Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies
Identifieur interne : 001100 ( Pmc/Checkpoint ); précédent : 001099; suivant : 001101Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies
Auteurs : B. Huber [France] ; A. Whibley [France] ; Y L Poul [France] ; N. Navarro [France] ; A. Martin [États-Unis] ; S. Baxter [Australie, Royaume-Uni] ; A. Shah [France, Allemagne] ; B. Gilles [France] ; T. Wirth [France] ; W O Mcmillan ; M. Joron [France]Source :
- Heredity [ 0018-067X ] ; 2015.
Abstract
Understanding the genetic architecture of adaptive traits has been at the centre of modern evolutionary biology since Fisher; however, evaluating how the genetic architecture of ecologically important traits influences their diversification has been hampered by the scarcity of empirical data. Now, high-throughput genomics facilitates the detailed exploration of variation in the genome-to-phenotype map among closely related taxa. Here, we investigate the evolution of wing pattern diversity in
Url:
DOI: 10.1038/hdy.2015.22
PubMed: 25806542
PubMed Central: 4815517
Affiliations:
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PMC:4815517Le document en format XML
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</nlm:aff>
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<author><name sortKey="Baxter, S" sort="Baxter, S" uniqKey="Baxter S" first="S" last="Baxter">S. Baxter</name>
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</nlm:aff>
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</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
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, Paris,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
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</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff9"><institution>Department of Animal Behaviour, Universität Bielefeld</institution>
, Bielefeld,<country>Germany</country>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
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<author><name sortKey="Gilles, B" sort="Gilles, B" uniqKey="Gilles B" first="B" last="Gilles">B. Gilles</name>
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, Paris,<country>France</country>
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<country xml:lang="fr">France</country>
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</nlm:aff>
<country xml:lang="fr">France</country>
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, Paris,<country>France</country>
</nlm:aff>
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<front><div type="abstract" xml:lang="en"><p>Understanding the genetic architecture of adaptive traits has been at the centre of modern evolutionary biology since Fisher; however, evaluating how the genetic architecture of ecologically important traits influences their diversification has been hampered by the scarcity of empirical data. Now, high-throughput genomics facilitates the detailed exploration of variation in the genome-to-phenotype map among closely related taxa. Here, we investigate the evolution of wing pattern diversity in <italic>Heliconius</italic>
, a clade of neotropical butterflies that have undergone an adaptive radiation for wing-pattern mimicry and are influenced by distinct selection regimes. Using crosses between natural wing-pattern variants, we used genome-wide restriction site-associated DNA (RAD) genotyping, traditional linkage mapping and multivariate image analysis to study the evolution of the architecture of adaptive variation in two closely related species: <italic>Heliconius hecale</italic>
and <italic>H. ismenius</italic>
. We implemented a new morphometric procedure for the analysis of whole-wing pattern variation, which allows visualising spatial heatmaps of genotype-to-phenotype association for each quantitative trait locus separately. We used the <italic>H. melpomene</italic>
reference genome to fine-map variation for each major wing-patterning region uncovered, evaluated the role of candidate genes and compared genetic architectures across the genus. Our results show that, although the loci responding to mimicry selection are highly conserved between species, their effect size and phenotypic action vary throughout the clade. Multilocus architecture is ancestral and maintained across species under directional selection, whereas the single-locus (supergene) inheritance controlling polymorphism in <italic>H. numata</italic>
appears to have evolved only once. Nevertheless, the conservatism in the wing-patterning toolkit found throughout the genus does not appear to constrain phenotypic evolution towards local adaptive optima.</p>
</div>
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<journal-title-group><journal-title>Heredity</journal-title>
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<title-group><article-title>Conservatism and novelty in the genetic architecture of adaptation in <italic>Heliconius</italic>
butterflies</article-title>
<alt-title alt-title-type="running">Genome-to-phenotype map for butterfly mimicry</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Huber</surname>
<given-names>B</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
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<given-names>A</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
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<contrib contrib-type="author"><name><surname>Poul</surname>
<given-names>Y L</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Navarro</surname>
<given-names>N</given-names>
</name>
<xref ref-type="aff" rid="aff4">4</xref>
<xref ref-type="aff" rid="aff5">5</xref>
<contrib-id contrib-id-type="orcid">http://orcid.org/0000-0001-5694-4201</contrib-id>
</contrib>
<contrib contrib-type="author"><name><surname>Martin</surname>
<given-names>A</given-names>
</name>
<xref ref-type="aff" rid="aff6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Baxter</surname>
<given-names>S</given-names>
</name>
<xref ref-type="aff" rid="aff7">7</xref>
<xref ref-type="aff" rid="aff8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shah</surname>
<given-names>A</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff9">9</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gilles</surname>
<given-names>B</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wirth</surname>
<given-names>T</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>McMillan</surname>
<given-names>W O</given-names>
</name>
<xref ref-type="aff" rid="aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Joron</surname>
<given-names>M</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff3">3</xref>
</contrib>
<aff id="aff1"><label>1</label>
<institution>Institut de Systématique, Evolution, et Biodiversité, UMR 7205 CNRS, Muséum National d'Histoire Naturelle</institution>
, Paris,<country>France</country>
</aff>
<aff id="aff2"><label>2</label>
<institution>Laboratoire Biologie Intégrative des Populations, Ecole Pratique des Hautes Etudes (EPHE)</institution>
, Paris,<country>France</country>
</aff>
<aff id="aff3"><label>3</label>
<institution>The Smithsonian Tropical Research Institute</institution>
, Balboa,<country>República de Panamá</country>
</aff>
<aff id="aff4"><label>4</label>
<institution>Laboratoire PALEVO, Ecole Pratique des Hautes Etudes</institution>
, Dijon,<country>France</country>
</aff>
<aff id="aff5"><label>5</label>
<institution>UMR uB/CNRS 6282-Biogéosciences, Université de Bourgogne</institution>
, Dijon,<country>France</country>
</aff>
<aff id="aff6"><label>6</label>
<institution>Department of Molecular and Cell Biology, University of California</institution>
, Berkeley, CA,<country>USA</country>
</aff>
<aff id="aff7"><label>7</label>
<institution>School of Molecular and Biomedical Science, The University of Adelaide</institution>
, Adelaide,<country>Australia</country>
</aff>
<aff id="aff8"><label>8</label>
<institution>Department of Zoology, University of Cambridge</institution>
, Cambridge,<country>UK</country>
</aff>
<aff id="aff9"><label>9</label>
<institution>Department of Animal Behaviour, Universität Bielefeld</institution>
, Bielefeld,<country>Germany</country>
</aff>
</contrib-group>
<author-notes><corresp id="caf1"><label>*</label>
<institution>Institut de Systématique, Evolution, et Biodiversité, Muséum National d'Histoire Naturelle, UMR 7205 CNRS EPHE MNHN UPMC</institution>
, 45 rue Buffon, CP50, Paris 75005, <country>France</country>
. E-mail: <email>babahuber@gmail.com</email>
or <email>mathieu.joron@cefe.cnrs.fr</email>
</corresp>
</author-notes>
<pub-date pub-type="ppub"><month>05</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="epub"><day>25</day>
<month>03</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>1</day>
<month>5</month>
<year>2015</year>
</pub-date>
<volume>114</volume>
<issue>5</issue>
<fpage>515</fpage>
<lpage>524</lpage>
<history><date date-type="received"><day>01</day>
<month>06</month>
<year>2014</year>
</date>
<date date-type="rev-recd"><day>01</day>
<month>02</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>04</day>
<month>02</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2015 The Genetics Society</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>The Genetics Society</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-sa/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-sa/4.0/">http://creativecommons.org/licenses/by-nc-sa/4.0/</ext-link>
</license-p>
</license>
</permissions>
<abstract><p>Understanding the genetic architecture of adaptive traits has been at the centre of modern evolutionary biology since Fisher; however, evaluating how the genetic architecture of ecologically important traits influences their diversification has been hampered by the scarcity of empirical data. Now, high-throughput genomics facilitates the detailed exploration of variation in the genome-to-phenotype map among closely related taxa. Here, we investigate the evolution of wing pattern diversity in <italic>Heliconius</italic>
, a clade of neotropical butterflies that have undergone an adaptive radiation for wing-pattern mimicry and are influenced by distinct selection regimes. Using crosses between natural wing-pattern variants, we used genome-wide restriction site-associated DNA (RAD) genotyping, traditional linkage mapping and multivariate image analysis to study the evolution of the architecture of adaptive variation in two closely related species: <italic>Heliconius hecale</italic>
and <italic>H. ismenius</italic>
. We implemented a new morphometric procedure for the analysis of whole-wing pattern variation, which allows visualising spatial heatmaps of genotype-to-phenotype association for each quantitative trait locus separately. We used the <italic>H. melpomene</italic>
reference genome to fine-map variation for each major wing-patterning region uncovered, evaluated the role of candidate genes and compared genetic architectures across the genus. Our results show that, although the loci responding to mimicry selection are highly conserved between species, their effect size and phenotypic action vary throughout the clade. Multilocus architecture is ancestral and maintained across species under directional selection, whereas the single-locus (supergene) inheritance controlling polymorphism in <italic>H. numata</italic>
appears to have evolved only once. Nevertheless, the conservatism in the wing-patterning toolkit found throughout the genus does not appear to constrain phenotypic evolution towards local adaptive optima.</p>
</abstract>
</article-meta>
</front>
<floats-group><fig id="fig1"><label>Figure 1</label>
<caption><p>Summary of crosses performed in <italic>H. hecale</italic>
and <italic>H. ismenius</italic>
. Geographic distribution of the subspecies used for the crosses are indicated by filling patterns, and sampling localities by circles and squares. The distribution of other <italic>H. hecale</italic>
races found in Northern South America is also shown: <italic>H. h. annetta</italic>
(I), <italic>H. h. rosalesi</italic>
(II), <italic>H. h. anderida</italic>
(III) and <italic>H. h. barcanti</italic>
(IV).</p>
</caption>
<graphic xlink:href="hdy201522f1"></graphic>
</fig>
<fig id="fig2"><label>Figure 2</label>
<caption><p>Fine mapping of wing-patterning loci in <italic>H. hecale</italic>
and <italic>H. ismenius</italic>
. Grey-shaded boxes show recombinant individuals found in a total of N offspring in <italic>H. hecale melicerta</italic>
× <italic>H. h. clearei</italic>
(<italic>mel/cle</italic>
), <italic>H. hecale melicerta</italic>
× <italic>H. h. zuleika</italic>
(<italic>mel/zul</italic>
) and <italic>H. ismenius boulleti</italic>
× <italic>H. i. telchinia</italic>
(<italic>bou/tel</italic>
) crosses. Annotated genes on each scaffold and candidate colour genes are represented by grey and black block arrows, respectively. Scaffolds on LG1 (top panel) are ordered according to the <italic>H. melpomene</italic>
reference genome, but the order is unknown for the three scaffolds indicated on the right (HE670375, HE671246 and HE668177).</p>
</caption>
<graphic xlink:href="hdy201522f2"></graphic>
</fig>
<fig id="fig3"><label>Figure 3</label>
<caption><p>Phenotypic effect of Mendelian wing-patterning loci and major QTLs identified in <italic>H. hecale</italic>
and <italic>H. ismenius</italic>
crosses. For each type of cross (<bold>a</bold>
–<bold>c</bold>
), panel I (left) shows the crosses performed, the phenotypes associated with inferred genotypes at the major Mendelian loci (colour <italic>HhK</italic>
; forewing melanisation <italic>HhAc</italic>
/<italic>HiAc</italic>
; forewing distal band layer/spot <italic>HhN</italic>
/<italic>HiN</italic>
; hindwing band <italic>HhBr</italic>
/<italic>HiBr</italic>
) and variation of the quantitative traits (dashed boxes: Hindwing spots Hspot, continuous melanisation Cm). Parental races (top left) are represented by their dorsal views, the F1 male siring the mapping families (top right) by its dorsal and ventral views and typical backcross specimens (bottom) have arrows pointing to the variable character. The name of the mapping families is written on the bottom of the panels of each cross type, with total number of offspring shown in brackets. Families labelled in bold were used to build the RAD libraries. Panel II (right) shows the genomic position and phenotypic effect of major QTLs. Coloured wing diagrams show the spatial distribution of individual QTL effects on pattern variation extracted from multivariate wing pattern analysis. Phenotypic variation is broken down into heatmaps for each of the three main colours (black, orange and yellow), representing, for every wing position, the strength of association between colour presence and allelic transition at the QTL (from blue to red). For analytical simplicity, both white and yellow elements in the <italic>H. hecale melicerta</italic>
× <italic>H. h. clearei</italic>
cross were considered as yellow elements. Genomic plots show genome-wide association (LOD) between wing pattern variation and markers along the 20 autosomes, with 5% (solid line) and 10% (dashed line) association thresholds. Panel aIII shows the detection of <italic>WntA</italic>
transcripts by <italic>in situ</italic>
hybridisation on wing imaginal discs of the last larval instar of <italic>H. h. melicerta</italic>
and <italic>H. h. zuleika</italic>
. <italic>WntA</italic>
expression shows marked differences along the discal crossvein (arrows), in the M3-Cu2 intervein region (brackets) and in the Cu2-Cu1 intervein region (arrowheads). Colour dots indicate vein intersection landmarks. Phenotypic variation controlled by the <italic>HhAc</italic>
locus is represented on the right.</p>
</caption>
<graphic xlink:href="hdy201522f3"></graphic>
</fig>
<fig id="fig4"><label>Figure 4</label>
<caption><p>Conservatism and novelty in the genetic architecture underlying the diversity of <italic>Heliconius</italic>
wing patterns. (<bold>a</bold>
) Known genetic architectures underlying pattern diversity throughout the clade mapped onto an unscaled phylogeny. Orange tree branches represent nine of the ten species in the silvaniform clade. Major colour variation loci are located on four chromosomes (top) and control variation in similar wing regions (arrows) throughout the genus. Wing phenotypes are represented based on <xref ref-type="bibr" rid="bib18">Holzinger and Holzinger (1994)</xref>
. Note that the effect of the <italic>Br</italic>
locus in <italic>H. cydno</italic>
is shown on the ventral side. Loci with names in brackets were described based exclusively on interspecific crosses. (<bold>b</bold>
) Comparative diagram of the distribution of the gene effects across the wing for toolkit loci in the silvaniform clade (excepting <italic>H. numata;</italic>
left) and in the <italic>H. melpomene</italic>
and <italic>H. erato</italic>
clades (right), showing the general conservatism of the regions affected by homologous elements of the multilocus architecture despite some flexibility.</p>
</caption>
<graphic xlink:href="hdy201522f4"></graphic>
</fig>
</floats-group>
</pmc>
<affiliations><list><country><li>Allemagne</li>
<li>Australie</li>
<li>France</li>
<li>Royaume-Uni</li>
<li>États-Unis</li>
</country>
</list>
<tree><noCountry><name sortKey="Mcmillan, W O" sort="Mcmillan, W O" uniqKey="Mcmillan W" first="W O" last="Mcmillan">W O Mcmillan</name>
</noCountry>
<country name="France"><noRegion><name sortKey="Huber, B" sort="Huber, B" uniqKey="Huber B" first="B" last="Huber">B. Huber</name>
</noRegion>
<name sortKey="Gilles, B" sort="Gilles, B" uniqKey="Gilles B" first="B" last="Gilles">B. Gilles</name>
<name sortKey="Huber, B" sort="Huber, B" uniqKey="Huber B" first="B" last="Huber">B. Huber</name>
<name sortKey="Joron, M" sort="Joron, M" uniqKey="Joron M" first="M" last="Joron">M. Joron</name>
<name sortKey="Navarro, N" sort="Navarro, N" uniqKey="Navarro N" first="N" last="Navarro">N. Navarro</name>
<name sortKey="Navarro, N" sort="Navarro, N" uniqKey="Navarro N" first="N" last="Navarro">N. Navarro</name>
<name sortKey="Poul, Y L" sort="Poul, Y L" uniqKey="Poul Y" first="Y L" last="Poul">Y L Poul</name>
<name sortKey="Shah, A" sort="Shah, A" uniqKey="Shah A" first="A" last="Shah">A. Shah</name>
<name sortKey="Whibley, A" sort="Whibley, A" uniqKey="Whibley A" first="A" last="Whibley">A. Whibley</name>
<name sortKey="Wirth, T" sort="Wirth, T" uniqKey="Wirth T" first="T" last="Wirth">T. Wirth</name>
<name sortKey="Wirth, T" sort="Wirth, T" uniqKey="Wirth T" first="T" last="Wirth">T. Wirth</name>
</country>
<country name="États-Unis"><noRegion><name sortKey="Martin, A" sort="Martin, A" uniqKey="Martin A" first="A" last="Martin">A. Martin</name>
</noRegion>
</country>
<country name="Australie"><noRegion><name sortKey="Baxter, S" sort="Baxter, S" uniqKey="Baxter S" first="S" last="Baxter">S. Baxter</name>
</noRegion>
</country>
<country name="Royaume-Uni"><noRegion><name sortKey="Baxter, S" sort="Baxter, S" uniqKey="Baxter S" first="S" last="Baxter">S. Baxter</name>
</noRegion>
</country>
<country name="Allemagne"><noRegion><name sortKey="Shah, A" sort="Shah, A" uniqKey="Shah A" first="A" last="Shah">A. Shah</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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