Allele surfing causes maladaptation in a Pacific salmon of conservation concern

PLoS Genet. 2023 Sep 8;19(9):e1010918. doi: 10.1371/journal.pgen.1010918. eCollection 2023 Sep.

Abstract

How various factors, including demography, recombination or genome duplication, may impact the efficacy of natural selection and the burden of deleterious mutations, is a central question in evolutionary biology and genetics. In this study, we show that key evolutionary processes, including variations in i) effective population size (Ne) ii) recombination rates and iii) chromosome inheritance, have influenced the genetic load and efficacy of selection in Coho salmon (Oncorhynchus kisutch), a widely distributed salmonid species on the west coast of North America. Using whole genome resequencing data from 14 populations at different migratory distances from their southern glacial refugium, we found evidence supporting gene surfing, wherein reduced Ne at the postglacial recolonization front, leads to a decrease in the efficacy of selection and a surf of deleterious alleles in the northernmost populations. Furthermore, our results indicate that recombination rates play a prime role in shaping the load along the genome. Additionally, we identified variation in polyploidy as a contributing factor to within-genome variation of the load. Overall, our results align remarkably well with expectations under the nearly neutral theory of molecular evolution. We discuss the fundamental and applied implications of these findings for evolutionary and conservation genomics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animals
  • Biological Evolution*
  • Evolution, Molecular
  • Oncorhynchus kisutch* / genetics
  • Selection, Genetic

Grants and funding

This research was supported by a Genome Canada strategic grant entitle EPIC4–Enhanced Production in Coho: Culture, Community Catch (grant ID: 229COH, Genome Canada) attributed to L.B. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.