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Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly

How natural diversity is maintained is an evolutionary puzzle. Genetic variation can be eroded by drift and directional selection but some polymorphisms persist for long time periods, implicating a role for balancing selection. Here, we investigate the maintenance of a chromosomal inversion polymorp...

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Autores principales: Mérot, Claire, Llaurens, Violaine, Normandeau, Eric, Bernatchez, Louis, Wellenreuther, Maren
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6997199/
https://www.ncbi.nlm.nih.gov/pubmed/32015341
http://dx.doi.org/10.1038/s41467-020-14479-7
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author Mérot, Claire
Llaurens, Violaine
Normandeau, Eric
Bernatchez, Louis
Wellenreuther, Maren
author_facet Mérot, Claire
Llaurens, Violaine
Normandeau, Eric
Bernatchez, Louis
Wellenreuther, Maren
author_sort Mérot, Claire
collection PubMed
description How natural diversity is maintained is an evolutionary puzzle. Genetic variation can be eroded by drift and directional selection but some polymorphisms persist for long time periods, implicating a role for balancing selection. Here, we investigate the maintenance of a chromosomal inversion polymorphism in the seaweed fly Coelopa frigida. Using experimental evolution and quantifying fitness, we show that the inversion underlies a life-history trade-off, whereby each haplotype has opposing effects on larval survival and adult reproduction. Numerical simulations confirm that such antagonistic pleiotropy can maintain polymorphism. Our results also highlight the importance of sex-specific effects, dominance and environmental heterogeneity, whose interaction enhances the maintenance of polymorphism through antagonistic pleiotropy. Overall, our findings directly demonstrate how overdominance and sexual antagonism can emerge from a life-history trade-off, inviting reconsideration of antagonistic pleiotropy as a key part of multi-headed balancing selection processes that enable the persistence of genetic variation.
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spelling pubmed-69971992020-02-05 Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly Mérot, Claire Llaurens, Violaine Normandeau, Eric Bernatchez, Louis Wellenreuther, Maren Nat Commun Article How natural diversity is maintained is an evolutionary puzzle. Genetic variation can be eroded by drift and directional selection but some polymorphisms persist for long time periods, implicating a role for balancing selection. Here, we investigate the maintenance of a chromosomal inversion polymorphism in the seaweed fly Coelopa frigida. Using experimental evolution and quantifying fitness, we show that the inversion underlies a life-history trade-off, whereby each haplotype has opposing effects on larval survival and adult reproduction. Numerical simulations confirm that such antagonistic pleiotropy can maintain polymorphism. Our results also highlight the importance of sex-specific effects, dominance and environmental heterogeneity, whose interaction enhances the maintenance of polymorphism through antagonistic pleiotropy. Overall, our findings directly demonstrate how overdominance and sexual antagonism can emerge from a life-history trade-off, inviting reconsideration of antagonistic pleiotropy as a key part of multi-headed balancing selection processes that enable the persistence of genetic variation. Nature Publishing Group UK 2020-02-03 /pmc/articles/PMC6997199/ /pubmed/32015341 http://dx.doi.org/10.1038/s41467-020-14479-7 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Mérot, Claire
Llaurens, Violaine
Normandeau, Eric
Bernatchez, Louis
Wellenreuther, Maren
Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly
title Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly
title_full Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly
title_fullStr Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly
title_full_unstemmed Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly
title_short Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly
title_sort balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6997199/
https://www.ncbi.nlm.nih.gov/pubmed/32015341
http://dx.doi.org/10.1038/s41467-020-14479-7
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