Shared ancestral polymorphism and chromosomal rearrangements as potential drivers of local adaptation in a marine fish

• Published in: Molecular Ecology
• Main Authors: Cayuela, Hugo, Rougemont, Quentin, Laporte, Martin, Mérot, Claire, Normandeau, Eric, Dorant, Yann, Tørresen, Ole K., Hoff, Siv Nam Khang, Jentoft, Sissel, Sirois, Pascal, Castonguay, Martin, Jansen, Teunis, Praebel, Kim, Clément, Marie, Bernatchez, Louis
• Format: Article in Journal/Newspaper
• Language: English
• Published: 2020
• Subjects: Speciation; Population genomics; RAD; Joint site frequency spectrum; Fish; Mallotus villosus; Inversion; ai; /dk/atira/pure/sustainabledevelopmentgoals/life_below_water; name=SDG 14 - Life Below Water; Northwest Atlantic
• Online Access: https://orbit.dtu.dk/en/publications/79dc19ac-0b4d-4eab-b769-aab709897a35; https://doi.org/10.1111/mec.15499; https://backend.orbit.dtu.dk/ws/files/215032317/BERAT_mec.15499.pdf

Gene flow has tremendous importance on local adaptation, by influencing the fate of de novo mutations, maintaining standing genetic variation, and driving adaptive introgression. Furthermore, structural variation as chromosomal rearrangements may facilitate adaptation despite high gene flow. However, our understanding of evolutionary mechanisms impending or favoring local adaptation in the presence of gene flow is still limited to a restricted number of study systems. In this study, we examined how demographic history, shared ancestral polymorphism, and gene flow among glacial lineages contribute to local adaptation to sea conditions in a marine fish, the capelin ( Mallotus villosus ). We first assembled a 490 Mbp draft genome of M. villosus to map our RAD sequence reads. Then, we used a large dataset of genome-wide single nucleotide polymorphisms (25,904 filtered SNPs) genotyped in 1,310 individuals collected from 31 spawning sites in the northwest Atlantic. We reconstructed the history of divergence among three glacial lineages and showed that they likely diverged from 3.8 to 1.8 MyA and experienced secondary contacts. Within each lineage, our analyses provided evidence for large Ne and high gene flow among spawning sites. Within the NWA lineage, we detected a polymorphic chromosomal rearrangement leading to the occurrence of three haplogroups. Genotype-environment associations revealed molecular signatures of local adaptation to environmental conditions prevailing at spawning sites. Our study also suggests that, both shared polymorphism among lineages, resulting from standing genetic variation or introgression, and chromosomal rearrangements may contribute to local adaptation in the presence of high gene flow.