Surgeons and suture zones: Hybridization among four surgeonfish species in the Indo-Pacific with variable evolutionary outcomes

Handle URI:
http://hdl.handle.net/10754/608225
Title:
Surgeons and suture zones: Hybridization among four surgeonfish species in the Indo-Pacific with variable evolutionary outcomes
Authors:
DiBattista, Joseph ( 0000-0002-5696-7574 ) ; Whitney, Jonathan; Craig, Matthew T.; Hobbs, Jean-Paul A.; Rocha, Luiz A.; Feldheim, Kevin A.; Berumen, Michael L. ( 0000-0003-2463-2742 ) ; Bowen, Brian W.
Abstract:
Closely related species can provide valuable insights into evolutionary processes through comparison of their ecology, geographic distribution and the history recorded in their genomes. In the Indo-Pacific, many reef fishes are divided into sister species that come into secondary contact at biogeographic borders, most prominently where Indian Ocean and Pacific Ocean faunas meet. It is unclear whether hybridization in this contact zone represents incomplete speciation, secondary contact, an evolutionary dead-end (for hybrids) or some combination of the above. To address these issues, we conducted comprehensive surveys of two widely-distributed surgeonfish species, Acanthurus leucosternon (N = 141) and A. nigricans (N = 412), with mtDNA cytochrome b sequences and ten microsatellite loci. These surgeonfishes are found primarily in the Indian and Pacific Oceans, respectively, but overlap at the Christmas and Cocos-Keeling Islands hybrid zone in the eastern Indian Ocean. We also sampled the two other Pacific members of this species complex, A. achilles (N = 54) and A. japonicus (N = 49), which are known to hybridize with A. nigricans where their ranges overlap. Our results indicate separation between the four species that range from the recent Pleistocene to late Pliocene (235,000 to 2.25 million years ago). The Pacific A. achilles is the most divergent (and possibly ancestral) species with mtDNA dcorr ≈ 0.04, whereas the other two Pacific species (A. japonicus and A. nigricans) are distinguishable only at a population or subspecies level (ΦST = 0.6533, P < 0.001). Little population structure was observed within species, with evidence of recent population expansion across all four geographic ranges. We detected sharing of mtDNA haplotypes between species and extensive hybridization based on microsatellites, consistent with later generation hybrids but also the effects of allele homoplasy. Despite extensive introgression, 98% of specimens had concordance between mtDNA lineage and species identification based on external morphology, indicating that species integrity may not be eroding. The A. nigricans complex demonstrates a range of outcomes from incomplete speciation to secondary contact to decreasing hybridization with increasing evolutionary depth.
KAUST Department:
Red Sea Research Center (RSRC); Biological and Environmental Sciences and Engineering (BESE) Division
Citation:
Surgeons and suture zones: Hybridization among four surgeonfish species in the Indo-Pacific with variable evolutionary outcomes 2016 Molecular Phylogenetics and Evolution
Publisher:
Elsevier BV
Journal:
Molecular Phylogenetics and Evolution
Issue Date:
30-Apr-2016
DOI:
10.1016/j.ympev.2016.04.036
Type:
Article
ISSN:
10557903
Sponsors:
This research was supported by the National Science Foundation grants OCE-0929031 to BWB, NOAA National Marine Sanctuaries Program MOA No. 2005-008/66882 to R.J. Toonen, Seaver Institute, KAUST Office of Competitive Research Funds under Award No. CRG-1-2012-BER-002 to MLB, baseline research funds to MLB, National Geographic Society Grant 9024-11 to JDD and by a Natural Sciences and Engineering Research Council of Canada postgraduate fellowship to JDD. For specimen collections we thank Kim Andersen, Paul Barber, J. Howard Choat, Richard Coleman, Joshua Copus, Toby Daly-Engel, Joshua Drew, Jeff Eble, Iria Fernandez-Silva, Kevin Flanagan, Michelle Gaither, Brian Greene, Song He, Matthew Iacchei, Stephen Karl, Randall Kosaki, Carl Meyer, Yannis Papastamatiou, David Pence, Mark Priest, Richard Pyle, Joshua Reece, D. Ross Robertson, Jennifer Schultz, Tane Sinclair-Taylor, Derek Smith, Zoltan Szabo, Kim Tenggardjaja, Bill Walsh, Ivor Willliams, Zeng Xiaoqi, Jill Zamzow and the crew of the R.V. Hi’ialakai. For logistic support we thank Robert Toonen, Randall Kosaki, Serge Planes, Jo-Ann Leong, Charles Sheppard, Salah Saeed Ahmed, Fouad Naseeb, Thabet Abdullah Khamis, Ahmed Issa Ali Affrar (Socotra Specialist Tours), Hawaii Department of Land and Natural Resources, Coral Reef Research Foundation, Papahānaumokuākea Marine National Monument, the Ocean University of China - College of Fisheries, Ministry of Water and Environment of Yemen, the Environment Protection Authority (EPA) Socotra, Administration of the British Indian Ocean Territory, Western Australia Department of Fisheries, Parks Australia and U.S. Fish and Wildlife Service. We thank Tane Sinclair-Taylor, Keoki Stender, Kenji Sorita and Hiroshi Senou (Kanagawa Prefectural Museum of Natural History) for providing images. Thanks to J. Howard Choat and Ben Victor for providing life-history information, Catherine Cullingham for providing a copy of HYBRIDLAB, Stefano Montanari for the map figure, members of the ToBo lab for logistic support and the Center for Genomics, Proteomics and Bioinformatics at the University of Hawai’i at Mānoa for their assistance with genotyping. We also thank Giacomo Bernardi and two anonymous reviewers for their helpful comments on an earlier version of this manuscript. This is contribution no. XX from the Hawai’i Institute of Marine Biology and no. XX from the School of Ocean and Earth Science and Technology.
Additional Links:
http://linkinghub.elsevier.com/retrieve/pii/S1055790316300793
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.authorDiBattista, Josephen
dc.contributor.authorWhitney, Jonathanen
dc.contributor.authorCraig, Matthew T.en
dc.contributor.authorHobbs, Jean-Paul A.en
dc.contributor.authorRocha, Luiz A.en
dc.contributor.authorFeldheim, Kevin A.en
dc.contributor.authorBerumen, Michael L.en
dc.contributor.authorBowen, Brian W.en
dc.date.accessioned2016-05-04T13:50:09Zen
dc.date.available2016-05-04T13:50:09Zen
dc.date.issued2016-04-30en
dc.identifier.citationSurgeons and suture zones: Hybridization among four surgeonfish species in the Indo-Pacific with variable evolutionary outcomes 2016 Molecular Phylogenetics and Evolutionen
dc.identifier.issn10557903en
dc.identifier.doi10.1016/j.ympev.2016.04.036en
dc.identifier.urihttp://hdl.handle.net/10754/608225en
dc.description.abstractClosely related species can provide valuable insights into evolutionary processes through comparison of their ecology, geographic distribution and the history recorded in their genomes. In the Indo-Pacific, many reef fishes are divided into sister species that come into secondary contact at biogeographic borders, most prominently where Indian Ocean and Pacific Ocean faunas meet. It is unclear whether hybridization in this contact zone represents incomplete speciation, secondary contact, an evolutionary dead-end (for hybrids) or some combination of the above. To address these issues, we conducted comprehensive surveys of two widely-distributed surgeonfish species, Acanthurus leucosternon (N = 141) and A. nigricans (N = 412), with mtDNA cytochrome b sequences and ten microsatellite loci. These surgeonfishes are found primarily in the Indian and Pacific Oceans, respectively, but overlap at the Christmas and Cocos-Keeling Islands hybrid zone in the eastern Indian Ocean. We also sampled the two other Pacific members of this species complex, A. achilles (N = 54) and A. japonicus (N = 49), which are known to hybridize with A. nigricans where their ranges overlap. Our results indicate separation between the four species that range from the recent Pleistocene to late Pliocene (235,000 to 2.25 million years ago). The Pacific A. achilles is the most divergent (and possibly ancestral) species with mtDNA dcorr ≈ 0.04, whereas the other two Pacific species (A. japonicus and A. nigricans) are distinguishable only at a population or subspecies level (ΦST = 0.6533, P < 0.001). Little population structure was observed within species, with evidence of recent population expansion across all four geographic ranges. We detected sharing of mtDNA haplotypes between species and extensive hybridization based on microsatellites, consistent with later generation hybrids but also the effects of allele homoplasy. Despite extensive introgression, 98% of specimens had concordance between mtDNA lineage and species identification based on external morphology, indicating that species integrity may not be eroding. The A. nigricans complex demonstrates a range of outcomes from incomplete speciation to secondary contact to decreasing hybridization with increasing evolutionary depth.en
dc.description.sponsorshipThis research was supported by the National Science Foundation grants OCE-0929031 to BWB, NOAA National Marine Sanctuaries Program MOA No. 2005-008/66882 to R.J. Toonen, Seaver Institute, KAUST Office of Competitive Research Funds under Award No. CRG-1-2012-BER-002 to MLB, baseline research funds to MLB, National Geographic Society Grant 9024-11 to JDD and by a Natural Sciences and Engineering Research Council of Canada postgraduate fellowship to JDD. For specimen collections we thank Kim Andersen, Paul Barber, J. Howard Choat, Richard Coleman, Joshua Copus, Toby Daly-Engel, Joshua Drew, Jeff Eble, Iria Fernandez-Silva, Kevin Flanagan, Michelle Gaither, Brian Greene, Song He, Matthew Iacchei, Stephen Karl, Randall Kosaki, Carl Meyer, Yannis Papastamatiou, David Pence, Mark Priest, Richard Pyle, Joshua Reece, D. Ross Robertson, Jennifer Schultz, Tane Sinclair-Taylor, Derek Smith, Zoltan Szabo, Kim Tenggardjaja, Bill Walsh, Ivor Willliams, Zeng Xiaoqi, Jill Zamzow and the crew of the R.V. Hi’ialakai. For logistic support we thank Robert Toonen, Randall Kosaki, Serge Planes, Jo-Ann Leong, Charles Sheppard, Salah Saeed Ahmed, Fouad Naseeb, Thabet Abdullah Khamis, Ahmed Issa Ali Affrar (Socotra Specialist Tours), Hawaii Department of Land and Natural Resources, Coral Reef Research Foundation, Papahānaumokuākea Marine National Monument, the Ocean University of China - College of Fisheries, Ministry of Water and Environment of Yemen, the Environment Protection Authority (EPA) Socotra, Administration of the British Indian Ocean Territory, Western Australia Department of Fisheries, Parks Australia and U.S. Fish and Wildlife Service. We thank Tane Sinclair-Taylor, Keoki Stender, Kenji Sorita and Hiroshi Senou (Kanagawa Prefectural Museum of Natural History) for providing images. Thanks to J. Howard Choat and Ben Victor for providing life-history information, Catherine Cullingham for providing a copy of HYBRIDLAB, Stefano Montanari for the map figure, members of the ToBo lab for logistic support and the Center for Genomics, Proteomics and Bioinformatics at the University of Hawai’i at Mānoa for their assistance with genotyping. We also thank Giacomo Bernardi and two anonymous reviewers for their helpful comments on an earlier version of this manuscript. This is contribution no. XX from the Hawai’i Institute of Marine Biology and no. XX from the School of Ocean and Earth Science and Technology.en
dc.language.isoenen
dc.publisherElsevier BVen
dc.relation.urlhttp://linkinghub.elsevier.com/retrieve/pii/S1055790316300793en
dc.rightsNOTICE: this is the author’s version of a work that was accepted for publication in Molecular Phylogenetics and Evolution. Changes resulting from the publishing process, such as peer review, editing, corrections, structural formatting, and other quality control mechanisms may not be reflected in this document. Changes may have been made to this work since it was submitted for publication. A definitive version was subsequently published in Molecular Phylogenetics and Evolution, 30 April 2016. DOI: 10.1016/j.ympev.2016.04.036.en
dc.subjectAcanthuridaeen
dc.subjectCoral reef fishen
dc.subjectIntrogressionen
dc.subjectReverse speciationen
dc.subjectSpecies complexen
dc.titleSurgeons and suture zones: Hybridization among four surgeonfish species in the Indo-Pacific with variable evolutionary outcomesen
dc.typeArticleen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.identifier.journalMolecular Phylogenetics and Evolutionen
dc.eprint.versionPost-printen
dc.contributor.institutionDepartment of Environment and Agriculture, Curtin University, PO Box U1987, Perth, WA 6845, Australiaen
dc.contributor.institutionHawai’i Institute of Marine Biology, Kāne’ohe, HI 96744, USAen
dc.contributor.institutionFisheries Resource Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanographic and Atmospheric Administration, 8901 La Jolla Shores Drive, La Jolla, CA 92037, USAen
dc.contributor.institutionSection of Ichthyology, California Academy of Sciences, San Francisco, CA 94118, USAen
dc.contributor.institutionField Museum, Pritzker Laboratory for Molecular Systematics and Evolution, Chicago, IL 60605, USAen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorDiBattista, Josephen
kaust.authorBerumen, Michael L.en
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