Skip to main content

Advertisement

SpringerLink
Log in

Genetic composition, population structure and phylogeography of the loggerhead sea turtle: colonization hypothesis for the Brazilian rookeries

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The loggerhead sea turtle, Caretta caretta, is the most common species of sea turtle nesting in Brazil and is listed as endangered by the IUCN. Our study characterizes the genetic structure of loggerheads in Brazil based on mitochondrial DNA control region variability and presents a hypothesis for the colonization of Brazilian rookeries. We analyzed 329 samples from Brazilian rookeries and an oceanic foraging ground, and we compared our results with previously published data for other loggerhead populations. Brazilian rookeries had four haplotypes, none of which have been reported for rookeries outside Brazil. Six haplotypes were found in the foraging aggregation. The presence of the CC-A4 haplotype at all sampled sites and the low nucleotide diversity suggest a common origin for all rookeries, with CC-A4 being the ancestral haplotype of the Brazilian populations. The occurrence of three haplotypes in the foraging aggregation that are known only from rookeries outside of Brazil is consistent with the transoceanic migratory behavior of loggerheads. Our results indicated that the colonization of Brazilian rookeries probably occurred from the southern USA stock. This recent colonization most likely followed a north to south route along the Brazilian coastline, influenced by the Brazilian warm current. Our results further suggest the existence of two genetic population units of loggerheads in Brazil and corroborate natal homing behavior in loggerheads.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abreu-Grobois FA, Horrocks J, Formia A, Dutton P, LeRoux R, Vélez Zuazo J, Soares L, Meylan A (2006) New mtDNA D-loop primers which work for a variety of marine turtle species may increase the resolution of mixed stock analysis. In: Frick M, Panagopoulous A, Rees AF, Williams K (eds) Proceedings of the 26th annual symposium on sea turtle biology and conservation. International Sea Turtle Society, Athens, Greece. Available from http://www.iucnmtsg.org/genetics/meth/primers/abreu_grobois_etal_new_dloop_primers.pdf

  • ACCSTR (2008) Archie Carr center for sea turtle research. Marine turtle DNA sequence patterns. University of Florida. Available from http://www.accstr.ufl.edu/ccmtdna.html. Accessed 15 Jan 2009

  • 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

    CAS  PubMed  Google Scholar 

  • Birky CW, Maruyama T, Fuerst P (1983) An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103:513–527

    PubMed  Google Scholar 

  • Bjorndal KA, Bolten AB (2008) Annual variation in source contributions to a mixed stock: implications for quantifying connectivity. Mol Ecol 17:2185–2193

    Article  PubMed  Google Scholar 

  • Bolten AB (2003) Active swimmers—passive drifters: the oceanic juvenile stage of loggerheads in the Atlantic system. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Institution Press, Washington, DC, pp 63–78

    Google Scholar 

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

    Article  Google Scholar 

  • Bowen BW (2003) What is a loggerhead turtle? The genetic perspective. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Institution Press, Washington, DC, pp 7–27

    Google Scholar 

  • Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Mol Ecol 16:4886–4907

    Article  CAS  PubMed  Google Scholar 

  • Bowen BW, Kamezaki N, Limpus CL, Hughes GL, Meylan AB, Avise JC (1994) Global phylogeography of the loggerhead turtle (Caretta caretta) as indicated by mitochondrial DNA haplotypes. Evol Int J Org Evol 48:1820–1828

    Google Scholar 

  • Bowen BW, Abreu-Grobois FA, Balazs GH, Kamezaki N, Limpus CJ, Ferl RJ (1995) Trans-Pacific migrations of the loggerhead sea turtle demonstrated with mitochondrial DNA markers. Proc Natl Acad Sci USA 92:3731–3734

    Article  CAS  PubMed  Google Scholar 

  • Bowen BW, Bass AL, Chow S-M, Bostrom M, Bjorndal KA, Bolten AB, Okuyama T, Bolker BM, Epperly S, Lacasella E, Shaver D, Dodd M, Hopkins-Murphy SR, Musick JA, Swingle M, Rankin-Baransky K, Teas W, Witzell WN, Dutton PH (2004) Natal homing in juvenile loggerhead turtles (Caretta caretta). Mol Ecol 13:3797–3808

    Article  PubMed  Google Scholar 

  • Bowen BW, Grant WS, Hillis-Starr Z, Shaver DJ, Bjorndal KA, Bolten AB, Bass AL (2007) Mixed-stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea. Mol Ecol 16:49–60

    Article  CAS  PubMed  Google Scholar 

  • Bugoni L, Krause L, Petry MV (2001) Marine debris and human impacts on sea turtles in southern Brazil. Mar Poll Bull 42:1330–1334

    Article  CAS  Google Scholar 

  • Carr A (1986) Rips, FADS, and little loggerheads. Bioscience 36:92–100

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Carreras C, Pont S, Maffucci F, Pascual M, Barceló A, Bentivegna F, Cardona L, Alegre F, SantFélix M, Fernández G, Aguilar A (2006) Genetic structuring of immature loggerhead sea turtles (Caretta caretta) in the Mediterranean Sea reflects water circulation patterns. Mar Biol 149:1269–1279

    Article  Google Scholar 

  • Castelloe J, Templeton AR (1994) Root probabilities for intraspecific gene trees under neutral coalescent theory. Mol Phyl Evol 3:102–113

    Article  CAS  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Damato ME, Corach D (1996) Genetic diversity of populations of the freshwater shrimp Macrobrachium borelli (Cardidea, Palaemonidae) evaluated by RAPD analysis. J Crustac Biol 16:650–655

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Excoffier L, Slatkin M (1995) Maximum-likelihood estimation of molecular haplotype frequencies in a diploid population. Mol Biol Evol 12:921–927

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2006) ARLEQUIN version 3.01: an integrated software package for population genetics data analysis. University of Bern, Institute of Zoology, Switzerland. Available from http://cmpg.unibe.ch/software/arlequin3

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  Google Scholar 

  • Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–511

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    CAS  PubMed  Google Scholar 

  • Harpending HC, Batzer MA, Gurven M, Jorde LB, Rogers AL, Sherry ST (1998) Genetic traces of ancient demography. Proc Natl Acad Sci USA 95:1961–1967

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877

    Article  CAS  PubMed  Google Scholar 

  • IUCN (2008) International union for the conservation of nature and natural resources. 2008 IUCN red list of threatened species. Available from http://www.iucnredlist.org/. Accessed 15 Jan 2009

  • Kotas JE, dos Santos S, de Azevedo VG, Gallo BM, Barata PC (2004) Incidental capture of loggerhead (Caretta caretta) and leatherback (Dermochelys coriacea) sea turtles by the pelagic longline fishery off southern Brazil. Fish Bull 102:93–399

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Marcovaldi MA, Chaloupka M (2007) Conservation status of the loggerhead sea turtle in Brazil: an encouraging outlook. Endanger Species Res 3:133–143

    Article  Google Scholar 

  • Marcovaldi MA, Patri V, Thomé JC (2005) Projeto TAMAR-IBAMA: twenty-five years protecting Brazilian sea turtles through a community-based conservation programme. Marit Stud 3:39–62

    Google Scholar 

  • Marcovaldi MA, Sales G, Thomé JC, Dias da Silva AC, Gallo BM, Lima EH, Lima EP, Bellini C (2006) Sea turtles and fishery interactions in Brazil: identifying and mitigating potential conflicts. Mar Turtle Newsl 112:4–8

    Google Scholar 

  • Meylan AB (1982) Sea turtle migration-evidence from tag returns. In: Bjorndal KA (ed) Biology and conservation of sea turtles. Smithsonian Institution Press, Washington, DC, pp 91–100

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Pella J, Masuda M (2001) Bayesian methods for analysis of stock mixtures from genetic characters. Fish Bull 99:151–167

    Google Scholar 

  • Pritchard PCH, Trebbau P (1984) The turtles of Venezuela. Contributions in herpetology 2, society for the study of amphibians and reptiles. Fundación de Internados Rurales, Caracas

    Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evol Int J Org Evol 49:1280–1283

    Google Scholar 

  • Reece JS, Ehrhart LM, Parkinson CL (2006) Mixed stock analysis of juvenile loggerheads (Caretta caretta) in Indian River Lagoon, Florida: implications for conservation planning. Cons Gen 7:345–352

    Article  Google Scholar 

  • Reis EC (2008) Caracterização genética e filogeografia de populações de tartarugas marinhas da espécie Caretta caretta (Linnaeus, 1758) no litoral brasileiro. M.Sc. thesis, Universidade do Estado do Rio de Janeiro, Rio de Janeiro

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

    CAS  PubMed  Google Scholar 

  • Sales G, Giffoni BG, Barata PCR (2008) Incidental catch of sea turtles by the Brazilian pelagic longline fishery. J Mar Biol Assoc UK 88:853–864

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Shanker K, Ramadevi J, Choudhury C, Singh L, Aggarwal RK (2004) Phylogeography of olive ridley turtles (Lepidochelys olivacea) on the east coast of India: implications for conservation theory. Mol Ecol 13:1899–1909

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Snover ML (2002) Growth and ontogeny of sea turtles using skeletochronology: methods, validation and application to conservation. Ph.D. thesis, Duke University, Durham

  • Soto JMR, Serafini TZ, Celini AAO (2003) Beach strandings of sea turtles in the state of Rio Grande do Sul: an indicator of gillnet interaction along the southern Brazilian coast. In: Seminoff JA (ed) Proceedings of the 22nd annual symposium on sea turtle biology and conservation. NOAA Technical Memorandum NMFS-SEFSC-503, p 276

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

    CAS  PubMed  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    Google Scholar 

Download references

Acknowledgments

We are grateful to CENPES/PETROBRAS (Centro de Pesquisas da PETROBRAS) for supporting the “Mamíferos e Quelônios Marinhos” project, which included this study. The Projeto TAMAR-ICMBio staff collected the samples and provided the necessary field assistance. We acknowledge CAPES, PROCIÊNCIA-SR2-UERJ, FAPERJ and CNPq/MCT for fellowships and grants. The present study followed all ethical guidelines and legal requirements of Brazil for sampling an endangered species.

Author information

Authors and Affiliations

  1. Departamento de Genética, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524, Maracanã, Rio de Janeiro, RJ, 20550-013, Brazil

    E. C. Reis & G. Lôbo-Hajdu

  2. Fundação Centro Brasileiro de Proteção e Pesquisa das Tartarugas Marinhas, Projeto TAMAR-ICMBio, Rio Vermelho, Salvador, BA, 41950-970, Brazil

    L. S. Soares

  3. Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, Belo Horizonte, MG, 31270-010, Brazil

    S. M. Vargas & F. R. Santos

  4. Departamento de Ciências Biológicas, Pontifícia Universidade Católica de Minas Gerais, Av. Dom José Gaspar 500, Coração Eucarístico, Belo Horizonte, MG, 30550-610, Brazil

    R. J. Young

  5. Archie Carr Center for Sea Turtle Research and Department of Biology, University of Florida, PO Box 118525, Gainesville, FL, 32611, USA

    K. A. Bjorndal & A. B. Bolten

Authors
  1. E. C. Reis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. S. Soares
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. M. Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. R. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. J. Young
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. K. A. Bjorndal
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. B. Bolten
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. G. Lôbo-Hajdu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. Lôbo-Hajdu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(PDF 204 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reis, E.C., Soares, L.S., Vargas, S.M. et al. Genetic composition, population structure and phylogeography of the loggerhead sea turtle: colonization hypothesis for the Brazilian rookeries. Conserv Genet 11, 1467–1477 (2010). https://doi.org/10.1007/s10592-009-9975-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-009-9975-0

Keywords

Search

Navigation