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Genetic Diversity of Gazelles (Gazella marica and Gazella gazella) in Southeast Turkey: A Special Emphasis on Ongoing Conservation Studies of Gazella marica in Turkey

Year 2019, Volume: 78 Issue: 2, 89 - 103, 06.12.2019

Abstract

Objective: The genetic diversity parameters for gazelle populations sampled in Turkey were estimated to assess the effects of captive breeding on the populations’ gene pools and effective population sizes. Materials and Methods: Four individuals from a recently discovered Gazella gazella population in Hatay and two captive gazelle populations were sampled (the Kızılkuyu State Farm (n=48) and the Erikçe State Farm (n=25)) and analyzed using nuclear DNA, mtDNA and Y-chromosome markers. Results: The mtDNA cyt-b partial sequence analysis assigned the Erikçe and Kızılkuyu samples to Gazella marica. The structure analysis differentiated significantly between them, and revealed samples originating from wild population. Both, the Y-chromosome INRA126 locus sequences of Gazella gazella and Gazella marica males and the mtDNA partial cyt-b region RFLP analysis from all the samples distinguished the two gazelle species from each other. Based on microsatellites, the estimated effective population sizes were 9.7, 8.9 and 6.4 for the Kızılkuyu, Erikçe and Hatay populations, respectively. When the Kızılkuyu and Erikçe populations (where severe inbreeding depressions seems to be occurring already) were pooled, the estimated Ne was 24.5. All these estimates were too small for the sustainability of either individual or pooled populations in the wild or even in captivity. Conclusion: The markers used in the study provided information on two of the gazelle species (Gazella marica, and Gazella gazella): their species identity, degree of divergences, effective population sizes and the presence of admixture within the populations. These results turned out to be invaluable in terms of their contribution to future studies for the conservation of these species. 

Supporting Institution

The project was financially supported by the Scientific and Technological Research Council of Turkey.

Project Number

KAMAG 109G016

References

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  • 36. Saitbekova N, Gaillard C, Obexer-Ruff G, Dolf G. Genetic diversity in Swiss goat breeds based on microsatellite analysis. Anim Genet 1999; 30 (1): 36-41.
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  • 39. Moore SS, Byrne K. Characterisation of 65 bovine microsatellites. Mamm Genome 1994; 5: 84-90.
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  • 58. Hassanin A, Douzery EJ. The tribal radiation of the family Bovidae (Artiodactyla) and the evolution of the mitochondrial cytochrome b gene. Mol Phylogenet Evol 1999; 13(2): 227-43.
  • 59. Murtskhvaladze M, Gurielidze Z, Kopaliani N, Tarkhnishvili D. Gene introgression between Gazella subgutturosa and G. marica: limitations of maternal inheritance analysis for species identification with conservation purposes. Acta Theriol 2012; 57: 383-6.
  • 60. Lerp, H., Wronski, T., Plath, M., Schröter, A., & Pfenninger, M. Phylogenetic and population genetic analyses suggest a potential species boundary between Mountain (Gazella gazella) and Arabian Gazelles (Gazella arabica) in the Levant. Mamm Biol 2013b; 78(5): 383-86.
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  • 62. Edwards CJ, Dolf G, Looft C, Loftus RT, Bradley DG. Relationships between the endangered Pustertaler-Sprinzen and three related European cattle breeds as analysed with 20 microsatellite loci. Anim Genet 2000; 31: 329-32.
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  • 64. Ruiz-Lopez MJ, Roldan ER, Espeso G, Gomendio M. Pedigrees and microsatellites among endangered ungulates: what do they tell us? Mol Ecol 2009; 18(7): 1352-64.
  • 65. Lerp H, Plath M, Wronski T, Bärmann EV, Malczyk A, Resch RR, et al. Utility of island populations in re-introduction programmesrelationships between Arabian gazelles (Gazella arabica) from the Farasan Archipelago and endangered mainland populations. Mol Ecol 2014; 23(8): 1910-22.
  • 66. Hadas L, Hermon D, Boldo A, Arieli G, Gafny R, King R, et. al. Wild Gazelles of the Southern Levant: genetic profiling defines new conservation priorities. PloS One 2015; 10(3).
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Year 2019, Volume: 78 Issue: 2, 89 - 103, 06.12.2019

Abstract

Project Number

KAMAG 109G016

References

  • 1. Groves CP, Grubb P. Ungulate taxonomy. Baltimore, Md.: JHUP; 2011.
  • 2. Lerp H, Wronski T, Plath M, Schröter A, Pfenninger M. Phylogenetic and population genetic analyses suggest a potential species boundary between Mountain (Gazella gazella) and Arabian Gazelles (Gazella arabica) in the Levant. Mamm Biol 2013; 78(5): 383-86.
  • 3. Mallon DP. Gazella subgutturosa. IUCN Red List of Threatened Species. Version 2011.2; 2008.
  • 4. Kasparek M. On the historical distribution and present situation of gazelles, Gazella ssp., in Turkey. Zool Middle East 1986; 1: 11-5.
  • 5. Kumerloeve, H. Die Säugetiere (Mammalia) Syriens und des Libanon. Spixiana 1975b; 18, 159-225.
  • 6. Kumerloeve, H. Bemerkungen zum Gazellen Vorkommen im südöstlichen Kleinasien. Z. Saugetierkd. 1969; 34, 113-20.
  • 7. Kumerloeve, H. Die Säugetiere (Mammalia) der Türkei. Spixiana 1975a; 18, 69-158.
  • 8. Turan N. Game and wildlife of Turkey mammals. Ongun Kardeşler Matbaacılık Sanayii, Turkey; 1984. 9. Tez C, Akalın H, Erkekkardeş M. Additional karyological data on goitered gazelle, Gazella subgutturosa, from Turkey. Arch Biol Sci 2009; 61(1):45-8.
  • 10. Durmuş M. Determination of home range size and habitat selection of gazelles (Gazella subgutturosa) by GPS Telemetry in Şanlıurfa. Middle East Technical University Graduate School of Natural and Applied Sciences, MSc Thesis. 2010.
  • 11. Kumerloeve H. Zur Verbreitung kleinasiatischer Raub- und Huftiere sowie einiger Großnager. Säugetierkd Mitt 1967; 15: 337-409.
  • 12. Turan N. Report on the protection and restoration of gazelle (Gazella subgutturosa) in Turkey. Turkish Department of GameWildlife: 7; 1977.
  • 13. Ölçer SY. Chapter 20: Turkey. Mallon DP, Kingswood SC, compilers. Antelopes Part 4: North Africa, the Middle East, and Asia Global survey and regional action plans SSC Antelope Specialist Group IUCN, Gland, Switzerland and Cambridge, UK; 2001. p.112-13.
  • 14. Çobanoğlu AE. Identification Of Demographic Structure and Population Viability Analysis of Gazella subgutturosa in Şanlıurfa. Middle East Technical University Graduate School of Natural and Applied Sciences, MSc Thesis. 2010.
  • 15. Kankılıç T, Özüt D, Gürler Ş, Kence M, Bozkaya F, Kence A. Rediscovery of a new mountain gazelle population and clarification of taxonomic status of the genus Gazella in Turkey using mtDNA sequencing. Folia Zool 2012; 61(2): 129-37.
  • 16. Wronski T, Sandouka M. Plath M, Cunningham P. Differences in sexual dimorphism among four gazelle taxa (Gazella spp.) in the Middle East. Anim Biol 2010; (60) 395-412.
  • 17. Hammond RL, Macasero W, Flores B, Mohammed OB, Wacher T, Bruford MW. Phylogenetic Reanalysis of the Saudi Gazelle and Its Implications for Conservation. Conserv. Biol. 2001; 15:1123-33.
  • 18. Wacher T, Wronski T, Hammond RL, Winney B, Blacket MJ, Hundertmark KJ, et al. Phylogenetic analysis of mitochondrial DNA sequences reveals polyphyly in the goitered gazelle (Gazella subgutturosa). Conserv Genet 2011; 12:827-31.
  • 19. Wronski T, Wacher T, Hammond RL, Winney B, Hundertmark KJ, Blacket MJ, et. al. Two reciprocally monophyletic mtDNA lineages elucidate the taxonomic status of Mountain gazelles (Gazella gazella), Syst Biodivers 2010; 8(1): 119-29.
  • 20. Lerp H, Wronski T, Pfenninger M, Plath M. A phylogeographic framework for the conservation of Saharan and Arabian Dorcas gazelles (Artiodactyla: Bovidae). Org Divers Evol 2011; 11(4): 31729.
  • 21. Groves CP, Harrison DL. The taxonomy of the gazelles (genus Gazella) of Arabia. J Zool London 1967; 152:381-7. 22. Groves CP. On the smaller gazelles of the Genus Gazella de Blainville, 1816. Z. Saugetierkd. 1969; 37:38-60.
  • 23. Lerp H, Wronski T, Butynski T, Plath M. Speciation of Arabian gazelles. In: Michalak P (ed.) Speciation: Natural Processes, Genetics and Biodiversity. Nova Science Publishers, Hauppauge, NY pp. 59-82; 2013.
  • 24. Oğurlu I. Wild ungulates of Turkey. Ongulés/Ungulates 1992; 91:575-7.
  • 25. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual, 2nd ed. Vol. 3, Cold Spring Harbor Laboratory, New York, USA; 1989.
  • 26. Winnepenninckx B, Backeljau T, de Wachter R. Extraction of high molecular weight DNA from molluscs. Trends in Genet 1993; 9 (12): 407.
  • 27. Wilson GA, Strobeck C, Wu L, Coffin JW. Characterization of microsatellite loci in caribou Ranginfer tarandus, and their use in other artiodactyls. Mol Ecol 1997; 6: 697-9. 28. Toldo S, Fries SR, Steffen P, Neibergs HL, Barendse W. Physically mapped cosmid-derived microsatellite markers as anchor loci on the bovine chromosome. Mamm Genome 1993; 4:720-7.
  • 29. Buchanan FC and Crawford AM. Ovine microsatellites at the OarFCB11, OarFCB128, OarFCB193, OarFCB266 and OARFCB304 loci. Anim Genet 1993; 24: 145.
  • 30. Mommens GW, Coppieters A. Dinucleotide repeat polymorphism at the bovine MM12E6 and MM8D3 loci. Anim Genet 1994; 25: 368.
  • 31. Bishop MD, Kappes SM. A genetic linkage map for cattle. Genetics 1994; 136:619-39.
  • 32. Kappes SM, Keele JW, Stone RT, McGraw RA, Sonstegard TS, Smith TP, et. al. A second-generation linkage map of the bovine genome. Genome Res 1997; 7(3): 235-49.
  • 33. Vaiman D, Mercier D. A set of 99 cattle microsatellites: characterisation, synteny mapping, and polymorphism. Mamm Genome 1994; 5:288-97.
  • 34. Mezzelani A, Zhang Y, Redaelli L, Castiglioni B, Leone P, Williams JL, et. al. Chromosomal localization and molecular characterization of 53 cosmid-derived bovine microsatellites. Mamm Genome 1995; 6(9): 62935.
  • 35. Steffen P, Eggen A. Isolation and mapping of polymorphic microsatellites in cattle. Anim Genet 1993; 24: 121-4.
  • 36. Saitbekova N, Gaillard C, Obexer-Ruff G, Dolf G. Genetic diversity in Swiss goat breeds based on microsatellite analysis. Anim Genet 1999; 30 (1): 36-41.
  • 37. Georges M, Massey J. Polymorphic DNA markers in Bovidae. J World Intellect Prop Publ No 92:13120, 1992
  • 38. Kemp SJ, Brezinsky L, Teale AJ. ILSTS002: a polymorphic bovine microsatellite. Anim Genet 1992; 23: 184.
  • 39. Moore SS, Byrne K. Characterisation of 65 bovine microsatellites. Mamm Genome 1994; 5: 84-90.
  • 40. Oosterhout C, Hutchinson WF, Wills DPM, Shipley PF. MicroChecker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 2004; 4:535-8.
  • 41. Excoffier L, Laval G, Schneider S. 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 2006.
  • 42. Goudet J (2001) FSTAT, A Program to Estimate and Test Gene Diversities and Fixation Indices, Version 2.9.3. http://www.unil.ch/ izea/softwares/fstat.html
  • 43. Sokal RR, Rohlf FJ. Biometry (3rd edn). WH Freman and company: New York; 1995.
  • 44. Kalinowski ST, Taper ML, Marshall TC. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 2007; 16(5): 1099-106.
  • 45. Wright S. The Interpretation of Population Structure by F-Statistics with Special Regard to Systems of Mating. Evolution (N Y) 1965; 19(3):395-420.
  • 46. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000; 155:94559.
  • 47. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 2005; 14:2611-20.
  • 48. Tapio M, Ozerov M, Tapio I, Toro M, Marzanov N, Cinkulov M, et. al. Microsatellite-based genetic diversity and population structure of domestic sheep in northern Eurasia. BMC Genetics 2010; 11:76.
  • 49. Jakobsson M, Rosenberg NA. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 2007; 23: 1801-6.
  • 50. Rosenberg NA. DISTRUCT: a program for the graphical display of population structure. Mol. Ecol. Notes 2004; 4: 137-8.
  • 51. Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR. Ne Estimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 2014; 14(1): 209-14.
  • 52. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablancha FX, et. al. Dynamics of mitochondrial DNA evolution in animals: amplification with conserved primers. PNAS USA 1989; 86: 6196200.
  • 53. Irwin D, Kocher T, Wilson A. Evolution of the cytochrome-b gene of mammals. J Mol Evol 1991; 32: 128-44.
  • 54. Hall TA (2013) BioEdit v 7.2. 3. Biological sequence alignment editor for Win 95/98/NT/2K/XP7.
  • 55. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol and Evol 2013; 30(12): 2725-9.
  • 56. Liu WS, Mariani P, Beattie CW, Alexander LJ, De León FAP. A radiation hybrid map for the bovine Y Chromosome. Mamm Genome 2002; 13(6): 320-6.
  • 57. Wright S. Vol. 4: Variability within and among natural populations. Chicago, University of Chicago Press; 1978.
  • 58. Hassanin A, Douzery EJ. The tribal radiation of the family Bovidae (Artiodactyla) and the evolution of the mitochondrial cytochrome b gene. Mol Phylogenet Evol 1999; 13(2): 227-43.
  • 59. Murtskhvaladze M, Gurielidze Z, Kopaliani N, Tarkhnishvili D. Gene introgression between Gazella subgutturosa and G. marica: limitations of maternal inheritance analysis for species identification with conservation purposes. Acta Theriol 2012; 57: 383-6.
  • 60. Lerp, H., Wronski, T., Plath, M., Schröter, A., & Pfenninger, M. Phylogenetic and population genetic analyses suggest a potential species boundary between Mountain (Gazella gazella) and Arabian Gazelles (Gazella arabica) in the Levant. Mamm Biol 2013b; 78(5): 383-86.
  • 61. Hanotte O, Okomo M, Verjee Y, Rege JEO, Teale A. A polymorphic Y chromosome microsatellite locus in cattle. Anim Genet 1997; 28(4): 318-9.
  • 62. Edwards CJ, Dolf G, Looft C, Loftus RT, Bradley DG. Relationships between the endangered Pustertaler-Sprinzen and three related European cattle breeds as analysed with 20 microsatellite loci. Anim Genet 2000; 31: 329-32.
  • 63. Zachos FE, Karami M, Ibenouazi Z, Hartl GB, Eckert I, Kirschning J. First genetic analysis of a free-living population of the threatened goitered gazelle (Gazella subgutturosa). Mamm Biol 2010; 5:27782.
  • 64. Ruiz-Lopez MJ, Roldan ER, Espeso G, Gomendio M. Pedigrees and microsatellites among endangered ungulates: what do they tell us? Mol Ecol 2009; 18(7): 1352-64.
  • 65. Lerp H, Plath M, Wronski T, Bärmann EV, Malczyk A, Resch RR, et al. Utility of island populations in re-introduction programmesrelationships between Arabian gazelles (Gazella arabica) from the Farasan Archipelago and endangered mainland populations. Mol Ecol 2014; 23(8): 1910-22.
  • 66. Hadas L, Hermon D, Boldo A, Arieli G, Gafny R, King R, et. al. Wild Gazelles of the Southern Levant: genetic profiling defines new conservation priorities. PloS One 2015; 10(3).
  • 67. Duo H, Na L, Hong Y, Zhang Y, Li D. Genetic diversity of Przewalski’s gazelle using noninvasive DNA and its implications for conservation. AJB 2015; 14(13): 1107-13.
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There are 70 citations in total.

Details

Primary Language English
Journal Section Research Articles
Authors

Fikriye Dilan Saatoglu This is me 0000-0003-3936-287X

Melis Denizci Oncu This is me 0000-0001-9140-1544

Hasan Emir This is me 0000-0002-2563-6545

Taner Hatipoglu This is me 0000-0002-6010-7315

Sinan Can Acan This is me 0000-0002-5534-0024

Tolga Kankilic This is me 0000-0002-9058-5166

İnci Togan This is me 0000-0002-2150-772X

Evren Koban Bastanlar

Project Number KAMAG 109G016
Publication Date December 6, 2019
Submission Date June 24, 2019
Published in Issue Year 2019 Volume: 78 Issue: 2

Cite

AMA Saatoglu FD, Denizci Oncu M, Emir H, Hatipoglu T, Acan SC, Kankilic T, Togan İ, Koban Bastanlar E. Genetic Diversity of Gazelles (Gazella marica and Gazella gazella) in Southeast Turkey: A Special Emphasis on Ongoing Conservation Studies of Gazella marica in Turkey. Eur J Biol. December 2019;78(2):89-103.