Cargando…
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...
Autores principales: | , , , , , |
---|---|
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 |
_version_ | 1784725605721309184 |
---|---|
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’. |
format | Online Article Text |
id | pubmed-9189497 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | The Royal Society |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT berdanemmal mutationaccumulationopposespolymorphismsupergenesandthecuriouscaseofbalancedlethals AT blanckaertalexandre mutationaccumulationopposespolymorphismsupergenesandthecuriouscaseofbalancedlethals AT butlinrogerk mutationaccumulationopposespolymorphismsupergenesandthecuriouscaseofbalancedlethals AT flattthomas mutationaccumulationopposespolymorphismsupergenesandthecuriouscaseofbalancedlethals AT slottetanja mutationaccumulationopposespolymorphismsupergenesandthecuriouscaseofbalancedlethals AT wielstraben mutationaccumulationopposespolymorphismsupergenesandthecuriouscaseofbalancedlethals |