The genomic basis of adaptation to profundal habitats across the Swiss Alpine whitefish radiation

Abstract When populations experience heterogenous environments multifarious divergent selection may lead to ecological speciation or even adaptive radiation. The underlying genetic architecture of adaptation can be simple or complex and is relevant for predicting evolutionary responses. Whitefish have radiated across Swiss perialpine lakes and within the radiation, more than 30 species have been taxonomically described. Across Swiss lake systems, several phenotypically similar species (i.e, ecomorphs) have evolved independently and utilise distinct environmental niches. Profundal species, adapted to spawn in depths below 60m, have repeatedly evolved in lakes Thun, Constance, Lucerne, Zug, and Walen. We here analysed whole-genome resequencing data of all three to six whitefish species of four of these lakes (Thun, Constance, Lucerne, and Walen) to identify genomic signals of parallel profundal adaptation. The results indicate that a small but spread-out fraction of the genome shows signals of parallel differentiation across all four studied lakes, with pairwise tests revealing more genomic regions with evidence of parallel evolution between profundal species when both were pelagic. Consistent with previous work investigating parallel divergence between two different Alpine whitefish ecomorphs, these results suggest a polygenic basis of adaptation including genotypic redundancy, which makes repeated evolution more likely but results in little repeatability of its genetic basis.