Geographic Patterns of Genetic Variation in a Broadly Distributed Marine Vertebrate: New Insights into Loggerhead Turtle Stock Structure from Expanded Mitochondrial DNA Sequences
Previous genetic studies have demonstrated that natal homing shapes the stock structure of marine turtle nesting populations. However, widespread sharing of common haplotypes based on short segments of the mitochondrial control region often limits resolution of the demographic connectivity of popula...
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| Veröffentlicht in: | PloS one Jg. 9; H. 1; S. e85956 |
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| Sprache: | Englisch |
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23.01.2014
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| Abstract | Previous genetic studies have demonstrated that natal homing shapes the stock structure of marine turtle nesting populations. However, widespread sharing of common haplotypes based on short segments of the mitochondrial control region often limits resolution of the demographic connectivity of populations. Recent studies employing longer control region sequences to resolve haplotype sharing have focused on regional assessments of genetic structure and phylogeography. Here we synthesize available control region sequences for loggerhead turtles from the Mediterranean Sea, Atlantic, and western Indian Ocean basins. These data represent six of the nine globally significant regional management units (RMUs) for the species and include novel sequence data from Brazil, Cape Verde, South Africa and Oman. Genetic tests of differentiation among 42 rookeries represented by short sequences (380 bp haplotypes from 3,486 samples) and 40 rookeries represented by long sequences (∼800 bp haplotypes from 3,434 samples) supported the distinction of the six RMUs analyzed as well as recognition of at least 18 demographically independent management units (MUs) with respect to female natal homing. A total of 59 haplotypes were resolved. These haplotypes belonged to two highly divergent global lineages, with haplogroup I represented primarily by CC-A1, CC-A4, and CC-A11 variants and haplogroup II represented by CC-A2 and derived variants. Geographic distribution patterns of haplogroup II haplotypes and the nested position of CC-A11.6 from Oman among the Atlantic haplotypes invoke recent colonization of the Indian Ocean from the Atlantic for both global lineages. The haplotypes we confirmed for western Indian Ocean RMUs allow reinterpretation of previous mixed stock analysis and further suggest that contemporary migratory connectivity between the Indian and Atlantic Oceans occurs on a broader scale than previously hypothesized. This study represents a valuable model for conducting comprehensive international cooperative data management and research in marine ecology. |
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| AbstractList | Previous genetic studies have demonstrated that natal homing shapes the stock structure of marine turtle nesting populations. However, widespread sharing of common haplotypes based on short segments of the mitochondrial control region often limits resolution of the demographic connectivity of populations. Recent studies employing longer control region sequences to resolve haplotype sharing have focused on regional assessments of genetic structure and phylogeography. Here we synthesize available control region sequences for loggerhead turtles from the Mediterranean Sea, Atlantic, and western Indian Ocean basins. These data represent six of the nine globally significant regional management units (RMUs) for the species and include novel sequence data from Brazil, Cape Verde, South Africa and Oman. Genetic tests of differentiation among 42 rookeries represented by short sequences (380 bp haplotypes from 3,486 samples) and 40 rookeries represented by long sequences (∼800 bp haplotypes from 3,434 samples) supported the distinction of the six RMUs analyzed as well as recognition of at least 18 demographically independent management units (MUs) with respect to female natal homing. A total of 59 haplotypes were resolved. These haplotypes belonged to two highly divergent global lineages, with haplogroup I represented primarily by CC-A1, CC-A4, and CC-A11 variants and haplogroup II represented by CC-A2 and derived variants. Geographic distribution patterns of haplogroup II haplotypes and the nested position of CC-A11.6 from Oman among the Atlantic haplotypes invoke recent colonization of the Indian Ocean from the Atlantic for both global lineages. The haplotypes we confirmed for western Indian Ocean RMUs allow reinterpretation of previous mixed stock analysis and further suggest that contemporary migratory connectivity between the Indian and Atlantic Oceans occurs on a broader scale than previously hypothesized. This study represents a valuable model for conducting comprehensive international cooperative data management and research in marine ecology. Previous genetic studies have demonstrated that natal homing shapes the stock structure of marine turtle nesting populations. However, widespread sharing of common haplotypes based on short segments of the mitochondrial control region often limits resolution of the demographic connectivity of populations. Recent studies employing longer control region sequences to resolve haplotype sharing have focused on regional assessments of genetic structure and phylogeography. Here we synthesize available control region sequences for loggerhead turtles from the Mediterranean Sea, Atlantic, and western Indian Ocean basins. These data represent six of the nine globally significant regional management units (RMUs) for the species and include novel sequence data from Brazil, Cape Verde, South Africa and Oman. Genetic tests of differentiation among 42 rookeries represented by short sequences (380 bp haplotypes from 3,486 samples) and 40 rookeries represented by long sequences (~800 bp haplotypes from 3,434 samples) supported the distinction of the six RMUs analyzed as well as recognition of at least 18 demographically independent management units (MUs) with respect to female natal homing. A total of 59 haplotypes were resolved. These haplotypes belonged to two highly divergent global lineages, with haplogroup I represented primarily by CC-A1, CC-A4, and CC-A11 variants and haplogroup II represented by CC-A2 and derived variants. Geographic distribution patterns of haplogroup II haplotypes and the nested position of CC-A11.6 from Oman among the Atlantic haplotypes invoke recent colonization of the Indian Ocean from the Atlantic for both global lineages. The haplotypes we confirmed for western Indian Ocean RMUs allow reinterpretation of previous mixed stock analysis and further suggest that contemporary migratory connectivity between the Indian and Atlantic Oceans occurs on a broader scale than previously hypothesized. This study represents a valuable model for conducting comprehensive international cooperative data management and research in marine ecology. Previous genetic studies have demonstrated that natal homing shapes the stock structure of marine turtle nesting populations. However, widespread sharing of common haplotypes based on short segments of the mitochondrial control region often limits resolution of the demographic connectivity of populations. Recent studies employing longer control region sequences to resolve haplotype sharing have focused on regional assessments of genetic structure and phylogeography. Here we synthesize available control region sequences for loggerhead turtles from the Mediterranean Sea, Atlantic, and western Indian Ocean basins. These data represent six of the nine globally significant regional management units (RMUs) for the species and include novel sequence data from Brazil, Cape Verde, South Africa and Oman. Genetic tests of differentiation among 42 rookeries represented by short sequences (380 bp haplotypes from 3,486 samples) and 40 rookeries represented by long sequences (∼800 bp haplotypes from 3,434 samples) supported the distinction of the six RMUs analyzed as well as recognition of at least 18 demographically independent management units (MUs) with respect to female natal homing. A total of 59 haplotypes were resolved. These haplotypes belonged to two highly divergent global lineages, with haplogroup I represented primarily by CC-A1, CC-A4, and CC-A11 variants and haplogroup II represented by CC-A2 and derived variants. Geographic distribution patterns of haplogroup II haplotypes and the nested position of CC-A11.6 from Oman among the Atlantic haplotypes invoke recent colonization of the Indian Ocean from the Atlantic for both global lineages. The haplotypes we confirmed for western Indian Ocean RMUs allow reinterpretation of previous mixed stock analysis and further suggest that contemporary migratory connectivity between the Indian and Atlantic Oceans occurs on a broader scale than previously hypothesized. This study represents a valuable model for conducting comprehensive international cooperative data management and research in marine ecology.Previous genetic studies have demonstrated that natal homing shapes the stock structure of marine turtle nesting populations. However, widespread sharing of common haplotypes based on short segments of the mitochondrial control region often limits resolution of the demographic connectivity of populations. Recent studies employing longer control region sequences to resolve haplotype sharing have focused on regional assessments of genetic structure and phylogeography. Here we synthesize available control region sequences for loggerhead turtles from the Mediterranean Sea, Atlantic, and western Indian Ocean basins. These data represent six of the nine globally significant regional management units (RMUs) for the species and include novel sequence data from Brazil, Cape Verde, South Africa and Oman. Genetic tests of differentiation among 42 rookeries represented by short sequences (380 bp haplotypes from 3,486 samples) and 40 rookeries represented by long sequences (∼800 bp haplotypes from 3,434 samples) supported the distinction of the six RMUs analyzed as well as recognition of at least 18 demographically independent management units (MUs) with respect to female natal homing. A total of 59 haplotypes were resolved. These haplotypes belonged to two highly divergent global lineages, with haplogroup I represented primarily by CC-A1, CC-A4, and CC-A11 variants and haplogroup II represented by CC-A2 and derived variants. Geographic distribution patterns of haplogroup II haplotypes and the nested position of CC-A11.6 from Oman among the Atlantic haplotypes invoke recent colonization of the Indian Ocean from the Atlantic for both global lineages. The haplotypes we confirmed for western Indian Ocean RMUs allow reinterpretation of previous mixed stock analysis and further suggest that contemporary migratory connectivity between the Indian and Atlantic Oceans occurs on a broader scale than previously hypothesized. This study represents a valuable model for conducting comprehensive international cooperative data management and research in marine ecology. |
| Audience | Academic |
| Author | Clusa, Marcel Monzón-Argüello, Catalina Carreras, Carlos Stewart, Kelly R. Nel, Ronel Nairn, Campbell J. Türkozan, Oguz Soares, Luciano S. Bjorndal, Karen A. Cardona, Luis Vilaça, Sibelle T. Yilmaz, Can Dutton, Peter H. Shamblin, Brian M. Nielsen, Janne T. Abreu-Grobois, F. Alberto Bolten, Alan B. |
| AuthorAffiliation | 10 Zoology Department, Nelson Mandela Metropolitan University, Summerstrand Campus South, University Way, Summerstrand, Port Elizabeth, South Africa 14 Adnan Menderes University, Faculty of Science and Arts, Department of Biology, Aydin, Turkey 11 Projeto TAMAR-ICMBio, Salvador, BA, Brazil 13 Laboratório de Biodiversidade e Evolução Molecular, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil 5 Department of Animal Biology and IRBio, Faculty of Biology, University of Barcelona, Barcelona, Spain 2 Marine Mammal and Turtle Division, Southwest Fisheries Science Center, National Atmospheric and Oceanic Administration Fisheries, La Jolla, California, United States of America 3 Archie Carr Center for Sea Turtle Research and Department of Biology, University of Florida, Gainesville, Florida, United States of America 7 Departamento de Biología, Universidad de Las Palmas de Gran Canaria, Campus de Tafira, Las Palmas de Gran Canaria, Spain 1 National Rese |
| AuthorAffiliation_xml | – name: 13 Laboratório de Biodiversidade e Evolução Molecular, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil – name: 3 Archie Carr Center for Sea Turtle Research and Department of Biology, University of Florida, Gainesville, Florida, United States of America – name: 6 Marine Turtle Research Group, College of Life and Environmental Sciences, University of Exeter, Cornwall Campus, Peryn, Cornwall, United Kingdom – name: 14 Adnan Menderes University, Faculty of Science and Arts, Department of Biology, Aydin, Turkey – name: Natural History Museum of Denmark, Denmark – name: 5 Department of Animal Biology and IRBio, Faculty of Biology, University of Barcelona, Barcelona, Spain – name: 7 Departamento de Biología, Universidad de Las Palmas de Gran Canaria, Campus de Tafira, Las Palmas de Gran Canaria, Spain – name: 9 Department of Biology, University of Miami, Coral Gables, Florida, United States of America – name: 11 Projeto TAMAR-ICMBio, Salvador, BA, Brazil – name: 12 The Ocean Foundation, Washington, D.C., United States of America – name: 10 Zoology Department, Nelson Mandela Metropolitan University, Summerstrand Campus South, University Way, Summerstrand, Port Elizabeth, South Africa – name: 2 Marine Mammal and Turtle Division, Southwest Fisheries Science Center, National Atmospheric and Oceanic Administration Fisheries, La Jolla, California, United States of America – name: 8 Daniel B. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia, United States of America – name: 4 Unidad Académica Mazatlán, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mazatlán, Sinaloa, México – name: 1 National Research Council Research Associateship Program, Washington, D.C., United States of America |
| Author_xml | – sequence: 1 givenname: Brian M. surname: Shamblin fullname: Shamblin, Brian M. – sequence: 2 givenname: Alan B. surname: Bolten fullname: Bolten, Alan B. – sequence: 3 givenname: F. Alberto surname: Abreu-Grobois fullname: Abreu-Grobois, F. Alberto – sequence: 4 givenname: Karen A. surname: Bjorndal fullname: Bjorndal, Karen A. – sequence: 5 givenname: Luis surname: Cardona fullname: Cardona, Luis – sequence: 6 givenname: Carlos surname: Carreras fullname: Carreras, Carlos – sequence: 7 givenname: Marcel surname: Clusa fullname: Clusa, Marcel – sequence: 8 givenname: Catalina surname: Monzón-Argüello fullname: Monzón-Argüello, Catalina – sequence: 9 givenname: Campbell J. surname: Nairn fullname: Nairn, Campbell J. – sequence: 10 givenname: Janne T. surname: Nielsen fullname: Nielsen, Janne T. – sequence: 11 givenname: Ronel surname: Nel fullname: Nel, Ronel – sequence: 12 givenname: Luciano S. surname: Soares fullname: Soares, Luciano S. – sequence: 13 givenname: Kelly R. surname: Stewart fullname: Stewart, Kelly R. – sequence: 14 givenname: Sibelle T. surname: Vilaça fullname: Vilaça, Sibelle T. – sequence: 15 givenname: Oguz surname: Türkozan fullname: Türkozan, Oguz – sequence: 16 givenname: Can surname: Yilmaz fullname: Yilmaz, Can – sequence: 17 givenname: Peter H. surname: Dutton fullname: Dutton, Peter H. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24465810$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Contributor | Universitat de Barcelona |
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| Copyright | COPYRIGHT 2014 Public Library of Science 2014. This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. cc-by (c) Shamblin, B.M. et al., 2014 info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/3.0/es 2014 |
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| DOI | 10.1371/journal.pone.0085956 |
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| DocumentTitleAlternate | Genetic Stock Structure of Loggerhead Turtles |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceived and designed the experiments: BMS ABB FA-G KAB LC CC MC CMA CJN JTN RN LSS KRS OT PHD. Performed the experiments: BMS CC MC CMA JTN LSS STV OT CY. Analyzed the data: BMS ABB FA-G KAB LC CC MC CMA CJN JTN RN LSS KRS STV OT CY PHD. Contributed reagents/materials/analysis tools: BMS ABB FA-G KAB LC CC MC CMA CJN JTN RN LSS KRS STV OT CY PHD. Wrote the paper: BMS ABB FA-G KAB LC CC MC CMA CJN JTN RN LSS KRS STV OT CY PHD. Competing Interests: The authors have declared that no competing interests exist. |
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| SubjectTerms | Animal behavior Animals Atlantic Ocean Basins Biology Caretta caretta Cheloniidae Colonization Conservation of Natural Resources Data management Demographics Deoxyribonucleic acid Dermochelyidae Distribution patterns DNA DNA sequencing DNA structure DNA, Mitochondrial - genetics Earth Sciences Ecology Endangered & extinct species Female Filogeografia Foraging behavior Gene sequencing Genetic aspects Genetic diversity Genetic research Genetic screening Genetic structure Genetic Variation Genetics, Population Genètica de poblacions Geographical distribution Haplotypes Homing Homing behavior Indian Ocean Information management Management Marine ecology Mediterranean Sea Mitochondria - genetics Mitochondrial DNA Molecular Sequence Data Nesting Nucleotide sequence Ocean basins Oceans Phylogeny Phylogeography Population Genetics Population studies Populations Regional analysis Sea turtles Securities analysis Sequence Analysis, DNA Stocks Tortugues marines Turtles Turtles - genetics |
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| Title | Geographic Patterns of Genetic Variation in a Broadly Distributed Marine Vertebrate: New Insights into Loggerhead Turtle Stock Structure from Expanded Mitochondrial DNA Sequences |
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