Skip to main content

Mitochondrial DNA diversity and phylogeography of endangered green turtle (Chelonia mydas) populations in Africa

Abstract

We analysed the genetic structure of seven nesting sites of the endangered green turtle (Chelonia mydas) in Africa using mitochondrial DNA control region sequences. Tissue samples were collected from 188 nesting females at six sites in West Africa and one in the Indian Ocean. A 488 bp fragment of the control region revealed 14 different haplotypes, 10 of which are previously undescribed. The most common haplotype (CM8) was observed in 157 individuals. All other haplotypes were closely related, except two divergent lineages: CM38, removed by four substitutions, and the three Indian Ocean haplotypes, distinguished by 31 substitutions. Significant differences in haplotype and nucleotide diversity were observed between Atlantic rookeries and among ocean basins. Analysis of molecular variance revealed high levels of differentiation between the Atlantic and the Indian Ocean populations but a much shallower Atlantic substructuring. Green turtle population genetic structure is thought to have been shaped by a dynamic succession of extinction and recolonisation of rookeries, by natal homing and occasional breakdown in nest-site fidelity. Mismatch distributions of pairwise differences between haplotypes at each rookery were found to be consistent with recent population expansion. We argue that demographic histories can be explained by scenarios at several temporal scales, including geological events, sea level fluctuations and more recent patterns of exploitation. We discuss management and conservation implications of our results for these threatened populations, identifying two ESUs (one in the Atlantic and one in the Indian ocean) and three MUs within the Atlantic.

This is a preview of subscription content, access via your institution.

References

  • Aka FT, Kusakabe M, Nagao K, Tanyileke G (2001) Noble gas isotopic compositions and water/gas chemistry of soda springs from the islands of Bioko, São Tome and Annobón, along with Cameroon Volcanic Line, West Africa. Appl. Geochem. 16: 323–338

    Article  CAS  Google Scholar 

  • Allard MW, Miyamoto MM, Bjorndal KA, Bolten AB, Bowen BW (1994) Support for natal homing in green turtles from mitochondrial DNA sequences. Copeia 1994: 34–41

    Article  Google Scholar 

  • Allen M., Engstrom AS, Meyers S, et al. (1998) Mitochondrial DNA sequencing of shed hairs and saliva on robbery caps: sensitivity and matching probabilities. J. Forensic Sci. 43: 453–464

    PubMed  CAS  Google Scholar 

  • Avise JC (1995) Mitochondrial DNA polymorphism and a connection between genetics and demography of relevance to conservation. Conserv. Biol. 9:686–690

    Article  Google Scholar 

  • Avise JC, Bowen BW, Lamb T, Meylan AB, Bermingham E (1992) Mitochondrial DNA evolution at a turtle's pace: evidence for low genetic variability and reduced microevolutionary rate in the Testudines. Mol. Biol. Evol., 9, 457–473

    Google Scholar 

  • Avise JC, Nelson WS, Bowen BW, Walker D (2000) Phylogeography of colonially nesting seabirds, with special reference to global matrilineal patterns in the sooty tern (Sterna fuscata). Mol. Ecol. 9: 1783–1792

    PubMed  Article  CAS  Google Scholar 

  • Bass AL, Good DA, Bjorndal KA, et al. (1996) Testing models of female reproductive migratory behaviour and population structure in the Caribbean hawksbill turtle, Eretmochelys imbricata, with mtDNA sequences. Mol. Ecol. 5: 321–328

    PubMed  Article  CAS  Google Scholar 

  • Bass AL, Lagueux CJ, Bowen BW (1998) Origin of green turtles, Chelonia mydas, at sleeping rooks off the northeast coast of Nicaragua. Copeia 1998: 1064–1069

    Article  Google Scholar 

  • Bass AL, Witzell WN (2000) Demographic composition of immature green turtles (Chelonia mydas) from the east central Florida coast: evidence from mtDNA markers. Herpetologica 56: 357–367

    Google Scholar 

  • Bolker B, Okuyama T, Bjorndal KA, Bolten AB (2003) Sea turtle stock estimation using genetic markers: accounting for sampling error of rare genotypes. Ecol. Appl. 13: 763–775

    Article  Google Scholar 

  • Bowen BW, Meylan AB, Avise JC (1989) An odyssey of the green turtle: Ascension Island revisited. P. Natl. Acad. Sci. USA 86: 573–576

    PubMed  Article  Google Scholar 

  • Bowen BW, Meylan AB, Ross JP, et al. (1992) Global poulation structure and natural history of the green turtle (Chelonia mydas) in terms of matriarchal phylogeny. Evolution 46: 865–881

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bowen BW, Abreu-Grobois FA, Balazs GH, et al. (1995) Trans-Pacific migrations of the loggerhead turtle (Caretta caretta) demonstrated with mitochondrial DNA markers. P. Natl. Acad. Sci. USA 92: 3731–3734

    PubMed  Article  CAS  Google Scholar 

  • Bowen BW, Bass AL, Garcia-Rodriguez A, et al. (1996) Origin of hawksbill turtles in a Caribbean feeding area as indicated by genetic markers. Ecol. Appl. 62: 566–572

    Article  Google Scholar 

  • Bowen BW, Clark AM, Abreu-Grobois FA, et al. (1998) Global phylogeography of the ridley sea turtles (Lepidochelys spp.) as inferred from mitochondrial DNA sequences. Genetica 101: 179–189

    Article  CAS  Google Scholar 

  • Briggs JC (1974) Marine Zoogeography. McGraw-Hill, New York

    Google Scholar 

  • Broderick D, Moritz C (1996) Hawksbill breeding and foraging populations in the Indo-Pacific region. In: Proceedings of the International Symposium on Sea Turtle Conservation Genetics (eds. Bowen BW, Witzell WN), pp. 119–128. NOAA Technical Memorandum NMFS-SEFSC-396, US Department of Commerce

  • Butynski TM, Koster SH (1989) Marine turtles on Bioko Island (Fernando Poo), Equatorial Guinea: a call for research and conservation. WWF unpublished report, Washington, DC

  • Carr A (1975) The Ascension Island green turtle colony. Copeia 3: 547–555

    Article  Google Scholar 

  • Carr A, Coleman PJ (1974) Seafloor spreading theory and the odyssey of the green turtle. Nature 249: 12–130

    Article  Google Scholar 

  • Catry P, Barbosa C, Indjai B, Almeida A, Godley BJ, Vié JC (2002) Biology and conservation of the green turtle (Chelonia mydas) nesting at Poilão, Bijagós Archipelago (Guinea Bissau). Oryx 36: 400–403

    Article  Google Scholar 

  • Clement M, Posada D, Cradall KA (2000) TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9: 1657–1660

    Article  PubMed  CAS  Google Scholar 

  • Dutton PH (1996a) Methods for collection and preservation of samples for sea turtle genetic studies. In: Proceedings of the International Symposium on Sea Turtle Conservation Genetics (eds. Bowen BW, Witzell WN), pp. 17–24. NOAA Technical Memorandum NMFS-SEFSC-396, US Department of Commerce

  • Dutton PH (1996b) Use of molecular markers for stock identification, fingerprinting, and the study of mating behavior in leatherback turtles. In: Proceedings of the International Symposium on Sea Turtle Conservation Genetics (eds. Bowen BW, Witzell WN), pp. 79–86. NOAA Technical Memorandum NMFS-SEFSC-396, US Department of Commerce

  • Dutton PH (2003) Molecular ecology of Chelonia mydas in the Eastern Pacific Ocean. In: Proceedings of the 22nd Annual Symposium on Sea Turtle Conservation and Biology (ed. Seminoff JA), p. 69. NOAA Technical Memorandum NMFS-SEFSC-503, US Department of Commerce

  • Dutton PH, Bowen BW, Owens DW, Barragan A, Davis SK (1999) Global phylogeography of the leatherback turtle (Dermochelys coriacea). J. Zool. 248: 397–409

    Article  Google Scholar 

  • Emerick DM, Duncan RA (1982) Age progressive volcanism in the Comores Archipelago, western Indian Ocean and implications for Somali plate tectonics. Earth Planet Sc. Lett. 60: 415–428

    Article  CAS  Google Scholar 

  • Encalada SE, Lahanas PN, Bjorndal KA, et al. (1996) Phylogeography and population structure of the Atlantic and Mediterranean green turtle Chelonia mydas: a mitochondrial DNA control region sequence assessment. Mol. Ecol. 5: 473–483

    PubMed  Article  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to mitochondrial DNA restriction data. Genetics 131: 479–491

    PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse PE (1994) Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. Genetics 136: 343–359

    PubMed  CAS  Google Scholar 

  • FitzSimmons NN, Moritz C, Moore SS (1995) Conservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Mol. Biol. Evol. 12:432–440

    PubMed  CAS  Google Scholar 

  • FitzSimmons NN, Moritz C, Limpus CJ, Pope L, Prince R (1997) Geographic structure of mitochondrial and nuclear gene polymorphisms in Australia green turtle populations and male-biased gene flow. Genetics 147: 1843–1854

    PubMed  CAS  Google Scholar 

  • Fretey J (2001) Biogeography and Conservation of Marine Turtles of the Atlantic Coast of Africa. CMS Technical Publication No. 6. UNEP/CMS Secretariat, Bonn

  • Formia A (1999) Les tortues marines de la Baie de Corisco. Canopée 14: i–ii

    Google Scholar 

  • Godley BJ, Broderick AC, Hays GC (2001) Nesting of green turtles (Chelonia mydas) at Ascension Island, South Atlantic. Biol. Conserv. 97:151–158

    Article  Google Scholar 

  • Harpending HC, Batzer MA, Gurven M, et al. (1998) Genetic traces of ancient demography. P. Natl. Acad. Sci. USA 95: 1961–1967

    PubMed  Article  CAS  Google Scholar 

  • Hirth HF (1997) Synopsis of the Biological Data on the Green Turtle Chelonia mydas (Linnaeus 1758). United States Fish and Wildlife Service Biological Report 97-1

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

    PubMed  CAS  Google Scholar 

  • Kichler K, Owens DW, Marquez R, Davis S (1998) Population bottleneck: how much genetic damage has man done to the Kemp’s ridley? In: Proceedings of the Sixteenth Annual Symposium on Sea Turtle Biology and Conservation (eds. Byles R, Fernandez Y), p. 83. NOAA Technical Memorandum NMFS-SEFSC-412, US Department of Commerce

  • Kumazawa Y, Nishida M (1999) Complete mitochondrial DNA sequences of the green turtle and blue-tailed mole skink: statistical evidence for archosaurian affinity of turtles. Mol. Biol. Evol. 16: 784–792

    PubMed  CAS  Google Scholar 

  • Lahanas PN, Bjorndal KA, Bolten AB, et al. (1998) Genetic composition of a green turtle (Chelonia mydas) feeding ground population: evidence for multiple origins. Mar. Biol. 130: 345–352

    Article  Google Scholar 

  • Lahanas PN, Miyamoto MM, Bjorndal KA, Bolten AB (1994) Molecular evolution and population genetics of Greater Caribbean green turtles (Chelonia mydas) as inferred from mitochondrial DNA control region sequences. Genetica 94: 57–67

    PubMed  Article  CAS  Google Scholar 

  • Laurent L, Casale P, Bradai MN, et al. (1998) Molecular resolution of marine turtle stock composition in fishery bycatch: a case study in the Mediterranean. Mol. Ecol. 7: 1529–1542

    PubMed  Article  CAS  Google Scholar 

  • Lee DC, Halliday AN, Fitton JG, Poli G (1994) Isotopic variations with distance and time in the volcanic islands of the Cameroon line: evidence for a mantle plume origin. Earth Planet Sc. Lett. 123: 119–138

    Article  CAS  Google Scholar 

  • Le Gall JY, Hughes GR (1987) Migrations de la tortue verte Chelonia mydas dans l’Océan Indien Sud-Ouest observées à partir des marquages sur les sites de ponte Europa et Tromelin (1970–1985). Amphibia-Reptilia 8: 277–282

    Article  Google Scholar 

  • Meylan AB, Bowen BW, Avise JC (1990) A genetic test of the natal homing versus social facilitation models for green turtle migration. Science 248: 724–727

    PubMed  Article  CAS  Google Scholar 

  • Milligan BG (1998) Total DNA isolation. In: Hoelzel AR (ed) Molecular Genetic Analysis of Populations, A Practical Approach, 2nd edn. IRL Press, Oxford, pp. 29–64

    Google Scholar 

  • Moritz C (1994a) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol. Evol. 9: 373–375

    Article  Google Scholar 

  • Moritz C (1994b) Applications of mitochondrial DNA analysis in conservation: a critical review. Mol. Ecol. 3: 401–411

    Article  CAS  Google Scholar 

  • Mortimer JA (1995) Factors influencing beach selection by nesting sea turtles. In: Bjorndal KA (ed) Biology and Conservation of Sea Turtles, Revised Edition. Smithsonian Institution Press, Washington DC, pp. 45–51

    Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29: 1–10

    Article  Google Scholar 

  • Norman JA, Moritz C, Limpus CJ (1994) Mitochondrial DNA control region polymorphisms: genetic markers for ecological studies of marine turtles. Mol. Ecol. 3: 363–373

    PubMed  Article  CAS  Google Scholar 

  • O’Corry-Crowe GM, Suydam RS, Rosenberg A, Frost KJ, Dizon AE (1997) Phylogeography, population structure and dispersal patterns of the beluga whale Delphinapterus leucas in the western Nearctic revealed by mitochondrial DNA. Mol. Ecol. 6: 955–970

    Article  CAS  Google Scholar 

  • Peare T, Parker PG (1996) Local genetic structure within two rookeries of Chelonia mydas (the green turtle). Heredity 77: 619–628

    PubMed  Article  Google Scholar 

  • Roberts MA, Schwartz TS, Karl SA (2004) Global population genetic structure and male-mediated gene flow in the green sea turtle (Chelonia mydas): analysis of microsatellite loci. Genetics 166: 1857–1870

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Rohling EJ, Fenton M, Jorissen FJ, Bertrand P, Ganssen G, Caulet JP (1998) Magnitudes of sea-level lowstands of the past 500,000 years. Nature 394: 162–165

    Article  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (1996,1997,1998) Primer3. Code available at http://www-genome.wi.mit.edu/genome_software/other/primer3.html

  • Sanderson MJ (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19: 301–302

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: A software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland

    Google Scholar 

  • Seminoff JA, Crouse D, Abreu-Grobois FA (2002) 2002 IUCN Red List Status Assessment- Green Turtle (Chelonia mydas). Marine Turtle Specialist Group, unpublished report

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236: 787–792

    PubMed  Article  CAS  Google Scholar 

  • Takahata N, Palumbi SR (1985) Extranuclear differentiation and gene flow in the finite island model. Genetics 109: 441–457

    PubMed  Google Scholar 

  • Tomás J, Castroviejo J, Raga JA (2000) Sea turtles in the south of Bioko Island (Equatorial Guinea), Africa. In: Proceedings of the Nineteenth Annual Symposium on Sea Turtle Conservation and Biology (eds. Kalb H, Wibbels T), pp. 247–250. NOAA Technical Memorandum NMFS-SEFSC-443, US Department of Commerce

  • *UNEP/CMS (2000) Conservation Measures for Marine Turtles of the Atlantic Coast of Africa. CMS Technical Series Publication No. 5, UNEP/CMS Secretariat, Bonn

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370

    Article  Google Scholar 

Download references

Acknowledgements

Numerous people and organisations provided invaluable field assistance. Sampling in São Tome and Principe was possible thanks to J. Fretey (Museum National d’Histoire Naturelle-Paris, PROTOMAC- Protection Tortues Marines d’Afrique Centrale), A. Billes (PROTOMAC), C.␣Aveling, J. Rosseel, O. Neves and B. Giannuzzi-Savelli (ECOFAC- Conservation et Utilisation Rationnelle des Ecosystemes Forestiers d’Afrique Centrale, funded by the European Union). Sampling in Equatorial Guinea was supported by L.␣Arranz and J. Mba (ECOFAC), R. Castelo Alvarez (Asociación Amigos de Doñana, Bioko), J.E. Garcia, J.C. Serrano and Julian Nzi Mba (CUREF – Conservación y Utilización Racional de los Ecosistemas Forestales, funded by the European Union), D. Eparalele (Ureca), C. Epota Nassau (Corisco). Sampling on Ascension Island was assisted by A.C. Broderick, F. Glenn and G.C. Hays (University of Wales, Swansea, UK) in association with the Ascension Island Turtle Group (as part of projects funded by the Ascension Island Administrator, Darwin Initiative, Foreign and Commonwealth Office Environment Fund and NERC – Natural Environment Research Council, UK). Sampling in Guinea Bissau was supported by P. Catry, C. Barbosa, A.␣Almeida, B. Indjai, P.J. Perrida, J. da Silva (IUCN, Ministry of Agriculture and Rural Development, Centre for Applied Research on Fisheries, National Institute for Research, the People of Canhabaque). Sampling in Comoros was carried out by S. Ahamada (Marine Conservation Programme – AIDE). We gratefully acknowledge the following for granting permits: Direcçao Geral das Florestas e Caça (Guinea Bissau), Ministere de la Production et de l’Environnement (Comoros), Ministério da Agricultura e Desenvolvimento Rural (São Tome and Principe), Ministerio de Bosques y Medio Ambiente (Equatorial Guinea), Department of the Environment Transport and the Regions (UK). We are also grateful to G. Hewitt, G.C. Hays and J.␣Tomás for helpful suggestions, Paola Ciccarelli for her help with some analysis, and two anonymous reviewers for valuable comments on the manuscript. This work was supported by a grant from the Marie Curie Training and Mobility of Researchers Programme of the European Union to A.F., by European Union support to ECOFAC in São Tome and Principe (J.-F.D.), and by grants from the Convention on Migratory Species, the Fondation Internationale du Banc D’Arguin, NERC and People’s Trust for Endangered Species to B.J.G.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Formia.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Formia, A., Godley, B., Dontaine, JF. et al. Mitochondrial DNA diversity and phylogeography of endangered green turtle (Chelonia mydas) populations in Africa. Conserv Genet 7, 353–369 (2006). https://doi.org/10.1007/s10592-005-9047-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-005-9047-z

Key words:

  • Africa
  • control region haplotypes
  • population structure
  • sea turtles
  • phylogeography