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Preen secretions encode information on MHC similarity in certain sex-dyads in a monogamous seabird

Identifieur interne : 000131 ( Pmc/Curation ); précédent : 000130; suivant : 000132

Preen secretions encode information on MHC similarity in certain sex-dyads in a monogamous seabird

Auteurs : Sarah Leclaire [France] ; Wouter F. D. Van Dongen [Autriche] ; Steeve Voccia [France] ; Thomas Merkling [France] ; Christine Ducamp [France] ; Scott A. Hatch [États-Unis] ; Pierrick Blanchard [France] ; Étienne Danchin [France] ; Richard H. Wagner [Autriche]

Source :

RBID : PMC:4220275

Abstract

Animals are known to select mates to maximize the genetic diversity of their offspring in order to achieve immunity against a broader range of pathogens. Although several bird species preferentially mate with partners that are dissimilar at the major histocompatibility complex (MHC), it remains unknown whether they can use olfactory cues to assess MHC similarity with potential partners. Here we combined gas chromatography data with genetic similarity indices based on MHC to test whether similarity in preen secretion chemicals correlated with MHC relatedness in the black-legged kittiwake (Rissa tridactyla), a species that preferentially mates with genetically dissimilar partners. We found that similarity in preen secretion chemicals was positively correlated with MHC relatedness in male-male and male-female dyads. This study provides the first evidence that preen secretion chemicals can encode information on MHC relatedness and suggests that odor-based mechanisms of MHC-related mate choice may occur in birds.


Url:
DOI: 10.1038/srep06920
PubMed: 25370306
PubMed Central: 4220275

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PMC:4220275

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Wouter F. D. Van Dongen
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<institution>Applied Ecology Research Group and Institute for Sustainability and Innovation, College of Engineering and Science, Victoria University – Footscray Park Campus</institution>
, PO Box 14428, Melbourne MC, VIC,
<country>Australia 8001</country>
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<wicri:noCountry code="nlm country">Australia 8001</wicri:noCountry>
</affiliation>

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<p>Animals are known to select mates to maximize the genetic diversity of their offspring in order to achieve immunity against a broader range of pathogens. Although several bird species preferentially mate with partners that are dissimilar at the major histocompatibility complex (MHC), it remains unknown whether they can use olfactory cues to assess MHC similarity with potential partners. Here we combined gas chromatography data with genetic similarity indices based on MHC to test whether similarity in preen secretion chemicals correlated with MHC relatedness in the black-legged kittiwake (
<italic>Rissa tridactyla</italic>
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</TEI>
<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Sci Rep</journal-id>
<journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id>
<journal-title-group>
<journal-title>Scientific Reports</journal-title>
</journal-title-group>
<issn pub-type="epub">2045-2322</issn>
<publisher>
<publisher-name>Nature Publishing Group</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">25370306</article-id>
<article-id pub-id-type="pmc">4220275</article-id>
<article-id pub-id-type="pii">srep06920</article-id>
<article-id pub-id-type="doi">10.1038/srep06920</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Preen secretions encode information on MHC similarity in certain sex-dyads in a monogamous seabird</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Leclaire</surname>
<given-names>Sarah</given-names>
</name>
<xref ref-type="corresp" rid="c1">a</xref>
<xref ref-type="aff" rid="a1">1</xref>
<xref ref-type="aff" rid="a2">2</xref>
<xref ref-type="author-notes" rid="n1">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>van Dongen</surname>
<given-names>Wouter F. D.</given-names>
</name>
<xref ref-type="aff" rid="a3">3</xref>
<xref ref-type="aff" rid="a4">4</xref>
<xref ref-type="author-notes" rid="n1">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Voccia</surname>
<given-names>Steeve</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>Merkling</surname>
<given-names>Thomas</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>Ducamp</surname>
<given-names>Christine</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>Hatch</surname>
<given-names>Scott A.</given-names>
</name>
<xref ref-type="aff" rid="a5">5</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Blanchard</surname>
<given-names>Pierrick</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>Danchin</surname>
<given-names>Étienne</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>Wagner</surname>
<given-names>Richard H.</given-names>
</name>
<xref ref-type="aff" rid="a3">3</xref>
</contrib>
<aff id="a1">
<label>1</label>
<institution>CNRS, UPS, ENFA; Laboratoire Évolution et Diversité Biologique (EDB), UMR5174</institution>
, 118 route de Narbonne, 31062 Toulouse,
<country>France</country>
</aff>
<aff id="a2">
<label>2</label>
<institution>Université de Toulouse, EDB, UMR5174</institution>
, 31062 Toulouse,
<country>France</country>
</aff>
<aff id="a3">
<label>3</label>
<institution>Konrad Lorenz Institute of Ethology, Department of Integrative Biology and Evolution, University of Veterinary Medicine Vienna</institution>
, Savoyenstrasse 1a, 1160 Vienna, Austria</aff>
<aff id="a4">
<label>4</label>
<institution>Applied Ecology Research Group and Institute for Sustainability and Innovation, College of Engineering and Science, Victoria University – Footscray Park Campus</institution>
, PO Box 14428, Melbourne MC, VIC,
<country>Australia 8001</country>
</aff>
<aff id="a5">
<label>5</label>
<institution>U.S. Geological Survey, Alaska Science Center, 4210 University Drive</institution>
, Anchorage, Alaska 99508,
<country>USA</country>
</aff>
</contrib-group>
<author-notes>
<corresp id="c1">
<label>a</label>
<email>sarah.leclaire@free.fr</email>
</corresp>
<fn id="n1">
<label>*</label>
<p>These authors contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>05</day>
<month>11</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="collection">
<year>2014</year>
</pub-date>
<volume>4</volume>
<elocation-id>6920</elocation-id>
<history>
<date date-type="received">
<day>18</day>
<month>07</month>
<year>2014</year>
</date>
<date date-type="accepted">
<day>13</day>
<month>10</month>
<year>2014</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2014, Macmillan Publishers Limited. All rights reserved</copyright-statement>
<copyright-year>2014</copyright-year>
<copyright-holder>Macmillan Publishers Limited. All rights reserved</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/4.0/">
<pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 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 in order 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-nd/4.0/">http://creativecommons.org/licenses/by-nc-nd/4.0/</ext-link>
</license-p>
</license>
</permissions>
<abstract>
<p>Animals are known to select mates to maximize the genetic diversity of their offspring in order to achieve immunity against a broader range of pathogens. Although several bird species preferentially mate with partners that are dissimilar at the major histocompatibility complex (MHC), it remains unknown whether they can use olfactory cues to assess MHC similarity with potential partners. Here we combined gas chromatography data with genetic similarity indices based on MHC to test whether similarity in preen secretion chemicals correlated with MHC relatedness in the black-legged kittiwake (
<italic>Rissa tridactyla</italic>
), a species that preferentially mates with genetically dissimilar partners. We found that similarity in preen secretion chemicals was positively correlated with MHC relatedness in male-male and male-female dyads. This study provides the first evidence that preen secretion chemicals can encode information on MHC relatedness and suggests that odor-based mechanisms of MHC-related mate choice may occur in birds.</p>
</abstract>
</article-meta>
</front>
<floats-group>
<fig id="f1">
<label>Figure 1</label>
<caption>
<title>Amino acid alignment of MHC Class II DRB alleles isolated from black-legged kittiwakes.</title>
<p>Dots indicate matching amino acids relative to Ritr_MHC01 and shaded areas indicate conserved residues as outlined in
<xref ref-type="bibr" rid="b50">50</xref>
. Plus signs above alignment correspond to putative antigen binding sites as inferred from
<xref ref-type="bibr" rid="b46">46</xref>
. Additional species and their associated GenBank accession numbers included in the alignment are
<italic>Pachyptila belcheri</italic>
(FJ588549),
<italic>Halobaena caerulea</italic>
(JF276893),
<italic>Gallus gallus</italic>
(DQ008584) and
<italic>Homo sapiens</italic>
(AM493435).</p>
</caption>
<graphic xlink:href="srep06920-f1"></graphic>
</fig>
<fig id="f2">
<label>Figure 2</label>
<caption>
<title>Relationship between MHC amino-acid distances and chemical distances (as described by Euclidean distances) in (a) male-male dyads, (b) cross-sex dyads, and (c) female-female dyads. Solid lines are linear model predicted values and SE.</title>
</caption>
<graphic xlink:href="srep06920-f2"></graphic>
</fig>
<table-wrap position="float" id="t1">
<label>Table 1</label>
<caption>
<title>MHC Class II DRB alleles isolated in this study and their corresponding Genbank accession numbers. Alleles have more than one accession number in cases where they are identical to multiple previously published sequences within the 258 bp fragment used in this study. In these cases, the previously published sequences only differ from each other outside the exon 2 fragment characterised here</title>
</caption>
<table frame="hsides" rules="groups" border="1">
<colgroup>
<col align="left"></col>
<col align="center"></col>
<col align="center"></col>
</colgroup>
<thead valign="bottom">
<tr>
<th align="justify" valign="top" charoff="50">Allele ID</th>
<th align="justify" valign="top" charoff="50">Accession number</th>
<th align="justify" valign="top" charoff="50">Study</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC01</td>
<td align="justify" valign="top" charoff="50">EU326254</td>
<td align="justify" valign="top" charoff="50">Mulard
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">HQ822398</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">HQ822408</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">HQ822414</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC02</td>
<td align="justify" valign="top" charoff="50">HQ822399</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC03</td>
<td align="justify" valign="top" charoff="50">KJ210580</td>
<td align="justify" valign="top" charoff="50">This study</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC04</td>
<td align="justify" valign="top" charoff="50">KJ210581</td>
<td align="justify" valign="top" charoff="50">This study</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC05</td>
<td align="justify" valign="top" charoff="50">HQ822402</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC06</td>
<td align="justify" valign="top" charoff="50">EU326259</td>
<td align="justify" valign="top" charoff="50">Mulard
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">HQ822439</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC07</td>
<td align="justify" valign="top" charoff="50">KJ210582</td>
<td align="justify" valign="top" charoff="50">This study</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC09</td>
<td align="justify" valign="top" charoff="50">KJ210583</td>
<td align="justify" valign="top" charoff="50">This study</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC10</td>
<td align="justify" valign="top" charoff="50">HQ822419</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC11</td>
<td align="justify" valign="top" charoff="50">HQ822460</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">HQ822472</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC18</td>
<td align="justify" valign="top" charoff="50">HQ822413</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC23</td>
<td align="justify" valign="top" charoff="50">HQ822406</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">HQ822443</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC24</td>
<td align="justify" valign="top" charoff="50">HQ822442</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC25</td>
<td align="justify" valign="top" charoff="50">KJ210586</td>
<td align="justify" valign="top" charoff="50">This study</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC27</td>
<td align="justify" valign="top" charoff="50">HQ822446</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">HQ822459</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC28</td>
<td align="justify" valign="top" charoff="50">HQ822423</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC30</td>
<td align="justify" valign="top" charoff="50">KJ210587</td>
<td align="justify" valign="top" charoff="50">This study</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC31</td>
<td align="justify" valign="top" charoff="50">KJ210588</td>
<td align="justify" valign="top" charoff="50">This study</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC32</td>
<td align="justify" valign="top" charoff="50">KJ210589</td>
<td align="justify" valign="top" charoff="50">This study</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC33</td>
<td align="justify" valign="top" charoff="50">HQ822440</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">HQ822462</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC34</td>
<td align="justify" valign="top" charoff="50">KJ210590</td>
<td align="justify" valign="top" charoff="50">This study</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC35</td>
<td align="justify" valign="top" charoff="50">HQ822430</td>
<td align="justify" valign="top" charoff="50">Serbielle
<italic>et al.</italic>
, unpublished</td>
</tr>
<tr>
<td align="justify" valign="top" charoff="50">Ritr_MHC36</td>
<td align="justify" valign="top" charoff="50">KJ210591</td>
<td align="justify" valign="top" charoff="50">This study</td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
</record>

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