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Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry

Identifieur interne : 001D30 ( Pmc/Corpus ); précédent : 001D29; suivant : 001D31

Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry

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

Source :

RBID : PMC:3717454

Abstract

Supergenes are tight clusters of loci that facilitate the co-segregation of adaptive variation, providing integrated control of complex adaptive phenotypes1. 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 mimicry35 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 challenge710. 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 species911, 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 Plocus, 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.


Url:
DOI: 10.1038/nature10341
PubMed: 21841803
PubMed Central: 3717454

Links to Exploration step

PMC:3717454

Le document en format XML

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<name sortKey="Becuwe, Michel" sort="Becuwe, Michel" uniqKey="Becuwe M" first="Michel" last="Becuwe">Michel Becuwe</name>
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<name sortKey="Ferguson, Laura" sort="Ferguson, Laura" uniqKey="Ferguson L" first="Laura" last="Ferguson">Laura Ferguson</name>
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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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<name sortKey="Davidson, Claire" sort="Davidson, Claire" uniqKey="Davidson C" first="Claire" last="Davidson">Claire Davidson</name>
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<nlm:aff id="A9">The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1HH, UK.</nlm:aff>
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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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<nlm:aff id="A9">The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1HH, UK.</nlm:aff>
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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="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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<div type="abstract" xml:lang="en">
<p id="P2">Supergenes are tight clusters of loci that facilitate the co-segregation of adaptive variation, providing integrated control of complex adaptive phenotypes
<sup>
<xref ref-type="bibr" rid="R1">1</xref>
</sup>
. Polymorphic supergenes, in which specific combinations of traits are maintained within a single population, were first described for ‘pin’ and ‘thrum’ floral types in
<italic>Primula</italic>
<sup>
<xref ref-type="bibr" rid="R1">1</xref>
</sup>
and
<italic>Fagopyrum</italic>
<sup>
<xref ref-type="bibr" rid="R2">2</xref>
</sup>
, but classic examples are also found in insect mimicry
<sup>
<xref ref-type="bibr" rid="R3">3</xref>
<xref ref-type="bibr" rid="R5">5</xref>
</sup>
and snail morphology
<sup>
<xref ref-type="bibr" rid="R6">6</xref>
</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>
<xref ref-type="bibr" rid="R7">7</xref>
<xref ref-type="bibr" rid="R10">10</xref>
</sup>
. Here we show that individual wing-pattern morphs in the polymorphic mimetic butterfly
<italic>Heliconius numata</italic>
are associated with different genomic rearrangements at the supergene locus
<italic>P</italic>
. These rearrangements tighten the genetic linkage between at least two colour-pattern loci that are known to recombine in closely related species
<sup>
<xref ref-type="bibr" rid="R9">9</xref>
<xref ref-type="bibr" rid="R11">11</xref>
</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
<italic>P</italic>
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
<italic>P</italic>
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.</p>
</div>
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<name>
<surname>Joron</surname>
<given-names>Mathieu</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="aff" rid="A3">3</xref>
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<name>
<surname>Frezal</surname>
<given-names>Lise</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="author-notes" rid="FN1">*</xref>
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<contrib contrib-type="author">
<name>
<surname>Jones</surname>
<given-names>Robert T.</given-names>
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<xref ref-type="aff" rid="A4">4</xref>
<xref ref-type="author-notes" rid="FN1">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chamberlain</surname>
<given-names>Nicola L.</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
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<contrib contrib-type="author">
<name>
<surname>Lee</surname>
<given-names>Siu F.</given-names>
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<xref ref-type="aff" rid="A5">5</xref>
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<contrib contrib-type="author">
<name>
<surname>Haag</surname>
<given-names>Christoph R.</given-names>
</name>
<xref ref-type="aff" rid="A6">6</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Whibley</surname>
<given-names>Annabel</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Becuwe</surname>
<given-names>Michel</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Baxter</surname>
<given-names>Simon W.</given-names>
</name>
<xref ref-type="aff" rid="A7">7</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ferguson</surname>
<given-names>Laura</given-names>
</name>
<xref ref-type="aff" rid="A7">7</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wilkinson</surname>
<given-names>Paul A.</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Salazar</surname>
<given-names>Camilo</given-names>
</name>
<xref ref-type="aff" rid="A8">8</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Davidson</surname>
<given-names>Claire</given-names>
</name>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Clark</surname>
<given-names>Richard</given-names>
</name>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Quail</surname>
<given-names>Michael A.</given-names>
</name>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Beasley</surname>
<given-names>Helen</given-names>
</name>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Glithero</surname>
<given-names>Rebecca</given-names>
</name>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lloyd</surname>
<given-names>Christine</given-names>
</name>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sims</surname>
<given-names>Sarah</given-names>
</name>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Jones</surname>
<given-names>Matthew C.</given-names>
</name>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rogers</surname>
<given-names>Jane</given-names>
</name>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Jiggins</surname>
<given-names>Chris D.</given-names>
</name>
<xref ref-type="aff" rid="A7">7</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>ffrench-Constant</surname>
<given-names>Richard H.</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
</contrib>
</contrib-group>
<aff id="A1">
<label>1</label>
CNRS UMR 7205, Muséum National d’Histoire Naturelle, CP50, 45 Rue Buffon, 75005 Paris, France.</aff>
<aff id="A2">
<label>2</label>
Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, King’s Buildings, West Mains Road, Edinburgh EH9 3JT, UK.</aff>
<aff id="A3">
<label>3</label>
Institute of Biology, Leiden University, Postbus 9505, 2300 RA Leiden, The Netherlands.</aff>
<aff id="A4">
<label>4</label>
Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn, Cornwall TR10 9EZ, UK.</aff>
<aff id="A5">
<label>5</label>
Department of Genetics, Bio21 Institute, University of Melbourne, 30 Flemington Road, Parkville, 3010 Victoria, Australia.</aff>
<aff id="A6">
<label>6</label>
Department of Biology, Ecology and Evolution, University of Fribourg, Chemin du Musée 10, CH-1700 Fribourg, Switzerland.</aff>
<aff id="A7">
<label>7</label>
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK.</aff>
<aff id="A8">
<label>8</label>
Smithsonian Tropical Research Institute, NAOS island, Causeway Amador, Panamá, República de Panamá.</aff>
<aff id="A9">
<label>9</label>
The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1HH, UK.</aff>
<author-notes>
<corresp id="CR1">Correspondence and requests for materials should be addressed to M.J. (
<email>joron@mnhn.fr</email>
).</corresp>
<fn fn-type="equal" id="FN1">
<label>*</label>
<p id="P1">These authors contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="nihms-submitted">
<day>5</day>
<month>7</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="epub">
<day>14</day>
<month>8</month>
<year>2011</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>22</day>
<month>7</month>
<year>2013</year>
</pub-date>
<volume>477</volume>
<issue>7363</issue>
<fpage>203</fpage>
<lpage>206</lpage>
<abstract>
<p id="P2">Supergenes are tight clusters of loci that facilitate the co-segregation of adaptive variation, providing integrated control of complex adaptive phenotypes
<sup>
<xref ref-type="bibr" rid="R1">1</xref>
</sup>
. Polymorphic supergenes, in which specific combinations of traits are maintained within a single population, were first described for ‘pin’ and ‘thrum’ floral types in
<italic>Primula</italic>
<sup>
<xref ref-type="bibr" rid="R1">1</xref>
</sup>
and
<italic>Fagopyrum</italic>
<sup>
<xref ref-type="bibr" rid="R2">2</xref>
</sup>
, but classic examples are also found in insect mimicry
<sup>
<xref ref-type="bibr" rid="R3">3</xref>
<xref ref-type="bibr" rid="R5">5</xref>
</sup>
and snail morphology
<sup>
<xref ref-type="bibr" rid="R6">6</xref>
</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>
<xref ref-type="bibr" rid="R7">7</xref>
<xref ref-type="bibr" rid="R10">10</xref>
</sup>
. Here we show that individual wing-pattern morphs in the polymorphic mimetic butterfly
<italic>Heliconius numata</italic>
are associated with different genomic rearrangements at the supergene locus
<italic>P</italic>
. These rearrangements tighten the genetic linkage between at least two colour-pattern loci that are known to recombine in closely related species
<sup>
<xref ref-type="bibr" rid="R9">9</xref>
<xref ref-type="bibr" rid="R11">11</xref>
</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
<italic>P</italic>
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
<italic>P</italic>
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.</p>
</abstract>
<funding-group>
<award-group>
<funding-source country="United Kingdom">Wellcome Trust : </funding-source>
<award-id>098051 || WT</award-id>
</award-group>
</funding-group>
</article-meta>
</front>
</pmc>
</record>

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