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Historical perspectives on population genetics and conservation of three marine turtle species

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Abstract

Considerable phylogeographic and population genetic research has been conducted on marine turtles. Less attention, however, has been paid to the historical patterns and processes that have led to present patterns of genetic structure, and particularly, how these populations have responded to major climatic changes in the past. To address these questions, we analyzed previously published mitochondrial haplotype data independently for three marine turtle species, the loggerhead (Caretta caretta), hawksbill (Eretmochelys imbricata), and green turtle (Chelonia mydas). Considering all three species, we conducted analyses on a total of 657 individuals from 36 nesting beaches in the Atlantic and Mediterranean. Our results suggest that much of the contemporary genetic structure has been significantly affected by complex patterns of historical population subdivision, long-distance dispersal, and restricted geneflow. These inferences also imply that the climatic and sea level fluctuations during the Pleistocene may have had contrasting effects on genetic structure (e.g., fragmenting versus homogenizing) and on population sizes. Estimates of historical and current effective population sizes further highlight differential demographic responses across species to historical climatic cycles. Collectively, our results provide evidence for the occurrence of historical refugia through climatic cycles and complex historical metapopulation dynamics, and identify common and unique patterns of metapopulation structure across species. These historical patterns provide a basis for predictive estimates of metapopulation responses to habitat loss, population extirpation, and global climatic change.

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References

  • WD Allmon G Rosenberg RW Portell K Schindler (1996) Diversity of Pliocene-Recent mollusks in the western Atlantic: Extinction, origination, and environmental change JBC Jackson AF Budd AG Coates (Eds) Evolution and Environment in Tropical America University of Chicago Press Chicago, IL

    Google Scholar 

  • WD Allmon (2001) ArticleTitleNutrients, temperature, disturbance, and evolution: A model for the late Cenozoic marine record of the western Atlantic Palaeogeog Palaeoclim. Palaeoecol. 166 9–26

    Google Scholar 

  • F Archaux (2003) ArticleTitleBirds and climate change Vie Milieu, 53 33–41

    Google Scholar 

  • S Aris-Brasou L Excoffier (1996) ArticleTitleThe impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism Mol. Biol. Evol. 13 494–504 Occurrence Handle8742638

    PubMed  Google Scholar 

  • Balaz GH (1980) Synopsis of the biological data on the green turtle in the Hawaiian Islands. NOAA Tech. Mem. NMFS-SWFC-7.

  • AL Bass DA Good KA Bjorndal JI Richardson ZM Hillis JA Horrocks BW Bowen (1996) ArticleTitleTesting models of female reproductive migratory behavior and population structure in the Caribbean hawksbill turtle, Eretmochelys imbricata, with mtDNA sequences Mol. Ecol. 5 321–328 Occurrence Handle1:CAS:528:DyaK28Xktlyntrs%3D Occurrence Handle8688954

    CAS  PubMed  Google Scholar 

  • G Bertorelle M Slatkin (1995) ArticleTitleThe number of segregating sites in expanding human populations, with implications for estimates of demographic parameters Mol. Biol. Evol. 12 887–892 Occurrence Handle1:CAS:528:DyaK2MXns1yqtrw%3D Occurrence Handle7476134

    CAS  PubMed  Google Scholar 

  • AB Bolten KA Bjorndal HR Martins T Dellinger MJ Biscoito SE Encalada BW Bowen (1998) ArticleTitleTransatlantic developmental migrations of loggerhead sea turtles demonstrated by mtDNA sequence analysis Ecol. Appl. 8 1–7

    Google Scholar 

  • AB Bolten BE Witherington (2003) Loggerhead Sea Turtles Smithsonian Institution Press Washington, DC 169–179

    Google Scholar 

  • BW Bowen AB Meylan JP Ross CJ Limpus GH Balazs JC Avise (1992) ArticleTitleGlobal population structure and natural history of the green turtle (Chelonia mydas) in terms of matriarchal phylogeny Evolution 46 865–881

    Google Scholar 

  • B Bowen JC Avise JI Richardson AB Meylan D Margaritoulis SR Hopkins-Murphy (1993) ArticleTitlePopulation Structure of Loggerhead Turtles (Caretta caretta) in the Northwestern Atlantic Ocean and Mediterranean Sea Conserv. Biol. 7 834–844

    Google Scholar 

  • B Bowen N Kamezaki CJ Limpus GR Hughes AB Meylan JC Avise (1994) ArticleTitleGlobal phylogeography of the loggerhead turtle (Caretta caretta) as indicated by mitochondrial haplotypes Evolution 48 1820–1828

    Google Scholar 

  • A Carr MH Carr AB Meylan (1978) ArticleTitleThe ecology and migrations of sea turtles: The West Caribbean green turtle colony Bull. Amer. Mus. Nat. Hist. 162 1–46

    Google Scholar 

  • A Carr (1987) ArticleTitleNew perspectives on the pelagic stage of sea turtle development Conserv. Biol. 1 103–121

    Google Scholar 

  • P Casale L Laurent G Gerosa R Argano (2002) ArticleTitleMolecular evidence of male-biased dispersal in loggerhead turtle juveniles J. Exp. Mar. Biol. Ecol. 2 139–145

    Google Scholar 

  • M Clement D Posada KA Crandall (2000) ArticleTitleTCS: A computer program to estimate genealogies Mol. Ecol. 9 1657–1659 Occurrence Handle1:CAS:528:DC%2BD3cXnvV2gtbw%3D Occurrence Handle11050560

    CAS  PubMed  Google Scholar 

  • AG Coates JA Obando (1996) The geological evolution of the Central American Isthmus JBC Jackson AF Budd AG Coates (Eds) Evol. Environ. Trop. Amer. University of Chicago Press Chicago, IL 21–56

    Google Scholar 

  • JL Crim (2002) ArticleTitleThe leatherback turtle, Dermochelys coriacea, exhibits both polyandry and polygyny Mol. Ecol., 11 2097–2106

    Google Scholar 

  • Cronin TM (1990) Evolution of Neogene and Quaternary Marine Ostracoda. United States Atlantic Coastal Plane: Evolution and speciation in Ostracoda, IV. US. Geol. Surv. Profrossional Paper 1367, 43 pp

  • A Diamond (1976) ArticleTitleBreeding biology and conservation of hawksbill turtles, Eretmochelys imbricata, on the Cousin Island, Seychelles Biol. Conserv., 9 199–215

    Google Scholar 

  • B Diekmann G. Kuhn (2002) ArticleTitleSedimentary record of the mid-Pleistocene climate transition in the southeastern South Atlantic (ODP Site 1090) Palaeogeog. Palaeoclim. Palaeoecol., 182 241–258

    Google Scholar 

  • CK Dodd SuffixJr. (1988) ArticleTitleSynopsis of the biological data on the loggerhead sea turtle Caretta caretta U.S. Fish and Wildlife Service Biological Report, 13 1–110

    Google Scholar 

  • LM Ehrhart DA Bagley WE Redfoot (2003) Loggerhead turtles in the Atlantic Ocean: geographic distribution, abundance, and population status AB Bolten BE Witherington (Eds) Loggerhead Sea Turtles Smithsonian Institution Washington, DC 157–174

    Google Scholar 

  • SE Encalada PN Lahanas KA Bjorndal AB Bolten MM Miyamoto BW Bowen (1996) ArticleTitlePhylogeography and population structure of the Atlantic and Mediterranean green turtle Chelonia mydas: A mitochondrial DNA control region sequence assessment Mol. Ecol., 5 473–483

    Google Scholar 

  • SE Encalada KA Bjorndal AB Bolten JC Zurita B Schroeder E Possardt CJ Sears BW Bowen (1998) ArticleTitlePopulation structure of the loggerhead turtle (Caretta caretta) nesting colonies in the Atlantic and Mediterranean as inferred from mitochondrial DNA control region sequences Mar. Biol., 130 567–575

    Google Scholar 

  • L Excoffier S Schneider (1999) ArticleTitleWhy hunter-gatherer populations do not show signs of Pleistocene demographic expansions Proc. Nat. Acad. Sci. USA, 96 10597–10602

    Google Scholar 

  • ESRI. Arc View 8.3. Dallas, TX

  • JW Fetzner KA Crandall (2003) ArticleTitleLinear habitats and the nested clade analysis: An empirical evaluation of geographic versus river distances using an Ozark crayfish (Decapoda: Cambaridae) Evolution, 57 2101–2118

    Google Scholar 

  • FitzSimmons NN (1998) Multiple paternity in green turtles. Proceedings of the Sixteenth Annual Symposium on Sea Turtle Biology and Conservation. NOAA Technical Memorandum NMFS-SEFSC-412, 45–46 pp.

  • NN FitzSimmons CJ Limpus JA Norman AR Goldizen JD Miller C Moritz (1997) ArticleTitlePhilopatry of male marine turtles inferred from mitochondrial DNA markers Proc. Nat. Acad. Sci., 94 8912–8917

    Google Scholar 

  • Y-X Fu (1997) ArticleTitleStatistical tests of neutrality of mutations against population growth, hitchhiking and background selection Genetics, 147 915–925

    Google Scholar 

  • Gitay H, Suárez A, Watson RT, Dokken DJ (2002) Climate Change and Biodiversity. Intergovernmental Panel on Climate Change, Technical Paper V, UNEP, 77 pp.

  • Hedgpeth JW (1954) An Introduction to the Zoogeography of the Northern Gulf of Mexico with Reference to the Invertebrate Fauna. Publication 3, Institute of Mar. Science, University of Texas Press, Port Aransas, TX, pp. 111–121.

  • Hoekert WEJ (2000) Multiple paternity in the olive ridley sea turtle. Proceedings of the Nineteenth Annual Symposium on Sea Turtle Biology and Conservation. U.S. Dept. Commerce. NOAA Technical Memorandum NMFS-SEFSC-443, 13–14 pp.

  • Hood GM (2003) PopTools version 2.5.9. Available on the internet. URL http://www.cse.csiro.au/poptools

  • SW Hostetler AC Mix (1999) ArticleTitleReassessment of ice-age cooling of the tropical ocean and atmosphere Nature, 399 673–676

    Google Scholar 

  • RR Hudson M Slatkin WP Maddison (1992) ArticleTitleEstimation of levels of geneflow from DNA sequence data Genetics, 132 583–589

    Google Scholar 

  • L Hughes (2000) ArticleTitleBiological consequences of global warming: Is the signal already apparent? Trends Ecol Evol., 15 56–61

    Google Scholar 

  • E Jansen U Bleil R Henrich L Kringstad B Slettemark (1988) ArticleTitlePaleoenvironmental changes in the Norwegian sea and the Northeast Atlantic during the last 2.8 m.y.: Deep Sea Drilling Project/Ocean Drilling Program sites 610, 642, 643, and 644 Paleocean., 3 563–581

    Google Scholar 

  • K Kameo (2002) ArticleTitleLate Pliocene Caribbean surface water dynamics and climatic changes based on calcareous nannofossil records Palaeogeog. Palaeoclim. Palaeoecol., 179 211–226

    Google Scholar 

  • SA Karl BW Bowen JC Avise (1992) ArticleTitleGlobal population structure and male-mediated gene flow in the green turtle (Chelonia midas): RFLP analyses of anonymous nuclear loci Genetics, 131 163–173

    Google Scholar 

  • LL Knowles WP Maddison (2002) ArticleTitleStatistical Phylogeography Mol. Ecol., 11 2623–2635

    Google Scholar 

  • L Laurent P Casale MN Bradai BJ Godley G Gerosa AC Broderick W Schroth B Schierwater AM Levy D Freggi EM Abd Ei-Mawla DA Hadoud HE Gomati M Domingo M Hadjichristophorou L Kornaraky F Demirayak CH Gautier (1998) ArticleTitleMolecular resolution of marine turtle stock composition in fishery bycatch: A case study in the Mediterranean Mol. Ecol., 7 1529–1542

    Google Scholar 

  • CJ Limpus JD Miller V Baker E McLachlan (1983) ArticleTitleThe hawksbill turtle, Eretmochelys imbricata, in north-eastern Australia: The Campbell Island rookery Austr. Wildl. Res., 10 187–197

    Google Scholar 

  • CJ Limpus JD Miller CJ Parmenter D Reimer N McLachlan R Webb (1992) ArticleTitleMigration of green (Chelonia mydas) and loggerhead (Caretta caretta) turtles to and from eastern Australian rookeries Wild. Res., 19 347–358

    Google Scholar 

  • Z Liu TD Herbert (2004) ArticleTitleHigh-latitude influence on the eastern equatorial Pacific climate in the early Pleistocene epoch Nature, 427 720–723

    Google Scholar 

  • SE Masta NM Laurent EJ Routman (2003) ArticleTitlePopulation genetic structure of the toad Bufo woodhousii: An empirical assessment of the effects of haplotype extinction on nested clade analysis Mol. Ecol., 12 1541–1554

    Google Scholar 

  • AB Meylan (1999) ArticleTitleStatus of the hawksbill turtle (Eretmochelys imbricata) in the Caribbean region Chelon. Cons. Biol., 3 177–184

    Google Scholar 

  • MK Moore RM Ball (2002) ArticleTitleMultiple paternity in loggerhead turtle (Caretta caretta) nests on Melbourne Beach, Florida: A microsatellite analysis Mol. Ecol., 11 281–288

    Google Scholar 

  • JA Motrimer A Carr (1987) ArticleTitleReproduction and migrations of the Ascension Island green turtle (Chelonia mydas) Copeia, 1987 103–113

    Google Scholar 

  • AEM Nairn FG Stehli (1986) The Ocean Basins and Margins Vol. 3 Plenum Press New York, NY

    Google Scholar 

  • M Nei (1973) ArticleTitleAnalysis of gene diversity in subdivided populations Proc. Nat. Acad. Sci., U.S.A. 70 3321–3323

    Google Scholar 

  • M Nei (1987) Molecular Evolutionary Genetics Columbia University Press Oxford, New York, NY

    Google Scholar 

  • CJ Parmenter (1983) ArticleTitleReproductive migration in the hawksbill turtle (Eretmochelys imbricata) Copeia, 1983 271–273

    Google Scholar 

  • Pearce AF (2001) Contrasting Population Structure of the Loggerhead Turtle (Caretta caretta) Using Mitochondrial and Nuclear DNA Markers. MS Thesis, University of Florida, Gainesville, FL.

  • D Posada KA Crandall AR Templeton (2000) ArticleTitleGeodis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes Mol. Ecol., 9 487–488

    Google Scholar 

  • PCH Pritchard P Trebbau (1984) The turtles of Venezuela. Contributions in Herpetology 2, Society for the Study of Amphibians and Reptiles Fundacion de Internados Rurales Caracas, Venezuela

    Google Scholar 

  • M Raymo DW Oppo W Curry (1977) ArticleTitleThe Mid-Pleistocene climate transition: A deep-sea carbon isotopic perspective Paleocean., 12 546

    Google Scholar 

  • MA Roberts TS Schwartz SA Karl (2004) ArticleTitleGlobal population structure and male-mediated gene flow in the green sea turtle (Chelonia mydas): Analysis of micro satellite loci Genetics, 166 1857–1870

    Google Scholar 

  • AR Rogers H Harpending (1992) ArticleTitlePopulation growth makes waves in the distribution of pairwise genetic differences Mol. Biol. Evol., 9 552–569

    Google Scholar 

  • AR Rogers (1995) ArticleTitleGenetic evidence for a Pleistocene population explosion Evolution, 49 608–615

    Google Scholar 

  • TL Root SH Schneider (2002) Climate change: Overview and implications for wildlife SH Schneider TL Root (Eds) Wildl. Respon. Clim. Change Island Press Washington, DC 1–56

    Google Scholar 

  • JJ Rozas C Sánchez-DelBarrio X Messeguer R Rozas (2003) ArticleTitleDnaSP, DNA polymorphism analyses by the coalescent and other methods Bioinformatics, 19 2496–2497

    Google Scholar 

  • S Schneider L Excoffier (1999) ArticleTitleEstimation of past demographic parameters from the distribution of pairwise differences when mutation rates vary among sites: Application to human mitochondrial DNA Genetics, 152 1079–1089

    Google Scholar 

  • Seminoff JA (2002) IUCN Red List Status Assessment for the Green Turtle (Chelonia mydas), Marine Turtle Specialist Group Status Assessment.

  • SM Stanley WF Ruddiman (1995) Neogene ice age in the North Atlantic region: Climatic changes, biotic effects, and forcing factors AH Knoll SM Stanley (Eds) Effects of Past Global Change on Life National Academy Press Washington, DC 118–133

    Google Scholar 

  • M Slatkin RR Hudson (1991) ArticleTitlePairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations Genetics, 129 555–562

    Google Scholar 

  • LC Stuart (1966) ArticleTitleThe environment of the Central American cold-blooded vertebrate fauna Copeia, 1966 684–699

    Google Scholar 

  • F Tajima (1983) ArticleTitleEvolutionary relationship of DNA sequences in fmite populations Genetics, 105 437–460

    Google Scholar 

  • F Tajima (1989) ArticleTitleStatistical method for testing the neutral mutation hypothesis by DNA polymorphism Genetics, 123 585–595

    Google Scholar 

  • F Tajima (1993) Measurement of DNA polymorphism N Takahata AG Clark (Eds) Mechanisms of Molecular Evolution Sinaur Associates. Inc. Sunderland, MA 37–59

    Google Scholar 

  • AR Templeton (2004) ArticleTitleStatistical phylogeography: Methods of evaluating and minimizing inference errors Mol. Ecol., 13 613–630

    Google Scholar 

  • AR Templeton (1998) ArticleTitleNested clade analyses of phylogeographic data: Testing hypotheses about geneflow and population history Mol. Ecol., 7 381–397

    Google Scholar 

  • AR Templeton KA Crandall CF Sing (1992) ArticleTitleA cladistic analysis of phenotypeic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III Cladogram estimation. Genetics, 132 619–633

    Google Scholar 

  • GR Walther E Post P Convey A Menzel C Parmesan TJC Beebee J-M Fromentin O Hoegh-Guldberg F Bairlein (2002) ArticleTitleEcological responses to recent climate change Nature, 416 389–395

    Google Scholar 

  • GA Watterson (1975) ArticleTitleOn the number of segregating sites in genetical models without recombination Theor. Pop. Biol., 7 256–276

    Google Scholar 

  • SD Webb (1990) Historical biogeography RL Myers JJ Ewell (Eds) Ecosystems of Florida University of Central Florida Press Orlando, FL 70–100

    Google Scholar 

  • JF Weishample DA Bagley LM Ehrhart (2004) ArticleTitleEarlier nesting by loggerhead sea turtles following sea surface warming Global Change Biol., 10 1425–1428

    Google Scholar 

  • H Westphal (1998) Carbonate platform slopes - a record of changing conditions: The Pliocene of the Bahamas Springer-Verlag Berlin

    Google Scholar 

  • WN Witzell AC Banner (1980) ArticleTitleThe hawksbill turtle (Eretmochelys imbricata) in Western Samoa Bull. Mar. Sci., 30 571–579

    Google Scholar 

  • S-M Zhang D-Q Wang Y-P Zhang (2003) ArticleTitleMitochondrial DNA variation, effective population size, and population history of the endangered Chinese sturgeon, Acipenser sinensis Conserv. Genetics, 4 673–683

    Google Scholar 

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Correspondence to Christopher L. Parkinson.

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Reece, J.S., Castoe, T.A. & Parkinson, C.L. Historical perspectives on population genetics and conservation of three marine turtle species. Conserv Genet 6, 235–251 (2005). https://doi.org/10.1007/s10592-004-7821-y

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