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Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution

Chromosomal inversions have been shown to play a major role in a local adaptation by suppressing recombination between alternative arrangements and maintaining beneficial allele combinations. However, so far, their importance relative to the remaining genome remains largely unknown. Understanding th...

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Autores principales: Koch, Eva L., Ravinet, Mark, Westram, Anja M., Johannesson, Kerstin, Butlin, Roger K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9826283/
https://www.ncbi.nlm.nih.gov/pubmed/35994296
http://dx.doi.org/10.1111/evo.14602
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author Koch, Eva L.
Ravinet, Mark
Westram, Anja M.
Johannesson, Kerstin
Butlin, Roger K.
author_facet Koch, Eva L.
Ravinet, Mark
Westram, Anja M.
Johannesson, Kerstin
Butlin, Roger K.
author_sort Koch, Eva L.
collection PubMed
description Chromosomal inversions have been shown to play a major role in a local adaptation by suppressing recombination between alternative arrangements and maintaining beneficial allele combinations. However, so far, their importance relative to the remaining genome remains largely unknown. Understanding the genetic architecture of adaptation requires better estimates of how loci of different effect sizes contribute to phenotypic variation. Here, we used three Swedish islands where the marine snail Littorina saxatilis has repeatedly evolved into two distinct ecotypes along a habitat transition. We estimated the contribution of inversion polymorphisms to phenotypic divergence while controlling for polygenic effects in the remaining genome using a quantitative genetics framework. We confirmed the importance of inversions but showed that contributions of loci outside inversions are of similar magnitude, with variable proportions dependent on the trait and the population. Some inversions showed consistent effects across all sites, whereas others exhibited site‐specific effects, indicating that the genomic basis for replicated phenotypic divergence is only partly shared. The contributions of sexual dimorphism as well as environmental factors to phenotypic variation were significant but minor compared to inversions and polygenic background. Overall, this integrated approach provides insight into the multiple mechanisms contributing to parallel phenotypic divergence.
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spelling pubmed-98262832023-01-09 Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution Koch, Eva L. Ravinet, Mark Westram, Anja M. Johannesson, Kerstin Butlin, Roger K. Evolution Original Articles Chromosomal inversions have been shown to play a major role in a local adaptation by suppressing recombination between alternative arrangements and maintaining beneficial allele combinations. However, so far, their importance relative to the remaining genome remains largely unknown. Understanding the genetic architecture of adaptation requires better estimates of how loci of different effect sizes contribute to phenotypic variation. Here, we used three Swedish islands where the marine snail Littorina saxatilis has repeatedly evolved into two distinct ecotypes along a habitat transition. We estimated the contribution of inversion polymorphisms to phenotypic divergence while controlling for polygenic effects in the remaining genome using a quantitative genetics framework. We confirmed the importance of inversions but showed that contributions of loci outside inversions are of similar magnitude, with variable proportions dependent on the trait and the population. Some inversions showed consistent effects across all sites, whereas others exhibited site‐specific effects, indicating that the genomic basis for replicated phenotypic divergence is only partly shared. The contributions of sexual dimorphism as well as environmental factors to phenotypic variation were significant but minor compared to inversions and polygenic background. Overall, this integrated approach provides insight into the multiple mechanisms contributing to parallel phenotypic divergence. John Wiley and Sons Inc. 2022-09-01 2022-10 /pmc/articles/PMC9826283/ /pubmed/35994296 http://dx.doi.org/10.1111/evo.14602 Text en © 2022 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Koch, Eva L.
Ravinet, Mark
Westram, Anja M.
Johannesson, Kerstin
Butlin, Roger K.
Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution
title Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution
title_full Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution
title_fullStr Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution
title_full_unstemmed Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution
title_short Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution
title_sort genetic architecture of repeated phenotypic divergence in littorina saxatilis ecotype evolution
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9826283/
https://www.ncbi.nlm.nih.gov/pubmed/35994296
http://dx.doi.org/10.1111/evo.14602
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