Genetic Diversity and Structure of the Nile Soft-Shelled Turtle (Trionyx triunguis) Along the Mediterranean coast of Turkey

Özgür Güçlü, Bülent Bozdoğan

Abstract


The Nile soft-shelled turtle (Trionyx triunguis) is distributed between Dalyan and Samandağ throughout the Mediterranean coast in Turkey. The Mediterranean subpopulation of the Nile soft-shelled turtle is listed as critically endangered in the IUCN Red List Categories. This investigation aimed to determinate levels of genetic variations and patterns of genetic structures among Mediterranean populations in Turkey by using T. triunguis-specific microsatellite primers. A total of 13 polymorphic microsatellite loci were studied among samples of 121 individuals collected from five populations in Turkey. Of 13 polymorphic microsatellite loci used, 3 new were identified in this study. The genetic differentiation among the 5 studied populations of T. triunguis was significant (p < 0.001). The analysis of molecular variance (AMOVA) indicated that genetic variations occurred mainly within populations (89.7%) rather than among populations (10.3%). Structure analysis showed presence of two main groups among the Mediterranean T. triunguis populations. However genetic variations among populations were not correlated with geographic distance between the locations. Analysis of data showed that one of the populations (Dalyan) had undergone a bottleneck effect. Migration analysis indicates that T. triunguis migrates between five Mediterranean populations in Turkey. We concluded that based on our results the status of ‘critically endangered’ of T. triunguis should be maintained. Long term population genetic survey studies should be undertaken and changes in habitats of T. triunguis populations, as well as their population size and structure should be monitored for each population to be able to establish a clear strategy for protection of T. triunguis.

Keywords


Mediterranean Basin; microsatellite; population structure; soft-shelled turtle; Trionyx triunguis

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References


Akçınar S. C. and Taşkavak E. (2017), «Population size and structure of the African Softshell Turtle, Trionyx triunguis, in Dalaman, southwestern Turkey», Zool. Middle East, 63(3), 202 – 209.

Allendorf F. W. and Luikart G. (2007), Conservation and the Genetics of Populations, Wiley-Blackwell Publishing: Hoboken, NJ, USA.

Atatür M. K. (1979), «Investigations on the morphology and osteology, biotope and distribution in Anatolia of Trionyx triunguis (Reptilia, Testudines) with some observations on its biology», Ege Univ. Fen. Fak. Monogr., 18, 1 – 75.

Bagda E., Bardakci F., and Türkozan O. (2012), «Lower genetic structuring in mitochondrial DNA than nuclear DNA among the nesting colonies of green turtle (Chelonia mydas) in the Mediterranean», Biochem. Syst. Ecol., 43, 192 – 199.

Baran I. and Kasparek M. (1989), Marine Turtles in Turkey: Status Survey 1988 and Recommendations for Conservation and Management, WWF, Heidelberg.

Carreras C., Pascual M., Cardona L., Aguilar A., Margaritoulis D., Rees A., Türkozan O., Levy Y., Gasith A., Aureggi M., and Khalil M. (2007), «The genetic structure of the loggerhead sea turtle (Caretta caretta) in the Mediterranean Sea revealed by nuclear and mitochondrial DNA and its conservation implications», Conserv. Gen., 8, 761 – 775.

Excoffier L. and Lischer H. E. L. (2010), «Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows», Mol. Ecol. Resource, 10, 564 – 567.

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

Furlan E., Stoklosa J., Griffiths J., Gust N., Ellis R., Huggins R. M., and Weeks A. R. (2012), «Small population size and extremely low levels of genetic diversity in island populations of the platypus, Ornithorhynchus anatinus», Ecol. Evol., 2, 844 – 857.

Gidis M. and Kaska Y. (2004), «Population size, reproductive ecology and heavy metals in eggshells of the Nile Soft-Shelled Turtle (Trionyx triunguis) around Thermal Lake Kükürtlü (Sulphurous), Muğla-Turkey», Fresenius Environm. Bull., 13(5), 405 – 412.

Gidiş M., Spinks P. Q., Çevik E., Kaska Y., and Shaffer H. B. (2010), «Shallow genetic divergence indicates a Congo-Nile riverine connection for the softshell turtle Trionyx triunguis», Conserv. Biol., 12, 589 – 594.

Glaubitz J. C. (2004), «CONVERT: a user friendly program to reformat diploid genotypic data for commonly used population genetic software packages», Mol. Ecol. Notes, 4, 309 – 310.

Glenn C. and Schable N. A. (2005), «Isolating microsatellite DNA loci», Meth. Enzymol., 395, 202 – 222.

Goudet J. (2001), FSTAT (ver. 2.9.3), a Program to Estimate and Test Gene Diversities and Fixation Indices, http:// www.unil.ch/izea/softwares/fstat.html.

Güçlü Ö., Ülger C., Türkozan O., Gemmel R., Reimann M., Levy Y., Ergene S., Uçar A., and Aymak C. (2009), «First assessment of mitochondrial DNA diversity in the endangered Nile Softshell Turtle, Trionyx triunguis, in the Mediterranean», Chelonian Conserv. Biol., 8(2), 222 – 226.

Güçlü Ö., Ülger C., and Türkozan O. (2011), «Genetic variation of the Nile Soft-Shelled Turtle (Trionyx triunguis)», Int. J. Mol. Sci., 12(10), 6418 – 6431.

Güçlü Ö., Durmuş S. H., Candan K., Beşer N., Türkyılmaz S., Yerli S., and Bozdoğan B. (2015), «Isolation and characterization of polymorphic microsatellite loci on Trionyx triunguis (Testudiniata: Trionychidae) in the Mediterranean Basin», Amphibia–Reptilia, 36, 318 – 324.

Hartl D. L. and Clark A. G. (2007), «Principles of Population Genetics», Écoscience, 14(4), 544 – 545.

Kasparek M. (1994), «Die Nil-Weichschildkröte-eine stark bed-rohte Reptilienart im Mittelmeergebiet», Herpetofauna, 16, 8 – 13.

Kasparek M. (1999), «An assessment on the status of the Nile Soft-shelled Turtle (Trionyx trunguis) in Turkey with recommendations for conservation», Testudo, 5(1), 40 – 52.

Kasparek M. (2001), «The Nile soft-shelled turtle, Trionyx triunguis, towards an action plan for the conservation in the Mediterranean», in: Report to the 21st Meeting of the Standing Committee of the Conservation of European Wild Life and Natural Habitats, Bern Convention, p. 10.

Limpus C. J., Limpus D. J., and Hamann M. (2002), «Freshwater turtle populations in the area to be flooded by the Walla weir, Burnett River, Queensland: Baseline study», Mem. Queensland Mus., 48(1), 155 – 168.

Luikart G., Allendorf F. W., Cornuet J. M., and Sherwin W. B. (1998), «Distortion of allele frequency distributions provides a test for recent population bottlenecks», J. Heredity, 89, 238 – 247.

Medasset (2003), Nile Soft-Shelled Turtle, Trionyx triunguis, Group of experts on the conservation of Amphibians and Reptiles, Report submitted to the Bern Convention, T-PVS, Vol. 18, p. 63.

Nei M., Maruyama T., and Chakraborty R. (1975), «The bottleneck effect and genetic variability in populations», Evolution, 29, 1 – 10.

Oruç A. (2001), «Trawl fisheries in the eastern Mediterranean and their impact on marine turtles», Zool. Middle East, 24, 119 – 125.

Paetkau D., Slade R., Burden M., and Estoup A. (2004), «Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power», Mol. Ecol., 13, 55 – 65.

Peakall R. and Smouse P. E. (2006), Genalex 6. Genetic Analysis in Excel, Population Genetic Software for Teaching and Research, The Australian National University, Canberra, Australia, http://www.anu.edu.au/BoZo/GenAlEx

Piry S., Luikart G., and Cornuet J. M. (1999), «BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data», J. Heredity, 90, 502 – 503.

Piry S., Alapetite A., Cornuet J. M., Paetkau D., Baudouin L., and Estoup A. (2004), «GeneClass2: a software for genetic assignment and first-generation migrant detection», J. Heredity, 95, 536 – 539.

Pöschel J., Heltai B., Graciá E., Quintana M. F., Velo-Antón G., Arribas O., Valdeón A., Wink M., Fritz U., and Vamberger M. (2018), «Complex hybridization patterns in European pond turtles (Emys orbicularis) in the Pyrenean Region», Sci. Rep., 8, 15925.

Pritchard J. K., Stephens M., and Donnelly P. (2000), «Inference of population structure using multilocus genotype data», Genetics, 155, 945 – 959.

Que Y., Bin Z., Rosenthal H., and Chang J. (2007), «Isolation and characterization of microsatellites in Chinese soft-shelled turtle, Pelodiscus sinensis», Mol. Ecol. Notes, 7, 1265 – 1267.

Raymond M. and Rousset F. (1995), «GENePOP (Version 1.2) Population genetics software for exact tests and ecumenicism», J. Heredity, 86, 248 – 249.

Rice W. R. (1989), «Analyzing tables of statistical tests», Evolution, 43, 223 – 225.

Selman W., Kreiser B., and Qualls C. (2013), «Conservation genetics of the yellow-blotched sawback Graptemys flavimaculata (Testudines: Emydidae)», Conserv. Gen., 14(6), 1193 – 1203.

Sambrook J. and Russell D. W. (2001), Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor.

Shanas U., Gidiş M., Kaska Y., Kimalov Y., Rosner O., and Shlomo R. (2012), «The Nile soft-shell turtle, Trionyx triunguis, of Israel and Turkey: Two genetically indistinguishable populations?» Zool. Middle East, 57, 61 – 68.

Taşkavak E. and Akçınar S. C. (2009), «Marine records of the Nile soft-shelled turtle, Trionyx triunguis from Turkey», Marine biodiversity records, published on-line, DOI: 10.1017/S1755267208000092.

Türkozan O. (2009), «Status and conservation of the soft-shell turtle, Trionyx triunguis, in Turkey», in: Proc. of the Seventh Annual Symp. on Conservation and Biology of Tortoises and Freshwater Turtles, 5 – 8 August, 2009, St. Louis, MO, USA, St. Louis, MO, USA.

Weir B. S. and Cockerham C. C. (1984), «Estimating F-statistics for the analysis of population structure», Evolution, 38, 1358 – 1370.

Wright S. (1951), «The genetical structure of populations», Ann. Eugenics, 1, 323 – 354.

Vamberger M., Stuckas H., Ayaz D., Graciá E., Aloufi A. A., Els J., Mazanaeva L. F., Kami H. G., and Fritz U. (2013), «Conservation genetics and phylogeography of the poorly known Middle Eastern terrapin Mauremys caspica (Testudines: Geoemydidae)», Organisms Divers. Evol., 13, 77 – 85.

Van Dijk P. P., Iverson J. B., Shaffer H. B., Bour R., and Rhodin A. G. J. (2012), «Turtles of the world, 2012 update: annotated checklist of taxonomy, synonymy, distribution, and conservation status», Chelonian Res. Monogr., 5, 243 – 328.

Van Oosterhout C., Hutchinson W. F., Wills D. P. M., and Shipley P. (2004), «MicroChecker: software for identifying and correcting genotyping errors in microsatellite data», Mol. Ecol. Notes, 4, 535 – 553

Venizelos L. and Kasparek M. (2006), «Trionyx triunguis: the brackish water turtle that also lives in the Mediterranean Sea», in: M. Frick, A. Panagopoulou, A. Rees, and K. Williams (eds.), Abstrs. of the 26th Annual Symp. on Sea Turtle Biology and Conservation, p. 168.




DOI: https://doi.org/10.30906/1026-2296-2020-27-6-307-315

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