Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling.
Identifieur interne : 002329 ( PubMed/Curation ); précédent : 002328; suivant : 002330Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling.
Auteurs : Richard W R. Wallbank [Royaume-Uni] ; Simon W. Baxter [Australie] ; Carolina Pardo-Diaz [Royaume-Uni] ; Joseph J. Hanly [Royaume-Uni] ; Simon H. Martin [Royaume-Uni] ; James Mallet [Panama] ; Kanchon K. Dasmahapatra [Panama] ; Camilo Salazar [Panama] ; Mathieu Joron [Panama] ; Nicola Nadeau [Royaume-Uni] ; W Owen Mcmillan [Panama] ; Chris D. Jiggins [Royaume-Uni]Source :
- PLoS biology [ 1545-7885 ] ; 2016.
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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 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.
DOI: 10.1371/journal.pbio.1002353
PubMed: 26771987
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Jiggins</name><affiliation wicri:level="1"><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></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></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">26771987</PMID><DateCreated><Year>2016</Year><Month>01</Month><Day>16</Day></DateCreated><DateCompleted><Year>2016</Year><Month>06</Month><Day>07</Day></DateCompleted><DateRevised><Year>2017</Year><Month>09</Month><Day>22</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1545-7885</ISSN><JournalIssue CitedMedium="Internet"><Volume>14</Volume><Issue>1</Issue><PubDate><Year>2016</Year><Month>Jan</Month></PubDate></JournalIssue><Title>PLoS biology</Title><ISOAbbreviation>PLoS Biol.</ISOAbbreviation></Journal><ArticleTitle>Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling.</ArticleTitle><Pagination><MedlinePgn>e1002353</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pbio.1002353</ELocationID><Abstract><AbstractText>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.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wallbank</LastName><ForeName>Richard W R</ForeName><Initials>RW</Initials><AffiliationInfo><Affiliation>Department of Zoology, University of Cambridge, Cambridge, United Kingdom.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Baxter</LastName><ForeName>Simon W</ForeName><Initials>SW</Initials><AffiliationInfo><Affiliation>School of Biological Sciences, University of Adelaide, Adelaide, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pardo-Diaz</LastName><ForeName>Carolina</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Department of Zoology, University of Cambridge, Cambridge, United Kingdom.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Biology Program, Faculty of Natural Sciences and Mathematics, Universidad del Rosario, Bogotá, D.C., Colombia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hanly</LastName><ForeName>Joseph J</ForeName><Initials>JJ</Initials><AffiliationInfo><Affiliation>Department of Zoology, University of Cambridge, Cambridge, United Kingdom.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Martin</LastName><ForeName>Simon H</ForeName><Initials>SH</Initials><AffiliationInfo><Affiliation>Department of Zoology, University of Cambridge, Cambridge, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mallet</LastName><ForeName>James</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Organismic and Evolutionary Biology, Harvard University, Harvard, Massachusetts, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dasmahapatra</LastName><ForeName>Kanchon K</ForeName><Initials>KK</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Biology, University of York, York, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Salazar</LastName><ForeName>Camilo</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Biology Program, Faculty of Natural Sciences and Mathematics, Universidad del Rosario, Bogotá, D.C., Colombia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Joron</LastName><ForeName>Mathieu</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institut de Systématique Evolution et Biodiversité, UMR 7205, CNRS MNHN UPMC EPHE, Muséum National d'Histoire Naturelle, CP50, Paris, France.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Centre d'Ecologie Fonctionnelle et Evolutive, UMR 5175, CNRS-Université de Montpellier-Université Paul-Valéry-EPHE, Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nadeau</LastName><ForeName>Nicola</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Dept. of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>McMillan</LastName><ForeName>W Owen</ForeName><Initials>WO</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jiggins</LastName><ForeName>Chris D</ForeName><Initials>CD</Initials><AffiliationInfo><Affiliation>Department of Zoology, University of Cambridge, Cambridge, United Kingdom.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institution, Balboa, Ancón, Panama.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>BB/G006903/1</GrantID><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>BB/H01439X/1</GrantID><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>H01439X/1</GrantID><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2016</Year><Month>01</Month><Day>15</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>PLoS 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UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005786" MajorTopicYN="Y">Gene Expression Regulation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010641" MajorTopicYN="N">Phenotype</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010858" MajorTopicYN="N">Pigmentation</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014921" MajorTopicYN="N">Wings, Animal</DescriptorName></MeshHeading></MeshHeadingList><OtherID Source="NLM">PMC4714872</OtherID></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2015</Year><Month>06</Month><Day>17</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2015</Year><Month>12</Month><Day>08</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2016</Year><Month>1</Month><Day>16</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2016</Year><Month>1</Month><Day>16</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2016</Year><Month>6</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">26771987</ArticleId><ArticleId IdType="doi">10.1371/journal.pbio.1002353</ArticleId><ArticleId IdType="pii">PBIOLOGY-D-15-01809</ArticleId><ArticleId IdType="pmc">PMC4714872</ArticleId></ArticleIdList></PubmedData></pubmed></record>Pour manipuler ce document sous Unix (Dilib)
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