Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling
Identifieur interne : 002F97 ( Ncbi/Merge ); précédent : 002F96; suivant : 002F98Evolutionary 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.
Descripteurs français
- KwdFr :
- MESH :
English descriptors
- KwdEn :
- MESH :
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
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PMC:4714872Le document en format XML
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<affiliation wicri:level="3"><nlm:aff id="aff008"><addr-line>Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175, CNRS–Université de Montpellier–Université Paul-Valéry–EPHE, Montpellier, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175, CNRS–Université de Montpellier–Université Paul-Valéry–EPHE, Montpellier</wicri:regionArea>
<placeName><region type="region">Occitanie (région administrative)</region>
<region type="old region">Languedoc-Roussillon</region>
<settlement type="city">Montpellier</settlement>
</placeName>
</affiliation>
</author>
<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>
</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"><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>
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</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>
</affiliation>
</author>
</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>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term>
<term>Biological Evolution</term>
<term>Butterflies (genetics)</term>
<term>Gene Expression Regulation</term>
<term>Phenotype</term>
<term>Pigmentation (genetics)</term>
<term>Wings, Animal</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Ailes d'animaux</term>
<term>Animaux</term>
<term>Papillons (génétique)</term>
<term>Phénotype</term>
<term>Pigmentation (génétique)</term>
<term>Régulation de l'expression des gènes</term>
<term>Évolution biologique</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Butterflies</term>
<term>Pigmentation</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Papillons</term>
<term>Pigmentation</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Animals</term>
<term>Biological Evolution</term>
<term>Gene Expression Regulation</term>
<term>Phenotype</term>
<term>Wings, Animal</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Ailes d'animaux</term>
<term>Animaux</term>
<term>Phénotype</term>
<term>Régulation de l'expression des gènes</term>
<term>Évolution biologique</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<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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<affiliation wicri:level="3"><nlm:aff id="aff007"><addr-line>Institut de Systématique Evolution et Biodiversité, UMR 7205, CNRS MNHN UPMC EPHE, Muséum National d'Histoire Naturelle, CP50, Paris, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut de Systématique Evolution et Biodiversité, UMR 7205, CNRS MNHN UPMC EPHE, Muséum National d'Histoire Naturelle, CP50, Paris</wicri:regionArea>
<placeName><region type="region">Île-de-France</region>
<region type="old region">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff008"><addr-line>Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175, CNRS–Université de Montpellier–Université Paul-Valéry–EPHE, Montpellier, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175, CNRS–Université de Montpellier–Université Paul-Valéry–EPHE, Montpellier</wicri:regionArea>
<placeName><region type="region">Occitanie (région administrative)</region>
<region type="old region">Languedoc-Roussillon</region>
<settlement type="city">Montpellier</settlement>
</placeName>
</affiliation>
</author>
<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>
</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"><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>
</affiliation>
</author>
</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>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<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="Jiggins, Chris D" sort="Jiggins, Chris D" uniqKey="Jiggins C" first="Chris D" last="Jiggins">Chris D. Jiggins</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling.</title>
<author><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>
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</author>
<author><name sortKey="Baxter, Simon W" sort="Baxter, Simon W" uniqKey="Baxter S" first="Simon W" last="Baxter">Simon W. Baxter</name>
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<country xml:lang="fr">Australie</country>
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<author><name sortKey="Pardo Diaz, Carolina" sort="Pardo Diaz, Carolina" uniqKey="Pardo Diaz C" first="Carolina" last="Pardo-Diaz">Carolina Pardo-Diaz</name>
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<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>
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</author>
<author><name sortKey="Hanly, Joseph J" sort="Hanly, Joseph J" uniqKey="Hanly J" first="Joseph J" last="Hanly">Joseph J. Hanly</name>
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<orgName type="university">Université de Cambridge</orgName>
<placeName><settlement type="city">Cambridge</settlement>
<region type="country">Angleterre</region>
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<author><name sortKey="Martin, Simon H" sort="Martin, Simon H" uniqKey="Martin S" first="Simon H" last="Martin">Simon H. Martin</name>
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<wicri:regionArea>Department of Zoology, University of Cambridge, Cambridge</wicri:regionArea>
<orgName type="university">Université de Cambridge</orgName>
<placeName><settlement type="city">Cambridge</settlement>
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<author><name sortKey="Mallet, James" sort="Mallet, James" uniqKey="Mallet J" first="James" last="Mallet">James Mallet</name>
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<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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</author>
<author><name sortKey="Dasmahapatra, Kanchon K" sort="Dasmahapatra, Kanchon K" uniqKey="Dasmahapatra K" first="Kanchon K" last="Dasmahapatra">Kanchon K. Dasmahapatra</name>
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<country xml:lang="fr">Panama</country>
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<wicri:noRegion>Ancón</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Salazar, Camilo" sort="Salazar, Camilo" uniqKey="Salazar C" first="Camilo" last="Salazar">Camilo Salazar</name>
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<country xml:lang="fr">Panama</country>
<wicri:regionArea>Smithsonian Tropical Research Institution, Balboa, Ancón</wicri:regionArea>
<wicri:noRegion>Ancón</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Joron, Mathieu" sort="Joron, Mathieu" uniqKey="Joron M" first="Mathieu" last="Joron">Mathieu Joron</name>
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</affiliation>
</author>
<author><name sortKey="Nadeau, Nicola" sort="Nadeau, Nicola" uniqKey="Nadeau N" first="Nicola" last="Nadeau">Nicola Nadeau</name>
<affiliation wicri:level="1"><nlm:affiliation>Dept. of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom.</nlm:affiliation>
<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:affiliation>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama.</nlm:affiliation>
<country xml:lang="fr">Panama</country>
<wicri:regionArea>Smithsonian Tropical Research Institution, Balboa, Ancón</wicri:regionArea>
<wicri:noRegion>Ancón</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"><nlm:affiliation>Department of Zoology, University of Cambridge, Cambridge, United Kingdom.</nlm:affiliation>
<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>
</author>
</analytic>
<series><title level="j">PLoS biology</title>
<idno type="eISSN">1545-7885</idno>
<imprint><date when="2016" type="published">2016</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term>
<term>Biological Evolution</term>
<term>Butterflies (genetics)</term>
<term>Gene Expression Regulation</term>
<term>Phenotype</term>
<term>Pigmentation (genetics)</term>
<term>Wings, Animal</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Ailes d'animaux</term>
<term>Animaux</term>
<term>Papillons (génétique)</term>
<term>Phénotype</term>
<term>Pigmentation (génétique)</term>
<term>Régulation de l'expression des gènes</term>
<term>Évolution biologique</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Butterflies</term>
<term>Pigmentation</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Papillons</term>
<term>Pigmentation</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Animals</term>
<term>Biological Evolution</term>
<term>Gene Expression Regulation</term>
<term>Phenotype</term>
<term>Wings, Animal</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Ailes d'animaux</term>
<term>Animaux</term>
<term>Phénotype</term>
<term>Régulation de l'expression des gènes</term>
<term>Évolution biologique</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en">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 Heliconius butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, dennis and ray. We hypothesise that these modules in non-coding sequence represent distinct cis-regulatory loci that control expression of the transcription factor optix, which in turn controls red pattern variation across Heliconius. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these cis-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 Heliconius melpomene at about the same time that ray originated in this group, while ray introgressed back into H. elevatus 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.</div>
</front>
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