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Genetic composition, origin and conservation of loggerhead sea turtles (Caretta caretta) frequenting the French Mediterranean coasts

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Abstract

This study aims to characterise the genetic structure and composition of 245 individuals of loggerhead sea turtles collected from stranding and bycatch events along the French Mediterranean coasts (Gulf of Lion, Provence and Corsica). We obtained sequences of the mitochondrial control region for two fragments (683 bp and 241 bp for 170 and 51 individuals, respectively). The analysis of the long fragment revealed that 163 samples (95.9%) are attributed to the haplogroup II (mainly Mediterranean) whereas only seven individuals are included in haplogroup IB (Atlantic Ocean). The mixed stock analysis performed on the same dataset indicated that the biggest rookeries from the eastern Mediterranean mainly contributed to the French stock, with major contributions being from Greece (36% and 56% for adults and juveniles, respectively), Crete (12% and 18%) and Western Turkey (14% and 4%). The thirteen microsatellite nuclear markers that have been analysed for 81 specimens did not reveal much genetic structure within sampled individuals, thus suggesting that the studied individuals could belong to the same genetic group. The microsatellite analyses revealed however that the nine individuals issuing from two nests sampled in Gulf of Lion and Provence are clearly differentiated from the remaining samples, thus suggesting a long-distance colonisation of the western Mediterranean. Our results allowed addressing the question of loggerhead turtle conservation in the western Mediterranean basin that until now is not considered as a Management Unit despite high densities of juveniles and recent nesting observed on French, Italian and Spanish coasts.

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References

  • Abreu-Grobois FA, Horrocks J, Formia A, et al. (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., Panagopoulou, A., Rees, A.F. and Williams, K. Book of Abstracts. Twenty Sixth Annual Symposium on Sea Turtle Biology and Conservation. International Sea Turtle Society, Athens, Greece. 376 pp.

  • Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Bass AL, Epperly SP, Braun-McNeill J (2004) Multi-year analysis of stock composition of a loggerhead turtle (Caretta caretta) foraging habitat using maximum likelihood and Bayesian methods. Conserv Genet 5:783–796

    Article  CAS  Google Scholar 

  • Bolker B (2012) mixstock: functions for mixed stock analysis. R package version 0.9.5.1. URL: https://cran.r-project.org/src/contrib/Archive/mixstock/.

  • Bolten AB, Bjorndal KA, Martins HR et al (1998) Transatlantic developmental migrations of loggerhead sea turtles demonstrated by mtDNA sequence analysis. Ecol Appl 8:1–7

    Article  Google Scholar 

  • Bolten AB, Witherington BE (2003) Loggerghead Sea Turtles. Smithsonian Books, Washington, DC

    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

    Article  CAS  PubMed  Google Scholar 

  • Bowen BW, Kamezaki N, Limpus CJ et al (1994) Global phylogeography of the loggerhead turtle (Caretta Caretta) as indicated by mitochondrial-DNA haplotypes. Evolution 48:1820–1828

    PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Broderick AC, Glen F, Godley BJ, Hays GC (2002) Estimating the number of green and loggerhead turtles nesting annually in the Mediterranean. Oryx 36:227–235

    Article  Google Scholar 

  • Cardona L, Hays GC (2018) Ocean currents, individual movements and genetic structuring of populations. Mar Biol 165:10

    Article  Google Scholar 

  • Carreras C, Pascual M, Cardona L et al (2007) The genetic structure of the loggerhead sea turtle (Caretta caretta) in the Mediterranean as revealed by nuclear and mitochondrial DNA and its conservation implications. Conserv Genet 8:761–775

    Article  CAS  Google Scholar 

  • Carreras C, Pascual M, Tomas J et al (2018) Sporadic nesting reveals long distance colonisation in the philopatric loggerhead sea turtle (Caretta caretta). Sci Rep 8:1435

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carreras C, Pont S, Maffucci F et al (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 

  • Casale P, Broderick AC, Caminas JA et al (2018) Mediterranean sea turtles: current knowledge and priorities for conservation and research. Endanger Species Res 36:229–267

    Article  Google Scholar 

  • Casale P, Freggi D, Basso R, Vallini C, Argano R (2007) A model of area fidelity, nomadism, and distribution patterns of loggerhead sea turtles (Caretta caretta) in the Mediterranean Sea. Mar Biol 152:1039–1049

    Article  Google Scholar 

  • Casale P, Margaritoulis D (2010) Sea Turtles in the Mediterranean: Distribution, Threats and Conservation Priorities. IUCN: Gland, Switzerland Gland, CH: IUCN.

  • Casale P, Tucker AD (2017) Caretta caretta (amended version of 2015 assessment). The IUCN Red List of Threatened Species 2017: e.T3897A119333622. https://doi.org/10.2305/ IUCN.UK.2017-2.RLTS.T3897A119333622.en. Downloaded on 16 September 2020.

  • Clusa M, Carreras C, Pascual M et al (2013) Mitochondrial DNA reveals pleistocenic colonisation of the mediterranean by loggerhead turtles (Caretta caretta). J Exp Mar Biol Ecol 439:15–24

    Article  Google Scholar 

  • Clusa M, Carreras C, Pascual M et al (2014) Fine-scale distribution of juvenile Atlantic and Mediterranean loggerhead turtles (Caretta caretta) in the Mediterranean Sea. Mar Biol 161:509–519

    Article  Google Scholar 

  • Clusa M, Carreras C, Cardona L et al (2018) Philipatry in loggerhead turtles Caretta caretta: beyond the gender paradigm. Mar Ecol Prog Ser 588:201–213

    Article  Google Scholar 

  • Darmon G, Miaud C, Claro F, Doremus G, Galgani F (2017) Risk assessment reveals high exposure of sea turtles to marine debris in French Mediterranean and metropolitan Atlantic waters. Deep-Sea Res Topic Stud Oceanogr 141:319–328

    Article  Google Scholar 

  • Delaugerre M, Cesarini C (2004) Confirmed nesting of the loggerhead turtle in Corsica. Mar Turt Newsl 104:12

    Google Scholar 

  • Dodd CK Jr (1988) Synopsis of the biological data on the loggerhead sea turtle Caretta caretta (Linnaeus 1758). Biol Rep 88:1–110

    Google Scholar 

  • Dray S, Dufour AB (2007) The ade4 package: Implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Article  Google Scholar 

  • Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192

    Article  CAS  PubMed  Google Scholar 

  • Duchene S, Frey A, Alfaro-Nunez A et al (2012) Marine turtle mitogenome phylogenetics and evolution. Mol Phylogenet Evol 65:241–250

    Article  PubMed  Google Scholar 

  • Earl DA, Vonholdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resources 4:359–361

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Garofalo L, Mastrogiacomo A, Casale P et al (2013) Genetic characterization of central Mediterranean stocks of the loggerhead turtle (Caretta caretta) using mitochondrial and nuclear markers, and conservation implications. Aquat Conserv Mar Freshw Ecosyst 23:868–884

    Article  Google Scholar 

  • Gérigny O, Claro F, PMoisson P, et al (2020) Hatching events of the loggerhead turtle in Corsica Island, France. Mar Turt Newsl 161:15–18

    Google Scholar 

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

    CAS  Google Scholar 

  • Hamabata T, Matsuo A, Sato MP et al (2020) Natal origin identification of green turtles in the north pacific by genome-wide population analysis with limited DNA samples. Front Mar Sci 7:658

    Article  Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Komoroske LM, Jensen MP, Stewart KR, Shamblin BM, Dutton PH (2017) Advances in the application of genetics in marine turtle biology and conservation. Front Mar Sci 4:156

    Article  Google Scholar 

  • Laurent L, Lescure J (1994) L’hivernage des tortues caouannes Caretta caretta (L.) dans le sud Tunisien. Rev Ecol (Terre et Vie) 49:63–85

    Google Scholar 

  • Laurent L, Lescure J, Excoffier L et al (1993) Genetic-Studies of Relationships between Mediterranean and Atlantic Populations of Loggerhead Turtle Caretta-Caretta with a Mitochondrial Marker. CR Acad Sci Ser III 316:1233–1239

    CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Maffucci F, Corrado R, Palatella L, et al. (2016) Seasonal heterogeneity of ocean warming: a mortality sink for ectotherm colonizers. Sci Rep 6.

  • Mansui J, Darmon G, Ballerini T et al (2020) Predicting marine litter accumulation patterns in the Mediterranean basin: Spatio-temporal variability and comparison with empirical data. Prog Oceanogr 182:102268

    Article  Google Scholar 

  • Margaritoulis D, Argano R, Baran I et al (2003) Loggerhead Turtles in the Mediterranean: present knowledge and conservation perspectives. In: Bolten AB, Witherington B (eds) Loggerhead sea turtles. Smithsonian Institution Press, Washington DC, USA, pp 175–198

    Google Scholar 

  • MedPAN (2016) The 2016 Status of Marine Protected Areas in the Mediterranean: Main Findings. Brochure MedPAN & UN Environment/MAP - SPA/RAC. Available at: https://drive.google.com/file/d/0Bw8D-TFFFccxRFNyZ21yMjEtenc/view.

  • Monzon-Argüello C, Munoz J, Marco A, Lopez-Jurado LF, Rico C (2008) Twelve new polymorphic microsatellite markers from the loggerhead sea turtle (Caretta caretta) and cross-species amplification on other marine turtle species. Conserv Genet 9:1045–1049

    Article  CAS  Google Scholar 

  • Monzon-Argüello C, Rico C, Naro-Maciel E et al (2010) Population structure and conservation implications for the loggerhead sea turtle of the Cape Verde Islands. Conserv Genet 11:1871–1884

    Article  Google Scholar 

  • Nishizawa H, Narazaki T, Fukuoka T et al (2014) Genetic composition of loggerhead turtle feeding aggregations: migration patterns in the North Pacific. Endangered Species Res 24:85–93

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pettex E, Lambert C, Laran S, et al. (2014) Suivi Aérien de la Mégafaune Marine en France métropolitaine - Rapport final Observatoire PELAGIS, pp. 1–169.

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raimbault P, Garcia N, Fornier M, Lafont M (2009) Évolution des apports en nutriments du Rhône à la Méditerranée. In: Quae (ed) Le golfe du Lion: Un observatoire de l’environnement en Méditerranée, Versailles, France, pp 91–104

  • Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in bayesian phylogenetics using tracer 1.7. Syst Biol 67:901–904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reid BN, Naro-Maciel E, Torres Hahn A, FitzSimmons NN, Gehara M (2019) Geography best explains global patterns of genetic diversity and postglacial co-expansion in marine turtles. Mol Ecol 28:3358–3370

    Article  PubMed  Google Scholar 

  • Revelles M, Cardona L, Aguilar A, San Felix M, Fernandez G (2007) Habitat use by immature loggerhead sea turtles in the Algerian Basin (western Mediterranean): swimming behaviour, seasonality and dispersal pattern. Mar Biol 151:1501–1515

    Article  Google Scholar 

  • Richardson TH, Richardson JI, Ruckdeschel C, Dix MW (1978) Remigration patterns of loggerhead sea turtles (Caretta caretta) nesting on little Cumberland and comberland islands, Georgia. In: Henderson GE (ed) Proceedings of the Florida and interregional conference on sea turtles, Jensen Beach, Florida, 24–25 July 1976, vol 33. Fla Mar Res Publi, pp 39–44

  • Sacchi J, Cesarini C, Gambaiani D, et al. (2020) FRANCE in Sea turtles in the Mediterranean Region - MTSG Annual Regional Report 2019. Report of the IUCN-SSC Marine Turtle Specialist Group, Marine Turtle Specialist Groups - Hochscheid S., Kaska Y and Aliki Panagopoulou A. (Eds) , p 306

  • Saied A, Maffucci F, Hochscheid S et al (2012) Loggerhead turtles nesting in Libya: an important management unit for the Mediterranean stock. Mar Ecol Prog Ser 450:207–218

    Article  Google Scholar 

  • Schofield G, Hobson VJ, Fossette S et al (2010) Fidelity to foraging sites, consistency of migration routes and habitat modulation of home range by sea turtles. Divers Distrib 16:840–853

    Article  Google Scholar 

  • Senegas JB, Hochscheid S, Groul J, Lagarrigue B, Bentivegna F (2009) Discovery of the northernmost loggerhead sea turtle (Caretta caretta) nest. Mar Biodiv Rec 2:e81

    Article  Google Scholar 

  • Shamblin BM, Bolten AB, Abreu-Grobois FA et al (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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shamblin BM, Faircloth BC, Dodd M et al (2007) Tetranucleotide microsatellites from the loggerhead sea turtle (Caretta caretta). Mol Ecol Notes 7:784–787

    Article  CAS  Google Scholar 

  • Splendiani A, Fioravanti T, Giovannotti M et al (2017) Mitochondrial DNA reveals the natal origin of Caretta caretta (Testudines: Cheloniidae) stranded or bycaught along the Southwestern Adriatic coasts. Eur Zool J 84:566–574

    Article  Google Scholar 

  • Suchard MA, Lemey P, Baele G et al (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 4:vey16

    Article  Google Scholar 

  • Tikochinski Y, Carreras C, Tikochinski G, Vilaça ST (2020) Population-specific signatures of intra-individual mitochondrial DNA heteroplasmy and their potential evolutionary advantages. Sci Rep 10:1–14

    CAS  Google Scholar 

  • Tolve L, Casale P, Formia A et al (2018) A comprehensive mitochondrial DNA mixed-stock analysis clarifies the composition of loggerhead turtle aggregates in the Adriatic Sea. Mar Biol 165:68

    Article  CAS  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Wallace BP, DiMatteo AD, Hurley BJ et al (2010) Regional management units for marine turtles: a novel framework for prioritizing conservation and research across multiple scales. PLoS ONE 5:e15465

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yilmaz C, Turkozan O, Bardakci F (2011) Genetic structure of loggerhead turtle (Caretta caretta) populations in Turkey. Biochem Syst Ecol 39:266–276

    Article  CAS  Google Scholar 

  • Zbinden JA, Aebischer A, Margaritoulis D, Arlettaz R (2008) Important areas at sea for adult loggerhead sea turtles in the Mediterranean Sea: satellite tracking corroborates findings from potentially biased sources. Mar Biol 153:899–906

    Article  Google Scholar 

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Acknowledgements

This article is dedicated to Mr. Jean Lescure, former researcher at the MNHN and president of the French Herpetological Society (SHF), for his pioneering action for a better knowledge of marine turtles in the Mediterranean Sea. We warmly thank all the people that made this study possible in collecting sea turtles along the French Mediterranean coasts: the volunteers of the French Mediterranean Stranding Network for Sea Turtles (Réseau Tortues Marines de Méditerranée Française, a committee of the SHF), especially the former responsible of this committee Guy Olivier, Sidonie Catteau, Gaëlle Darmon and Dr Jean-Marie Péricard; the staff and volunteers of the CESTMED rescue center (Centre d’Etude et de Sauvegarde des Tortues Marines de Méditerranée); the veterinarian of the Departmental Analysis Laboratory of Gard (Laboratoire Départemental d’Analyses du Gard), Dr Joanne Béfort and the fishermen involved in recovering sea turtles from bycatch.

Funding

Parts of this work have been funded by a Grant (N#05/06/2014) from the TOTAL foundation and thank to the agreement between the French Herpetological Society (SHF), the French Biodiversity Agency (AFB) and the Ecole Pratique des Hautes Etudes (EPHE), aiming at increasing knowledge on sea turtles along the French marine facades. Anaïs Loisier and Marie-Paule Savelli’s Master grants have been funded by EPHE.

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Authors and Affiliations

  1. CEFE, Univ Montpellier, CNRS, EPHE-PSL University (Biogéographie et Écologie des Vertébrés), IRD, Univ Paul Valéry Montpellier 3, Montpellier, France

    Anaïs Loisier, Marie-Paule Savelli, Véronique Arnal, Delphine Gambaiani, Claude Miaud & Claudine Montgelard

  2. Muséum National D’Histoire Naturelle, UMS PatriNat OFB CNRS MNHN, Paris, France

    Françoise Claro

  3. Centre d’Etude et de Sauvegarde des Tortues Marines de Méditerranée (CESTMed), Le Grau du Roi, France

    Delphine Gambaiani & Jean Baptiste Sénégas

  4. Société Herpétologique de France, Réseau Tortues Marines de Méditerranée Française, CP4157, Paris, France

    Delphine Gambaiani, Cathy Cesarini & Jacques Sacchi

  5. Department of Zoology, Centre for Ecological Genomics and Wildlife Conservation, University of Johannesburg, Johannesburg, South Africa

    Claudine Montgelard

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  1. Anaïs Loisier
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  2. Marie-Paule Savelli
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  3. Véronique Arnal
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  4. Françoise Claro
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  8. Jacques Sacchi
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  9. Claude Miaud
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  10. Claudine Montgelard
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Correspondence to Claudine Montgelard.

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All authors declare no conflict of interest.

Ethics approval

Loggerhead turtles are strictly protected in France (national decree of October 14, 2005) and the sample collection was allowed by the decree of December 31, 2012 on the renewal of the environmental protection approval of the Société Herpétologique de France (SHF), and the decree of October 24, 2016 on the collection of biological data in the event of sea turtle stranding or bycatch on French metropolitan coasts (NOR: DEVL1500415N) for the mainland sea turtle observatory program of the National Museum of Natural History (MNHN).

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Loisier, A., Savelli, MP., Arnal, V. et al. Genetic composition, origin and conservation of loggerhead sea turtles (Caretta caretta) frequenting the French Mediterranean coasts. Mar Biol 168, 52 (2021). https://doi.org/10.1007/s00227-021-03855-6

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