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Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry

Identifieur interne : 007124 ( Main/Merge ); précédent : 007123; suivant : 007125

Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry

Auteurs : Mathieu Joron [France, Royaume-Uni, Pays-Bas] ; Lise Frezal [France] ; Robert T. Jones [Royaume-Uni] ; Nicola L. Chamberlain [Royaume-Uni] ; Siu F. Lee [Australie] ; Christoph R. Haag [Suisse] ; Annabel Whibley [France] ; Michel Becuwe [Royaume-Uni] ; Simon W. Baxter [Royaume-Uni] ; Laura Ferguson [Royaume-Uni] ; Paul A. Wilkinson [Royaume-Uni] ; Camilo Salazar [Panama] ; Claire Davidson [Royaume-Uni] ; Richard Clark [Royaume-Uni] ; Michael A. Quail [Royaume-Uni] ; Helen Beasley [Royaume-Uni] ; Rebecca Glithero [Royaume-Uni] ; Christine Lloyd [Royaume-Uni] ; Sarah Sims [Royaume-Uni] ; Matthew C. Jones [Royaume-Uni] ; Jane Rogers [Royaume-Uni] ; Chris D. Jiggins [Royaume-Uni] ; Richard H. Ffrench-Constant [Royaume-Uni]

Source :

RBID : Pascal:11-0403590

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English descriptors

Abstract

Supergenes are tight clusters of loci that facilitate the co-segregation of adaptive variation, providing integrated control of complex adaptive phenotypes'. Polymorphic supergenes, in which specific combinations of traits are maintained within a single population, were first described for 'pin' and 'thrum' floral types in Primula1 and Fagopyrum2, but classic examples are also found in insect mimicry3-5 and snail morphology6. Understanding the evolutionary mechanisms that generate these co-adapted gene sets, as well as the mode of limiting the production of unfit recombinant forms, remains a substantial challenge7-10. Here we show that individual wing-pattern morphs in the polymorphic mimetic butterfly Heliconius numata are associated with different genomic rearrangements at the supergene locus P. These rearrangements tighten the genetic linkage between at least two colour-pattern loci that are known to recombine in closely related species9-11, with complete suppression of recombination being observed in experimental crosses across a 400-kilobase interval containing at least 18 genes. In natural populations, notable patterns of linkage disequilibrium (LD) are observed across the entire P region. The resulting divergent haplotype clades and inversion breakpoints are found in complete association with wing-pattern morphs. Our results indicate that allelic combinations at known wing-patterning loci have become locked together in a polymorphic rearrangement at the P locus, forming a supergene that acts as a simple switch between complex adaptive phenotypes found in sympatry. These findings highlight how genomic rearrangements can have a central role in the coexistence of adaptive phenotypes involving several genes acting in concert, by locally limiting recombination and gene flow.

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Pascal:11-0403590

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</inist:fA14>
<country>France</country>
<placeName>
<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="4">
<inist:fA14 i1="02">
<s1>Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, King's Buildings, West Mains Road</s1>
<s2>Edinburgh EH9 3JT</s2>
<s3>GBR</s3>
<sZ>1 aut.</sZ>
<sZ>8 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>Edinburgh EH9 3JT</wicri:noRegion>
<orgName type="university">Université d'Édimbourg</orgName>
<placeName>
<settlement type="city">Édimbourg</settlement>
<region type="country">Écosse</region>
</placeName>
</affiliation>
<affiliation wicri:level="1">
<inist:fA14 i1="03">
<s1>Institute of Biology, Leiden University, Postbus 9505</s1>
<s2>2300 RA Leiden</s2>
<s3>NLD</s3>
<sZ>1 aut.</sZ>
</inist:fA14>
<country>Pays-Bas</country>
<wicri:noRegion>2300 RA Leiden</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Frezal, Lise" sort="Frezal, Lise" uniqKey="Frezal L" first="Lise" last="Frezal">Lise Frezal</name>
<affiliation wicri:level="1">
<inist:fA14 i1="01">
<s1>CNRS UMR 7205, Museum National d'Histoire Naturelle, CP50, 45 Rue Buffon</s1>
<s2>75005 Paris</s2>
<s3>FRA</s3>
<sZ>1 aut.</sZ>
<sZ>2 aut.</sZ>
<sZ>7 aut.</sZ>
</inist:fA14>
<country>France</country>
<wicri:noRegion>75005 Paris</wicri:noRegion>
<placeName>
<settlement type="city">Paris</settlement>
<region type="région" nuts="2">Île-de-France</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Jones, Robert T" sort="Jones, Robert T" uniqKey="Jones R" first="Robert T." last="Jones">Robert T. Jones</name>
<affiliation wicri:level="1">
<inist:fA14 i1="04">
<s1>Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn</s1>
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</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>Cornwall TR10 9EZ</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Chamberlain, Nicola L" sort="Chamberlain, Nicola L" uniqKey="Chamberlain N" first="Nicola L." last="Chamberlain">Nicola L. Chamberlain</name>
<affiliation wicri:level="1">
<inist:fA14 i1="04">
<s1>Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn</s1>
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</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>Cornwall TR10 9EZ</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Lee, Siu F" sort="Lee, Siu F" uniqKey="Lee S" first="Siu F." last="Lee">Siu F. Lee</name>
<affiliation wicri:level="4">
<inist:fA14 i1="05">
<s1>Department of Genetics, Bio21 Institute, University of Melbourne, 30 Flemington Road</s1>
<s2>Parkville, 3010 Victoria</s2>
<s3>AUS</s3>
<sZ>5 aut.</sZ>
</inist:fA14>
<country>Australie</country>
<wicri:noRegion>Parkville, 3010 Victoria</wicri:noRegion>
<orgName type="university">Université de Melbourne</orgName>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Haag, Christoph R" sort="Haag, Christoph R" uniqKey="Haag C" first="Christoph R." last="Haag">Christoph R. Haag</name>
<affiliation wicri:level="4">
<inist:fA14 i1="06">
<s1>Department of Biology, Ecology and Evolution, University of Fribourg, Chemin du Musee 10</s1>
<s2>1700 Fribourg</s2>
<s3>CHE</s3>
<sZ>6 aut.</sZ>
</inist:fA14>
<country>Suisse</country>
<wicri:noRegion>1700 Fribourg</wicri:noRegion>
<orgName type="university">Université de Fribourg</orgName>
<placeName>
<settlement type="city">Fribourg</settlement>
<region nuts="3" type="region">Canton de Fribourg</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Whibley, Annabel" sort="Whibley, Annabel" uniqKey="Whibley A" first="Annabel" last="Whibley">Annabel Whibley</name>
<affiliation wicri:level="1">
<inist:fA14 i1="01">
<s1>CNRS UMR 7205, Museum National d'Histoire Naturelle, CP50, 45 Rue Buffon</s1>
<s2>75005 Paris</s2>
<s3>FRA</s3>
<sZ>1 aut.</sZ>
<sZ>2 aut.</sZ>
<sZ>7 aut.</sZ>
</inist:fA14>
<country>France</country>
<wicri:noRegion>75005 Paris</wicri:noRegion>
<placeName>
<settlement type="city">Paris</settlement>
<region type="région" nuts="2">Île-de-France</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Becuwe, Michel" sort="Becuwe, Michel" uniqKey="Becuwe M" first="Michel" last="Becuwe">Michel Becuwe</name>
<affiliation wicri:level="4">
<inist:fA14 i1="02">
<s1>Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, King's Buildings, West Mains Road</s1>
<s2>Edinburgh EH9 3JT</s2>
<s3>GBR</s3>
<sZ>1 aut.</sZ>
<sZ>8 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>Edinburgh EH9 3JT</wicri:noRegion>
<orgName type="university">Université d'Édimbourg</orgName>
<placeName>
<settlement type="city">Édimbourg</settlement>
<region type="country">Écosse</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Baxter, Simon W" sort="Baxter, Simon W" uniqKey="Baxter S" first="Simon W." last="Baxter">Simon W. Baxter</name>
<affiliation wicri:level="4">
<inist:fA14 i1="07">
<s1>Department of Zoology, University of Cambridge, Downing Street</s1>
<s2>Cambridge CB2 3EJ</s2>
<s3>GBR</s3>
<sZ>9 aut.</sZ>
<sZ>10 aut.</sZ>
<sZ>22 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>Cambridge CB2 3EJ</wicri:noRegion>
<orgName type="university">Université de Cambridge</orgName>
<placeName>
<settlement type="city">Cambridge</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Angleterre de l'Est</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Ferguson, Laura" sort="Ferguson, Laura" uniqKey="Ferguson L" first="Laura" last="Ferguson">Laura Ferguson</name>
<affiliation wicri:level="4">
<inist:fA14 i1="07">
<s1>Department of Zoology, University of Cambridge, Downing Street</s1>
<s2>Cambridge CB2 3EJ</s2>
<s3>GBR</s3>
<sZ>9 aut.</sZ>
<sZ>10 aut.</sZ>
<sZ>22 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>Cambridge CB2 3EJ</wicri:noRegion>
<orgName type="university">Université de Cambridge</orgName>
<placeName>
<settlement type="city">Cambridge</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Angleterre de l'Est</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Wilkinson, Paul A" sort="Wilkinson, Paul A" uniqKey="Wilkinson P" first="Paul A." last="Wilkinson">Paul A. Wilkinson</name>
<affiliation wicri:level="1">
<inist:fA14 i1="04">
<s1>Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn</s1>
<s2>Cornwall TR10 9EZ</s2>
<s3>GBR</s3>
<sZ>3 aut.</sZ>
<sZ>4 aut.</sZ>
<sZ>11 aut.</sZ>
<sZ>23 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>Cornwall TR10 9EZ</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Salazar, Camilo" sort="Salazar, Camilo" uniqKey="Salazar C" first="Camilo" last="Salazar">Camilo Salazar</name>
<affiliation wicri:level="1">
<inist:fA14 i1="08">
<s1>Smithsonian Tropical Research Institute, NAOS island, Causeway Amador</s1>
<s2>Panamá</s2>
<s3>PAN</s3>
<sZ>12 aut.</sZ>
</inist:fA14>
<country>Panama</country>
<wicri:noRegion>Panamá</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Davidson, Claire" sort="Davidson, Claire" uniqKey="Davidson C" first="Claire" last="Davidson">Claire Davidson</name>
<affiliation wicri:level="1">
<inist:fA14 i1="09">
<s1>The Wellcome Trust Sanger Institute</s1>
<s2>Hinxton, Cambridge CB10 1HH</s2>
<s3>GBR</s3>
<sZ>13 aut.</sZ>
<sZ>14 aut.</sZ>
<sZ>15 aut.</sZ>
<sZ>16 aut.</sZ>
<sZ>17 aut.</sZ>
<sZ>18 aut.</sZ>
<sZ>19 aut.</sZ>
<sZ>20 aut.</sZ>
<sZ>21 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>The Wellcome Trust Sanger Institute</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Clark, Richard" sort="Clark, Richard" uniqKey="Clark R" first="Richard" last="Clark">Richard Clark</name>
<affiliation wicri:level="1">
<inist:fA14 i1="09">
<s1>The Wellcome Trust Sanger Institute</s1>
<s2>Hinxton, Cambridge CB10 1HH</s2>
<s3>GBR</s3>
<sZ>13 aut.</sZ>
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<sZ>19 aut.</sZ>
<sZ>20 aut.</sZ>
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</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>The Wellcome Trust Sanger Institute</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Quail, Michael A" sort="Quail, Michael A" uniqKey="Quail M" first="Michael A." last="Quail">Michael A. Quail</name>
<affiliation wicri:level="1">
<inist:fA14 i1="09">
<s1>The Wellcome Trust Sanger Institute</s1>
<s2>Hinxton, Cambridge CB10 1HH</s2>
<s3>GBR</s3>
<sZ>13 aut.</sZ>
<sZ>14 aut.</sZ>
<sZ>15 aut.</sZ>
<sZ>16 aut.</sZ>
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<sZ>19 aut.</sZ>
<sZ>20 aut.</sZ>
<sZ>21 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>The Wellcome Trust Sanger Institute</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Beasley, Helen" sort="Beasley, Helen" uniqKey="Beasley H" first="Helen" last="Beasley">Helen Beasley</name>
<affiliation wicri:level="1">
<inist:fA14 i1="09">
<s1>The Wellcome Trust Sanger Institute</s1>
<s2>Hinxton, Cambridge CB10 1HH</s2>
<s3>GBR</s3>
<sZ>13 aut.</sZ>
<sZ>14 aut.</sZ>
<sZ>15 aut.</sZ>
<sZ>16 aut.</sZ>
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<sZ>19 aut.</sZ>
<sZ>20 aut.</sZ>
<sZ>21 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>The Wellcome Trust Sanger Institute</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Glithero, Rebecca" sort="Glithero, Rebecca" uniqKey="Glithero R" first="Rebecca" last="Glithero">Rebecca Glithero</name>
<affiliation wicri:level="1">
<inist:fA14 i1="09">
<s1>The Wellcome Trust Sanger Institute</s1>
<s2>Hinxton, Cambridge CB10 1HH</s2>
<s3>GBR</s3>
<sZ>13 aut.</sZ>
<sZ>14 aut.</sZ>
<sZ>15 aut.</sZ>
<sZ>16 aut.</sZ>
<sZ>17 aut.</sZ>
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<sZ>19 aut.</sZ>
<sZ>20 aut.</sZ>
<sZ>21 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>The Wellcome Trust Sanger Institute</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Lloyd, Christine" sort="Lloyd, Christine" uniqKey="Lloyd C" first="Christine" last="Lloyd">Christine Lloyd</name>
<affiliation wicri:level="1">
<inist:fA14 i1="09">
<s1>The Wellcome Trust Sanger Institute</s1>
<s2>Hinxton, Cambridge CB10 1HH</s2>
<s3>GBR</s3>
<sZ>13 aut.</sZ>
<sZ>14 aut.</sZ>
<sZ>15 aut.</sZ>
<sZ>16 aut.</sZ>
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<sZ>19 aut.</sZ>
<sZ>20 aut.</sZ>
<sZ>21 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>The Wellcome Trust Sanger Institute</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Sims, Sarah" sort="Sims, Sarah" uniqKey="Sims S" first="Sarah" last="Sims">Sarah Sims</name>
<affiliation wicri:level="1">
<inist:fA14 i1="09">
<s1>The Wellcome Trust Sanger Institute</s1>
<s2>Hinxton, Cambridge CB10 1HH</s2>
<s3>GBR</s3>
<sZ>13 aut.</sZ>
<sZ>14 aut.</sZ>
<sZ>15 aut.</sZ>
<sZ>16 aut.</sZ>
<sZ>17 aut.</sZ>
<sZ>18 aut.</sZ>
<sZ>19 aut.</sZ>
<sZ>20 aut.</sZ>
<sZ>21 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>The Wellcome Trust Sanger Institute</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Jones, Matthew C" sort="Jones, Matthew C" uniqKey="Jones M" first="Matthew C." last="Jones">Matthew C. Jones</name>
<affiliation wicri:level="1">
<inist:fA14 i1="09">
<s1>The Wellcome Trust Sanger Institute</s1>
<s2>Hinxton, Cambridge CB10 1HH</s2>
<s3>GBR</s3>
<sZ>13 aut.</sZ>
<sZ>14 aut.</sZ>
<sZ>15 aut.</sZ>
<sZ>16 aut.</sZ>
<sZ>17 aut.</sZ>
<sZ>18 aut.</sZ>
<sZ>19 aut.</sZ>
<sZ>20 aut.</sZ>
<sZ>21 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>The Wellcome Trust Sanger Institute</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Rogers, Jane" sort="Rogers, Jane" uniqKey="Rogers J" first="Jane" last="Rogers">Jane Rogers</name>
<affiliation wicri:level="1">
<inist:fA14 i1="09">
<s1>The Wellcome Trust Sanger Institute</s1>
<s2>Hinxton, Cambridge CB10 1HH</s2>
<s3>GBR</s3>
<sZ>13 aut.</sZ>
<sZ>14 aut.</sZ>
<sZ>15 aut.</sZ>
<sZ>16 aut.</sZ>
<sZ>17 aut.</sZ>
<sZ>18 aut.</sZ>
<sZ>19 aut.</sZ>
<sZ>20 aut.</sZ>
<sZ>21 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>The Wellcome Trust Sanger Institute</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Jiggins, Chris D" sort="Jiggins, Chris D" uniqKey="Jiggins C" first="Chris D." last="Jiggins">Chris D. Jiggins</name>
<affiliation wicri:level="4">
<inist:fA14 i1="07">
<s1>Department of Zoology, University of Cambridge, Downing Street</s1>
<s2>Cambridge CB2 3EJ</s2>
<s3>GBR</s3>
<sZ>9 aut.</sZ>
<sZ>10 aut.</sZ>
<sZ>22 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>Cambridge CB2 3EJ</wicri:noRegion>
<orgName type="university">Université de Cambridge</orgName>
<placeName>
<settlement type="city">Cambridge</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Angleterre de l'Est</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Ffrench Constant, Richard H" sort="Ffrench Constant, Richard H" uniqKey="Ffrench Constant R" first="Richard H." last="Ffrench-Constant">Richard H. Ffrench-Constant</name>
<affiliation wicri:level="1">
<inist:fA14 i1="04">
<s1>Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn</s1>
<s2>Cornwall TR10 9EZ</s2>
<s3>GBR</s3>
<sZ>3 aut.</sZ>
<sZ>4 aut.</sZ>
<sZ>11 aut.</sZ>
<sZ>23 aut.</sZ>
</inist:fA14>
<country>Royaume-Uni</country>
<wicri:noRegion>Cornwall TR10 9EZ</wicri:noRegion>
</affiliation>
</author>
</analytic>
<series>
<title level="j" type="main">Nature : (London)</title>
<title level="j" type="abbreviated">Nature : (Lond.)</title>
<idno type="ISSN">0028-0836</idno>
<imprint>
<date when="2011">2011</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
<seriesStmt>
<title level="j" type="main">Nature : (London)</title>
<title level="j" type="abbreviated">Nature : (Lond.)</title>
<idno type="ISSN">0028-0836</idno>
</seriesStmt>
</fileDesc>
<profileDesc>
<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>Coexistence</term>
<term>Gene</term>
<term>Gene rearrangement</term>
<term>Lepidoptera</term>
<term>Mimetism</term>
<term>Morphology</term>
<term>Phenotype</term>
<term>Polymorphism</term>
<term>Wing</term>
</keywords>
<keywords scheme="Pascal" xml:lang="fr">
<term>Réarrangement génique</term>
<term>Polymorphisme</term>
<term>Gène</term>
<term>Mimétisme</term>
<term>Morphologie</term>
<term>Aile</term>
<term>Coexistence</term>
<term>Phénotype</term>
<term>Lepidoptera</term>
<term>Heliconius numata</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">Supergenes are tight clusters of loci that facilitate the co-segregation of adaptive variation, providing integrated control of complex adaptive phenotypes'. Polymorphic supergenes, in which specific combinations of traits are maintained within a single population, were first described for 'pin' and 'thrum' floral types in Primula
<sup>1</sup>
and Fagopyrum
<sup>2</sup>
, but classic examples are also found in insect mimicry
<sup>3-5</sup>
and snail morphology
<sup>6</sup>
. Understanding the evolutionary mechanisms that generate these co-adapted gene sets, as well as the mode of limiting the production of unfit recombinant forms, remains a substantial challenge
<sup>7-10</sup>
. Here we show that individual wing-pattern morphs in the polymorphic mimetic butterfly Heliconius numata are associated with different genomic rearrangements at the supergene locus P. These rearrangements tighten the genetic linkage between at least two colour-pattern loci that are known to recombine in closely related species
<sup>9-11</sup>
, with complete suppression of recombination being observed in experimental crosses across a 400-kilobase interval containing at least 18 genes. In natural populations, notable patterns of linkage disequilibrium (LD) are observed across the entire P region. The resulting divergent haplotype clades and inversion breakpoints are found in complete association with wing-pattern morphs. Our results indicate that allelic combinations at known wing-patterning loci have become locked together in a polymorphic rearrangement at the P locus, forming a supergene that acts as a simple switch between complex adaptive phenotypes found in sympatry. These findings highlight how genomic rearrangements can have a central role in the coexistence of adaptive phenotypes involving several genes acting in concert, by locally limiting recombination and gene flow.</div>
</front>
</TEI>
<affiliations>
<list>
<country>
<li>Australie</li>
<li>France</li>
<li>Panama</li>
<li>Pays-Bas</li>
<li>Royaume-Uni</li>
<li>Suisse</li>
</country>
<region>
<li>Angleterre</li>
<li>Angleterre de l'Est</li>
<li>Canton de Fribourg</li>
<li>Victoria (État)</li>
<li>Écosse</li>
<li>Île-de-France</li>
</region>
<settlement>
<li>Cambridge</li>
<li>Fribourg</li>
<li>Melbourne</li>
<li>Paris</li>
<li>Édimbourg</li>
</settlement>
<orgName>
<li>Université d'Édimbourg</li>
<li>Université de Cambridge</li>
<li>Université de Fribourg</li>
<li>Université de Melbourne</li>
</orgName>
</list>
<tree>
<country name="France">
<region name="Île-de-France">
<name sortKey="Joron, Mathieu" sort="Joron, Mathieu" uniqKey="Joron M" first="Mathieu" last="Joron">Mathieu Joron</name>
</region>
<name sortKey="Frezal, Lise" sort="Frezal, Lise" uniqKey="Frezal L" first="Lise" last="Frezal">Lise Frezal</name>
<name sortKey="Whibley, Annabel" sort="Whibley, Annabel" uniqKey="Whibley A" first="Annabel" last="Whibley">Annabel Whibley</name>
</country>
<country name="Royaume-Uni">
<region name="Écosse">
<name sortKey="Joron, Mathieu" sort="Joron, Mathieu" uniqKey="Joron M" first="Mathieu" last="Joron">Mathieu Joron</name>
</region>
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