Conservation Genetics

, Volume 7, Issue 5, pp 773–781 | Cite as

Extensive hybridization in hawksbill turtles (Eretmochelys imbricata) nesting in Brazil revealed by mtDNA analyses

  • P. Lara-Ruiz
  • G. G. Lopez
  • F. R. Santos
  • L. S. Soares
Short communication


Bahia state hosts over 90% of hawksbill (Eretmochelys imbricata) nests registered in the main nesting sites monitored by Projeto Tamar-IBAMA in Brazil. The genetic diversity of this hawksbill population (n=119) was assayed through the analyses of 752 bp of the mitochondrial DNA control region in nesting females. Seven distinct haplotypes, defined by 125 polymorphic sites, were found. Most of the individuals (n=67) display four typical hawksbill haplotypes, 50 individuals display two haplotypes characteristic of the loggerhead turtle (Caretta caretta) and two individuals had a haplotype affiliated with the olive ridley (Lepidochelys olivacea). These results demonstrate hybridization between the hawksbills and two species that nest along the Bahia coast. Of special interest is the high occurrence of loggerhead × hawksbill hybrids (42%), which display loggerhead mtDNA haplotypes but are characterized morphologically as hawksbills. The true hawksbill haplotypes present only three variable sites and low genetic diversity values (h=0.358±0.069; π=0.0005±0.0001). The occurrence of several nesting individuals with identical mtDNA from another species may also suggest a long history of introgression between species producing likely F2 or further generation hybrids. Marine turtle hybrids have been previously reported, but the high frequency observed in Bahia is unprecedented. Such introgression may influence evolutionary pathways for all three species, or may introduce novel morphotypes that develop apart from the parental species. The presence of a unique hybrid swarm has profound conservation implications and will significantly influence the development and implementation of appropriate management strategies for these species.

Key words

haplotype diversity hawksbill turtles hybridization introgression mitochondrial DNA 


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This study was made possible thanks to the support of the Brazilian Environmental Ministry (PROBIO) and to CENPES\PETROBRAS. The Projeto Tamar-Ibama staff collected the samples and provided the necessary field assistance while Libia W. Silva helped with sample processing at the laboratory. Special thanks to Dr F. Alberto Abreu-Grobois (Instituto de Ciencias del Mar y Limnología-Mazatlán) who kindly provided the primers sequences and advised us throughout this research. We also would like to thank Dr Brian Bowen, Dr Julia Horrocks and three anonymous reviewers for their comments on early versions of the manuscript.


  1. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Tree 16, 613–622Google Scholar
  2. Bass AL (1999) Genetic analysis to elucidate the natural history and behavior of hawksbill turtles (Eretmochelys imbricata) in the wider Caribbean: a review and re-Analysis. Chelonian Cons. Biol. 3(2), 195–199Google Scholar
  3. Bass AL, Good DA, Bjorndal KA, Richardson JI, Hillis ZM, Horrocks JA, Bowen BW (1996) Testing models of female reproductive migratory behavior and population structure in the Caribbean hawksbill turtle, Eretmochelys imbricata, with mtDNA sequences. Mol. Ecol. 5, 321–328PubMedCrossRefGoogle Scholar
  4. Bolten AB, Bjorndal KA, Martins HR, Dellinger T, Biscoito MJ, Encalada SE, Bowen BW (1998) Transatlantic developmental migrations of loggerhead sea turtles demonstrated by mtDNA sequence analysis. Ecol. Appl. 8, 1–7CrossRefGoogle Scholar
  5. Bowen BW, Karl SA (1996) Population genetics, phylogeography and molecular evolution. In: Biology of Sea Turtles (eds. Lutz P, Musick JA), pp. 29–50. CRC Press, Boca Raton, FloridaGoogle Scholar
  6. Bowen BW, Bass AL, Soares L, Toonen RJ (2005) Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Mol. Ecol. 14(8), 2389–2402PubMedCrossRefGoogle Scholar
  7. Bowen BW, Clark AM, Abreu-Grobois FA, Chaves A, Reichart HA, Ferl RJ (1997) Global phylogeography of the ridley sea turtles (Lepidochelys spp.) as inferred from mitochondrial DNA sequences. Genetica 101, 179–189PubMedCrossRefGoogle Scholar
  8. 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 Tech. Memo. NMFSSEFSC-396Google Scholar
  9. Broderick D, Moritz C, Miller JD, Guinea M, Prince RJ, Limpus CJ (1994) Genetic studies of the hawksbill turtle Eretmochelys imbricata: evidence for multiple stocks in Australian waters. Pac. Cons. Biol. 1, 123–131Google Scholar
  10. Conceição MB, Levy JA, Marcovaldi MA (1990) Eletrophoretic characterization of a hybrid between Eretmochelys imbricata and Caretta caretta (Cheloniidae). Comp. Biochem. Physiol. B 97, 275–278CrossRefGoogle Scholar
  11. Díaz-Fernández R, Okayama T, Uchiyama T, Carrillo E, Espinosa G, Márquez R, Diez C, Koike H (1999) Genetic sourcing for the hawksbill turtle, Eretmochelys imbricata, in the northern Caribbean region. Chelonian Cons. Biol. 3, 296–300Google Scholar
  12. Eckert KL, Bjorndal KA, Abreu-Gobrois FA, Donnelly M (1999) Research and Management Techniques for the Conservation of Sea Turtles. IUCN/SSC Marine Turtle Specialist Group Publication No. 4Google Scholar
  13. Ewing B, Hillier L, Wendi M, Green P (1998) Basecalling of automated sequencer traces using Phred I: accuracy assesment. Genome Res. 8, 175–185PubMedGoogle Scholar
  14. FitzSimmons NN, Limpus CJ, Moritz C (1997a) Philopatry of male marine turtles inferred from mitochondrial DNA markers. Proc. Natl. Acad. Sci. USA 94, 8912–8917CrossRefGoogle Scholar
  15. FitzSimmons NN, Moritz C, Limpus CJ, Pope L, Prince R (1997b) Geographic structure of mitochondrial and nuclear gene polymorphisms in Australian green turtle populations and male-biased gene flow. Genetics 147, 1843–1854Google Scholar
  16. Godfrey MH, D'Amato AF, Marcovaldi MA, Mrosovsky N (1999) Pivotal temperature and predicted sex rations for hatchling hawksball turtles from Brazil. Can. J. Zool. 77, 1465–1473CrossRefGoogle Scholar
  17. Gordon D, Abajian C, Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res. 8, 195–202PubMedGoogle Scholar
  18. Green P (1994) Phrap. Scholar
  19. Groombridge BC, Luxmoore RA (1989) The green turtle and hawksbill (Reptilia: Cheloniidae) world status, exploitation and trade. CITES Secretariat, 601 ppGoogle Scholar
  20. IUCN (2004) 2004 IUCN Red List of Threatened Species. <>. Downloaded on 14 December 2004Google Scholar
  21. Karl SA, Bowen BW, Avise JC (1995) Hybridization among the ancient mariners: characterization of marine turtle hybrids with molecular genetic assays. J. Hered. 86(4), 262–268PubMedGoogle Scholar
  22. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Arizona State University, ArizonaGoogle Scholar
  23. Marcovaldi MA, Marcovaldi GG (1999) Marine turtles of Brazil: the history and structure of Projeto TAMAR-IBAMA. Biol. Cons. 91, 35–41CrossRefGoogle Scholar
  24. Marcovaldi MA, Vieitas CF, Godfrey MH (1999) Nesting and conservation of hawksbill turtles (Eretmochelys imbricata) in northern Bahia, Brazil. Chelonian Cons. Biol. 3, 301–307Google Scholar
  25. Okayama T, Diaz R, Koike H, Diez CE, Márquez MR, Espinosa G (1996) Mitochondrial DNA analysis of the hawksbill turtle. I. Haplotype detection among samples in the Pacific and Atlantic Oceans. International Symposium on Network and Evolution of Molecular Information, 20–22 April, TokyoGoogle Scholar
  26. Pritchard PCH, Mortimer JA (1999) Taxonomy, external morphology, and species identification. In: Research and Management Techniques for the Conservation of Sea Turtles (eds. Eckert KL, Bjorndal KA, Abreu-Grobois FA, Donnelly M), pp. 21–38. IUCN/SSC Marine Turtle Specialist Group Publication No. 4Google Scholar
  27. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst. 27, 83–109CrossRefGoogle Scholar
  28. Rozas J, Sanches-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analysis by the coalescent and other methods. Bioinformatics 19, 2496–2497PubMedCrossRefGoogle Scholar
  29. Sambrook E, Fritsch F, Maniatis T (1989) Molecular Cloning, 2nd edn. Cold Spring Harbor Press, New YorkGoogle Scholar
  30. Seehausen O, VanAlphen JJM, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277, 1808–1811CrossRefGoogle Scholar
  31. Soares LS (2004) O uso da análise genética da região controle do mtDNA na identificação das populações de tartarugas cabeçudas (Caretta caretta, Linnaeus 1758) nas áreas de desova e captura incidental no litoral brasileiro. MSc Thesis, Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte, BrazilGoogle Scholar
  32. Troëng S, Dutton PH, Evans D (2005) Migration of hawksbill turtles Eretmochelys imbricata from Tortuguero, Costa Rica. Ecography 28, 394–402CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • P. Lara-Ruiz
    • 1
  • G. G. Lopez
    • 2
  • F. R. Santos
    • 1
  • L. S. Soares
    • 2
  1. 1.Laboratório de Biodiversidade e Evolução Molecular (LBEM), Instituto de Ciências BiológicasUniversidade Federal de Minas Gerais (UFMG)Belo HorizonteBrazil
  2. 2.Projeto Tamar-IbamaSalvadorBrazil

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