Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci

Supergenes are genetic architectures associated with discrete and concerted variation in multiple traits. It has long been suggested that supergenes control these complex polymorphisms by suppressing recombination between sets of coadapted genes. However, because recombination suppression hinders the dissociation of the individual effects of genes within supergenes, there is still little evidence that supergenes evolve by tightening linkage between coadapted genes. Here, combining a landmark-free phenotyping algorithm with multivariate genome-wide association studies, we dissected the genetic basis of wing pattern variation in the butterfly Heliconius numata. We show that the supergene controlling the striking wing pattern polymorphism displayed by this species contains several independent loci associated with different features of wing patterns. The three chromosomal inversions of this supergene suppress recombination between these loci, supporting the hypothesis that they may have evolved because they captured beneficial combinations of alleles. Some of these loci are, however, associated with colour variations only in a subset of morphs where the phenotype is controlled by derived inversion forms, indicating that they were recruited after the formation of the inversions. Our study shows that supergenes and clusters of adaptive loci in general may form via the evolution of chromosomal rearrangements suppressing recombination between co-adapted loci but also via the subsequent recruitment of linked adaptive mutations.

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Main Authors: Jay, Paul, Leroy, Manon, Le Poul, Yann, Whibley, Annabel, Arias, Monica, Chouteau, Mathieu, Joron, Mathieu
Format: article biblioteca
Language:eng
Subjects:variation génétique, supergène, phénotype, polymorphisme génétique, phylogénie, carte génétique, variation phénotypique, locus, comportement animal, évolution, génome, http://aims.fao.org/aos/agrovoc/c_15975, http://aims.fao.org/aos/agrovoc/c_14695, http://aims.fao.org/aos/agrovoc/c_5776, http://aims.fao.org/aos/agrovoc/c_24031, http://aims.fao.org/aos/agrovoc/c_13325, http://aims.fao.org/aos/agrovoc/c_24002, http://aims.fao.org/aos/agrovoc/c_903c4959, http://aims.fao.org/aos/agrovoc/c_24869, http://aims.fao.org/aos/agrovoc/c_8811, http://aims.fao.org/aos/agrovoc/c_2745, http://aims.fao.org/aos/agrovoc/c_3224,
Online Access:http://agritrop.cirad.fr/603316/
http://agritrop.cirad.fr/603316/1/Jayetal2022.pdf
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spelling dig-cirad-fr-6033162024-04-24T13:12:00Z http://agritrop.cirad.fr/603316/ http://agritrop.cirad.fr/603316/ Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci. Jay Paul, Leroy Manon, Le Poul Yann, Whibley Annabel, Arias Monica, Chouteau Mathieu, Joron Mathieu. 2022. Philosophical Transactions - Royal Society. Biological Sciences, 377 (1856), dossier Genomic architecture of supergenes: causes and evolutionary consequences, 14 p.https://doi.org/10.1098/rstb.2021.0193 <https://doi.org/10.1098/rstb.2021.0193> Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci Jay, Paul Leroy, Manon Le Poul, Yann Whibley, Annabel Arias, Monica Chouteau, Mathieu Joron, Mathieu eng 2022 Philosophical Transactions - Royal Society. Biological Sciences variation génétique supergène phénotype polymorphisme génétique phylogénie carte génétique variation phénotypique locus comportement animal évolution génome http://aims.fao.org/aos/agrovoc/c_15975 http://aims.fao.org/aos/agrovoc/c_14695 http://aims.fao.org/aos/agrovoc/c_5776 http://aims.fao.org/aos/agrovoc/c_24031 http://aims.fao.org/aos/agrovoc/c_13325 http://aims.fao.org/aos/agrovoc/c_24002 http://aims.fao.org/aos/agrovoc/c_903c4959 http://aims.fao.org/aos/agrovoc/c_24869 http://aims.fao.org/aos/agrovoc/c_8811 http://aims.fao.org/aos/agrovoc/c_2745 http://aims.fao.org/aos/agrovoc/c_3224 Supergenes are genetic architectures associated with discrete and concerted variation in multiple traits. It has long been suggested that supergenes control these complex polymorphisms by suppressing recombination between sets of coadapted genes. However, because recombination suppression hinders the dissociation of the individual effects of genes within supergenes, there is still little evidence that supergenes evolve by tightening linkage between coadapted genes. Here, combining a landmark-free phenotyping algorithm with multivariate genome-wide association studies, we dissected the genetic basis of wing pattern variation in the butterfly Heliconius numata. We show that the supergene controlling the striking wing pattern polymorphism displayed by this species contains several independent loci associated with different features of wing patterns. The three chromosomal inversions of this supergene suppress recombination between these loci, supporting the hypothesis that they may have evolved because they captured beneficial combinations of alleles. Some of these loci are, however, associated with colour variations only in a subset of morphs where the phenotype is controlled by derived inversion forms, indicating that they were recruited after the formation of the inversions. Our study shows that supergenes and clusters of adaptive loci in general may form via the evolution of chromosomal rearrangements suppressing recombination between co-adapted loci but also via the subsequent recruitment of linked adaptive mutations. article info:eu-repo/semantics/article Journal Article info:eu-repo/semantics/publishedVersion http://agritrop.cirad.fr/603316/1/Jayetal2022.pdf text cc_by_nd info:eu-repo/semantics/openAccess https://creativecommons.org/licenses/by-nd/4.0/ https://doi.org/10.1098/rstb.2021.0193 10.1098/rstb.2021.0193 info:eu-repo/semantics/altIdentifier/doi/10.1098/rstb.2021.0193 info:eu-repo/semantics/altIdentifier/purl/https://doi.org/10.1098/rstb.2021.0193 info:eu-repo/semantics/reference/purl/https://github.com/PaulYannJay/HeliconiusGWAS info:eu-repo/grantAgreement/ERC//ANR-12-JSV7-0005//(FRA) Origines des innovations évolutives et hybridation/HybEvol info:eu-repo/grantAgreement/ERC//ANR-18-CE02-0019//(FRA) Les conséquences de l'évolution d'un supergène/Supergene
institution CIRAD FR
collection DSpace
country Francia
countrycode FR
component Bibliográfico
access En linea
databasecode dig-cirad-fr
tag biblioteca
region Europa del Oeste
libraryname Biblioteca del CIRAD Francia
language eng
topic variation génétique
supergène
phénotype
polymorphisme génétique
phylogénie
carte génétique
variation phénotypique
locus
comportement animal
évolution
génome
http://aims.fao.org/aos/agrovoc/c_15975
http://aims.fao.org/aos/agrovoc/c_14695
http://aims.fao.org/aos/agrovoc/c_5776
http://aims.fao.org/aos/agrovoc/c_24031
http://aims.fao.org/aos/agrovoc/c_13325
http://aims.fao.org/aos/agrovoc/c_24002
http://aims.fao.org/aos/agrovoc/c_903c4959
http://aims.fao.org/aos/agrovoc/c_24869
http://aims.fao.org/aos/agrovoc/c_8811
http://aims.fao.org/aos/agrovoc/c_2745
http://aims.fao.org/aos/agrovoc/c_3224
variation génétique
supergène
phénotype
polymorphisme génétique
phylogénie
carte génétique
variation phénotypique
locus
comportement animal
évolution
génome
http://aims.fao.org/aos/agrovoc/c_15975
http://aims.fao.org/aos/agrovoc/c_14695
http://aims.fao.org/aos/agrovoc/c_5776
http://aims.fao.org/aos/agrovoc/c_24031
http://aims.fao.org/aos/agrovoc/c_13325
http://aims.fao.org/aos/agrovoc/c_24002
http://aims.fao.org/aos/agrovoc/c_903c4959
http://aims.fao.org/aos/agrovoc/c_24869
http://aims.fao.org/aos/agrovoc/c_8811
http://aims.fao.org/aos/agrovoc/c_2745
http://aims.fao.org/aos/agrovoc/c_3224
spellingShingle variation génétique
supergène
phénotype
polymorphisme génétique
phylogénie
carte génétique
variation phénotypique
locus
comportement animal
évolution
génome
http://aims.fao.org/aos/agrovoc/c_15975
http://aims.fao.org/aos/agrovoc/c_14695
http://aims.fao.org/aos/agrovoc/c_5776
http://aims.fao.org/aos/agrovoc/c_24031
http://aims.fao.org/aos/agrovoc/c_13325
http://aims.fao.org/aos/agrovoc/c_24002
http://aims.fao.org/aos/agrovoc/c_903c4959
http://aims.fao.org/aos/agrovoc/c_24869
http://aims.fao.org/aos/agrovoc/c_8811
http://aims.fao.org/aos/agrovoc/c_2745
http://aims.fao.org/aos/agrovoc/c_3224
variation génétique
supergène
phénotype
polymorphisme génétique
phylogénie
carte génétique
variation phénotypique
locus
comportement animal
évolution
génome
http://aims.fao.org/aos/agrovoc/c_15975
http://aims.fao.org/aos/agrovoc/c_14695
http://aims.fao.org/aos/agrovoc/c_5776
http://aims.fao.org/aos/agrovoc/c_24031
http://aims.fao.org/aos/agrovoc/c_13325
http://aims.fao.org/aos/agrovoc/c_24002
http://aims.fao.org/aos/agrovoc/c_903c4959
http://aims.fao.org/aos/agrovoc/c_24869
http://aims.fao.org/aos/agrovoc/c_8811
http://aims.fao.org/aos/agrovoc/c_2745
http://aims.fao.org/aos/agrovoc/c_3224
Jay, Paul
Leroy, Manon
Le Poul, Yann
Whibley, Annabel
Arias, Monica
Chouteau, Mathieu
Joron, Mathieu
Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci
description Supergenes are genetic architectures associated with discrete and concerted variation in multiple traits. It has long been suggested that supergenes control these complex polymorphisms by suppressing recombination between sets of coadapted genes. However, because recombination suppression hinders the dissociation of the individual effects of genes within supergenes, there is still little evidence that supergenes evolve by tightening linkage between coadapted genes. Here, combining a landmark-free phenotyping algorithm with multivariate genome-wide association studies, we dissected the genetic basis of wing pattern variation in the butterfly Heliconius numata. We show that the supergene controlling the striking wing pattern polymorphism displayed by this species contains several independent loci associated with different features of wing patterns. The three chromosomal inversions of this supergene suppress recombination between these loci, supporting the hypothesis that they may have evolved because they captured beneficial combinations of alleles. Some of these loci are, however, associated with colour variations only in a subset of morphs where the phenotype is controlled by derived inversion forms, indicating that they were recruited after the formation of the inversions. Our study shows that supergenes and clusters of adaptive loci in general may form via the evolution of chromosomal rearrangements suppressing recombination between co-adapted loci but also via the subsequent recruitment of linked adaptive mutations.
format article
topic_facet variation génétique
supergène
phénotype
polymorphisme génétique
phylogénie
carte génétique
variation phénotypique
locus
comportement animal
évolution
génome
http://aims.fao.org/aos/agrovoc/c_15975
http://aims.fao.org/aos/agrovoc/c_14695
http://aims.fao.org/aos/agrovoc/c_5776
http://aims.fao.org/aos/agrovoc/c_24031
http://aims.fao.org/aos/agrovoc/c_13325
http://aims.fao.org/aos/agrovoc/c_24002
http://aims.fao.org/aos/agrovoc/c_903c4959
http://aims.fao.org/aos/agrovoc/c_24869
http://aims.fao.org/aos/agrovoc/c_8811
http://aims.fao.org/aos/agrovoc/c_2745
http://aims.fao.org/aos/agrovoc/c_3224
author Jay, Paul
Leroy, Manon
Le Poul, Yann
Whibley, Annabel
Arias, Monica
Chouteau, Mathieu
Joron, Mathieu
author_facet Jay, Paul
Leroy, Manon
Le Poul, Yann
Whibley, Annabel
Arias, Monica
Chouteau, Mathieu
Joron, Mathieu
author_sort Jay, Paul
title Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci
title_short Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci
title_full Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci
title_fullStr Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci
title_full_unstemmed Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci
title_sort association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci
url http://agritrop.cirad.fr/603316/
http://agritrop.cirad.fr/603316/1/Jayetal2022.pdf
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