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Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics, Population biology

Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow

Rodríguez de Cara, María Ángeles1 ; Jay, Paul1  ; Rougemont, Quentin1   ; Chouteau, Mathieu1, 2; Whibley, Annabel3, 4; Huber, Barbara5; Piron-Prunier, Florence3; Ramos, Renato Rogner6; Freitas, André V. L.6; Salazar, Camilo7; Silva-Brandão, Karina Lucas8; Torres, Tatiana Teixeira9; Joron, Mathieu1 
1 Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France
2 Laboratoire Ecologie, Evolution, Interactions Des Systèmes Amazoniens (LEEISA), Université de Guyane, IFREMER, CNRS, Cayenne, Guyane Française
3 Institut de Systématique Evolution Biodiversité (ISYEB), Museum National d’Histoire Naturelle, CNRS, Sorbonne-Université, EPHE, Université des Antilles, Paris, France
4 School of Biological Sciences, University of Auckland, Auckland, New Zealand
5 Instituto de Ciencias Ecológicas y Ambientales (ICAE), Univ de los Andes, Mérida, Venezuela
6 Departamento de Biologia Animal, Instituto de Biologia, Unicamp, Campinas, São Paulo, Brazil
7 Department of Biology, Faculty of Natural Sciences, Universidad del Rosario, Carrera 24 No 63C- 69, Bogotá 111221, Colombia
8 Museum of Nature Hamburg, Leibniz Institute for the Analysis of Biodiversity Change. Martin-Luther-King-Platz 3, 20146 Hamburg, Germany
9 Department of Genetics and Evolutionary Biology, Institute of Biosciences, University of São Paulo (USP), São Paulo, Brazil

10.24072/pcjournal.298 - Peer Community Journal, Volume 3 (2023), article no. e65.

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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.

Published online:
DOI: 10.24072/pcjournal.298
Type: Research article
Keywords: balancing selection, gene flow, supergene, mimetism, inversion
Rodríguez de Cara, María Ángeles 1; Jay, Paul 1; Rougemont, Quentin 1; Chouteau, Mathieu 1, 2; Whibley, Annabel 3, 4; Huber, Barbara 5; Piron-Prunier, Florence 3; Ramos, Renato Rogner 6; Freitas, André V. L. 6; Salazar, Camilo 7; Silva-Brandão, Karina Lucas 8; Torres, Tatiana Teixeira 9; Joron, Mathieu 1

1 Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France
2 Laboratoire Ecologie, Evolution, Interactions Des Systèmes Amazoniens (LEEISA), Université de Guyane, IFREMER, CNRS, Cayenne, Guyane Française
3 Institut de Systématique Evolution Biodiversité (ISYEB), Museum National d’Histoire Naturelle, CNRS, Sorbonne-Université, EPHE, Université des Antilles, Paris, France
4 School of Biological Sciences, University of Auckland, Auckland, New Zealand
5 Instituto de Ciencias Ecológicas y Ambientales (ICAE), Univ de los Andes, Mérida, Venezuela
6 Departamento de Biologia Animal, Instituto de Biologia, Unicamp, Campinas, São Paulo, Brazil
7 Department of Biology, Faculty of Natural Sciences, Universidad del Rosario, Carrera 24 No 63C- 69, Bogotá 111221, Colombia
8 Museum of Nature Hamburg, Leibniz Institute for the Analysis of Biodiversity Change. Martin-Luther-King-Platz 3, 20146 Hamburg, Germany
9 Department of Genetics and Evolutionary Biology, Institute of Biosciences, University of São Paulo (USP), São Paulo, Brazil
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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     author = {Rodr{\'\i}guez de Cara, Mar{\'\i}a \'Angeles and Jay, Paul and Rougemont, Quentin and Chouteau, Mathieu and Whibley, Annabel and Huber, Barbara and Piron-Prunier, Florence and Ramos, Renato Rogner and Freitas, Andr\'e V. L. and Salazar, Camilo and Silva-Brand\~ao, Karina Lucas and Torres, Tatiana Teixeira and Joron, Mathieu},
     title = {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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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, Volume 3 (2023), article  no. e65. doi : 10.24072/pcjournal.298. https://peercommunityjournal.org/articles/10.24072/pcjournal.298/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100522

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

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