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Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals

Supergenes offer spectacular examples of long-term balancing selection in nature, but their origin and maintenance remain a mystery. Reduced recombination between arrangements, a critical aspect of many supergenes, protects adaptive multi-trait phenotypes but can lead to mutation accumulation. Mutat...

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Autores principales: Berdan, Emma L., Blanckaert, Alexandre, Butlin, Roger K., Flatt, Thomas, Slotte, Tanja, Wielstra, Ben
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9189497/
https://www.ncbi.nlm.nih.gov/pubmed/35694750
http://dx.doi.org/10.1098/rstb.2021.0199
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author Berdan, Emma L.
Blanckaert, Alexandre
Butlin, Roger K.
Flatt, Thomas
Slotte, Tanja
Wielstra, Ben
author_facet Berdan, Emma L.
Blanckaert, Alexandre
Butlin, Roger K.
Flatt, Thomas
Slotte, Tanja
Wielstra, Ben
author_sort Berdan, Emma L.
collection PubMed
description Supergenes offer spectacular examples of long-term balancing selection in nature, but their origin and maintenance remain a mystery. Reduced recombination between arrangements, a critical aspect of many supergenes, protects adaptive multi-trait phenotypes but can lead to mutation accumulation. Mutation accumulation can stabilize the system through the emergence of associative overdominance (AOD), destabilize the system, or lead to new evolutionary outcomes. One outcome is the formation of maladaptive balanced lethal systems, where only heterozygotes remain viable and reproduce. We investigated the conditions under which these different outcomes occur, assuming a scenario of introgression after divergence. We found that AOD aided the invasion of a new supergene arrangement and the establishment of a polymorphism. However, this polymorphism was easily destabilized by further mutation accumulation, which was often asymmetric, disrupting the quasi-equilibrium state. Mechanisms that accelerated degeneration tended to amplify asymmetric mutation accumulation between the supergene arrangements and vice-versa. As the evolution of balanced lethal systems requires symmetric degeneration of both arrangements, this leaves only restricted conditions for their evolution, namely small population sizes and low rates of gene conversion. The dichotomy between the persistence of polymorphism and degeneration of supergene arrangements likely underlies the rarity of balanced lethal systems in nature. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.
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spelling pubmed-91894972022-06-21 Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals Berdan, Emma L. Blanckaert, Alexandre Butlin, Roger K. Flatt, Thomas Slotte, Tanja Wielstra, Ben Philos Trans R Soc Lond B Biol Sci Articles Supergenes offer spectacular examples of long-term balancing selection in nature, but their origin and maintenance remain a mystery. Reduced recombination between arrangements, a critical aspect of many supergenes, protects adaptive multi-trait phenotypes but can lead to mutation accumulation. Mutation accumulation can stabilize the system through the emergence of associative overdominance (AOD), destabilize the system, or lead to new evolutionary outcomes. One outcome is the formation of maladaptive balanced lethal systems, where only heterozygotes remain viable and reproduce. We investigated the conditions under which these different outcomes occur, assuming a scenario of introgression after divergence. We found that AOD aided the invasion of a new supergene arrangement and the establishment of a polymorphism. However, this polymorphism was easily destabilized by further mutation accumulation, which was often asymmetric, disrupting the quasi-equilibrium state. Mechanisms that accelerated degeneration tended to amplify asymmetric mutation accumulation between the supergene arrangements and vice-versa. As the evolution of balanced lethal systems requires symmetric degeneration of both arrangements, this leaves only restricted conditions for their evolution, namely small population sizes and low rates of gene conversion. The dichotomy between the persistence of polymorphism and degeneration of supergene arrangements likely underlies the rarity of balanced lethal systems in nature. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’. The Royal Society 2022-08-01 2022-06-13 /pmc/articles/PMC9189497/ /pubmed/35694750 http://dx.doi.org/10.1098/rstb.2021.0199 Text en © 2022 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Articles
Berdan, Emma L.
Blanckaert, Alexandre
Butlin, Roger K.
Flatt, Thomas
Slotte, Tanja
Wielstra, Ben
Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals
title Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals
title_full Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals
title_fullStr Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals
title_full_unstemmed Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals
title_short Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals
title_sort mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9189497/
https://www.ncbi.nlm.nih.gov/pubmed/35694750
http://dx.doi.org/10.1098/rstb.2021.0199
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