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

Hugo Cayuela*, Quentin Rougemont, Martin Laporte, Claire Mérot, Eric Normandeau, Yann Dorant, Ole K. Tørresen, Siv Nam Khang Hoff, Sissel Jentoft, Pascal Sirois, Martin Castonguay, Teunis Jansen, Kim Praebel, Marie Clément, Louis Bernatchez

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

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.
Original languageEnglish
JournalMolecular Ecology
Volume29
Issue number13
Pages (from-to)2379-2398
Number of pages20
ISSN0962-1083
DOIs
Publication statusPublished - 2020

Keywords

  • Speciation
  • Population genomics
  • RAD
  • Joint site frequency spectrum
  • Fish
  • Mallotus villosus
  • Inversion
  • ai

Cite this

Cayuela, H., Rougemont, Q., Laporte, M., Mérot, C., Normandeau, E., Dorant, Y., Tørresen, O. K., Hoff, S. N. K., Jentoft, S., Sirois, P., Castonguay, M., Jansen, T., Praebel, K., Clément, M., & Bernatchez, L. (2020). Shared ancestral polymorphism and chromosomal rearrangements as potential drivers of local adaptation in a marine fish. Molecular Ecology, 29(13), 2379-2398. https://doi.org/10.1111/mec.15499