Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis

Abstract Chromosomal inversions have long been recognized for their role in local adaptation. By suppressing recombination in heterozygous individuals, they can maintain coadapted gene complexes and protect them from homogenizing effects of gene flow. However, to fully understand their importance fo...

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Main Authors: Eva L. Koch, Hernán E. Morales, Jenny Larsson, Anja M. Westram, Rui Faria, Alan R. Lemmon, E. Moriarty Lemmon, Kerstin Johannesson, Roger K. Butlin
Format: Article
Language:English
Published: Oxford University Press 2021-06-01
Series:Evolution Letters
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Online Access:https://doi.org/10.1002/evl3.227
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author Eva L. Koch
Hernán E. Morales
Jenny Larsson
Anja M. Westram
Rui Faria
Alan R. Lemmon
E. Moriarty Lemmon
Kerstin Johannesson
Roger K. Butlin
author_facet Eva L. Koch
Hernán E. Morales
Jenny Larsson
Anja M. Westram
Rui Faria
Alan R. Lemmon
E. Moriarty Lemmon
Kerstin Johannesson
Roger K. Butlin
author_sort Eva L. Koch
collection DOAJ
description Abstract Chromosomal inversions have long been recognized for their role in local adaptation. By suppressing recombination in heterozygous individuals, they can maintain coadapted gene complexes and protect them from homogenizing effects of gene flow. However, to fully understand their importance for local adaptation we need to know their influence on phenotypes under divergent selection. For this, the marine snail Littorina saxatilis provides an ideal study system. Divergent ecotypes adapted to wave action and crab predation occur in close proximity on intertidal shores with gene flow between them. Here, we used F2 individuals obtained from crosses between the ecotypes to test for associations between genomic regions and traits distinguishing the Crab‐/Wave‐adapted ecotypes including size, shape, shell thickness, and behavior. We show that most of these traits are influenced by two previously detected inversion regions that are divergent between ecotypes. We thus gain a better understanding of one important underlying mechanism responsible for the rapid and repeated formation of ecotypes: divergent selection acting on inversions. We also found that some inversions contributed to more than one trait suggesting that they may contain several loci involved in adaptation, consistent with the hypothesis that suppression of recombination within inversions facilitates differentiation in the presence of gene flow.
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spelling doaj.art-4f910a753f6f495182c1b8c92182b2882023-09-02T07:37:49ZengOxford University PressEvolution Letters2056-37442021-06-015319621310.1002/evl3.227Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilisEva L. Koch0Hernán E. Morales1Jenny Larsson2Anja M. Westram3Rui Faria4Alan R. Lemmon5E. Moriarty Lemmon6Kerstin Johannesson7Roger K. Butlin8Department of Animal and Plant Sciences University of Sheffield Sheffield United KingdomEvolutionary Genetics Section Globe Institute University of Copenhagen Copenhagen DenmarkDepartment of Animal and Plant Sciences University of Sheffield Sheffield United KingdomDepartment of Animal and Plant Sciences University of Sheffield Sheffield United KingdomDepartment of Animal and Plant Sciences University of Sheffield Sheffield United KingdomDepartment of Scientific Computing Florida State University Tallahassee Florida FL 32306‐4120Department of Biological Science Florida State University Tallahassee Florida FL 32306‐4295Department of Marine Sciences University of Gothenburg Strömstad 45296 SwedenDepartment of Animal and Plant Sciences University of Sheffield Sheffield United KingdomAbstract Chromosomal inversions have long been recognized for their role in local adaptation. By suppressing recombination in heterozygous individuals, they can maintain coadapted gene complexes and protect them from homogenizing effects of gene flow. However, to fully understand their importance for local adaptation we need to know their influence on phenotypes under divergent selection. For this, the marine snail Littorina saxatilis provides an ideal study system. Divergent ecotypes adapted to wave action and crab predation occur in close proximity on intertidal shores with gene flow between them. Here, we used F2 individuals obtained from crosses between the ecotypes to test for associations between genomic regions and traits distinguishing the Crab‐/Wave‐adapted ecotypes including size, shape, shell thickness, and behavior. We show that most of these traits are influenced by two previously detected inversion regions that are divergent between ecotypes. We thus gain a better understanding of one important underlying mechanism responsible for the rapid and repeated formation of ecotypes: divergent selection acting on inversions. We also found that some inversions contributed to more than one trait suggesting that they may contain several loci involved in adaptation, consistent with the hypothesis that suppression of recombination within inversions facilitates differentiation in the presence of gene flow.https://doi.org/10.1002/evl3.227Divergence with gene flowhybrid zoneQTLrecombinationstructural variantsvariance partitioning
spellingShingle Eva L. Koch
Hernán E. Morales
Jenny Larsson
Anja M. Westram
Rui Faria
Alan R. Lemmon
E. Moriarty Lemmon
Kerstin Johannesson
Roger K. Butlin
Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis
Evolution Letters
Divergence with gene flow
hybrid zone
QTL
recombination
structural variants
variance partitioning
title Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis
title_full Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis
title_fullStr Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis
title_full_unstemmed Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis
title_short Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis
title_sort genetic variation for adaptive traits is associated with polymorphic inversions in littorina saxatilis
topic Divergence with gene flow
hybrid zone
QTL
recombination
structural variants
variance partitioning
url https://doi.org/10.1002/evl3.227
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