Abstract
Genetic variability and phylogenetic relationships of the Eurasian lynx (Lynx lynx) have been reported by various researchers from species’ range. As genetic data of Turkish lynx comes from a single genetic study that only contains limited number of lynx samples from the Anatolian part of Turkey, there is still a lack of genetic information for the Eurasian lynx population distributed in Turkey. In this study, mitochondrial Cyt b (1140 bp) and COI (630 bp) sequences were obtained from eight Anatolian samples of the Eurasian lynx. The Anatolian lynx sequences were compared to those of conspecific populations published in GenBank. We found two COI (630 bp) and four Cyt b (1140 bp) haplotypes among the eight Anatolian lynx sequences. Despite the limited number of the Anatolian lynx sequences, Bayesian, Maximum Likelihood, Neighbor-Joining and Network analyses revealed that there was a significant genetic differentiation in the Eurasian lynx, in that at least there were two main mitochondrial lineages within the sampling area. Also, the present study suggested that the Anatolian lynx might have a relatively high genetic variability despite the scarce samples.
Similar content being viewed by others
REFERENCES
Status and Conservation of the Eurasian Lynx (Lynx lynx) in Europe in 2001, von Arx, M., Breitenmoser-Würsten, C., Zimmermann, F., and Breitenmoser, U., Eds., Muri, Switzerland: KORA, 2004.
Wilson, D.E. and Reeder, D.M., Mammal Species of the World: A Taxonomic and Geographic Reference, Baltimore: Johns Hopkins University Press, 2005, 3rd ed.
Breitenmoser, U., Breitenmoser-Würsten, C., Lanz, T., et al., Lynx lynx (errata version published in 2017), The IUCN Red List of Threatened Species2015. eT12519A121707666. Accessed April 25, 2018.
Aulagnier, S., Haffner, P., Mitchell-Jones, A.J., et al., Mammals of Europe, North Africa and the Middle East, London: A. and C. Black, 2009.
Hellborg, K., Walker, C.W., Rueness, E.K., et al., Differentiation and levels of genetic variation in northern European lynx (Lynx lynx) populations revealed by microsatellites and mitochondrial DNA analysis, Conserv. Genet., 2002, vol. 3, no. 2, pp. 97—111.
Johnson, W.E., Godoy, J.A., Palomares, F., et al., Phylogenetic and phylogeographic analysis of Iberian lynx populations, J. Hered., 2004, vol. 95, no. 1, pp. 19—28.
Gugolz, D., Bernasconi, M.V., Breitenmoser-Würsten, C., and Wandeler, P., Historical DNA reveals the phylogenetic position of the extinct Alpine lynx, J. Zool., 2008, vol. 275, no. 2, pp. 201—208.
Ratkiewicz, M., Matosiuk, M., Kowalczyk, R., et al., High levels of population differentiation in Eurasian lynx at the edge of the species' western range in Europe revealed by mitochondrial DNA analyses, Anim. Conserv., 2012, vol. 15, no. 6, pp. 603—612.
Ratkiewicz, M., Matosiuk, M., Saveljev, A.P., et al., Long-range gene flow and the effects of climatic and ecological factors on genetic structuring in a large, solitary carnivore: the Eurasian lynx, PLoS One, 2014, vol. 9, no. 12. e115160
Sindičić, M., Gomerčić, T., Galov, A., Repetitive sequences in Eurasian lynx (Lynx lynx L.) mitochondrial DNA control region, Mitochondrial DNA, 2012, vol. 23, no. 3, pp. 201—207.
Rueness, E.K., Naidenko, S., Trosvik, P., and Stenseth, N.C., Large-scale genetic structuring of a widely distributed carnivore—the Eurasian lynx (Lynx lynx), PLoS One, 2014, vol. 9, no. 4. e93675
Ning, Y., Liu, H., Jiang, G., and Ma, J., Phylogenetic relationship of Eurasian lynx (Lynx lynx) revealed by complete mitochondrial genome, Mitochondrial DNA, Part A, 2016, vol. 27, no. 5, pp. 3477—3478.
Cömert, N., Carlı, O., and Dinçtürk, H.B., The missing lynx of Eurasia at its southern edge: a connection to the critically endangered Balkan lynx, Mitochondrial DNA, Part A, 2018. https://doi.org/10.1080/24701394.2018.1445240
Rueness, E.K., Jorde, P.E., Hellborg, L., et al., Cryptic population structure in a large, mobile mammalian predator: the Scandinavian lynx, Mol. Ecol., 2003, vol. 12, no. 10, pp. 2623—2633.
Bull, J.K., Heurich, M., Saveljev, A.P., et al., The effect of reintroductions on the genetic variability in Eurasian lynx populations: the cases of Bohemian–Bavarian and Vosges–Palatinian populations, Conserv. Genet., 2016, vol. 17, no. 5, pp. 1229—1234.
Wang, X., Wei, K., Zhang, Z., et al., Major histocompatibility complex class II DRB exon-2 diversity of the Eurasian lynx (Lynx lynx) in China, J. Nat. Hist., 2009, vol. 43, nos. 3—4, pp. 245—257.
Can, Ö.E., Status, Conservation and Management of Large Carnivores in Turkey, Strasbourg: Convention on the Conservation of European Wildlife and Natural Habitats, 2004.
Kryštufek, B. and Vohralik, V., Mammals of Turkey and Cyprus: Rodentia II: Cricetinae, Muridae, Spalacidae, Calomyscidae, Capromyidae, Hystricidae, Castoridae, Koper: Knjiznica Annales Majora, 2009, 1st ed.
Albayrak, İ., New record of Lynx lynx (L., 1758) in Turkey (Mammalia: Carnivora), Tr. J. Zool., 2012, vol. 36, no. 6, pp. 814—819.
Chynoweth, M.W., Çoban, E., and Şekercioğlu, Ç.H., Conservation of a new breeding population of Caucasian lynx (Lynx lynx dinniki) in eastern Turkey, Tr.J. Zool., 2015, vol. 39, no. 3, pp. 541—543.
Cooperation in the European Mountains: 2: The Caucasus, Price, M.F., Ed., Gland, Switzerland: IUCN, 2000.
Baskaya, S. and Bilgili, E., Does the leopard Panthera pardus still exist in the Eastern Karadeniz Mountains of Turkey?, Oryx, 2004, vol. 38, no. 2, pp. 228—232.
Can, Ö.E., Large Carnivores in Turkey, Species 38, Quebec: World Conservation Union, 2002.
Johnson, K., The status of mammalian carnivores in Turkey, Endangered Species UPDATE, 2002, vol. 19, no. 6, pp. 232—237.
Johnson, K., Species at risk status and distribution of the leopard (Panthera pardus) in Turkey and the Caucasus Mountains, Endangered Species UPDATE, 2003, vol. 20, no. 3, pp. 107—122.
Giannatos, G., Albayrak, T., and Erdogan, A., Status of the caracal in protected areas in south-western Turkey, CATnews, 2006, no. 45, pp. 23—24.
De Marinis, A. and Masseti, M., Mammalian fauna of the Temessos National Park, Turkey, Animal Biodiversity in the Middle East (Proc. First Middle Eastern Biodiversity Congress, Aqaba, Jordan, 20–23 October 2008), Neubert, E., Amr, Z., Taiti, S., and Gümüs, B., Eds., ZooKeys, 2009, no. 31, pp. 221—228.
Ambarlı, H., Mengüllüoğlu, D., and Bilgin, C.C., First camera trap pictures of Eurasian lynx from Turkey, CATnews, 2010, no. 52, p. 32.
Ucarli, Y., Usability of large carnivore as a keystone species in Eastern Black Sea Region, Turkey, Afr. J. Biotechnol., 2011, vol. 10, no. 11, pp. 2032—2036.
Albayrak, T., Giannatos, G., and Kabasakal, B., Carnivore and ungulate populations in the Beydağları Mountains (Antalya, Turkey): border region between Asia and Europe, Pol. J. Ecol., 2012, vol. 60, no. 2, pp. 419—428.
Avgan, A., Zimmermann, F., Güntert, M., et al., The first density estimation of an isolated Eurasian lynx population in southwest Asia, Wildlife Biol., 2014, vol. 20, no. 4, pp. 217—221.
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R., DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates, Mol. Mar. Biol. Biotechnol., 1994, vol. 3, no. 5, pp. 294—299.
Irwin, D.M., Kocher, T.D., and Wilson, A.C., Evolution of cytochrome b gene of mammals, J. Mol. Evol., 1991, vol. 32, no. 2, pp. 128—144.
Koepfli, K.P. and Wayne, R.K., Phylogenetic relationships of otters (Carnivora; Mustelidae) based on mitochondrial cytochrome b sequences, J. Zool., 1998, vol. 246, no. 4, pp. 401—416.
Katoh, K., Misawa, K., Kuma, K., and Miyata, T., MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucleic Acids Res., 2002, vol. 30, no. 14, pp. 3059—3066.
Librado, P. and Rozas, J., DnaSP v5, a software for comprehensive analysis of DNA polymorphism data, Bioinformatics, 2009, vol. 25, no. 11, pp. 1451—1452.
Kumar, S., Stecher, G., and Tamura, K., MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 2016, vol. 33, no. 7, pp. 1870—1874.
Kimura, M., A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide substitutions, J. Mol. Evol., 1980, vol. 16, no. 2, pp. 111—120.
Darriba, D., Taboada, G.L., Doallo, R., and Posada, D., jModelTest 2: more models, new heuristics and parallel computing, Nat. Methods, 2012, vol. 9, no. 8, p. 772.
Ronquist, F., Teslenko, M., Van Der Mark, P., et al., and Huelsenbeck, J.P., MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space, Syst. Biol., 2012, vol. 61, no. 3, pp. 539—542.
Rambaut, A., FigTree: Tree Figure Drawing Tool, Version 1.3.1, Institute of Evolutionary Biology, University of Edinburgh, 2009.
Wei, L., Wu, X., Zhu, L., and Jiang, Z., Mitogenomic analysis of the genus Panthera,Sci. China, Life Sci., 2011, vol. 54, no. 10, pp. 917—930.
Zhang, W., Yue, B., Wang, X., et al., Analysis of variable sites between two complete South China tiger (Panthera tigris amoyensis) mitochondrial genomes, Mol. Biol. Rep., 2011, vol. 38, no. 7, pp. 4257—4264.
Bandelt, H.J., Forster, P., and Röhl, A., Median-joining networks for inferring intraspecific phylogenies, Mol. Phylogenet. Evol., 1999, vol. 16, no. 1, pp. 37—48.
Spong, G., and Hellborg, L., A near-extinction event in lynx: do microsatellite data tell the tale?, Conserv. Ecol., 2002, vol. 6, no. 1, p. 15.
Schmidt, K., Kowalczyk, R., Ozolins, J., et al., Genetic structure of the Eurasian lynx population in north-eastern Poland and the Baltic States, Conserv. Genet., 2009, vol. 10, no. 2, pp. 497—501.
Schmidt, K., Ratkiewicz, K., and Konopiński, M.K., The importance of genetic variability and population differentiation in the Eurasian lynx Lynx lynx for conservation, in the context of habitat and climate change, Mamm. Rev., 2011, vol. 41, no. 2, pp. 112—124.
Sunnucks, P., Efficient genetic markers for population biology, Trends Ecol. Evol., 2000, vol. 15, no. 5, pp. 199—203.
Perry, E.A., Carr, S.M., Bartlett, S.E., and Davidson, W.S., A phylogenetic perspective on the evolution of reproductive behavior in pagophlis seals of the northwest Atlantic as indicated by DNA sequences, J. Mammal., 1995, vol. 76, no. 1, pp. 22—31.
Taberlet, P., Fumagalli, L., Wust-Sauci, A.G., and Cosson, J.F., Comparative phylogeography and postglacial colonization routes in Europe, Mol. Ecol., 1998, vol. 7, no. 4, pp. 453—464.
Rokas, A., Atkinson, R.J., Webster, L.M.I., et al., Out of Anatolia: longitudinal gradients in genetic diversity support an eastern origin for a circum-Mediterranean oak gallwasp Andricus quercustozae,Mol. Ecol., 2003, vol. 12, no. 8, pp. 2153—2174.
Gündüz, İ., Jaarola, M., Tez, C., et al., Multigenic and morphometric differentiation of ground squirrels (Spermophilus, Scuiridae, Rodentia) in Turkey, with a description of a new species, Mol. Phylogenet. Evol., 2007, vol. 43, no. 3, pp. 916—935.
Fritz, U., Ayaz, D., Hundsdörfer, A.K., et al., Mitochondrial diversity of European pond turtles (Emys orbicularis) in Anatolia and the Ponto-Caspian Region: multiple old refuges, hotspot of extant diversification and critically endangered endemics, Org. Divers. Evol., 2009, vol. 9, no. 2, pp. 100—114.
Stamatis, C., Suchentrunk, F., Moutou, K.A., et al., Phylogeography of the brown hare (Lepus europaeus) in Europe: a legacy of south-eastern Mediterranean refugia?, J. Biogeog., 2009, vol. 36, no. 3, pp. 515—528.
Akın, C., Bilgin, C.C., Beerli, P., et al., Phylogeographic patterns of genetic diversity in eastern Mediterranean water frogs were determined by ecological processes and climate change in the Late Cenozoic, J. Biogeogr., 2010, vol. 37, no. 11, pp. 2111—2124.
Perktaş, U., Barrowclough, G.F., and Groth, J.G., Phylogeography and species limits in the green woodpecker complex (Aves: Picidae): multiple Pleistocene refugia and range expansion across Europe and Near East, Biol. J. Linn. Soc., 2011, vol. 104, no. 3, pp. 710—723.
Gür, H., The effects of the Late Quaternary glacial-interglacial cycles on Anatolian ground squirrels: range expansion during the glacial periods?, Biol. J. Linn. Soc., 2013, vol. 109, no. 1, pp. 19—32.
İbiş, O., Tez, C., and Özcan, S., Phylogenetic status of the Turkish red fox (Vulpes vulpes), based on partial sequences of the mitochondrial cytochrome b gene, Vert. Zool., 2014, vol. 64, no. 2, pp. 273—284.
İbiş, O., Aksöyek, E., Özcan, S., and Tez, C., A preliminary phylogenetic analysis of golden jackals (Canis aureus) (Canidae: Carnivora: Mammalia) from Turkey based on mitochondrial D-loop sequences, Vert. Zool., 2015, vol. 65, no. 3, pp. 391—397.
Korkmaz, E.M., Lunt, D.H., Çıplak, B., et al., The contribution of Anatolia to European phylogeography: the centre of origin of the meadow grasshopper, Chorthippus parallelus,J. Biogeog., 2014, vol. 41, no. 9, pp. 1793—1805.
Bilgin, R., Back to the suture: the distribution of intraspecific genetic diversity in and around Anatolia, Int. J. Mol. Sci., 2011, vol. 12, no. 6, pp. 4080—4103.
Şekercioğlu, Ç.H., Anderson, S., Akçay, E., et al., Turkey’s globally important biodiversity in crisis, Biol. Conserv., 2011, vol. 144, no. 12, pp. 2752—2769.
Aksöyek, E., İbiş, O., Özcan, S., et al., DNA barcoding of three species (Canis aureus, Canis lupus, Vulpes vulpes) of Canidae, Mitochondrial DNA, Part A, 2017, vol. 28, no. 5, pp. 747—755.
ACKNOWLEDGMENTS
This study was supported by the Scientific Research Fund at Erciyes University (Project Nr: FHD-2016-6554). We would like to thank to the Wildlife Conservation, Rescue, Rehabilitation, Application and Research Center, Kafkas University, and Dr. Sami Şimşek for his assistance in providing the samples, and Donna Sue Özcan for English editing.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
Rights and permissions
About this article
Cite this article
İbİş, O., Özcan, S., Kırmanoğlu, C. et al. Genetic Analysis of Turkish lynx (Lynx lynx) Based on Mitochondrial DNA Sequences. Russ J Genet 55, 1426–1437 (2019). https://doi.org/10.1134/S1022795419110061
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1022795419110061