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

Detalhes bibliográficos
Autor(a) principal: Berdan, Emma L.
Data de Publicação: 2022
Outros Autores: Blanckaert, Alexandre, Butlin, Roger K., Flatt, Thomas, Slotte, Tanja, Wielstra, Ben
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10451/53566
Resumo: 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 Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethalsSupergenes 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 SocietyRepositório da Universidade de LisboaBerdan, Emma L.Blanckaert, AlexandreButlin, Roger K.Flatt, ThomasSlotte, TanjaWielstra, Ben2022-06-29T18:28:02Z20222022-01-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10451/53566engBerdan EL, Blanckaert A,Butlin RK, Flatt T, Slotte T, Wielstra B. 2022Mutation accumulation opposes polymorphism:supergenes and the curious case of balancedlethals.Phil. Trans. R. Soc. B377: 20210199.https://doi.org/10.1098/rstb.2021.019910.1098/rstb.2021.0199info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-11-08T16:59:22Zoai:repositorio.ul.pt:10451/53566Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T22:04:28.461837Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv 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
spellingShingle Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals
Berdan, Emma L.
title_short 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_sort Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals
author Berdan, Emma L.
author_facet Berdan, Emma L.
Blanckaert, Alexandre
Butlin, Roger K.
Flatt, Thomas
Slotte, Tanja
Wielstra, Ben
author_role author
author2 Blanckaert, Alexandre
Butlin, Roger K.
Flatt, Thomas
Slotte, Tanja
Wielstra, Ben
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Repositório da Universidade de Lisboa
dc.contributor.author.fl_str_mv Berdan, Emma L.
Blanckaert, Alexandre
Butlin, Roger K.
Flatt, Thomas
Slotte, Tanja
Wielstra, Ben
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’.
publishDate 2022
dc.date.none.fl_str_mv 2022-06-29T18:28:02Z
2022
2022-01-01T00:00:00Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10451/53566
url http://hdl.handle.net/10451/53566
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Berdan EL, Blanckaert A,Butlin RK, Flatt T, Slotte T, Wielstra B. 2022Mutation accumulation opposes polymorphism:supergenes and the curious case of balancedlethals.Phil. Trans. R. Soc. B377: 20210199.https://doi.org/10.1098/rstb.2021.0199
10.1098/rstb.2021.0199
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
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dc.publisher.none.fl_str_mv The Royal Society
publisher.none.fl_str_mv The Royal Society
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
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