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Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing
Heliconius butterflies represent a recent radiation of species, in which wing pattern divergence has been implicated in speciation. Several loci that control wing pattern phenotypes have been mapped and two were identified through sequencing. These same gene regions play a role in adaptation across...
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Published in: | Philosophical transactions of the Royal Society of London. Series B. Biological sciences 2012-02, Vol.367 (1587), p.343-353 |
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creator | Nadeau, Nicola J. Whibley, Annabel Jones, Robert T. Davey, John W. Dasmahapatra, Kanchon K. Baxter, Simon W. Quail, Michael A. Joron, Mathieu ffrench-Constant, Richard H. Blaxter, Mark L. Mallet, James Jiggins, Chris D. |
description | Heliconius butterflies represent a recent radiation of species, in which wing pattern divergence has been implicated in speciation. Several loci that control wing pattern phenotypes have been mapped and two were identified through sequencing. These same gene regions play a role in adaptation across the whole Heliconius radiation. Previous studies of population genetic patterns at these regions have sequenced small amplicons. Here, we use targeted next-generation sequence capture to survey patterns of divergence across these entire regions in divergent geographical races and species of Heliconius. This technique was successful both within and between species for obtaining high coverage of almost all coding regions and sufficient coverage of non-coding regions to perform population genetic analyses. We find major peaks of elevated population differentiation between races across hybrid zones, which indicate regions under strong divergent selection. These ‘islands’ of divergence appear to be more extensive between closely related species, but there is less clear evidence for such islands between more distantly related species at two further points along the ‘speciation continuum’. We also sequence fosmid clones across these regions in different Heliconius melpomene races. We find no major structural rearrangements but many relatively large (greater than 1 kb) insertion/deletion events (including gain/loss of transposable elements) that are variable between races. |
doi_str_mv | 10.1098/rstb.2011.0198 |
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Several loci that control wing pattern phenotypes have been mapped and two were identified through sequencing. These same gene regions play a role in adaptation across the whole Heliconius radiation. Previous studies of population genetic patterns at these regions have sequenced small amplicons. Here, we use targeted next-generation sequence capture to survey patterns of divergence across these entire regions in divergent geographical races and species of Heliconius. This technique was successful both within and between species for obtaining high coverage of almost all coding regions and sufficient coverage of non-coding regions to perform population genetic analyses. We find major peaks of elevated population differentiation between races across hybrid zones, which indicate regions under strong divergent selection. These ‘islands’ of divergence appear to be more extensive between closely related species, but there is less clear evidence for such islands between more distantly related species at two further points along the ‘speciation continuum’. We also sequence fosmid clones across these regions in different Heliconius melpomene races. We find no major structural rearrangements but many relatively large (greater than 1 kb) insertion/deletion events (including gain/loss of transposable elements) that are variable between races.</description><identifier>ISSN: 0962-8436</identifier><identifier>EISSN: 1471-2970</identifier><identifier>DOI: 10.1098/rstb.2011.0198</identifier><identifier>PMID: 22201164</identifier><language>eng</language><publisher>England: The Royal Society</publisher><subject>Adaptation, Biological - genetics ; Animals ; Base Sequence ; Butterflies ; Butterflies - classification ; Butterflies - genetics ; Butterflies - physiology ; Chromosomes, Insect - genetics ; Colour Pattern ; Divergence ; Evolutionary genetics ; Gene flow ; Genes, Insect ; Genetic Loci ; Genetic Speciation ; Genetic Variation ; Genetics, Population ; Genome, Insect ; Genomes ; Genomic Islands ; Genomics ; Heliconius ; Heliconius melpomene ; Hybridity ; Molecular Mimicry ; Molecular Sequence Data ; Nucleotides ; Phylogeny ; Sequence Analysis, DNA - methods ; Sequencing ; Speciation ; Species Specificity ; Target Enrichment ; Wings, Animal - physiology</subject><ispartof>Philosophical transactions of the Royal Society of London. Series B. Biological sciences, 2012-02, Vol.367 (1587), p.343-353</ispartof><rights>Copyright © 2011 The Royal Society</rights><rights>This journal is © 2011 The Royal Society</rights><rights>This journal is © 2011 The Royal Society 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c525t-e7b164e2cd47ad338a4d817b3694cd509e0df383da442c9944fe77e8d03cba393</citedby><cites>FETCH-LOGICAL-c525t-e7b164e2cd47ad338a4d817b3694cd509e0df383da442c9944fe77e8d03cba393</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41433526$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41433526$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22201164$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nadeau, Nicola J.</creatorcontrib><creatorcontrib>Whibley, Annabel</creatorcontrib><creatorcontrib>Jones, Robert T.</creatorcontrib><creatorcontrib>Davey, John W.</creatorcontrib><creatorcontrib>Dasmahapatra, Kanchon K.</creatorcontrib><creatorcontrib>Baxter, Simon W.</creatorcontrib><creatorcontrib>Quail, Michael A.</creatorcontrib><creatorcontrib>Joron, Mathieu</creatorcontrib><creatorcontrib>ffrench-Constant, Richard H.</creatorcontrib><creatorcontrib>Blaxter, Mark L.</creatorcontrib><creatorcontrib>Mallet, James</creatorcontrib><creatorcontrib>Jiggins, Chris D.</creatorcontrib><title>Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing</title><title>Philosophical transactions of the Royal Society of London. Series B. Biological sciences</title><addtitle>Phil. Trans. R. Soc. B</addtitle><addtitle>Phil. Trans. R. Soc. B</addtitle><description>Heliconius butterflies represent a recent radiation of species, in which wing pattern divergence has been implicated in speciation. Several loci that control wing pattern phenotypes have been mapped and two were identified through sequencing. These same gene regions play a role in adaptation across the whole Heliconius radiation. Previous studies of population genetic patterns at these regions have sequenced small amplicons. Here, we use targeted next-generation sequence capture to survey patterns of divergence across these entire regions in divergent geographical races and species of Heliconius. This technique was successful both within and between species for obtaining high coverage of almost all coding regions and sufficient coverage of non-coding regions to perform population genetic analyses. We find major peaks of elevated population differentiation between races across hybrid zones, which indicate regions under strong divergent selection. These ‘islands’ of divergence appear to be more extensive between closely related species, but there is less clear evidence for such islands between more distantly related species at two further points along the ‘speciation continuum’. We also sequence fosmid clones across these regions in different Heliconius melpomene races. We find no major structural rearrangements but many relatively large (greater than 1 kb) insertion/deletion events (including gain/loss of transposable elements) that are variable between races.</description><subject>Adaptation, Biological - genetics</subject><subject>Animals</subject><subject>Base Sequence</subject><subject>Butterflies</subject><subject>Butterflies - classification</subject><subject>Butterflies - genetics</subject><subject>Butterflies - physiology</subject><subject>Chromosomes, Insect - genetics</subject><subject>Colour Pattern</subject><subject>Divergence</subject><subject>Evolutionary genetics</subject><subject>Gene flow</subject><subject>Genes, Insect</subject><subject>Genetic Loci</subject><subject>Genetic Speciation</subject><subject>Genetic Variation</subject><subject>Genetics, Population</subject><subject>Genome, Insect</subject><subject>Genomes</subject><subject>Genomic Islands</subject><subject>Genomics</subject><subject>Heliconius</subject><subject>Heliconius melpomene</subject><subject>Hybridity</subject><subject>Molecular Mimicry</subject><subject>Molecular Sequence Data</subject><subject>Nucleotides</subject><subject>Phylogeny</subject><subject>Sequence Analysis, DNA - methods</subject><subject>Sequencing</subject><subject>Speciation</subject><subject>Species Specificity</subject><subject>Target Enrichment</subject><subject>Wings, Animal - physiology</subject><issn>0962-8436</issn><issn>1471-2970</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><recordid>eNqFkc1v1DAUxCMEokvhyg3kG6cs_kpsX5DQqrSgSgipIMTFcuyXrZds3NpORfjrcbRlBQfEybHfzE-TN1X1nOA1wUq-jil3a4oJWWOi5INqRbggNVUCP6xWWLW0lpy1J9WTlHYYY9UI_rg6oXSxtHxV3Z7DGPbeIp8GM7qEQo-cv4O4hdEC8iO6nrvonf_pxy26gMHbMPopoW7KGWI_eEjIOxiz7z041M1oMMVcJ2sGQHn5zuU9we1UiAXytHrUmyHBs_vztPr87uxqc1Fffjx_v3l7WduGNrkG0ZWAQK3jwjjGpOFOEtGxVnHrGqwAu55J5gzn1CrFeQ9CgHSY2c4wxU6rNwfuzdTtwdkSMZpB30S_N3HWwXj992T013ob7jSjjAlCCuDVPSCGEj5lvffJwlD2BGFKWtFWyrLS9v9KQhWRDV6U64PSxpBShP6Yh2C9FKqXQvXSjl4KLYaXf_7FUf67wSJgB0EMc1lnsB7yrHdhimO5_hv74uDapRzikcoJZ6yhS876MPcpw4_j3MTvuhVMNPqL5Hrz6etV-4F_04r9AqREyhU</recordid><startdate>20120205</startdate><enddate>20120205</enddate><creator>Nadeau, Nicola J.</creator><creator>Whibley, Annabel</creator><creator>Jones, Robert T.</creator><creator>Davey, John W.</creator><creator>Dasmahapatra, Kanchon K.</creator><creator>Baxter, Simon W.</creator><creator>Quail, Michael A.</creator><creator>Joron, Mathieu</creator><creator>ffrench-Constant, Richard H.</creator><creator>Blaxter, Mark L.</creator><creator>Mallet, James</creator><creator>Jiggins, Chris D.</creator><general>The Royal Society</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7SS</scope><scope>5PM</scope></search><sort><creationdate>20120205</creationdate><title>Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing</title><author>Nadeau, Nicola J. ; Whibley, Annabel ; Jones, Robert T. ; Davey, John W. ; Dasmahapatra, Kanchon K. ; Baxter, Simon W. ; Quail, Michael A. ; Joron, Mathieu ; ffrench-Constant, Richard H. ; Blaxter, Mark L. ; Mallet, James ; Jiggins, Chris D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c525t-e7b164e2cd47ad338a4d817b3694cd509e0df383da442c9944fe77e8d03cba393</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Adaptation, Biological - genetics</topic><topic>Animals</topic><topic>Base Sequence</topic><topic>Butterflies</topic><topic>Butterflies - classification</topic><topic>Butterflies - genetics</topic><topic>Butterflies - physiology</topic><topic>Chromosomes, Insect - genetics</topic><topic>Colour Pattern</topic><topic>Divergence</topic><topic>Evolutionary genetics</topic><topic>Gene flow</topic><topic>Genes, Insect</topic><topic>Genetic Loci</topic><topic>Genetic Speciation</topic><topic>Genetic Variation</topic><topic>Genetics, Population</topic><topic>Genome, Insect</topic><topic>Genomes</topic><topic>Genomic Islands</topic><topic>Genomics</topic><topic>Heliconius</topic><topic>Heliconius melpomene</topic><topic>Hybridity</topic><topic>Molecular Mimicry</topic><topic>Molecular Sequence Data</topic><topic>Nucleotides</topic><topic>Phylogeny</topic><topic>Sequence Analysis, DNA - methods</topic><topic>Sequencing</topic><topic>Speciation</topic><topic>Species Specificity</topic><topic>Target Enrichment</topic><topic>Wings, Animal - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nadeau, Nicola J.</creatorcontrib><creatorcontrib>Whibley, Annabel</creatorcontrib><creatorcontrib>Jones, Robert T.</creatorcontrib><creatorcontrib>Davey, John W.</creatorcontrib><creatorcontrib>Dasmahapatra, Kanchon K.</creatorcontrib><creatorcontrib>Baxter, Simon W.</creatorcontrib><creatorcontrib>Quail, Michael A.</creatorcontrib><creatorcontrib>Joron, Mathieu</creatorcontrib><creatorcontrib>ffrench-Constant, Richard H.</creatorcontrib><creatorcontrib>Blaxter, Mark L.</creatorcontrib><creatorcontrib>Mallet, James</creatorcontrib><creatorcontrib>Jiggins, Chris D.</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Entomology Abstracts (Full archive)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Philosophical transactions of the Royal Society of London. Series B. Biological sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nadeau, Nicola J.</au><au>Whibley, Annabel</au><au>Jones, Robert T.</au><au>Davey, John W.</au><au>Dasmahapatra, Kanchon K.</au><au>Baxter, Simon W.</au><au>Quail, Michael A.</au><au>Joron, Mathieu</au><au>ffrench-Constant, Richard H.</au><au>Blaxter, Mark L.</au><au>Mallet, James</au><au>Jiggins, Chris D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing</atitle><jtitle>Philosophical transactions of the Royal Society of London. Series B. Biological sciences</jtitle><stitle>Phil. Trans. R. Soc. B</stitle><addtitle>Phil. Trans. R. Soc. B</addtitle><date>2012-02-05</date><risdate>2012</risdate><volume>367</volume><issue>1587</issue><spage>343</spage><epage>353</epage><pages>343-353</pages><issn>0962-8436</issn><eissn>1471-2970</eissn><abstract>Heliconius butterflies represent a recent radiation of species, in which wing pattern divergence has been implicated in speciation. Several loci that control wing pattern phenotypes have been mapped and two were identified through sequencing. These same gene regions play a role in adaptation across the whole Heliconius radiation. Previous studies of population genetic patterns at these regions have sequenced small amplicons. Here, we use targeted next-generation sequence capture to survey patterns of divergence across these entire regions in divergent geographical races and species of Heliconius. This technique was successful both within and between species for obtaining high coverage of almost all coding regions and sufficient coverage of non-coding regions to perform population genetic analyses. We find major peaks of elevated population differentiation between races across hybrid zones, which indicate regions under strong divergent selection. These ‘islands’ of divergence appear to be more extensive between closely related species, but there is less clear evidence for such islands between more distantly related species at two further points along the ‘speciation continuum’. We also sequence fosmid clones across these regions in different Heliconius melpomene races. We find no major structural rearrangements but many relatively large (greater than 1 kb) insertion/deletion events (including gain/loss of transposable elements) that are variable between races.</abstract><cop>England</cop><pub>The Royal Society</pub><pmid>22201164</pmid><doi>10.1098/rstb.2011.0198</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation, Biological - genetics Animals Base Sequence Butterflies Butterflies - classification Butterflies - genetics Butterflies - physiology Chromosomes, Insect - genetics Colour Pattern Divergence Evolutionary genetics Gene flow Genes, Insect Genetic Loci Genetic Speciation Genetic Variation Genetics, Population Genome, Insect Genomes Genomic Islands Genomics Heliconius Heliconius melpomene Hybridity Molecular Mimicry Molecular Sequence Data Nucleotides Phylogeny Sequence Analysis, DNA - methods Sequencing Speciation Species Specificity Target Enrichment Wings, Animal - physiology |
title | Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing |
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