Skip to main content
Log in

Comparison of reproductive output of hybrid sea turtles and parental species

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Globally, sea turtle hybridization has been reported at very low frequencies. However, in Brazil, a high incidence (>40% of morphologically assigned hawksbills) of hybridization between loggerheads and hawksbills has been reported. To the best of our knowledge, this is the first analysis of the effect of hybridization on the reproductive output of sea turtle hybrids. We used nuclear and mitochondrial markers to assign a status of hawksbill (Eretmochelys imbricata), loggerhead (Caretta caretta), or hybrid to 146 females that deposited 478 nests. Hybrids do not appear to be at either a reproductive advantage or disadvantage relative to their parental species based on the parameters analyzed (female curved carapace length, clutch size, emergence success, incubation period, hatchling production, observed clutch frequency, and observed breeding frequency). Although emergence success is lower in hybrids, hatchling production per clutch, as well as clutch frequency and breeding frequency, is similar among the three groups. These results show that hybrids may persist in this region. Further research on hybrid survival rates at different life stages, as well as growth rates and their ecological roles, will be fundamental to predict the fate of hybrid turtles. Sea turtle populations that overlap with other sea turtle species in space and time on nesting beaches should be screened for hybridization with the appropriate genetic markers.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R, Butlin RK, Dieckmann U, Eroukhmanoff F, Grill A, Cahan SH, Hermansen JS, Hewitt G, Hudson AG, Jiggins C, Jones J, Keller B, Marczewski T, Mallet J, Martinez-Rodriguez P, Möst M, Mullen S, Nichols R, Nolte AW, Parisod C, Pfennig K, Rice AM, Ritchie MG, Seifer B, Smadja CM, Stelkens R, Szymura JM, Väinölä R, Wolf JBW, Zinner D (2013) Hybridization and speciation. J Evol Biol 26:229–246. doi:10.1111/j.1420-9101.2012.02599.x

    Article  CAS  Google Scholar 

  • Alatalo RV, Gustafsson L, Lundberg A (1982) Hybridization and breeding success of collared and pied flycatchers on the island of gotland. Am Ornithol 99:285–291

    Google Scholar 

  • Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622

    Article  Google Scholar 

  • Arnold ML, Hodges SA (1995) Are natural hybrids fit or unfit relative to their parents? TREE 10:67–71

    CAS  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

    CAS  Google Scholar 

  • Benson JF, Hostetler JA, Onorato DP, Johnson WE, Roelke ME, O’Brien SJ, Jansen D, Oli MK (2011) Intentional genetic introgression influences survival of adults and sub-adults in a small, inbred felid population. J Anim Ecol 80:958–967

    Article  Google Scholar 

  • Bickham JW (1981) Two-hundred-million-year-old chromosomes: deceleration of the rate of karyotypic evolution in turtles. Science 212:1291–1293

    Article  CAS  Google Scholar 

  • Bjorndal KA, Parsons J, Mustin W, Bolten AB (2013) Threshold to maturity in a long-lived reptile: interactions of age, size, and growth. Mar Biol 160:607–616

    Article  Google Scholar 

  • Bolten A (1990) Techniques for measuring turtles. In: Eckert KL, Bjorndal KA, Abreu-Grobois FA, Donnelly M. (eds) Research and management techniques for the conservation of sea turtles. IUCN/SSC Marine Turtle Specialist Group Publication No. 4, pp 110–114

  • Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Mol Ecol 16:4886–4907. doi:10.1111/j.1365-294X.2007.03542.x

    Article  CAS  Google Scholar 

  • Bowen BW, Bass AL, Soares L, Toonen RJ (2005) Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Mol Ecol 14:2389–2402. doi:10.1111/j.1365-294X.2005.02598.x

    Article  CAS  Google Scholar 

  • Chaloupka MY, Limpus CJ (1997) Robust statistical modelling of hawksbill sea turtle growth rates (southern Great Barrler Reef). Mar Ecol Prog Ser 146:1–8

    Article  Google Scholar 

  • Conceicao MB, Levy JA, Marins LF, Marcovaldi MA (1990) Electrophoretic characterization of a hybrid between Eretmochelys imbricata and Caretta caretta (Cheloniidae). Comp Biochem Physiol 97B:275–278

    CAS  Google Scholar 

  • Ehrhart LM (1995) A review of sea turtle reproduction. In: Bjorndal KA (ed) Biology and conservation of sea turtles. Smithsonian Institution Press, Washington, pp 29–38

    Google Scholar 

  • Ferreira AGA, Amos W (2006) Inbreeding depression and multiple regions showing heterozygote advantage in Drosophila melanogaster exposed to stress. Mol Ecol 15:3885–3893

    Article  CAS  Google Scholar 

  • Flockhar DTT, Wiebe KL (2009) Absence of reproductive consequences of hybridization in the Northern Flicker (Colaptes auratus) hybrid zone. Auk 126:351–358. doi:10.1525/auk.2009.08086

    Article  Google Scholar 

  • Frazier J (1988) Sea turtles in the land of the dragon. Sanctuary (Asia) 8:15–23

    Google Scholar 

  • Garman S (1888) Reptiles and batrachians from the Caymans and the Bahamas. Bull Essex Inst 20:1–13

    Article  Google Scholar 

  • Glen F, Mrosovsky N (2004) Antigua revisited: the impact of climate change on sand and nest temperatures at a hawksbill turtle (Eretmochelys imbricata) nesting beach. Glob Change Biol 10:2036–2045

    Article  Google Scholar 

  • Godfrey MH, Amato AFD, Marcovaldi MÂ, Mrosovsky N (1999) Pivotal temperature and predicted sex ratios for hatchling hawksbill turtles from Brazil. Can J Zool 77:1465–1473

    Article  Google Scholar 

  • Hoffman W, Wiens JA, Scott JM (1978) Hybridization between gulls (Larus glaucescens and L. occidentalis) in the Pacific Northwest. Auk 95:441–458

    Google Scholar 

  • Hostetler JA, Onorato DP, Nichols JD, Johnson WE, Roelke ME, O’Brien SJ, Jansen D, Oli MK (2010) Genetic introgression and the survival of Florida panther kittens. Biol Conserv 143:2789–2796

    Article  Google Scholar 

  • Hostetler JA, Onorato DP, Bolker BM, Johnson WE, O’Brien SJ, Jansen D, Oli MK (2012) Does genetic introgression improve female reproductive performance? A test on the endangered Florida panther. Oecologia 168:289–300. doi:10.1007/s00442-011-2083-0

    Article  Google Scholar 

  • Kamezaki N (1983) The possibility of hybridization between the loggerhead turtle, Caretta caretta, and the hawksbill turtle, Eretmochelys imbricata, in specimens hatched from eggs collected in Chita Peninsula. Jpn J Herpetol 10:52–53

    Google Scholar 

  • Kearse M, Moir R, Wilson A et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  Google Scholar 

  • Kelez S, Velez-Zuazo X, Pacheco AS (2016) First record of hybridization between green Chelonia mydas and hawksbill Eretmochelys imbricata sea turtles in the Southeast Pacific. PeerJ 4:e1712

    Article  Google Scholar 

  • Lara-Ruiz P, Lopez GG, Santos FR, Soares LS (2006) Extensive hybridization in hawksbill turtles (Eretmochelys imbricata) nesting in Brazil revealed by mtDNA analyses. Conserv Genet 7:773–781

    Article  CAS  Google Scholar 

  • Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Marcovaldi MA, Laurent A (1996) A six season study of marine turtle nesting at Praia do Forte, Bahia, Brazil, with implications for conservation and management. Herpetologica 2:55–59

    Google Scholar 

  • Marcovaldi MA, Marcovaldi GG (1999) Marine turtles of Brazil: the history and structure of Projeto TAMAR-IBAMA. Biol Conserv 91:35–41. doi:10.1016/S0006-3207(99)00043

    Article  Google Scholar 

  • Marcovaldi MA, Godfrey MH, Mrosovsky N (1997) Estimating sex ratios of loggerhead turtles in Brazil from pivotal incubation durations. Can J Zool 75:755–770

    Article  Google Scholar 

  • Marcovaldi MA, Lopez GG, Soares LS, Santos AJB, Bellini C, Barata PCR (2007) Fifteen years of hawksbill sea turtle (Eretmochelys imbricata) nesting in Northern Brazil. Chelonian Conserv Biol 6:223–228

    Article  Google Scholar 

  • Marcovaldi MA, Santos AJB, Santos AS, Soares LS, Lopez GG, Godfrey MH, Fuentes MMPB (2014) Spatio-temporal variation in the incubation duration and sex ratio of hawksbill hatchlings: implication for future management. J Therm Biol 44:70–77. doi:10.1016/j.jtherbio.2014.06.010

    Article  Google Scholar 

  • Naro-Maciel E, Le M, FitzSimmons NN, Amato G (2008) Evolutionary relationships of marine turtles: a molecular phylogeny based on nuclear and mitochondrial genes. Mol Phylogenet Evol 49:659–662

    Article  CAS  Google Scholar 

  • Ortego J, Calabuig G, Cordero PJ, Aparicio JM (2007) Egg production and individual genetic diversity in lesser kestrels. Mol Ecol 16:2383–2392

    Article  CAS  Google Scholar 

  • Proietti MC, Reisser J, Marins LF, Marcovaldi MA, Soares LS, Monteiro DS, Wijeratne S, Pattiaratchi C, Secchi ER (2014a) Hawksbill × loggerhead sea turtle hybrids at Bahia, Brazil: where do their offspring go? PeerJ 2:e255

    Article  Google Scholar 

  • Proietti MC, Reisser J, Marins LF, Rodriguez-Zarate C, Marcovaldi MA, Monteiro DS, Pattiaratchi C, Secchi ER (2014b) Genetic structure and natal origins of immature hawksbill turtles (Eretmochelys imbricata) in Brazilian waters. PLoS ONE. doi:10.1371/journal.pone.0088746

    Google Scholar 

  • Prosdocimi L, Bruno I, Diaz L, Carman VG, Albareda DA, Remis MI (2014) Southernmost reports of the hawksbill sea turtle, Eretmochelys imbricata, in temperate waters of Argentina and evidence of a hybrid origin supported by Mitochodrial DNA analysis. Herpetol Rev 451:1–5

    Google Scholar 

  • Reis EC, Soares LS, Vargas SM, Santos FR, Young RJ, Bjorndal KA, Bolten AB, Lobo-Hajdu G (2010a) Genetic composition, population structure and phylogeography of the loggerhead sea turtle: colonization hypothesis for the Brazilian rookeries. Conserv Genet 11:1467–1477. doi:10.1007/s10592-009-9975-0

    Article  Google Scholar 

  • Reis EC, Soares LS, Lôbo-Hajdu G (2010b) Evidence of olive ridley mitochondrial genome introgression into loggerhead turtle rookeries of Sergipe, Brazil. Conserv Genet 11:1587–1591

    Article  CAS  Google Scholar 

  • Rhymer M, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Shamblin BM, Bolten AB, Abreu-Grobois FA, Bjorndal KA, Cardona L, Carreras C, Clusa M, Monzón-Argüello C, Nairn CJ, Nielsen JT, Nel R, Soares LS, Stewart KR, Vilaça ST, Türkozan O, Yilmaz C, Dutton PH (2014) Geographic patterns of genetic variation in a broadly distributed marine vertebrate: new insights into loggerhead turtle stock structure from expanded mitochondrial DNA sequences. PLoS ONE 9:e85956. doi:10.1371/journal.pone.0085956

    Article  Google Scholar 

  • Slate J, Kruuk LEB, Marshall TC, Pemberton JM, Clutton-Brock TH (2000) Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proc R Soc Lond B 267:1657–1662

    Article  CAS  Google Scholar 

  • Van Buskirk J, Crowder LB (1994) Life-history variation in marine turtles. Copeia 1994:66–81

    Article  Google Scholar 

  • Vilaça ST, Vargas SM, Lara-Ruiz P, Molfetti E, Reis EC, Lobo-Hadju G, Soares LS, Santos FR (2012) Nuclear markers reveal a complex introgression pattern among marine turtle species on the Brazilian coast. Mol Ecol 21:4300–4312. doi:10.1111/j.1365-294X.2012.05685.x

    Article  Google Scholar 

  • Vilaça ST, Lara-Ruiz P, Marcovaldi MA, Soares LS, Santos FR (2013) Population origin and historical demography in hawksbill (Eretmochelys imbricata) feeding and nesting aggregates from Brazil. J Exp Mar Biol Ecol 446:334–344

    Article  Google Scholar 

  • Wood JR, Wood FE, Critchley K (1983) Hybridization of chelonia mydas and eretmochelys imbricata. Copeia 1983(3):839–842

    Article  Google Scholar 

  • Zangerl R (1980) Patterns of Phylogenetic Differentiation in the Toxochelyid and Cheloniid Sea Turtles. Am Zool 20:585–596. doi:10.1093/icb/20.3.585

    Article  Google Scholar 

  • Zárate P, Bjorndal KA, Parra M, Dutton PH, Seminoff JA, Bolten AB (2013) Hatching and emergence success in green turtle Chelonia mydas nests in the Galápagos Islands. Aquat Bio 19(3):217–229. doi:10.3354/ab00534

    Article  Google Scholar 

Download references

Acknowledgements

We are very grateful to Projeto TAMAR biologists and trainees for their help collecting the data, especially L. Verissímo, B. Canal, P. Luz, R. Machado and D. Mora. We thank A. Santos and G. Maurutto for assisting with extracting data from Projeto TAMAR dataset and for their help with Fig. 1. We are also grateful to R. Lo and M. Schlig for the indispensable help processing the genetic samples. S. McDaniel and A. Payton for providing equipment and expertise on the preparation and analyses of the genetic samples. We also thank three anonymous reviewers for comments that improved this manuscript. Our studies were supported by the following funding sources: Archie Carr Center for Sea Turtle Research general funds, Tropical Conservation and Development Grant, PADI Foundation, Maturo Excellence Fund, Lerner-Gray Memorial Fund, Beckmam Foundation and the Michael L. May Research Grants.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luciano S. Soares.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the University of Florida and Projeto TAMAR-ICMBio at which the studies were conducted. This research was approved by the Institutional Animal Care and Use Committees at the University of Florida (201101985) and conducted under SISBIO permit 28938-3 from the Brazilian Ministry of the Environment. Samples were exported under CITES permit 13BR010456/DF and were imported into the USA under CITES permits 13US724540/9 (Archie Carr Center for Sea Turtle Research).

Additional information

Responsible Editor: L. Avens.

Reviewed by B. Bowen, K. Stewart and an undisclosed expert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soares, L.S., Bolten, A.B., Wayne, M.L. et al. Comparison of reproductive output of hybrid sea turtles and parental species. Mar Biol 164, 9 (2017). https://doi.org/10.1007/s00227-016-3035-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-3035-3

Keywords

Navigation