of genes tended to experience convergent shifts in selections in extremophile fish taxa, including convergent acceleration and positive selection. These genes were associated with several key functions, such as nervous system development, reproduction, ion transport and immune response, and included genes that previously have been implicated for saline or alkaline tolerance in fish. Additionally, comparative transcriptomic analyses defined the convergent roles of differentially expressed genes under selection in extremophile fish taxa during convergent adaptation. Taken together, our work provides insights into the genomic basis of convergent adaptation to extreme environments in fish.