Allele surfing causes maladaptation in a Pacific salmon of conservation concern.

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 variatio...

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Main Authors: Quentin Rougemont, Thibault Leroy, Eric B Rondeau, Ben Koop, Louis Bernatchez
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-09-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1010918
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author Quentin Rougemont
Thibault Leroy
Eric B Rondeau
Ben Koop
Louis Bernatchez
author_facet Quentin Rougemont
Thibault Leroy
Eric B Rondeau
Ben Koop
Louis Bernatchez
author_sort Quentin Rougemont
collection DOAJ
description 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.
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spelling doaj.art-584fc5ffa1614a58b531be3a1f8d0e632023-10-14T05:31:52ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042023-09-01199e101091810.1371/journal.pgen.1010918Allele surfing causes maladaptation in a Pacific salmon of conservation concern.Quentin RougemontThibault LeroyEric B RondeauBen KoopLouis BernatchezHow 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.https://doi.org/10.1371/journal.pgen.1010918
spellingShingle Quentin Rougemont
Thibault Leroy
Eric B Rondeau
Ben Koop
Louis Bernatchez
Allele surfing causes maladaptation in a Pacific salmon of conservation concern.
PLoS Genetics
title Allele surfing causes maladaptation in a Pacific salmon of conservation concern.
title_full Allele surfing causes maladaptation in a Pacific salmon of conservation concern.
title_fullStr Allele surfing causes maladaptation in a Pacific salmon of conservation concern.
title_full_unstemmed Allele surfing causes maladaptation in a Pacific salmon of conservation concern.
title_short Allele surfing causes maladaptation in a Pacific salmon of conservation concern.
title_sort allele surfing causes maladaptation in a pacific salmon of conservation concern
url https://doi.org/10.1371/journal.pgen.1010918
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