Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals
Autor(a) principal: | |
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Data de Publicação: | 2022 |
Outros Autores: | , , , , |
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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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 |
dc.format.none.fl_str_mv |
application/pdf |
dc.publisher.none.fl_str_mv |
The Royal Society |
publisher.none.fl_str_mv |
The Royal Society |
dc.source.none.fl_str_mv |
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Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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