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

Abstract

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.

Genomic signature of ongoing alkaline adaptation in a Schizothoracine fish (Cyprinidae) inhabiting soda lake on the Tibetan Plateau

“…2C). Besides the newly reconstructed phylogeny within Schizothoracine fishes, the strongly supported (100%) phylogeny also had similar topology to recent phylogenomics studies on Schizothoracine fishes and other teleost fishes (Tong, Fei, et al 2017;Zhang et al 2017;Chi et al 2017).…”

“…Comparative genomics has begun to elucidate the genomic basis of harsh environment adaptation in Tibetan fish species, but insight into the alkaline adaptation in Schizothoracine fishes has lagged behind. Building on previous comparative genomic or transcriptomic studies specifically focused on hypoxia and cold adaptation of Tibetan fishes (Yang et al 2014;Chi et al 2017;Kang et al 2017;Wang et al 2015;Zhang et al 2017;Tong, Tian, et al 2017;Ma et al 2015), we performed one of the first comparative genomics studies to identify the signature of ongoing alkaline adaptation in Schizothoracine fishes on the Tibetan Plateau. These putative genomic signatures included expansions of lineage-specific genes associated with ion transport and transmembrane functions, genome-wide elevated rate of molecular evolution in Schizothoracine fishes relative to other model teleost fish species.…”

“…We also searched all published Schizothoracine fish transcriptomes (Tong, Fei, et al 2017;Zhang et al 2017;Chi et al 2017) and downloaded the sequencing reads from NCBI SRA database (https://www.ncbi.nlm.nih.gov/sra) (supplementary table S1). We assembled all the download RNA-seq data following above pipeline.…”

Analysis of Multiplicity of Hypoxia-Inducible Factors in the Evolution of Triplophysa Fish (Osteichthyes: Nemacheilinae) Reveals Hypoxic Environments Adaptation to Tibetan Plateau

“…Tibetan Plateau is commonly referred to as the "Roof of the World" (Zhou et al, 2006), which is the highest and largest plateau on earth. Its inhospitable environment, characterized by severe coldness, severe hypoxia and strong ultraviolet radiation (Su and Wang, 1992;Bickler and Buck, 2007;Cheviron and Brumfield, 2012), has profound effects on animal survival and thus, it is regarded as a global biodiversity hotspot and a natural laboratory for long-term hypoxia and cold adaptation studies research (Wu and Wu, 1992;Scheinfeldt and Tishkoff, 2010;Wang et al, 2011;Qi et al, 2012;Zhang et al, 2017). The oxygen content varies markedly daily, seasonally, and spatially (Soitamo et al, 2001).…”

Evidence for relaxed selection of mitogenome in rapid-flow cyprinids

“…Some may reduce oxygen consumption by shifting metabolic pathways and regulating expression of key genes, on the other hand, some will increase oxygen delivery by stimulating angiogenesis and regulating the proliferation of red blood cells (Nikinmaa 2005 ). Recent transcriptomic studies on fish adaptation to hypoxia provided us insights into molecular evolution and adaption to hypoxia (Yang et al 2014a , b ; Zhang et al 2017 ). Species living under high oxygen concentration may partially lose the ability in hypoxia adaptation, but the underlying molecular mechanisms are not well known (Fu et al 2014 ).…”