Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: simulations and empirical data from pine‐feeding hymenopterans

Detalhes bibliográficos
Autor(a) principal: Bendall, Emily E.
Data de Publicação: 2022
Outros Autores: Bagley, Robin K., Sousa, Vitor C, Linnen, Catherine R.
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10451/51569
Resumo: Although haplodiploidy is widespread in nature, the evolutionary consequences of this mode of reproduction are not well characterized. Here, we examine how genome-wide hemizygosity and a lack of recombination in haploid males affects genomic differentiation in populations that diverge via natural selection while experiencing gene flow. First, we simulated diploid and haplodiploid “genomes” (500-kb loci) evolving under an isolation-with-migration model with mutation, drift, selection, migration, and recombination; and examined differentiation at neutral sites both tightly and loosely linked to a divergently selected site. So long as there is divergent selection and migration, sex-limited hemizygosity and recombination cause elevated differentiation (i.e., produce a “faster-haplodiploid effect”) in haplodiploid populations relative to otherwise equivalent diploid populations, for both recessive and codominant mutations. Second, we used genome-wide SNP data to model divergence history and describe patterns of genomic differentiation between sympatric populations of Neodiprion lecontei and N. pinetum, a pair of pine sawfly species (order: Hymenoptera; family: Diprionidae) that are specialized on different pine hosts. These analyses support a history of continuous gene exchange throughout divergence and reveal a pattern of heterogeneous genomic differentiation that is consistent with divergent selection on many unlinked loci. Third, using simulations of haplodiploid and diploid populations evolving according to the estimated divergence history of N. lecontei and N. pinetum, we found that divergent selection would lead to higher differentiation in haplodiploids. Based on these results, we hypothesize that haplodiploids undergo divergence-with-gene-flow and sympatric speciation more readily than diploids.
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spelling Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: simulations and empirical data from pine‐feeding hymenopteransAlthough haplodiploidy is widespread in nature, the evolutionary consequences of this mode of reproduction are not well characterized. Here, we examine how genome-wide hemizygosity and a lack of recombination in haploid males affects genomic differentiation in populations that diverge via natural selection while experiencing gene flow. First, we simulated diploid and haplodiploid “genomes” (500-kb loci) evolving under an isolation-with-migration model with mutation, drift, selection, migration, and recombination; and examined differentiation at neutral sites both tightly and loosely linked to a divergently selected site. So long as there is divergent selection and migration, sex-limited hemizygosity and recombination cause elevated differentiation (i.e., produce a “faster-haplodiploid effect”) in haplodiploid populations relative to otherwise equivalent diploid populations, for both recessive and codominant mutations. Second, we used genome-wide SNP data to model divergence history and describe patterns of genomic differentiation between sympatric populations of Neodiprion lecontei and N. pinetum, a pair of pine sawfly species (order: Hymenoptera; family: Diprionidae) that are specialized on different pine hosts. These analyses support a history of continuous gene exchange throughout divergence and reveal a pattern of heterogeneous genomic differentiation that is consistent with divergent selection on many unlinked loci. Third, using simulations of haplodiploid and diploid populations evolving according to the estimated divergence history of N. lecontei and N. pinetum, we found that divergent selection would lead to higher differentiation in haplodiploids. Based on these results, we hypothesize that haplodiploids undergo divergence-with-gene-flow and sympatric speciation more readily than diploids.WileyRepositório da Universidade de LisboaBendall, Emily E.Bagley, Robin K.Sousa, Vitor CLinnen, Catherine R.2023-03-01T01:30:30Z2022-032022-03-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10451/51569engBendall, E.E., Bagley, R.K., Sousa, V.C. and Linnen, C.R. (2022), Faster-haplodiploid evolution under divergence-with-gene-flow: simulations and empirical data from pine-feeding hymenopterans. Mol Ecol. Accepted Author Manuscript. https://doi.org/10.1111/mec.1641010.1111/mec.16410info: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:RCAAP2023-11-08T16:56:21Zoai:repositorio.ul.pt:10451/51569Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T22:02:50.834366Repositório 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 Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: simulations and empirical data from pine‐feeding hymenopterans
title Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: simulations and empirical data from pine‐feeding hymenopterans
spellingShingle Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: simulations and empirical data from pine‐feeding hymenopterans
Bendall, Emily E.
title_short Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: simulations and empirical data from pine‐feeding hymenopterans
title_full Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: simulations and empirical data from pine‐feeding hymenopterans
title_fullStr Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: simulations and empirical data from pine‐feeding hymenopterans
title_full_unstemmed Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: simulations and empirical data from pine‐feeding hymenopterans
title_sort Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: simulations and empirical data from pine‐feeding hymenopterans
author Bendall, Emily E.
author_facet Bendall, Emily E.
Bagley, Robin K.
Sousa, Vitor C
Linnen, Catherine R.
author_role author
author2 Bagley, Robin K.
Sousa, Vitor C
Linnen, Catherine R.
author2_role author
author
author
dc.contributor.none.fl_str_mv Repositório da Universidade de Lisboa
dc.contributor.author.fl_str_mv Bendall, Emily E.
Bagley, Robin K.
Sousa, Vitor C
Linnen, Catherine R.
description Although haplodiploidy is widespread in nature, the evolutionary consequences of this mode of reproduction are not well characterized. Here, we examine how genome-wide hemizygosity and a lack of recombination in haploid males affects genomic differentiation in populations that diverge via natural selection while experiencing gene flow. First, we simulated diploid and haplodiploid “genomes” (500-kb loci) evolving under an isolation-with-migration model with mutation, drift, selection, migration, and recombination; and examined differentiation at neutral sites both tightly and loosely linked to a divergently selected site. So long as there is divergent selection and migration, sex-limited hemizygosity and recombination cause elevated differentiation (i.e., produce a “faster-haplodiploid effect”) in haplodiploid populations relative to otherwise equivalent diploid populations, for both recessive and codominant mutations. Second, we used genome-wide SNP data to model divergence history and describe patterns of genomic differentiation between sympatric populations of Neodiprion lecontei and N. pinetum, a pair of pine sawfly species (order: Hymenoptera; family: Diprionidae) that are specialized on different pine hosts. These analyses support a history of continuous gene exchange throughout divergence and reveal a pattern of heterogeneous genomic differentiation that is consistent with divergent selection on many unlinked loci. Third, using simulations of haplodiploid and diploid populations evolving according to the estimated divergence history of N. lecontei and N. pinetum, we found that divergent selection would lead to higher differentiation in haplodiploids. Based on these results, we hypothesize that haplodiploids undergo divergence-with-gene-flow and sympatric speciation more readily than diploids.
publishDate 2022
dc.date.none.fl_str_mv 2022-03
2022-03-01T00:00:00Z
2023-03-01T01:30:30Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
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dc.identifier.uri.fl_str_mv http://hdl.handle.net/10451/51569
url http://hdl.handle.net/10451/51569
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Bendall, E.E., Bagley, R.K., Sousa, V.C. and Linnen, C.R. (2022), Faster-haplodiploid evolution under divergence-with-gene-flow: simulations and empirical data from pine-feeding hymenopterans. Mol Ecol. Accepted Author Manuscript. https://doi.org/10.1111/mec.16410
10.1111/mec.16410
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
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