First genealogy for a wild marine fish population reveals multigenerational philopatry
Identifieur interne : 000931 ( Pmc/Checkpoint ); précédent : 000930; suivant : 000932First genealogy for a wild marine fish population reveals multigenerational philopatry
Auteurs : Océane C. Salles [France] ; Benoit Pujol [France] ; Jeffrey A. Maynard [France] ; Glenn R. Almany [France] ; Michael L. Berumen [Arabie saoudite] ; Geoffrey P. Jones [Australie] ; Pablo Saenz-Agudelo [Chili] ; Maya Srinivasan [Australie] ; Simon R. Thorrold ; Serge Planes [France]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2016.
Abstract
Evidence for natal philopatry, the return of individuals to their natal location for reproduction, is scarce in marine fish populations despite being common in anadromous fishes. The proportion of individuals returning to natal sites is an important metric for estimating the effects of inbreeding and the potential for local adaptation to generate resilience to climate change. Here, we present the first multigenerational pedigree for a wild marine fish. We resolved the genealogical tree of families of orange clownfish
Url:
DOI: 10.1073/pnas.1611797113
PubMed: 27799530
PubMed Central: 5135361
Affiliations:
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<affiliation wicri:level="1"><nlm:aff id="aff1">Ecole Pratique des Hautes Etudes,<institution>Paris Siences et Lettres Research University</institution>
, Université de Perpignan Via Domitia, CNRS, USR 3278 Centre de Recherches Insulaires et Observatoire de l'environnement, F-66360 Perpignan,<country>France</country>
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28411;</nlm:aff>
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<author><name sortKey="Berumen, Michael L" sort="Berumen, Michael L" uniqKey="Berumen M" first="Michael L." last="Berumen">Michael L. Berumen</name>
<affiliation wicri:level="1"><nlm:aff id="aff5">Red Sea Research Center, Division of Biological and Environmental Sciences and Engineering,<institution>King Abdullah University of Science and Technology</institution>
, Thuwal 23955,<country>Saudi Arabia</country>
;</nlm:aff>
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<author><name sortKey="Jones, Geoffrey P" sort="Jones, Geoffrey P" uniqKey="Jones G" first="Geoffrey P." last="Jones">Geoffrey P. Jones</name>
<affiliation wicri:level="1"><nlm:aff id="aff6">Australian Research Council Centre of Excellence for Coral Reef Studies, and College of Science and Engineering, James Cook University, Townsville, Queensland 4811,<country>Australia</country>
;</nlm:aff>
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<author><name sortKey="Saenz Agudelo, Pablo" sort="Saenz Agudelo, Pablo" uniqKey="Saenz Agudelo P" first="Pablo" last="Saenz-Agudelo">Pablo Saenz-Agudelo</name>
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, Valdivia 5090000,<country>Chile</country>
;</nlm:aff>
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;</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Thorrold, Simon R" sort="Thorrold, Simon R" uniqKey="Thorrold S" first="Simon R." last="Thorrold">Simon R. Thorrold</name>
<affiliation><nlm:aff id="aff8">Biology Department,<institution>Woods Hole Oceanographic Institution</institution>
, Woods Hole,<addr-line>MA</addr-line>
02543</nlm:aff>
</affiliation>
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<author><name sortKey="Planes, Serge" sort="Planes, Serge" uniqKey="Planes S" first="Serge" last="Planes">Serge Planes</name>
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, Université de Perpignan Via Domitia, CNRS, USR 3278 Centre de Recherches Insulaires et Observatoire de l'environnement, F-66360 Perpignan,<country>France</country>
;</nlm:aff>
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<front><div type="abstract" xml:lang="en"><title>Significance</title>
<p>Evidence for natal philopatry, the return of individuals to their natal location for reproduction, is scarce in marine fish populations despite being common in anadromous fishes. The proportion of individuals returning to natal sites is an important metric for estimating the effects of inbreeding and the potential for local adaptation to generate resilience to climate change. Here, we present the first multigenerational pedigree for a wild marine fish. We resolved the genealogical tree of families of orange clownfish <italic>Amphiprion percula</italic>
spanning up to five generations, using data from a 10-year genetic survey of a population at Kimbe Island, Papua New Guinea. We found that longitudinal philopatry plays a significant role in driving population renewal of the orange clownfish.</p>
</div>
</front>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
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<article-id pub-id-type="doi">10.1073/pnas.1611797113</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject>
<subj-group><subject>Population Biology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>First genealogy for a wild marine fish population reveals multigenerational philopatry</article-title>
<alt-title alt-title-type="short">Multigeneration philopatry in marine fish</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Salles</surname>
<given-names>Océane C.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pujol</surname>
<given-names>Benoit</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Maynard</surname>
<given-names>Jeffrey A.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Almany</surname>
<given-names>Glenn R.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Berumen</surname>
<given-names>Michael L.</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jones</surname>
<given-names>Geoffrey P.</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Saenz-Agudelo</surname>
<given-names>Pablo</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Srinivasan</surname>
<given-names>Maya</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Thorrold</surname>
<given-names>Simon R.</given-names>
</name>
<xref ref-type="aff" rid="aff8"><sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Planes</surname>
<given-names>Serge</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<aff id="aff1"><sup>a</sup>
Ecole Pratique des Hautes Etudes,<institution>Paris Siences et Lettres Research University</institution>
, Université de Perpignan Via Domitia, CNRS, USR 3278 Centre de Recherches Insulaires et Observatoire de l'environnement, F-66360 Perpignan,<country>France</country>
;</aff>
<aff id="aff2"><sup>b</sup>
Laboratoire d’Excellence “CORAIL,” F-66360 Perpignan,<country>France</country>
</aff>
<aff id="aff3"><sup>c</sup>
CNRS,<institution>Université Toulouse 3 Paul Sabatier</institution>
, Ecole Nationale supérieure de la Formation de l'enseignement Agricole, UMR5174 Laboratoire Évolution et Diversité Biologique, 31062 Toulouse,<country>France</country>
;</aff>
<aff id="aff4"><sup>d</sup>
SymbioSeas and the<institution>Marine Applied Research Center</institution>
, Wilmington,<addr-line>NC</addr-line>
28411;</aff>
<aff id="aff5"><sup>e</sup>
Red Sea Research Center, Division of Biological and Environmental Sciences and Engineering,<institution>King Abdullah University of Science and Technology</institution>
, Thuwal 23955,<country>Saudi Arabia</country>
;</aff>
<aff id="aff6"><sup>f</sup>
Australian Research Council Centre of Excellence for Coral Reef Studies, and College of Science and Engineering, James Cook University, Townsville, Queensland 4811,<country>Australia</country>
;</aff>
<aff id="aff7"><sup>g</sup>
Instituto de Ciencias Ambientales y Evolutivas,<institution>Universidad Austral de Chile</institution>
, Valdivia 5090000,<country>Chile</country>
;</aff>
<aff id="aff8"><sup>h</sup>
Biology Department,<institution>Woods Hole Oceanographic Institution</institution>
, Woods Hole,<addr-line>MA</addr-line>
02543</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>1</sup>
To whom correspondence should be addressed. Email: <email>oceane.salles@gmail.com</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited by Nancy Knowlton, Smithsonian Institution, DC, Washington, and approved September 30, 2016 (received for review July 18, 2016)</p>
</fn>
<fn fn-type="con"><p>Author contributions: G.P.J., S.R.T., and S.P. designed research; G.R.A., M.L.B., G.P.J., M.S., S.R.T., and S.P. performed research; O.C.S., B.P., G.R.A., and M.L.B. contributed new reagents/analytic tools; O.C.S., B.P., and P.S.-A. analyzed data; and O.C.S., B.P., J.A.M., M.L.B., G.P.J., P.S.-A., S.R.T., and S.P. wrote the paper.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>15</day>
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<year>2016</year>
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</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>113</volume>
<issue>46</issue>
<fpage>13245</fpage>
<lpage>13250</lpage>
<permissions><license license-type="open-access"><license-p>Freely available online through the PNAS open access option.</license-p>
</license>
</permissions>
<self-uri xlink:title="pdf" xlink:href="pnas.201611797.pdf"></self-uri>
<abstract abstract-type="executive-summary"><title>Significance</title>
<p>Evidence for natal philopatry, the return of individuals to their natal location for reproduction, is scarce in marine fish populations despite being common in anadromous fishes. The proportion of individuals returning to natal sites is an important metric for estimating the effects of inbreeding and the potential for local adaptation to generate resilience to climate change. Here, we present the first multigenerational pedigree for a wild marine fish. We resolved the genealogical tree of families of orange clownfish <italic>Amphiprion percula</italic>
spanning up to five generations, using data from a 10-year genetic survey of a population at Kimbe Island, Papua New Guinea. We found that longitudinal philopatry plays a significant role in driving population renewal of the orange clownfish.</p>
</abstract>
<abstract><p>Natal philopatry, the return of individuals to their natal area for reproduction, has advantages and disadvantages for animal populations. Natal philopatry may generate local genetic adaptation, but it may also increase the probability of inbreeding that can compromise persistence. Although natal philopatry is well documented in anadromous fishes, marine fish may also return to their birth site to spawn. How philopatry shapes wild fish populations is, however, unclear because it requires constructing multigenerational pedigrees that are currently lacking for marine fishes. Here we present the first multigenerational pedigree for a marine fish population by repeatedly genotyping all individuals in a population of the orange clownfish (<italic>Amphiprion percula</italic>
) at Kimbe Island (Papua New Guinea) during a 10-y period. Based on 2927 individuals, our pedigree analysis revealed that longitudinal philopatry was recurrent over five generations. Progeny tended to settle close to their parents, with related individuals often sharing the same colony. However, successful inbreeding was rare, and genetic diversity remained high, suggesting occasional inbreeding does not impair local population persistence. Local reproductive success was dependent on the habitat larvae settled into, rather than the habitat they came from. Our study suggests that longitudinal philopatry can influence both population replenishment and local adaptation of marine fishes. Resolving multigenerational pedigrees during a relatively short period, as we present here, provides a framework for assessing the ability of marine populations to persist and adapt to accelerating climate change.</p>
</abstract>
<kwd-group><kwd><italic>Amphiprion percula</italic>
</kwd>
<kwd>self-recruitment</kwd>
<kwd>multigenerational pedigree</kwd>
<kwd>inbreeding</kwd>
<kwd>parental effects</kwd>
</kwd-group>
<funding-group><award-group id="gs1"><funding-source id="sp1">Labex CORAIL</funding-source>
<award-id rid="sp1">ANR-10-LABX-0008-01</award-id>
</award-group>
<award-group id="gs2"><funding-source id="sp2">Australian Research Council Center of Excellence for Coral Reef Studies</funding-source>
<award-id rid="sp2">CE140100020</award-id>
</award-group>
</funding-group>
<counts><page-count count="6"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Arabie saoudite</li>
<li>Australie</li>
<li>Chili</li>
<li>France</li>
</country>
</list>
<tree><noCountry><name sortKey="Thorrold, Simon R" sort="Thorrold, Simon R" uniqKey="Thorrold S" first="Simon R." last="Thorrold">Simon R. Thorrold</name>
</noCountry>
<country name="France"><noRegion><name sortKey="Salles, Oceane C" sort="Salles, Oceane C" uniqKey="Salles O" first="Océane C." last="Salles">Océane C. Salles</name>
</noRegion>
<name sortKey="Almany, Glenn R" sort="Almany, Glenn R" uniqKey="Almany G" first="Glenn R." last="Almany">Glenn R. Almany</name>
<name sortKey="Almany, Glenn R" sort="Almany, Glenn R" uniqKey="Almany G" first="Glenn R." last="Almany">Glenn R. Almany</name>
<name sortKey="Maynard, Jeffrey A" sort="Maynard, Jeffrey A" uniqKey="Maynard J" first="Jeffrey A." last="Maynard">Jeffrey A. Maynard</name>
<name sortKey="Planes, Serge" sort="Planes, Serge" uniqKey="Planes S" first="Serge" last="Planes">Serge Planes</name>
<name sortKey="Planes, Serge" sort="Planes, Serge" uniqKey="Planes S" first="Serge" last="Planes">Serge Planes</name>
<name sortKey="Pujol, Benoit" sort="Pujol, Benoit" uniqKey="Pujol B" first="Benoit" last="Pujol">Benoit Pujol</name>
<name sortKey="Salles, Oceane C" sort="Salles, Oceane C" uniqKey="Salles O" first="Océane C." last="Salles">Océane C. Salles</name>
</country>
<country name="Arabie saoudite"><noRegion><name sortKey="Berumen, Michael L" sort="Berumen, Michael L" uniqKey="Berumen M" first="Michael L." last="Berumen">Michael L. Berumen</name>
</noRegion>
</country>
<country name="Australie"><noRegion><name sortKey="Jones, Geoffrey P" sort="Jones, Geoffrey P" uniqKey="Jones G" first="Geoffrey P." last="Jones">Geoffrey P. Jones</name>
</noRegion>
<name sortKey="Srinivasan, Maya" sort="Srinivasan, Maya" uniqKey="Srinivasan M" first="Maya" last="Srinivasan">Maya Srinivasan</name>
</country>
<country name="Chili"><noRegion><name sortKey="Saenz Agudelo, Pablo" sort="Saenz Agudelo, Pablo" uniqKey="Saenz Agudelo P" first="Pablo" last="Saenz-Agudelo">Pablo Saenz-Agudelo</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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