Genomic signature of highland adaptation in fish: A case study in Tibetan Schizothoracinae species

Abstract

Background: Genome-wide studies on highland adaptation mechanism in terrestrial animal have been widely reported with few available for aquatic animals. Tibetan Schizothoracinae species are ideal model systems to study speciation and adaptation of fish. The Schizothoracine fish, Gymnocypris przewalskii ganzihonensis had underwent the ecological niche shift from salt water to freshwater, and also experienced a recent split from Gymnocypris przewalskii przewalskii. In addition, G. p. ganzihonensis inhabited harsh aquatic environment including low temperature and hypoxia as well as other Schizothoracinae species, its genetic mechanism of highland adaptation have yet to be determined. Results: Our study used comparative genomic analysis based on the transcriptomic data of G. p. ganzihonensis and other four fish genome datasets to investigate the genetic basis of highland adaptation in Schizothoracine fish. We found that Schizothoracine fish lineage on the terminal branch had an elevated dN/dS ratio than its ancestral branch. A total of 202 gene ontology (GO) categories involved into transport, energy metabolism and immune response had accelerated evolutionary rates than zebrafish. Interestingly, we also identified 162 genes showing signature of positive selection (PSG) involved into energy metabolism, transport and immune response in G. p. ganzihonesis. While, we failed to find any PSG related to hypoxia response as previous studies. Conclusions: Comparative genomic analysis based on G. p. ganzihonensis transcriptome data revealed significant genomic signature of accelerated evolution ongoing within Tibetan Schizothoracinae species lineage. Molecular evolution analysis suggested that genes involved in energy metabolism, transport and immune response functions in Schizothoracine fish underwent positive selection, especially in innate immunity including toll-like receptor signaling pathway genes. Taken together, our result as a case study in Schizothoracinae species provides novel insights in understanding the aquatic animal adaptation to extreme environment on the Tibetan Plateau, and also provides valuable genomic resource for further functional verification studies.