Genetic Adaptation of Schizothoracine Fish to the Phased Uplifting of the Qinghai–Tibetan Plateau

Many species of Schizothoracine, a subfamily of Cyprinidae, are highly endemic to the Qinghai–Tibetan Plateau (QTP). To characterize the adaptive changes associated with the Schizothoracine expansion at high altitudes, we sequenced tissue transcriptomes of two highland and two subhighland Schizothoracines and analyzed gene evolution patterns by comparing with lowland cyprinids. Phylogenetic tree reconstruction and divergence time estimation indicated that the common ancestor of Schizothoracine fish lived ∼32.7 million years ago (MYA), coinciding with the timing of the first phase of QTP uplifting. Both high- and subhigh-Schizothoracines demonstrated elevated dN/dS ratios in the protein-coding genes compared to lowland cyprinids, from which some biological processes implicated in altitude adaptation were commonly identified. On the other hand, the highland and subhighland lineages presented drastically divergent landscapes of positively selected genes (PSGs), enriched with very different gene ontology (GO) profiles, including those in “sensory organ morphogenesis,” “regulation of protein ubiquitination,” “blood circulation,” and “blood vessel development.” These results indicated different selection pressures imposed on the highland and subhighland lineages of the Schizothoracine subfamily, with a higher number of genes in the high-altitude species involved in adaptations such as sensory perception, blood circulation, and protein metabolism. Our study indicated divergent genetic adaptations in the aquatic species facing the phased uplifting of QTP.