Loading…

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...

Full description

Saved in:
Bibliographic Details
Published in:Philosophical transactions of the Royal Society of London. Series B. Biological sciences 2012-02, Vol.367 (1587), p.343-353
Main Authors: 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.
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c525t-e7b164e2cd47ad338a4d817b3694cd509e0df383da442c9944fe77e8d03cba393
cites cdi_FETCH-LOGICAL-c525t-e7b164e2cd47ad338a4d817b3694cd509e0df383da442c9944fe77e8d03cba393
container_end_page 353
container_issue 1587
container_start_page 343
container_title Philosophical transactions of the Royal Society of London. Series B. Biological sciences
container_volume 367
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
format article
fullrecord <record><control><sourceid>jstor_royal</sourceid><recordid>TN_cdi_royalsociety_journals_10_1098_rstb_2011_0198</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>41433526</jstor_id><sourcerecordid>41433526</sourcerecordid><originalsourceid>FETCH-LOGICAL-c525t-e7b164e2cd47ad338a4d817b3694cd509e0df383da442c9944fe77e8d03cba393</originalsourceid><addsrcrecordid>eNqFkc1v1DAUxCMEokvhyg3kG6cs_kpsX5DQqrSgSgipIMTFcuyXrZds3NpORfjrcbRlBQfEybHfzE-TN1X1nOA1wUq-jil3a4oJWWOi5INqRbggNVUCP6xWWLW0lpy1J9WTlHYYY9UI_rg6oXSxtHxV3Z7DGPbeIp8GM7qEQo-cv4O4hdEC8iO6nrvonf_pxy26gMHbMPopoW7KGWI_eEjIOxiz7z041M1oMMVcJ2sGQHn5zuU9we1UiAXytHrUmyHBs_vztPr87uxqc1Fffjx_v3l7WduGNrkG0ZWAQK3jwjjGpOFOEtGxVnHrGqwAu55J5gzn1CrFeQ9CgHSY2c4wxU6rNwfuzdTtwdkSMZpB30S_N3HWwXj992T013ob7jSjjAlCCuDVPSCGEj5lvffJwlD2BGFKWtFWyrLS9v9KQhWRDV6U64PSxpBShP6Yh2C9FKqXQvXSjl4KLYaXf_7FUf67wSJgB0EMc1lnsB7yrHdhimO5_hv74uDapRzikcoJZ6yhS876MPcpw4_j3MTvuhVMNPqL5Hrz6etV-4F_04r9AqREyhU</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>912918506</pqid></control><display><type>article</type><title>Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing</title><source>Open Access: PubMed Central</source><source>JSTOR Archival Journals and Primary Sources Collection</source><source>Royal Society Publishing Jisc Collections Royal Society Journals Read &amp; Publish Transitional Agreement 2025 (reading list)</source><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.</creator><creatorcontrib>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.</creatorcontrib><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><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>
fulltext fulltext
identifier ISSN: 0962-8436
ispartof Philosophical transactions of the Royal Society of London. Series B. Biological sciences, 2012-02, Vol.367 (1587), p.343-353
issn 0962-8436
1471-2970
language eng
recordid cdi_royalsociety_journals_10_1098_rstb_2011_0198
source Open Access: PubMed Central; JSTOR Archival Journals and Primary Sources Collection; Royal Society Publishing Jisc Collections Royal Society Journals Read & Publish Transitional Agreement 2025 (reading list)
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
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-27T11%3A25%3A04IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_royal&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Genomic%20islands%20of%20divergence%20in%20hybridizing%20Heliconius%20butterflies%20identified%20by%20large-scale%20targeted%20sequencing&rft.jtitle=Philosophical%20transactions%20of%20the%20Royal%20Society%20of%20London.%20Series%20B.%20Biological%20sciences&rft.au=Nadeau,%20Nicola%20J.&rft.date=2012-02-05&rft.volume=367&rft.issue=1587&rft.spage=343&rft.epage=353&rft.pages=343-353&rft.issn=0962-8436&rft.eissn=1471-2970&rft_id=info:doi/10.1098/rstb.2011.0198&rft_dat=%3Cjstor_royal%3E41433526%3C/jstor_royal%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c525t-e7b164e2cd47ad338a4d817b3694cd509e0df383da442c9944fe77e8d03cba393%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=912918506&rft_id=info:pmid/22201164&rft_jstor_id=41433526&rfr_iscdi=true