Climate Adaptation and Drift Shape the Genomes of Two Eel-Goby Sister Species Endemic to Contrasting Latitude

SIMPLE SUMMARY: Climate is one of the most important drivers for adaptive evolution and ecological speciation in teleost species. Using whole-genome re-sequencing technology, this study evaluated the role of divergent climate selection in shaping the genetic divergence of two eel-goby sister species spanning contrasting latitude gradients. High baseline genetic differentiation was found between them. Substantial elevated divergent loci were detected to be widespread throughout their genomes, which may arise from divergent climate selection, in addition to historical demographic processes. The loci exhibiting selective signatures highlighted the roles of genes associated with substance metabolism, energy production, response to environmental cues, and reproductive activity in latitude gradient adaptation and hence the climate-driven divergence of the two species. The results provided important insights into how climate changes related to latitude may drive genetic differentiation and thereby ecological speciation in marine teleosts. ABSTRACT: Deciphering the role of climate adaptation in generating genetic divergence and hence speciation is a central question in evolution. Comparisons of genomes of closely related species spanning selective climate gradients are particularly informative in discerning the signatures of selection and thereby providing valuable information concerning the role of climate adaptation in speciation. Here we re-sequenced 99 genomes of the two sister eel-goby species Odontamblyopus lacepedii and O. rebecca, which are endemic to tidal mudflats spanning contrasting latitude gradients, to estimate the influence of divergent climate selection on shaping genome-wide patterns of divergence. The results indicated that genome-wide differentiation between the two species was evident (genome-wide FST = 0.313). Against a background of high baseline genomic divergence, 588 and 1202 elevated divergent loci were detected to be widespread throughout their genomes, as opposed to focused within small islands of genomic regions. These patterns of divergence may arise from divergent climate selection in addition to genetic drift acting through past glacial segregation (1.46 million years ago). We identified several candidate genes that exhibited elevated divergence between the two species, including genes associated with substance metabolism, energy production, and response to environmental cues, all putative candidates closely linked to thermal adaptation expected from the latitude gradient. Interestingly, several candidates related to gamete recognition and time of puberty, and also exhibited elevated divergence, indicating their possible role in pre-zygote isolation and speciation of the two species. Our results would expand our knowledge on the roles of latitude climate adaptation and genetic drift in generating and maintaining biodiversity in marine teleosts.