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Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry

Identifieur interne : 004586 ( PascalFrancis/Curation ); précédent : 004585; suivant : 004587

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

Descripteurs français

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.
pA  
A01 01  1    @0 0028-0836
A02 01      @0 NATUAS
A03   1    @0 Nature : (Lond.)
A05       @2 477
A06       @2 7363
A08 01  1  ENG  @1 Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry
A11 01  1    @1 JORON (Mathieu)
A11 02  1    @1 FREZAL (Lise)
A11 03  1    @1 JONES (Robert T.)
A11 04  1    @1 CHAMBERLAIN (Nicola L.)
A11 05  1    @1 LEE (Siu F.)
A11 06  1    @1 HAAG (Christoph R.)
A11 07  1    @1 WHIBLEY (Annabel)
A11 08  1    @1 BECUWE (Michel)
A11 09  1    @1 BAXTER (Simon W.)
A11 10  1    @1 FERGUSON (Laura)
A11 11  1    @1 WILKINSON (Paul A.)
A11 12  1    @1 SALAZAR (Camilo)
A11 13  1    @1 DAVIDSON (Claire)
A11 14  1    @1 CLARK (Richard)
A11 15  1    @1 QUAIL (Michael A.)
A11 16  1    @1 BEASLEY (Helen)
A11 17  1    @1 GLITHERO (Rebecca)
A11 18  1    @1 LLOYD (Christine)
A11 19  1    @1 SIMS (Sarah)
A11 20  1    @1 JONES (Matthew C.)
A11 21  1    @1 ROGERS (Jane)
A11 22  1    @1 JIGGINS (Chris D.)
A11 23  1    @1 FFRENCH-CONSTANT (Richard H.)
A14 01      @1 CNRS UMR 7205, Museum National d'Histoire Naturelle, CP50, 45 Rue Buffon @2 75005 Paris @3 FRA @Z 1 aut. @Z 2 aut. @Z 7 aut.
A14 02      @1 Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, King's Buildings, West Mains Road @2 Edinburgh EH9 3JT @3 GBR @Z 1 aut. @Z 8 aut.
A14 03      @1 Institute of Biology, Leiden University, Postbus 9505 @2 2300 RA Leiden @3 NLD @Z 1 aut.
A14 04      @1 Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn @2 Cornwall TR10 9EZ @3 GBR @Z 3 aut. @Z 4 aut. @Z 11 aut. @Z 23 aut.
A14 05      @1 Department of Genetics, Bio21 Institute, University of Melbourne, 30 Flemington Road @2 Parkville, 3010 Victoria @3 AUS @Z 5 aut.
A14 06      @1 Department of Biology, Ecology and Evolution, University of Fribourg, Chemin du Musee 10 @2 1700 Fribourg @3 CHE @Z 6 aut.
A14 07      @1 Department of Zoology, University of Cambridge, Downing Street @2 Cambridge CB2 3EJ @3 GBR @Z 9 aut. @Z 10 aut. @Z 22 aut.
A14 08      @1 Smithsonian Tropical Research Institute, NAOS island, Causeway Amador @2 Panamá @3 PAN @Z 12 aut.
A14 09      @1 The Wellcome Trust Sanger Institute @2 Hinxton, Cambridge CB10 1HH @3 GBR @Z 13 aut. @Z 14 aut. @Z 15 aut. @Z 16 aut. @Z 17 aut. @Z 18 aut. @Z 19 aut. @Z 20 aut. @Z 21 aut.
A20       @1 203-206
A21       @1 2011
A23 01      @0 ENG
A43 01      @1 INIST @2 142 @5 354000508979910180
A44       @0 0000 @1 © 2011 INIST-CNRS. All rights reserved.
A45       @0 30 ref.
A47 01  1    @0 11-0403590
A60       @1 P @3 CR
A61       @0 A
A64 01  1    @0 Nature : (London)
A66 01      @0 GBR
C01 01    ENG  @0 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.
C02 01  X    @0 002A07C01A
C03 01  X  FRE  @0 Réarrangement génique @5 01
C03 01  X  ENG  @0 Gene rearrangement @5 01
C03 01  X  SPA  @0 Redisposición génica @5 01
C03 02  X  FRE  @0 Polymorphisme @5 02
C03 02  X  ENG  @0 Polymorphism @5 02
C03 02  X  SPA  @0 Polimorfismo @5 02
C03 03  X  FRE  @0 Gène @5 03
C03 03  X  ENG  @0 Gene @5 03
C03 03  X  SPA  @0 Gen @5 03
C03 04  X  FRE  @0 Mimétisme @5 04
C03 04  X  ENG  @0 Mimetism @5 04
C03 04  X  SPA  @0 Mimetismo @5 04
C03 05  X  FRE  @0 Morphologie @5 05
C03 05  X  ENG  @0 Morphology @5 05
C03 05  X  SPA  @0 Morfología @5 05
C03 06  X  FRE  @0 Aile @5 06
C03 06  X  ENG  @0 Wing @5 06
C03 06  X  SPA  @0 Ala @5 06
C03 07  X  FRE  @0 Coexistence @5 07
C03 07  X  ENG  @0 Coexistence @5 07
C03 07  X  SPA  @0 Coexistencia @5 07
C03 08  X  FRE  @0 Phénotype @5 08
C03 08  X  ENG  @0 Phenotype @5 08
C03 08  X  SPA  @0 Fenotipo @5 08
C03 09  X  FRE  @0 Lepidoptera @2 NS @5 55
C03 09  X  ENG  @0 Lepidoptera @2 NS @5 55
C03 09  X  SPA  @0 Lepidoptera @2 NS @5 55
C03 10  X  FRE  @0 Heliconius numata @4 INC @5 87
C07 01  X  FRE  @0 Insecta @2 NS
C07 01  X  ENG  @0 Insecta @2 NS
C07 01  X  SPA  @0 Insecta @2 NS
C07 02  X  FRE  @0 Arthropoda @2 NS
C07 02  X  ENG  @0 Arthropoda @2 NS
C07 02  X  SPA  @0 Arthropoda @2 NS
C07 03  X  FRE  @0 Invertebrata @2 NS
C07 03  X  ENG  @0 Invertebrata @2 NS
C07 03  X  SPA  @0 Invertebrata @2 NS
N21       @1 276

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Pascal:11-0403590

Le document en format XML

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<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>
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<title xml:lang="en" level="a">Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry</title>
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<name sortKey="Joron, Mathieu" sort="Joron, Mathieu" uniqKey="Joron M" first="Mathieu" last="Joron">Mathieu Joron</name>
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<s1>Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, King's Buildings, West Mains Road</s1>
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<s1>Institute of Biology, Leiden University, Postbus 9505</s1>
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<country>Pays-Bas</country>
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<name sortKey="Lee, Siu F" sort="Lee, Siu F" uniqKey="Lee S" first="Siu F." last="Lee">Siu F. Lee</name>
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<country>Suisse</country>
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<name sortKey="Salazar, Camilo" sort="Salazar, Camilo" uniqKey="Salazar C" first="Camilo" last="Salazar">Camilo Salazar</name>
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<s1>Smithsonian Tropical Research Institute, NAOS island, Causeway Amador</s1>
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<country>Panama</country>
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<name sortKey="Clark, Richard" sort="Clark, Richard" uniqKey="Clark R" first="Richard" last="Clark">Richard Clark</name>
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<name sortKey="Quail, Michael A" sort="Quail, Michael A" uniqKey="Quail M" first="Michael A." last="Quail">Michael A. Quail</name>
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<name sortKey="Beasley, Helen" sort="Beasley, Helen" uniqKey="Beasley H" first="Helen" last="Beasley">Helen Beasley</name>
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<name sortKey="Glithero, Rebecca" sort="Glithero, Rebecca" uniqKey="Glithero R" first="Rebecca" last="Glithero">Rebecca Glithero</name>
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<name sortKey="Lloyd, Christine" sort="Lloyd, Christine" uniqKey="Lloyd C" first="Christine" last="Lloyd">Christine Lloyd</name>
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<s1>The Wellcome Trust Sanger Institute</s1>
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<name sortKey="Sims, Sarah" sort="Sims, Sarah" uniqKey="Sims S" first="Sarah" last="Sims">Sarah Sims</name>
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<author>
<name sortKey="Jones, Matthew C" sort="Jones, Matthew C" uniqKey="Jones M" first="Matthew C." last="Jones">Matthew C. Jones</name>
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<s1>The Wellcome Trust Sanger Institute</s1>
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<name sortKey="Rogers, Jane" sort="Rogers, Jane" uniqKey="Rogers J" first="Jane" last="Rogers">Jane Rogers</name>
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<s1>The Wellcome Trust Sanger Institute</s1>
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</author>
<author>
<name sortKey="Jiggins, Chris D" sort="Jiggins, Chris D" uniqKey="Jiggins C" first="Chris D." last="Jiggins">Chris D. Jiggins</name>
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<s1>Department of Zoology, University of Cambridge, Downing Street</s1>
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</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>
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<s1>Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn</s1>
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<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>
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<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>
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<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>
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<fA11 i1="15" i2="1">
<s1>QUAIL (Michael A.)</s1>
</fA11>
<fA11 i1="16" i2="1">
<s1>BEASLEY (Helen)</s1>
</fA11>
<fA11 i1="17" i2="1">
<s1>GLITHERO (Rebecca)</s1>
</fA11>
<fA11 i1="18" i2="1">
<s1>LLOYD (Christine)</s1>
</fA11>
<fA11 i1="19" i2="1">
<s1>SIMS (Sarah)</s1>
</fA11>
<fA11 i1="20" i2="1">
<s1>JONES (Matthew C.)</s1>
</fA11>
<fA11 i1="21" i2="1">
<s1>ROGERS (Jane)</s1>
</fA11>
<fA11 i1="22" i2="1">
<s1>JIGGINS (Chris D.)</s1>
</fA11>
<fA11 i1="23" i2="1">
<s1>FFRENCH-CONSTANT (Richard H.)</s1>
</fA11>
<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>
</fA14>
<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>
</fA14>
<fA14 i1="03">
<s1>Institute of Biology, Leiden University, Postbus 9505</s1>
<s2>2300 RA Leiden</s2>
<s3>NLD</s3>
<sZ>1 aut.</sZ>
</fA14>
<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>
</fA14>
<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>
</fA14>
<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>
</fA14>
<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>
</fA14>
<fA14 i1="08">
<s1>Smithsonian Tropical Research Institute, NAOS island, Causeway Amador</s1>
<s2>Panamá</s2>
<s3>PAN</s3>
<sZ>12 aut.</sZ>
</fA14>
<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>
</fA14>
<fA20>
<s1>203-206</s1>
</fA20>
<fA21>
<s1>2011</s1>
</fA21>
<fA23 i1="01">
<s0>ENG</s0>
</fA23>
<fA43 i1="01">
<s1>INIST</s1>
<s2>142</s2>
<s5>354000508979910180</s5>
</fA43>
<fA44>
<s0>0000</s0>
<s1>© 2011 INIST-CNRS. All rights reserved.</s1>
</fA44>
<fA45>
<s0>30 ref.</s0>
</fA45>
<fA47 i1="01" i2="1">
<s0>11-0403590</s0>
</fA47>
<fA60>
<s1>P</s1>
<s3>CR</s3>
</fA60>
<fA61>
<s0>A</s0>
</fA61>
<fA64 i1="01" i2="1">
<s0>Nature : (London)</s0>
</fA64>
<fA66 i1="01">
<s0>GBR</s0>
</fA66>
<fC01 i1="01" l="ENG">
<s0>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.</s0>
</fC01>
<fC02 i1="01" i2="X">
<s0>002A07C01A</s0>
</fC02>
<fC03 i1="01" i2="X" l="FRE">
<s0>Réarrangement génique</s0>
<s5>01</s5>
</fC03>
<fC03 i1="01" i2="X" l="ENG">
<s0>Gene rearrangement</s0>
<s5>01</s5>
</fC03>
<fC03 i1="01" i2="X" l="SPA">
<s0>Redisposición génica</s0>
<s5>01</s5>
</fC03>
<fC03 i1="02" i2="X" l="FRE">
<s0>Polymorphisme</s0>
<s5>02</s5>
</fC03>
<fC03 i1="02" i2="X" l="ENG">
<s0>Polymorphism</s0>
<s5>02</s5>
</fC03>
<fC03 i1="02" i2="X" l="SPA">
<s0>Polimorfismo</s0>
<s5>02</s5>
</fC03>
<fC03 i1="03" i2="X" l="FRE">
<s0>Gène</s0>
<s5>03</s5>
</fC03>
<fC03 i1="03" i2="X" l="ENG">
<s0>Gene</s0>
<s5>03</s5>
</fC03>
<fC03 i1="03" i2="X" l="SPA">
<s0>Gen</s0>
<s5>03</s5>
</fC03>
<fC03 i1="04" i2="X" l="FRE">
<s0>Mimétisme</s0>
<s5>04</s5>
</fC03>
<fC03 i1="04" i2="X" l="ENG">
<s0>Mimetism</s0>
<s5>04</s5>
</fC03>
<fC03 i1="04" i2="X" l="SPA">
<s0>Mimetismo</s0>
<s5>04</s5>
</fC03>
<fC03 i1="05" i2="X" l="FRE">
<s0>Morphologie</s0>
<s5>05</s5>
</fC03>
<fC03 i1="05" i2="X" l="ENG">
<s0>Morphology</s0>
<s5>05</s5>
</fC03>
<fC03 i1="05" i2="X" l="SPA">
<s0>Morfología</s0>
<s5>05</s5>
</fC03>
<fC03 i1="06" i2="X" l="FRE">
<s0>Aile</s0>
<s5>06</s5>
</fC03>
<fC03 i1="06" i2="X" l="ENG">
<s0>Wing</s0>
<s5>06</s5>
</fC03>
<fC03 i1="06" i2="X" l="SPA">
<s0>Ala</s0>
<s5>06</s5>
</fC03>
<fC03 i1="07" i2="X" l="FRE">
<s0>Coexistence</s0>
<s5>07</s5>
</fC03>
<fC03 i1="07" i2="X" l="ENG">
<s0>Coexistence</s0>
<s5>07</s5>
</fC03>
<fC03 i1="07" i2="X" l="SPA">
<s0>Coexistencia</s0>
<s5>07</s5>
</fC03>
<fC03 i1="08" i2="X" l="FRE">
<s0>Phénotype</s0>
<s5>08</s5>
</fC03>
<fC03 i1="08" i2="X" l="ENG">
<s0>Phenotype</s0>
<s5>08</s5>
</fC03>
<fC03 i1="08" i2="X" l="SPA">
<s0>Fenotipo</s0>
<s5>08</s5>
</fC03>
<fC03 i1="09" i2="X" l="FRE">
<s0>Lepidoptera</s0>
<s2>NS</s2>
<s5>55</s5>
</fC03>
<fC03 i1="09" i2="X" l="ENG">
<s0>Lepidoptera</s0>
<s2>NS</s2>
<s5>55</s5>
</fC03>
<fC03 i1="09" i2="X" l="SPA">
<s0>Lepidoptera</s0>
<s2>NS</s2>
<s5>55</s5>
</fC03>
<fC03 i1="10" i2="X" l="FRE">
<s0>Heliconius numata</s0>
<s4>INC</s4>
<s5>87</s5>
</fC03>
<fC07 i1="01" i2="X" l="FRE">
<s0>Insecta</s0>
<s2>NS</s2>
</fC07>
<fC07 i1="01" i2="X" l="ENG">
<s0>Insecta</s0>
<s2>NS</s2>
</fC07>
<fC07 i1="01" i2="X" l="SPA">
<s0>Insecta</s0>
<s2>NS</s2>
</fC07>
<fC07 i1="02" i2="X" l="FRE">
<s0>Arthropoda</s0>
<s2>NS</s2>
</fC07>
<fC07 i1="02" i2="X" l="ENG">
<s0>Arthropoda</s0>
<s2>NS</s2>
</fC07>
<fC07 i1="02" i2="X" l="SPA">
<s0>Arthropoda</s0>
<s2>NS</s2>
</fC07>
<fC07 i1="03" i2="X" l="FRE">
<s0>Invertebrata</s0>
<s2>NS</s2>
</fC07>
<fC07 i1="03" i2="X" l="ENG">
<s0>Invertebrata</s0>
<s2>NS</s2>
</fC07>
<fC07 i1="03" i2="X" l="SPA">
<s0>Invertebrata</s0>
<s2>NS</s2>
</fC07>
<fN21>
<s1>276</s1>
</fN21>
</pA>
</standard>
</inist>
</record>

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