Selection and environmental adaptation along a path to speciation in the Tibetan frog Nanorana parkeri

Significance Central topics in evolutionary biology include uncovering the processes and genetic bases of speciation and documenting environmental adaptations and processes responsible for them. The challenging environment of the Qinghai-Tibetan Plateau (QTP) facilitates such investigations, and the Tibetan frog, Nanorana parkeri, offers a unique opportunity to investigate these processes. A cohort of whole-genome sequences of 63 individuals from across its entire range opens avenues for incorporating population genomics into studies of speciation. Natural selection plays an important role in maintaining and driving the continuing divergence and reproductive isolation of populations of the species. The QTP is a natural laboratory for studying how selection drives adaptation, how environments influence evolutionary history, and how these factors can interact to provide insight into speciation.
Tibetan frogs, Nanorana parkeri, are differentiated genetically but not morphologically along geographical and elevational gradients in a challenging environment, presenting a unique opportunity to investigate processes leading to speciation. Analyses of whole genomes of 63 frogs reveal population structuring and historical demography, characterized by highly restricted gene flow in a narrow geographic zone lying between matrilines West (W) and East (E). A population found only along a single tributary of the Yalu Zangbu River has the mitogenome only of E, whereas nuclear genes of W comprise 89–95% of the nuclear genome. Selection accounts for 579 broadly scattered, highly divergent regions (HDRs) of the genome, which involve 365 genes. These genes fall into 51 gene ontology (GO) functional classes, 14 of which are likely to be important in driving reproductive isolation. GO enrichment analyses of E reveal many overrepresented functional categories associated with adaptation to high elevations, including blood circulation, response to hypoxia, and UV radiation. Four genes, including DNAJC8 in the brain, TNNC1 and ADORA1 in the heart, and LAMB3 in the lung, differ in levels of expression between low- and high-elevation populations. High-altitude adaptation plays an important role in maintaining and driving continuing divergence and reproductive isolation. Use of total genomes enabled recognition of selection and adaptation in and between populations, as well as documentation of evolution along a stepped cline toward speciation.