A major gene controls mimicry and crypsis in butterflies and moths
Identifieur interne : 002C24 ( Pmc/Curation ); précédent : 002C23; suivant : 002C25A major gene controls mimicry and crypsis in butterflies and moths
Auteurs : Nicola J. Nadeau [Royaume-Uni, Panama] ; Carolina Pardo-Diaz [Colombie] ; Annabel Whibley [France] ; Megan Supple [Panama, Australie] ; Suzanne V. Saenko [France] ; Richard W. R. Wallbank [Panama, Royaume-Uni] ; Grace C. Wu [États-Unis] ; Luana Maroja [États-Unis] ; Laura Ferguson [Royaume-Uni] ; Joseph J. Hanly [Panama, Royaume-Uni] ; Heather Hines [États-Unis] ; Camilo Salazar [Colombie] ; Richard Merrill [Panama, Royaume-Uni] ; Andrea Dowling [Royaume-Uni] ; Richard Ffrench-Constant [Royaume-Uni] ; Violaine Llaurens [France] ; Mathieu Joron [France] ; W. Owen Mcmillan [Panama] ; Chris D. Jiggins [Royaume-Uni, Panama]Source :
- Nature [ 0028-0836 ] ; 2016.
Abstract
The wing patterns of butterflies and moths (Lepidoptera) are diverse and striking examples of evolutionary diversification by natural selection
Url:
DOI: 10.1038/nature17961
PubMed: 27251285
PubMed Central: 5094491
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Annabel Whibley<affiliation><nlm:aff id="A5">Cell and Developmental Biology, John Innes Centre, Norwich, UK, NR4 7UH</nlm:aff>
<wicri:noCountry code="subfield">NR4 7UH</wicri:noCountry>
</affiliation>
Le document en format XML
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<affiliation wicri:level="1"><nlm:aff id="A4">Institut de Systématique, Evolution et Biodiversité (UMR 7205 CNRS, MNHN, UPMC, EPHE, Sorbonne Université), Museum National d’Histoire Naturelle, CP50, 57 rue Cuvier, 75005 PARIS, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut de Systématique, Evolution et Biodiversité (UMR 7205 CNRS, MNHN, UPMC, EPHE, Sorbonne Université), Museum National d’Histoire Naturelle, CP50, 57 rue Cuvier, 75005 PARIS</wicri:regionArea>
</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="A2">Smithsonian Tropical Research Institute, Panama</nlm:aff>
<country xml:lang="fr">Panama</country>
<wicri:regionArea>Smithsonian Tropical Research Institute</wicri:regionArea>
</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="1"><nlm:aff id="A7">Department of Zoology, University of Cambridge, UK</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Department of Zoology, University of Cambridge</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="A2">Smithsonian Tropical Research Institute, Panama</nlm:aff>
<country xml:lang="fr">Panama</country>
<wicri:regionArea>Smithsonian Tropical Research Institute</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">Nature</title>
<idno type="ISSN">0028-0836</idno>
<idno type="eISSN">1476-4687</idno>
<imprint><date when="2016">2016</date>
</imprint>
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<front><div type="abstract" xml:lang="en"><p id="P1">The wing patterns of butterflies and moths (Lepidoptera) are diverse and striking examples of evolutionary diversification by natural selection<xref rid="R1" ref-type="bibr">1</xref>
,<xref rid="R2" ref-type="bibr">2</xref>
. Lepidopteran wing colour patterns are a key innovation, consisting of arrays of coloured scales. We still lack a general understanding of how these patterns are controlled and if there is any commonality across the 160,000 moth and 17,000 butterfly species. Here, we identify a gene, <italic>cortex,</italic>
through fine-scale mapping using population genomics and gene expression analyses, which regulates pattern switches in multiple species across the mimetic radiation in <italic>Heliconius</italic>
butterflies. <italic>cortex</italic>
belongs to a fast evolving subfamily of the otherwise highly conserved fizzy family of cell cycle regulators<xref rid="R3" ref-type="bibr">3</xref>
, suggesting that it most likely regulates pigmentation patterning through regulation of scale cell development. In parallel with findings in the peppered moth (<italic>Biston betularia</italic>
)<xref rid="R4" ref-type="bibr">4</xref>
, our results suggest that this mechanism is common within Lepidoptera and that <italic>cortex</italic>
has become a major target for natural selection acting on colour and pattern variation in this group of insects.</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<pmc-dir>properties manuscript</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-journal-id">0410462</journal-id>
<journal-id journal-id-type="pubmed-jr-id">6011</journal-id>
<journal-id journal-id-type="nlm-ta">Nature</journal-id>
<journal-id journal-id-type="iso-abbrev">Nature</journal-id>
<journal-title-group><journal-title>Nature</journal-title>
</journal-title-group>
<issn pub-type="ppub">0028-0836</issn>
<issn pub-type="epub">1476-4687</issn>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27251285</article-id>
<article-id pub-id-type="pmc">5094491</article-id>
<article-id pub-id-type="doi">10.1038/nature17961</article-id>
<article-id pub-id-type="manuscript">EMS68288</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>A major gene controls mimicry and crypsis in butterflies and moths</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Nadeau</surname>
<given-names>Nicola J.</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pardo-Diaz</surname>
<given-names>Carolina</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Whibley</surname>
<given-names>Annabel</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
<xref ref-type="aff" rid="A5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Supple</surname>
<given-names>Megan</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="aff" rid="A6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Saenko</surname>
<given-names>Suzanne V.</given-names>
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<xref ref-type="aff" rid="A4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wallbank</surname>
<given-names>Richard W. R.</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="aff" rid="A7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wu</surname>
<given-names>Grace C.</given-names>
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<xref ref-type="aff" rid="A8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Maroja</surname>
<given-names>Luana</given-names>
</name>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ferguson</surname>
<given-names>Laura</given-names>
</name>
<xref ref-type="aff" rid="A10">10</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hanly</surname>
<given-names>Joseph J.</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="aff" rid="A7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hines</surname>
<given-names>Heather</given-names>
</name>
<xref ref-type="aff" rid="A11">11</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Salazar</surname>
<given-names>Camilo</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Merrill</surname>
<given-names>Richard</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="aff" rid="A7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dowling</surname>
<given-names>Andrea</given-names>
</name>
<xref ref-type="aff" rid="A12">12</xref>
</contrib>
<contrib contrib-type="author"><name><surname>ffrench-Constant</surname>
<given-names>Richard</given-names>
</name>
<xref ref-type="aff" rid="A12">12</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Llaurens</surname>
<given-names>Violaine</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Joron</surname>
<given-names>Mathieu</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>McMillan</surname>
<given-names>W. Owen</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jiggins</surname>
<given-names>Chris D.</given-names>
</name>
<xref ref-type="aff" rid="A7">7</xref>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
</contrib-group>
<aff id="A1"><label>1</label>
Department of Animal and Plant Sciences, University of Sheffield, UK</aff>
<aff id="A2"><label>2</label>
Smithsonian Tropical Research Institute, Panama</aff>
<aff id="A3"><label>3</label>
Biology Program, Faculty of Natural Sciences and Mathematics. Universidad del Rosario. Cra. 24 No 63C-69, Bogotá D.C., 111221, Colombia</aff>
<aff id="A4"><label>4</label>
Institut de Systématique, Evolution et Biodiversité (UMR 7205 CNRS, MNHN, UPMC, EPHE, Sorbonne Université), Museum National d’Histoire Naturelle, CP50, 57 rue Cuvier, 75005 PARIS, France</aff>
<aff id="A5"><label>5</label>
Cell and Developmental Biology, John Innes Centre, Norwich, UK, NR4 7UH</aff>
<aff id="A6"><label>6</label>
The Australian National University, ACT, Australia</aff>
<aff id="A7"><label>7</label>
Department of Zoology, University of Cambridge, UK</aff>
<aff id="A8"><label>8</label>
Energy and Resources Group, University of California at Berkeley, CA, USA</aff>
<aff id="A9"><label>9</label>
Department of Biology, Williams College, MA, USA</aff>
<aff id="A10"><label>10</label>
Department of Zoology, University of Oxford, UK</aff>
<aff id="A11"><label>11</label>
Penn State University, 517 Mueller, University Park, PA 16802</aff>
<aff id="A12"><label>12</label>
School of Biosciences, University of Exeter in Cornwall, Penryn, UK TR10 9EZ</aff>
<author-notes><corresp id="CR1">Correspondence and requests for materials should be addressed to <email>n.nadeau@sheffield.ac.uk</email>
or <email>c.jiggins@zoo.cam.ac.uk</email>
</corresp>
</author-notes>
<pub-date pub-type="nihms-submitted"><day>8</day>
<month>9</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub"><day>1</day>
<month>6</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><day>1</day>
<month>6</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>01</day>
<month>12</month>
<year>2016</year>
</pub-date>
<volume>534</volume>
<issue>7605</issue>
<fpage>106</fpage>
<lpage>110</lpage>
<pmc-comment>elocation-id from pubmed: 10.1038/nature17961</pmc-comment>
<permissions><license><license-p>Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:<ext-link ext-link-type="uri" xlink:href="http://www.nature.com/authors/editorial_policies/license.html#terms">http://www.nature.com/authors/editorial_policies/license.html#terms</ext-link>
</license-p>
</license>
</permissions>
<abstract><p id="P1">The wing patterns of butterflies and moths (Lepidoptera) are diverse and striking examples of evolutionary diversification by natural selection<xref rid="R1" ref-type="bibr">1</xref>
,<xref rid="R2" ref-type="bibr">2</xref>
. Lepidopteran wing colour patterns are a key innovation, consisting of arrays of coloured scales. We still lack a general understanding of how these patterns are controlled and if there is any commonality across the 160,000 moth and 17,000 butterfly species. Here, we identify a gene, <italic>cortex,</italic>
through fine-scale mapping using population genomics and gene expression analyses, which regulates pattern switches in multiple species across the mimetic radiation in <italic>Heliconius</italic>
butterflies. <italic>cortex</italic>
belongs to a fast evolving subfamily of the otherwise highly conserved fizzy family of cell cycle regulators<xref rid="R3" ref-type="bibr">3</xref>
, suggesting that it most likely regulates pigmentation patterning through regulation of scale cell development. In parallel with findings in the peppered moth (<italic>Biston betularia</italic>
)<xref rid="R4" ref-type="bibr">4</xref>
, our results suggest that this mechanism is common within Lepidoptera and that <italic>cortex</italic>
has become a major target for natural selection acting on colour and pattern variation in this group of insects.</p>
</abstract>
</article-meta>
</front>
<floats-group><fig id="F1" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>A homologous genomic region controls a diversity of phenotypes across the Lepidoptera. Left: phylogenetic relationships<xref rid="R29" ref-type="bibr">29</xref>
. Right: chromosome maps with colour pattern intervals in grey, coloured bars represent markers used to assign homology<xref rid="R5" ref-type="bibr">5</xref>
,<xref rid="R8" ref-type="bibr">8</xref>
–<xref rid="R10" ref-type="bibr">10</xref>
, the first and last genes from <xref ref-type="fig" rid="F2">Fig 2</xref>
shown in red. In <italic>He</italic>
the <italic>HeCr</italic>
locus controls the yellow hind-wing bar phenotype (grey boxed races). In <italic>Hm</italic>
it controls both the yellow hind-wing bar (<italic>HmYb,</italic>
pink box) and the yellow forewing band (<italic>HmN,</italic>
blue box). In <italic>Hn</italic>
it modulates black, yellow and orange elements on both wings (<italic>HnP</italic>
), producing phenotypes that mimic butterflies in the genus <italic>Melinaea</italic>
. Morphs/races of <italic>Heliconius</italic>
species included in this study are shown with names.</p>
</caption>
<graphic xlink:href="emss-68288-f001"></graphic>
</fig>
<fig id="F2" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>Association analyses across the genomic region known to contain major colour pattern loci in <italic>Heliconius.</italic>
A) Association in <italic>He</italic>
with the yellow hind-wing bar (n=45). Coloured SNPs are fixed for a unique state in <italic>He demophoon</italic>
(orange) or <italic>He favorinus</italic>
(purple). B) Genes in <italic>He</italic>
with direct homologs in <italic>Hm</italic>
. Genes are in different colours with exons (coding and UTRs) connected by a line. Grey bars are transposable elements. C) <italic>Hm</italic>
genes and transposable elements: colours correspond to homologous <italic>He</italic>
genes; MicroRNAs<xref rid="R30" ref-type="bibr">30</xref>
in black. D) Association in the <italic>Hm/timareta</italic>
/silvaniform group with the yellow hind-wing bar (red) and yellow forewing band (blue) (n=49). E) Association in <italic>Hn</italic>
with the <italic>bicoloratus</italic>
morph (n=26); inversion positions<xref rid="R13" ref-type="bibr">13</xref>
shown below. In all cases black/dark coloured points are above the strongest associations found outside the colour pattern scaffolds (<italic>He</italic>
p=1.63e-05; <italic>Hm</italic>
p=2.03e-05 and p=2.58e-05; <italic>Hn</italic>
p=6.81e-06).</p>
</caption>
<graphic xlink:href="emss-68288-f002"></graphic>
</fig>
<fig id="F3" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>Differential gene expression across the genomic region known to contain major colour pattern loci in <italic>Heliconius melpomene.</italic>
Expression differences in day 3 pupae, for all genes in the <italic>Yb</italic>
interval (A,D) and tiling probes spanning the central portion of the interval (B,C,E,F). Expression is compared between races for each wing region (A,B,C) and between proximal and distal forewing sections for each race (D,E,F). C and F: magnitude and direction of expression difference (log<sub>2</sub>
fold-change) for tiling probes showing significant differences (p≤0.05); probes in known <italic>cortex</italic>
exons shown in dark colours. Gene <italic>HM00052</italic>
was differentially expressed between other races in RNA sequence data (<xref ref-type="supplementary-material" rid="SD3">Supplementary Information</xref>
) but is not differentially expressed here.</p>
</caption>
<graphic xlink:href="emss-68288-f003"></graphic>
</fig>
<fig id="F4" orientation="portrait" position="float"><label>Figure 4</label>
<caption><p><italic>In situ</italic>
hybridisations of <italic>cortex</italic>
in hind-wings of final instar larvae. B) <italic>Hn tarapotensis</italic>
; adult wing shown in A, coloured points indicate landmarks, yellow arrows highlight adult pattern elements corresponding to the <italic>cortex</italic>
staining. D) <italic>Hm rosina</italic>
; adult wing shown in C, staining patterns in other <italic>Hm</italic>
races (<italic>meriana</italic>
and <italic>aglaope</italic>
) appeared similar. The probe used was complementary to the <italic>cortex</italic>
isoform with the longest open reading frame (also the most common, <xref ref-type="supplementary-material" rid="SD3">Supplementary Information</xref>
).</p>
</caption>
<graphic xlink:href="emss-68288-f004"></graphic>
</fig>
</floats-group>
</pmc>
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