Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow
Selection shapes genetic diversity around target mutations, yet little is known about how selection on specific loci affects the genetic trajectories of populations, including their genome-wide patterns of diversity and demographic responses. Here we study the patterns of genetic variation and geogr...
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2023-07-01
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| Online Access: | https://peercommunityjournal.org/articles/10.24072/pcjournal.298/ |
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| author | Rodríguez de Cara, María Ángeles Jay, Paul Rougemont, Quentin Chouteau, Mathieu Whibley, Annabel Huber, Barbara Piron-Prunier, Florence Ramos, Renato Rogner Freitas, André V. L. Salazar, Camilo Silva-Brandão, Karina Lucas Torres, Tatiana Teixeira Joron, Mathieu |
| author_facet | Rodríguez de Cara, María Ángeles Jay, Paul Rougemont, Quentin Chouteau, Mathieu Whibley, Annabel Huber, Barbara Piron-Prunier, Florence Ramos, Renato Rogner Freitas, André V. L. Salazar, Camilo Silva-Brandão, Karina Lucas Torres, Tatiana Teixeira Joron, Mathieu |
| author_sort | Rodríguez de Cara, María Ángeles |
| collection | DOAJ |
| description | Selection shapes genetic diversity around target mutations, yet little is known about how selection on specific loci affects the genetic trajectories of populations, including their genome-wide patterns of diversity and demographic responses. Here we study the patterns of genetic variation and geographic structure in a neotropical butterfly, Heliconius numata, and its closely related allies in the so-called melpomene-silvaniform clade. H. numata is known to have evolved an inversion supergene which controls variation in wing patterns involved in mimicry associations with distinct groups of co-mimics whereas it is associated to disassortative mate preferences and heterozygote advantage at this locus. We contrasted patterns of genetic diversity and structure 1) among extant polymorphic and monomorphic populations of H. numata, 2) between H. numata and its close relatives, and 3) between ancestral lineages. We show that H. numata populations which carry the inversions as a balanced polymorphism show markedly distinct patterns of diversity compared to all other taxa. They show the highest genetic diversity and effective population size estimates in the entire clade, as well as a low level of geographic structure and isolation by distance across the entire Amazon basin. By contrast, monomorphic populations of H. numata as well as its sister species and their ancestral lineages all show lower effective population sizes and genetic diversity, and higher levels of geographical structure across the continent. One hypothesis is that the large effective population size of polymorphic populations could be caused by the shift to a regime of balancing selection due to the genetic load and disassortative preferences associated with inversions. Testing this hypothesis with forward simulations supported the observation of increased diversity in populations with the supergene. Our results are consistent with the hypothesis that the formation of the supergene triggered a change in gene flow, causing a general increase in genetic diversity and the homogenisation of genomes at the continental scale.
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| format | Article |
| id | doaj-art-31128d69f1b74b03a9e60fa7ca7c2c63 |
| institution | Kabale University |
| issn | 2804-3871 |
| language | English |
| publishDate | 2023-07-01 |
| publisher | Peer Community In |
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| series | Peer Community Journal |
| spelling | doaj-art-31128d69f1b74b03a9e60fa7ca7c2c632025-02-07T10:16:49ZengPeer Community InPeer Community Journal2804-38712023-07-01310.24072/pcjournal.29810.24072/pcjournal.298Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow Rodríguez de Cara, María Ángeles0Jay, Paul1https://orcid.org/0000-0001-5979-1263Rougemont, Quentin2https://orcid.org/0000-0003-2987-3801Chouteau, Mathieu3Whibley, Annabel4Huber, Barbara5Piron-Prunier, Florence6Ramos, Renato Rogner7Freitas, André V. L.8Salazar, Camilo9Silva-Brandão, Karina Lucas10Torres, Tatiana Teixeira11Joron, Mathieu12https://orcid.org/0000-0003-1043-4147Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Univ Montpellier, CNRS, EPHE, IRD, Montpellier, FranceCentre d’Ecologie Fonctionnelle et Evolutive (CEFE), Univ Montpellier, CNRS, EPHE, IRD, Montpellier, FranceCentre d’Ecologie Fonctionnelle et Evolutive (CEFE), Univ Montpellier, CNRS, EPHE, IRD, Montpellier, FranceCentre d’Ecologie Fonctionnelle et Evolutive (CEFE), Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France; Laboratoire Ecologie, Evolution, Interactions Des Systèmes Amazoniens (LEEISA), Université de Guyane, IFREMER, CNRS, Cayenne, Guyane FrançaiseInstitut de Systématique Evolution Biodiversité (ISYEB), Museum National d’Histoire Naturelle, CNRS, Sorbonne-Université, EPHE, Université des Antilles, Paris, France; School of Biological Sciences, University of Auckland, Auckland, New ZealandInstituto de Ciencias Ecológicas y Ambientales (ICAE), Univ de los Andes, Mérida, VenezuelaInstitut de Systématique Evolution Biodiversité (ISYEB), Museum National d’Histoire Naturelle, CNRS, Sorbonne-Université, EPHE, Université des Antilles, Paris, FranceDepartamento de Biologia Animal, Instituto de Biologia, Unicamp, Campinas, São Paulo, BrazilDepartamento de Biologia Animal, Instituto de Biologia, Unicamp, Campinas, São Paulo, BrazilDepartment of Biology, Faculty of Natural Sciences, Universidad del Rosario, Carrera 24 No 63C- 69, Bogotá 111221, ColombiaMuseum of Nature Hamburg, Leibniz Institute for the Analysis of Biodiversity Change. Martin-Luther-King-Platz 3, 20146 Hamburg, GermanyDepartment of Genetics and Evolutionary Biology, Institute of Biosciences, University of São Paulo (USP), São Paulo, BrazilCentre d’Ecologie Fonctionnelle et Evolutive (CEFE), Univ Montpellier, CNRS, EPHE, IRD, Montpellier, FranceSelection shapes genetic diversity around target mutations, yet little is known about how selection on specific loci affects the genetic trajectories of populations, including their genome-wide patterns of diversity and demographic responses. Here we study the patterns of genetic variation and geographic structure in a neotropical butterfly, Heliconius numata, and its closely related allies in the so-called melpomene-silvaniform clade. H. numata is known to have evolved an inversion supergene which controls variation in wing patterns involved in mimicry associations with distinct groups of co-mimics whereas it is associated to disassortative mate preferences and heterozygote advantage at this locus. We contrasted patterns of genetic diversity and structure 1) among extant polymorphic and monomorphic populations of H. numata, 2) between H. numata and its close relatives, and 3) between ancestral lineages. We show that H. numata populations which carry the inversions as a balanced polymorphism show markedly distinct patterns of diversity compared to all other taxa. They show the highest genetic diversity and effective population size estimates in the entire clade, as well as a low level of geographic structure and isolation by distance across the entire Amazon basin. By contrast, monomorphic populations of H. numata as well as its sister species and their ancestral lineages all show lower effective population sizes and genetic diversity, and higher levels of geographical structure across the continent. One hypothesis is that the large effective population size of polymorphic populations could be caused by the shift to a regime of balancing selection due to the genetic load and disassortative preferences associated with inversions. Testing this hypothesis with forward simulations supported the observation of increased diversity in populations with the supergene. Our results are consistent with the hypothesis that the formation of the supergene triggered a change in gene flow, causing a general increase in genetic diversity and the homogenisation of genomes at the continental scale. https://peercommunityjournal.org/articles/10.24072/pcjournal.298/balancing selection, gene flow, supergene, mimetism, inversion |
| spellingShingle | Rodríguez de Cara, María Ángeles Jay, Paul Rougemont, Quentin Chouteau, Mathieu Whibley, Annabel Huber, Barbara Piron-Prunier, Florence Ramos, Renato Rogner Freitas, André V. L. Salazar, Camilo Silva-Brandão, Karina Lucas Torres, Tatiana Teixeira Joron, Mathieu Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow Peer Community Journal balancing selection, gene flow, supergene, mimetism, inversion |
| title | Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow
|
| title_full | Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow
|
| title_fullStr | Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow
|
| title_full_unstemmed | Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow
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| title_short | Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow
|
| title_sort | balancing selection at a wing pattern locus is associated with major shifts in genome wide patterns of diversity and gene flow |
| topic | balancing selection, gene flow, supergene, mimetism, inversion |
| url | https://peercommunityjournal.org/articles/10.24072/pcjournal.298/ |
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