Abstract
The population genetic structure of the loggerhead sea turtle (Caretta caretta) nesting in the eastern Mediterranean was assessed by sequencing a fragment of the control region of the mitochondrial DNA (n = 190) and seven microsatellites (n = 112). The two types of markers revealed genetic structuring (mtDNA: γst = 0.212, P < 0.001; nDNA F st = 0.006, P < 0.001), thus indicating that both females and males are philopatric and that gene flow between populations is restricted. Mitochondrial DNA data indicate that the female populations nesting on the islands of Crete and Cyprus have suffered a recent bottleneck or colonization event. However, no bottleneck or founder effect was revealed by nuclear markers, thus indicating male-mediated gene flow from other populations that would increase nuclear genetic variability. Crete, and to a lower extent Cyprus, are thought to play a central role in such male-mediated gene flow that may reduce the negative effect of genetic drift or inbreeding on the small populations of Lebanon and Israel. This population structure indicates that assessing population relevance only on the basis of genetic variability and size would be misleading, as some populations not fulfilling those requirements may play a relevant role in genetic exchange and hence contribute to the overall genetic variability.
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Baldwin R, Hughes GR, Prionce RIT (2003) Loggerhead turtles in the Indian Ocean. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Books, Washington D.C., pp 218–232
Beerli P (2002) MIGRATE version 1.7.6.1 – Documentation and Program. Available at http://evolution.genetics.washington.edu/lamark.html
Beerli P, Felsenstein J (1999) Maximum likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773
Birky CWJ, Marayama 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
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 8:1–7
Bowen BW (2003) What is a loggerhead turtle? The genetic perspective. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Books, Washington D.C., pp 7–27
Bowen BW, Meylan AB, Ross JP, Limpus CJ, Balazs GH, Avise JC (1992) Global population structure and natural history of the green turtle (Chelonia mydas) in terms of matriarchal phylogeny. Evolution 46:865–881
Bowen BW, Avise JC, Richardson JI, Meylan AB, Margaritoulis D, Hopkins-Murphy SR (1993) Population structure of loggerhead turtles (Caretta caretta) in the Northwestern Atlantic Ocean and Mediterranean Sea. Conserv Biol 7:834–844
Bowen BW, Clark AM, Abreu-Grobois FA, Chaves A, Reichart HA, Ferl RJ (1998) Global phylogeography of the ridley sea turtles (Lepidochelys spp.) as inferred from mitochondrial DNA sequences. Genetica 101:179–189
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
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
Cabin RJ, Mitchell RJ (2000) To Bonferroni or not to Bonferroni: when and how are the questions. Bull Ecol Soc Am 81:246–248
Carreras C, Pont S, Maffucci F, Pascual M, Barceló A, Bentivegna F, Cardona L, Alegre F, SanFélix 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
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Cuadras CM (1983) Problemas de probabilidad y estadística. PPU, Barcelona
Delaugerre M, Cesarini C (2004) Confirmed nesting of the loggerhead turtle in Corsica. Mar Turtl Newslett 104:12
Ehrhart LM, Bagley DA, Redfoot WE (2003) Loggerhead turtles in the Atlantic Ocean. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Books, Washington D.C., pp 157–174
Encalada SE, Lahanas PN, Bjorndal KA, Bolten AB, Miyamoto MM, Bowen BW (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
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
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
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
FitzSimmons NN, Moritz C, Limpus CJ et al (1996) Comparative genetic structure of green, loggerhead, and flatback populations in Australia based on variable mtDNA and nDNA regions. In: Bowen BW, Witzell WN (eds) Proceedings of the international symposium on sea turtle conservation genetics. NOAA Technical Memorandum NMFS-SEFSC-396. National Technical Information Service, Springfield, Virginia, pp 25–32
FitzSimmons NN, Limpus CJ, Norman JA, Goldizen AR, Miller JD, Moritz C (1997a) Philopatry of male marine turtles inferred from mitochondrial DNA markers. Proc Natl Acad Sci USA 94:8912–8917
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 147:1843–1854
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. University Press, Cambridge
Groombridge B (1990) Marine turtles in the Mediterranean: distribution, population status, conservation. Nat Environ Ser (Council of Europe) 48:1–98
Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics 48:361–372
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
Hofrichter R, Kern W, Beckel L, Domnig I, Zankl A, Hein A (2004) Geografía y clima. In: Hofrichter R (ed) El Mar Mediterráneo. Parte general. Ediciones Omega, Barcelona, pp 102–195
IUCN (2006) 2004 IUCN red list of threatened species
Karl SA, Bowen BW, Avise JC (1992) Global population genetic structure and male mediated gene flow in the green turtle (Chelonia mydas): RFLP analyses of anonymous nuclear loci. Genetics 131:163–173
Kaska Y (2000) Genetic structure of Mediterranean sea turtle populations. Turk J Zool 24:191–197
Khalil M, Syed H, Aureggi M, Venizelos L (in press) Marine turtle nesting at El Monsouri, South Lebanon. In: Proceedings of the second Mediterranean conference on marine turtles. Antalya, Turkey 4–7 May 2005
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. C R Acad Sci Vie III Sci Vie 316:1233–1239
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
Llorente GA, Carretero MA, Pascual X, Perez A (1992) New record of a nesting loggerhead turtle Caretta caretta in western Mediterranean. Br Herp Soc Bull 42:14–17
Margaritoulis D (1998) Interchange of nesting loggerheads among Greek beaches. In: Epperly SP, Braun J (eds) Proceedings of the seventeenth annual sea turtle symposium. NOAA Technical Memorandum NMFS-SEFSC-415. National Marine Fisheries Service, Southeast Fisheries Science Center, Orlando, FL, pp 225–227
Margaritoulis D, Argano R, Baran I et al (2003) Loggerhead turtles in the Mediterranean Sea: present knowledge and conservation perspectives. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Books, Washington D.C., pp 175–198
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
Miller JD (1997) Reproduction in sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 51–81
Moore MK, Ball RM (2002) Multiple paternity in loggerhead turtle (Caretta caretta) nests on Melbourne Beach, Florida: a microsatellite analysis. Mol Ecol 11:281–288
Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100(2):403–405
Nei M (1982) Evolution of human races at the gene level. In: Bone-Tamir B, Cohen T, Goodman RM (eds) Human genetics part A: the unfolding genome. Alan R Liss, New York, pp 167–181
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Norman JA, Moritz C, Limpus CJ (1994) Mitochondrial DNA control region polymorphisms: genetic markers for ecological studies of marine turtles. Mol Ecol 3:363
Perneger TV (1998) What’s wrong with Bonferroni adjustments. Br Med J 316:1236–1238
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pulliam HR (1988) Sources, sinks and population regulation. Am Nat 132:652–661
Pulliam HR, Danielson BJ (1991) Sources, sinks and habitat selection: a landscape perspective on population dynamics. Am Nat 137:S50–S66
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Roberts MA, Schwartz TS, Karl S (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
Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
Ruckelshaus M, McElhany P, Ford MJ (2003) Recovering species of conservation concern – are populations expendable? In: Kareiva P, Levin SA (eds) The importance of species. Perspectives on expendability and triage. Princeton University Press, Princeton Oxford, pp 305–329
Schroth W, Streit B, Schierwater B (1996) Evolutionary handicap for turtles. Nature 384:521–522
Sella I (1982) Sea turtles in the eastern Mediterranean and northern Red Sea. In: Bjorndal KA (ed) Biology and conservation of sea turtles. Smithsonian Institution Press, Washington DC, pp 417–423
Shanker K, Ramadevi J, Choudhury BC, Singh L, Aggarwal RK (2004) Phylogeography of the olive ridley turtles (Lepidochelys olivacea) on the east coast of India: implications for conservation theory. Mol Ecol 13:1899–1909
Takahata N, Palumbi SR (1985) Extranuclear differentiation and gene flow in the finite island model. Genetics 109:441–457
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
Tichy G, Tomek C, Hsü KJ, Hofrichter R (2004) Geología y genesis. In: Hofrichter R (ed) El Mar Mediterráneo. Parte general. Ediciones Omega, Barcelona, pp 56–101
Tomas J, Mons JL, Martin JJ, Bellido JJ, Castillo JJ (2002) Study of the first reported nest of loggerhead sea turtle, Caretta caretta, in the Spanish Mediterranean coast. J Mar Biol Assoc UK 82:1005–1007
Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: F-ST not equal 1/(4Nm+1). Heredity 82:117–125
Wright S (1951) The genetical structure of populations. Ann Eug 15:323–354
Zaykin DV, Pudovkin AI (1993) Two programs to estimate significance of X2 values using pseudo-probability tests. J Hered 84:152
Acknowledgements
The Fundació pel Desenvolupament Sostenible provided logistic support for the fieldwork. This study was funded by the EU project “Protección de Praderas de Posidonia en LICs de Baleares” LIFE00NAT/E/7303, the project BOS2003-05904 of the Spanish Government (CICYT) and the Regional Activity Center for Specially Protected Areas (RAC/SPA) of the Mediterranean Action Plan (United Nations Environment Programme) in Tunis. Samples from Lebanon were collected under the aegis of MEDASSET 2004 sea turtle conservation project. We thank S. Roques for her comments to the manuscript and Daniel Cebrián (RAC/SPA) for his involvement in the project. AFR and DM thank Sonja Baker, Christina Davy and Sandra Muller for sample collection in Greece. We also thank two anonymous referees for their helpful comments.
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Carreras, C., Pascual, M., Cardona, L. et al. 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 (2007). https://doi.org/10.1007/s10592-006-9224-8
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DOI: https://doi.org/10.1007/s10592-006-9224-8