Genomic signature of shifts in selection and alkaline adaptation in highland fish

Understanding how organisms adapt to aquatic life at high altitude is fundamental in evolutionary biology. This objective has been addressed primarily related to hypoxia adaptation by recent comparative studies, whereas highland fish has also long suffered extreme alkaline environment, insight into the genomic basis of alkaline adaptation has rarely been provided. Here, we compared the genomes or transcriptomes of 15 fish species, including two alkaline tolerant highland fish species and their six alkaline intolerant relatives, three alkaline tolerant lowland fish species and four alkaline intolerant species. We found putatively consistent patterns of molecular evolution in alkaline tolerant species in a large number of shared orthologs within highland and lowland fish taxa. Remarkably, we identified consistent signatures of accelerated evolution and positive selection in a set of shared genes associated with ion transport, apoptosis, immune response and energy metabolisms in alkaline tolerant species within both highland and lowland fish taxa. This is one of the first comparative studies that began to elucidate the consistent genomic signature of alkaline adaptation shared by highland and lowland fish. This finding also highlights the adaptive molecular evolution changes that support fish adapting to extreme environments at high altitude. Significance StatementLittle is known about how wild fish responds to extreme alkaline stress besides hypoxia at high altitude. Comparative genomics has begun to elucidate the genomic basis of alkaline adaptation in lowland fish, such as killifish, but insight from highland fish has lagged behind. The common role of adaptive molecular evolution during alkaline adaptation in highland and lowland fish has rarely been discussed. We address this question by comparing 15 fish omics data. We find numbers of shared orthologs exhibited consistent patterns of molecular evolution in alkaline tolerant species relative to intolerant species. We further identify remarkably consistent signatures of rapidly evolving and positive selection in a substantial shared core of genes in both highland and lowland alkaline tolerant species.