Post-glacial recolonization and multiple scales of secondary contact contribute to contemporary Atlantic salmon (Salmo salar) genomic variation in North America

Aim: In northern environments, periods of isolation during Pleistocene glaciations and subsequent recolonization and secondary contact have had a significant influence on contemporary diversity of many species. The recent advent of high-resolution genomic analyses allows unprecedented power to resolve genomic signatures of such events in northern species. Here, we provide the highest resolution genomic characterization of Atlantic salmon in North America to date to infer glacial refugia and the geographic scales of post-glacial secondary contact. Location: North America. Taxon: Atlantic salmon, Salmo salar. Methods: Samples were collected for 5455 individuals from 148 populations, encompassing the majority of the Atlantic salmon's native range in North America, from Labrador to Maine. Individuals were genotyped using a 220K single nucleotide polymorphism array aligned to the Atlantic salmon (Salmo salar) genome. Spatial genetic structure (principal component analysis, k-means clustering, admixture) was evaluated in conjunction with genomic comparisons of these identified lineages to infer the refugia during the last glacial maximum and regions of secondary contact following recolonization. Results: Spatial genomic analyses identified three phylogeographic groups, consistent with the northward recolonization from two southern glacial refugia in North America (a western Maritime lineage and an eastern Newfoundland and Labrador lineage), with subsequent differentiation of the eastern lineage into two separate groups. Secondary contact among these North American groups was observed within the northern Gulf of St. Lawrence, and evidence of trans-Atlantic secondary contact was detected within the eastern Newfoundland and Labrador lineage. Comparison of groups from insular Newfoundland with those from mainland Labrador suggests genomic regions displaying high differentiation were characterized by elevated European admixture, suggesting a possible role of European secondary contact in population divergence. Main Conclusions: These findings present the first evidence suggesting that genomic diversity in extant North American Atlantic salmon populations has resulted from allopatric isolation in two glacial refugia followed by both regional and trans-Atlantic recolonization and secondary contact and demonstrate the power of genomic tools to resolve historical drivers of diversity in wild populations.