Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling
Identifieur interne : 000954 ( Pmc/Checkpoint ); précédent : 000953; suivant : 000955Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling
Auteurs : Richard W. R. Wallbank [Royaume-Uni, Panama] ; Simon W. Baxter [Australie] ; Carolina Pardo-Diaz [Royaume-Uni, Panama, Colombie] ; Joseph J. Hanly [Royaume-Uni, Panama] ; Simon H. Martin [Royaume-Uni] ; James Mallet [Panama, États-Unis] ; Kanchon K. Dasmahapatra [Panama, Royaume-Uni] ; Camilo Salazar [Panama, Colombie] ; Mathieu Joron [Panama, France] ; Nicola Nadeau [Royaume-Uni] ; W. Owen Mcmillan [Panama] ; Chris D. Jiggins [Royaume-Uni, Panama]Source :
- PLoS Biology [ 1544-9173 ] ; 2016.
Abstract
An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian
Url:
DOI: 10.1371/journal.pbio.1002353
PubMed: 26771987
PubMed Central: 4714872
Affiliations:
- Australie, Colombie, France, Panama, Royaume-Uni, États-Unis
- Angleterre, Angleterre de l'Est, Languedoc-Roussillon, Massachusetts, Occitanie (région administrative), Île-de-France
- Cambridge, Cambridge (Massachusetts), Montpellier, Paris
- Université Harvard, Université de Cambridge
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PMC:4714872Le document en format XML
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<author><name sortKey="Nadeau, Nicola" sort="Nadeau, Nicola" uniqKey="Nadeau N" first="Nicola" last="Nadeau">Nicola Nadeau</name>
<affiliation wicri:level="1"><nlm:aff id="aff009"><addr-line>Dept. of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom</addr-line>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Dept. of Animal and Plant Sciences, University of Sheffield, Sheffield</wicri:regionArea>
<wicri:noRegion>Sheffield</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Mcmillan, W Owen" sort="Mcmillan, W Owen" uniqKey="Mcmillan W" first="W. Owen" last="Mcmillan">W. Owen Mcmillan</name>
<affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama</addr-line>
</nlm:aff>
<country xml:lang="fr">Panama</country>
<wicri:regionArea>Smithsonian Tropical Research Institution, Balboa, Ancón</wicri:regionArea>
<wicri:noRegion>Ancón</wicri:noRegion>
</affiliation>
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<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"><nlm:aff id="aff001"><addr-line>Department of Zoology, University of Cambridge, Cambridge, United Kingdom</addr-line>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Department of Zoology, University of Cambridge, Cambridge</wicri:regionArea>
<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>
<affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama</addr-line>
</nlm:aff>
<country xml:lang="fr">Panama</country>
<wicri:regionArea>Smithsonian Tropical Research Institution, Balboa, Ancón</wicri:regionArea>
<wicri:noRegion>Ancón</wicri:noRegion>
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</analytic>
<series><title level="j">PLoS Biology</title>
<idno type="ISSN">1544-9173</idno>
<idno type="eISSN">1545-7885</idno>
<imprint><date when="2016">2016</date>
</imprint>
</series>
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<front><div type="abstract" xml:lang="en"><p>An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian <italic>Heliconius</italic>
butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, <italic>dennis</italic>
and <italic>ray</italic>
. We hypothesise that these modules in non-coding sequence represent distinct <italic>cis</italic>
-regulatory loci that control expression of the transcription factor <italic>optix</italic>
, which in turn controls red pattern variation across <italic>Heliconius</italic>
. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these <italic>cis</italic>
-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into <italic>Heliconius melpomene</italic>
at about the same time that ray originated in this group, while ray introgressed back into <italic>H</italic>
. <italic>elevatus</italic>
much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.</p>
</div>
</front>
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<author><name sortKey="Xie, D" uniqKey="Xie D">D Xie</name>
</author>
<author><name sortKey="Rambaut, A" uniqKey="Rambaut A">A Rambaut</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Gernhard, T" uniqKey="Gernhard T">T Gernhard</name>
</author>
</analytic>
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<biblStruct></biblStruct>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Biol</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS Biol</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosbiol</journal-id>
<journal-title-group><journal-title>PLoS Biology</journal-title>
</journal-title-group>
<issn pub-type="ppub">1544-9173</issn>
<issn pub-type="epub">1545-7885</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">26771987</article-id>
<article-id pub-id-type="pmc">4714872</article-id>
<article-id pub-id-type="doi">10.1371/journal.pbio.1002353</article-id>
<article-id pub-id-type="publisher-id">PBIOLOGY-D-15-01809</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling</article-title>
<alt-title alt-title-type="running-head">Evolution of Novel Butterfly Wing Patterns</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Wallbank</surname>
<given-names>Richard W. R.</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Baxter</surname>
<given-names>Simon W.</given-names>
</name>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pardo-Diaz</surname>
<given-names>Carolina</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff004"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hanly</surname>
<given-names>Joseph J.</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Martin</surname>
<given-names>Simon H.</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mallet</surname>
<given-names>James</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dasmahapatra</surname>
<given-names>Kanchon K.</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff006"><sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Salazar</surname>
<given-names>Camilo</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff004"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Joron</surname>
<given-names>Mathieu</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff007"><sup>7</sup>
</xref>
<xref ref-type="aff" rid="aff008"><sup>8</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Nadeau</surname>
<given-names>Nicola</given-names>
</name>
<xref ref-type="aff" rid="aff009"><sup>9</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>McMillan</surname>
<given-names>W. Owen</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jiggins</surname>
<given-names>Chris D.</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref rid="cor001" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="aff001"><label>1</label>
<addr-line>Department of Zoology, University of Cambridge, Cambridge, United Kingdom</addr-line>
</aff>
<aff id="aff002"><label>2</label>
<addr-line>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama</addr-line>
</aff>
<aff id="aff003"><label>3</label>
<addr-line>School of Biological Sciences, University of Adelaide, Adelaide, Australia</addr-line>
</aff>
<aff id="aff004"><label>4</label>
<addr-line>Biology Program, Faculty of Natural Sciences and Mathematics, Universidad del Rosario, Bogotá, D.C., Colombia</addr-line>
</aff>
<aff id="aff005"><label>5</label>
<addr-line>Organismic and Evolutionary Biology, Harvard University, Harvard, Massachusetts, United States of America</addr-line>
</aff>
<aff id="aff006"><label>6</label>
<addr-line>Department of Biology, University of York, York, United Kingdom</addr-line>
</aff>
<aff id="aff007"><label>7</label>
<addr-line>Institut de Systématique Evolution et Biodiversité, UMR 7205, CNRS MNHN UPMC EPHE, Muséum National d'Histoire Naturelle, CP50, Paris, France</addr-line>
</aff>
<aff id="aff008"><label>8</label>
<addr-line>Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175, CNRS–Université de Montpellier–Université Paul-Valéry–EPHE, Montpellier, France</addr-line>
</aff>
<aff id="aff009"><label>9</label>
<addr-line>Dept. of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Barton</surname>
<given-names>Nick H.</given-names>
</name>
<role>Academic Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>Institute of Science and Technology Austria (IST Austria), AUSTRIA</addr-line>
</aff>
<author-notes><fn fn-type="conflict" id="coi001"><p>The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con" id="contrib001"><p>Conceived and designed the experiments: CDJ SWB RWRW CPD. Performed the experiments: SWB RWRW CPD. Analyzed the data: SWB RWRW CPD SHM NN CS JJH. Contributed reagents/materials/analysis tools: WOM JM KKD MJ CS. Wrote the paper: CDJ RWRW CPD SWB WOM JM KKD MJ JJH.</p>
</fn>
<corresp id="cor001">* E-mail: <email>c.jiggins@zoo.cam.ac.uk</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>15</day>
<month>1</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><month>1</month>
<year>2016</year>
</pub-date>
<volume>14</volume>
<issue>1</issue>
<elocation-id>e1002353</elocation-id>
<history><date date-type="received"><day>17</day>
<month>6</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>8</day>
<month>12</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-statement>© 2016 Wallbank et al</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Wallbank et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="pbio.1002353.pdf"></self-uri>
<abstract><p>An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian <italic>Heliconius</italic>
butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, <italic>dennis</italic>
and <italic>ray</italic>
. We hypothesise that these modules in non-coding sequence represent distinct <italic>cis</italic>
-regulatory loci that control expression of the transcription factor <italic>optix</italic>
, which in turn controls red pattern variation across <italic>Heliconius</italic>
. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these <italic>cis</italic>
-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into <italic>Heliconius melpomene</italic>
at about the same time that ray originated in this group, while ray introgressed back into <italic>H</italic>
. <italic>elevatus</italic>
much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.</p>
</abstract>
<abstract abstract-type="toc"><p>Novel butterfly wing patterns have arisen via the sharing of gene regulatory elements between lineages through introgression and recombination; new combinations of regulatory elements offer a rapid route to the evolution of new patterns.</p>
</abstract>
<abstract abstract-type="summary"><title>Author Summary</title>
<p>Butterflies show an amazing diversity of patterns on their wings. In fact, most of the 18,000 species of butterfly can be distinguished on the basis of their wing pattern. Much of this diversity is thought to arise through novel switches in the genome that turn genes on in new contexts during wing development, thereby producing new patterns. Here we study a set of switches that control the expression of <italic>optix</italic>
, a gene that places red patches onto the wings of <italic>Heliconius</italic>
butterflies. We show that two patterning switches—one that produces red rays on the hindwing and the other a red patch on the base of the forewing—are located adjacent to one another in the genome. These switches have each evolved just once among a group of 16 species but have then been repeatedly shared between species by hybridisation and introgression. Despite the fact that they are now part of a common pattern in the Amazon basin, these two pattern components actually arose in completely different species before being brought together through hybridisation. In addition, recombination among these switches has produced new combinations of patterns within species. Such sharing of genetic variation is one way in which mimicry can evolve, whereby patterns are shared between species to send a common signal to predators. Our work suggests a new mechanism for generating evolutionary novelty, by shuffling these genetic switches among lineages and within species.</p>
</abstract>
<funding-group><funding-statement>This study was funded by the Biotechnology and Biological Sciences Research Council <ext-link ext-link-type="uri" xlink:href="http://www.bbsrc.ac.uk">http://www.bbsrc.ac.uk</ext-link>
grant number H01439X/1 to CDJ; the European Research Council MimEvol grant to MJ and the European Research Council Speciation Genetics to CDJ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><fig-count count="5"></fig-count>
<table-count count="1"></table-count>
<page-count count="16"></page-count>
</counts>
<custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>All complete genome sequence data are available through the Short Read Archive with project accession number ERP009041 (full details in Samples <xref rid="pbio.1002353.s006" ref-type="supplementary-material">S3 Table</xref>
). The sequence alignment, association data and other raw data are available on DataDryad <ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.5061/dryad.t3r02">http://dx.doi.org/10.5061/dryad.t3r02</ext-link>
.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>All complete genome sequence data are available through the Short Read Archive with project accession number ERP009041 (full details in Samples <xref rid="pbio.1002353.s006" ref-type="supplementary-material">S3 Table</xref>
). The sequence alignment, association data and other raw data are available on DataDryad <ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.5061/dryad.t3r02">http://dx.doi.org/10.5061/dryad.t3r02</ext-link>
.</p>
</notes>
</front>
</pmc>
<affiliations><list><country><li>Australie</li>
<li>Colombie</li>
<li>France</li>
<li>Panama</li>
<li>Royaume-Uni</li>
<li>États-Unis</li>
</country>
<region><li>Angleterre</li>
<li>Angleterre de l'Est</li>
<li>Languedoc-Roussillon</li>
<li>Massachusetts</li>
<li>Occitanie (région administrative)</li>
<li>Île-de-France</li>
</region>
<settlement><li>Cambridge</li>
<li>Cambridge (Massachusetts)</li>
<li>Montpellier</li>
<li>Paris</li>
</settlement>
<orgName><li>Université Harvard</li>
<li>Université de Cambridge</li>
</orgName>
</list>
<tree><country name="Royaume-Uni"><region name="Angleterre"><name sortKey="Wallbank, Richard W R" sort="Wallbank, Richard W R" uniqKey="Wallbank R" first="Richard W. R." last="Wallbank">Richard W. R. Wallbank</name>
</region>
<name sortKey="Dasmahapatra, Kanchon K" sort="Dasmahapatra, Kanchon K" uniqKey="Dasmahapatra K" first="Kanchon K." last="Dasmahapatra">Kanchon K. Dasmahapatra</name>
<name sortKey="Hanly, Joseph J" sort="Hanly, Joseph J" uniqKey="Hanly J" first="Joseph J." last="Hanly">Joseph J. Hanly</name>
<name sortKey="Jiggins, Chris D" sort="Jiggins, Chris D" uniqKey="Jiggins C" first="Chris D." last="Jiggins">Chris D. Jiggins</name>
<name sortKey="Martin, Simon H" sort="Martin, Simon H" uniqKey="Martin S" first="Simon H." last="Martin">Simon H. Martin</name>
<name sortKey="Nadeau, Nicola" sort="Nadeau, Nicola" uniqKey="Nadeau N" first="Nicola" last="Nadeau">Nicola Nadeau</name>
<name sortKey="Pardo Diaz, Carolina" sort="Pardo Diaz, Carolina" uniqKey="Pardo Diaz C" first="Carolina" last="Pardo-Diaz">Carolina Pardo-Diaz</name>
</country>
<country name="Panama"><noRegion><name sortKey="Wallbank, Richard W R" sort="Wallbank, Richard W R" uniqKey="Wallbank R" first="Richard W. R." last="Wallbank">Richard W. R. Wallbank</name>
</noRegion>
<name sortKey="Dasmahapatra, Kanchon K" sort="Dasmahapatra, Kanchon K" uniqKey="Dasmahapatra K" first="Kanchon K." last="Dasmahapatra">Kanchon K. Dasmahapatra</name>
<name sortKey="Hanly, Joseph J" sort="Hanly, Joseph J" uniqKey="Hanly J" first="Joseph J." last="Hanly">Joseph J. Hanly</name>
<name sortKey="Jiggins, Chris D" sort="Jiggins, Chris D" uniqKey="Jiggins C" first="Chris D." last="Jiggins">Chris D. Jiggins</name>
<name sortKey="Joron, Mathieu" sort="Joron, Mathieu" uniqKey="Joron M" first="Mathieu" last="Joron">Mathieu Joron</name>
<name sortKey="Mallet, James" sort="Mallet, James" uniqKey="Mallet J" first="James" last="Mallet">James Mallet</name>
<name sortKey="Mcmillan, W Owen" sort="Mcmillan, W Owen" uniqKey="Mcmillan W" first="W. Owen" last="Mcmillan">W. Owen Mcmillan</name>
<name sortKey="Pardo Diaz, Carolina" sort="Pardo Diaz, Carolina" uniqKey="Pardo Diaz C" first="Carolina" last="Pardo-Diaz">Carolina Pardo-Diaz</name>
<name sortKey="Salazar, Camilo" sort="Salazar, Camilo" uniqKey="Salazar C" first="Camilo" last="Salazar">Camilo Salazar</name>
</country>
<country name="Australie"><noRegion><name sortKey="Baxter, Simon W" sort="Baxter, Simon W" uniqKey="Baxter S" first="Simon W." last="Baxter">Simon W. Baxter</name>
</noRegion>
</country>
<country name="Colombie"><noRegion><name sortKey="Pardo Diaz, Carolina" sort="Pardo Diaz, Carolina" uniqKey="Pardo Diaz C" first="Carolina" last="Pardo-Diaz">Carolina Pardo-Diaz</name>
</noRegion>
<name sortKey="Salazar, Camilo" sort="Salazar, Camilo" uniqKey="Salazar C" first="Camilo" last="Salazar">Camilo Salazar</name>
</country>
<country name="États-Unis"><region name="Massachusetts"><name sortKey="Mallet, James" sort="Mallet, James" uniqKey="Mallet J" first="James" last="Mallet">James Mallet</name>
</region>
</country>
<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="Joron, Mathieu" sort="Joron, Mathieu" uniqKey="Joron M" first="Mathieu" last="Joron">Mathieu Joron</name>
</country>
</tree>
</affiliations>
</record>
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