First genealogy for a wild marine fish population reveals multigenerational philopatry

Handle URI:
http://hdl.handle.net/10754/622754
Title:
First genealogy for a wild marine fish population reveals multigenerational philopatry
Authors:
Salles, Océane C.; Pujol, Benoit; Maynard, Jeffrey A.; Almany, Glenn R.; Berumen, Michael L. ( 0000-0003-2463-2742 ) ; Jones, Geoffrey P.; Saenz-Agudelo, Pablo; Srinivasan, Maya; Thorrold, Simon R.; Planes, Serge
Abstract:
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 (Amphiprion percula) 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.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Red Sea Research Center (RSRC)
Citation:
Salles OC, Pujol B, Maynard JA, Almany GR, Berumen ML, et al. (2016) First genealogy for a wild marine fish population reveals multigenerational philopatry. Proceedings of the National Academy of Sciences 113: 13245–13250. Available: http://dx.doi.org/10.1073/pnas.1611797113.
Publisher:
Proceedings of the National Academy of Sciences
Journal:
Proceedings of the National Academy of Sciences
Issue Date:
1-Nov-2016
DOI:
10.1073/pnas.1611797113
Type:
Article
ISSN:
0027-8424; 1091-6490
Sponsors:
We thank the large number of volunteers who assisted in the field and collected tissue samples: R. Brooker, S. Choukroun, P. Costello, J. Davies, D. Dixson, K. Furby, M. Giru, B. Grover, J. Hill, N. Jones, K. McMahon, G. Nanninga, M. Noble, S. Noonan, N. Raventos Klein, M. Pinsky, M. Priest, J. Roberts, J. Smith, T. Sinclair Taylor, N. Tolou, M. Takahashi, P. Waldie, and M. White. Mahonia and FeBrina provided essential logistic support. We are grateful to the traditional owners of the reefs near Kimbe Island for allowing us access to their reefs. Finally, we thank the two anonymous reviewers for their many insightful comments and their contributions to the final draft. This research was supported by Laboratoire d'Excellence CORAIL, Expenditure Review Committee, Coral Reef Initiatives for the Pacific, the Global Environment Facility Coral Reef Targeted Research Connectivity Working Group, National Science Foundation, the Australian Research Council Centre of Excellence Coral Reef Studies, The Nature Conservancy, Total Foundation, James Cook University, King Abdullah University of Science and Techology, and Woods Hole Oceanographic Institution. Research visas were approved by the Papua New Guinea (PNG) government and research protocols were endorsed by the Board of Mahonia Na Dari Research and Conservation Centre, Kimbe, PNG.
Additional Links:
http://www.pnas.org/content/113/46/13245.full
Appears in Collections:
Articles; Red Sea Research Center (RSRC); Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorSalles, Océane C.en
dc.contributor.authorPujol, Benoiten
dc.contributor.authorMaynard, Jeffrey A.en
dc.contributor.authorAlmany, Glenn R.en
dc.contributor.authorBerumen, Michael L.en
dc.contributor.authorJones, Geoffrey P.en
dc.contributor.authorSaenz-Agudelo, Pabloen
dc.contributor.authorSrinivasan, Mayaen
dc.contributor.authorThorrold, Simon R.en
dc.contributor.authorPlanes, Sergeen
dc.date.accessioned2017-01-29T13:51:36Z-
dc.date.available2017-01-29T13:51:36Z-
dc.date.issued2016-11-01en
dc.identifier.citationSalles OC, Pujol B, Maynard JA, Almany GR, Berumen ML, et al. (2016) First genealogy for a wild marine fish population reveals multigenerational philopatry. Proceedings of the National Academy of Sciences 113: 13245–13250. Available: http://dx.doi.org/10.1073/pnas.1611797113.en
dc.identifier.issn0027-8424en
dc.identifier.issn1091-6490en
dc.identifier.doi10.1073/pnas.1611797113en
dc.identifier.urihttp://hdl.handle.net/10754/622754-
dc.description.abstractNatal 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 (Amphiprion percula) 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.en
dc.description.sponsorshipWe thank the large number of volunteers who assisted in the field and collected tissue samples: R. Brooker, S. Choukroun, P. Costello, J. Davies, D. Dixson, K. Furby, M. Giru, B. Grover, J. Hill, N. Jones, K. McMahon, G. Nanninga, M. Noble, S. Noonan, N. Raventos Klein, M. Pinsky, M. Priest, J. Roberts, J. Smith, T. Sinclair Taylor, N. Tolou, M. Takahashi, P. Waldie, and M. White. Mahonia and FeBrina provided essential logistic support. We are grateful to the traditional owners of the reefs near Kimbe Island for allowing us access to their reefs. Finally, we thank the two anonymous reviewers for their many insightful comments and their contributions to the final draft. This research was supported by Laboratoire d'Excellence CORAIL, Expenditure Review Committee, Coral Reef Initiatives for the Pacific, the Global Environment Facility Coral Reef Targeted Research Connectivity Working Group, National Science Foundation, the Australian Research Council Centre of Excellence Coral Reef Studies, The Nature Conservancy, Total Foundation, James Cook University, King Abdullah University of Science and Techology, and Woods Hole Oceanographic Institution. Research visas were approved by the Papua New Guinea (PNG) government and research protocols were endorsed by the Board of Mahonia Na Dari Research and Conservation Centre, Kimbe, PNG.en
dc.publisherProceedings of the National Academy of Sciencesen
dc.relation.urlhttp://www.pnas.org/content/113/46/13245.fullen
dc.subjectInbreedingen
dc.subjectParental effectsen
dc.subjectSelf-recruitmenten
dc.subjectAmphiprion Perculaen
dc.subjectMultigenerational Pedigreeen
dc.titleFirst genealogy for a wild marine fish population reveals multigenerational philopatryen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalProceedings of the National Academy of Sciencesen
dc.contributor.institutionLaboratoire d'Excellenceen
dc.contributor.institutionCNRS, Université Toulouse 3 Paul Sabatier, Ecole Nationale supérieure de la Formation de l'enseignement Agricole, UMR5174 Laboratoire Évolution et Diversité Biologique, 31062 Toulouse, France.en
dc.contributor.institutionSymbioSeas and the Marine Applied Research Center, Wilmington, NC 28411.en
dc.contributor.institutionAustralian Research Council Centre of Excellence for Coral Reef Studies, and College of Science and Engineering, James Cook University, Townsville, Queensland 4811, Australia.en
dc.contributor.institutionInstituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia 5090000, Chile.en
dc.contributor.institutionBiology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543.en
kaust.authorBerumen, Michael L.en
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