BACKGROUND: The rat snake genus Elaphe once comprised several dozens of species distributed in temperate through tropical zones of the New and Old World. Based on molecular-genetic analyses in early 2000s, the genus was split into several separate genera, leaving only 15 Palearctic and Oriental species as its members. One of the three species also occurring in Europe is Elaphe sauromates, a robust snake from the Balkans, Anatolia, Caucasus, Ponto-Caspian steppes, and Levant that has been suspected to be composed of two or more genetically diverse populations. Here, we studied the genetic structure and morphological variation of E. sauromates, aiming to better understand its inter-population relationships and biogeography, and subsequently revise its taxonomy. METHODS: We reconstructed the phylogeography and analyzed the genetic structure of E. sauromates populations originating from most of its geographic range using both mitochondrial (COI, ND4) and nuclear (C-MOS, MC1R, PRLR, RAG1) DNA gene fragments. We employed Maximum likelihood and Bayesian inference methods for the phylogenetic tree reconstructions, supplemented with species delimitation methods, analysis of haplotype networks, and calculation of uncorrected p-distances. Morphological variation in 15 metric and 18 meristic characters was studied using parametric univariate tests as well as multivariate general linearized models. In total, we analyzed sequences originating from 63 specimens and morphological data from 95 specimens of E. sauromates sensu lato. RESULTS: The molecular phylogeny identified two clearly divergent sister lineages within E. sauromates, with both forming a lineage sister to E. quatuorlineata. The genetic distance between them (5.80-8.24% in mtDNA) is similar to the distances among several other species of the genus Elaphe. Both lineages are also moderately morphologically differentiated and, while none of the characters are exclusively diagnostic, their combination can be used for confident lineage identification. Here, following the criteria of genetic and evolutionary species concepts, we describe the lineage from eastern Anatolia and parts of the Lesser and Great Caucasus as a new species E. urartica sp. nov. DISCUSSION: Elaphe urartica sp. nov. represents a cryptic species whose ancestors presumably diverged from their common ancestor with E. sauromates around the Miocene-Pliocene boundary. The intraspecific genetic structure indicates that the recent diversity of both species has been predominantly shaped by Pleistocene climatic oscillations, with glacial refugia mainly located in the Balkans, Crimea, and/or Anatolia in E. sauromates and Anatolia and/or the Caucasus in E. urartica sp. nov.

Department of Biodiversity Studies and Ecological Monitoring T 1 Vyazemski Karadag Research Station Nature Reserve Russian Academy of Sciences Theodosia Crimea

Department of Biology Faculty of Science and Arts Adnan Menderes University Aydın Turkey

Department of Biology Faculty of Science Dokuz Eylül University Buca İzmir Turkey

Department of Zoology Charles University Prague Prague Czech Republic

Department of Zoology Comenius University in Bratislava Bratislava Slovakia

Laboratory of Herpetology Institute of Zoology National Academy of Sciences of Azerbaijan Baku Azerbaijan

Laboratory of Herpetology Zoological Institute Russian Academy of Sciences Saint Petersburg Russia

Research and Application Center for Fauna and Flora Dokuz Eylül University Buca İzmir Turkey

Scientific Department Federal State Institution Sochi National Park Sochi Russia

Zoological Department Tula State Regional Exotarium Ministry of Culture of Tula Region Tula Russia

Zobrazit více v PubMed

Aghasyan A, Avci A, Tuniyev B, Lymberakis P, Andrén C, Cogalniceanu D, Wilkinson J, Ananjeva NB, Üzüm N, Orlov NL, Podloucky R, Tuniyev S, Kaya U, Böhme W, Sindaco R, Borkin L, Milto K, Golynsky E, Rustamov A, Nuridjanov D, Munkhbayar K, Shestapol A. Elaphe sauromates. The IUCN Red List of Threatened Species. 2017;2017:e.T157265A746010. doi: 10.2305/IUCN.UK.2017-2.RLTS.T157265A746010.en. DOI

Ahmadzadeh F, Flecks M, Rödder D, Böhme W, Ilgaz Ç, Harris DJ, Engler NU, Üzüm N, Carretero MA. Multiple dispersal out of Anatolia: biogeography and evolution of oriental green lizards. Biological Journal of the Linnean Society. 2013;110(2):398–408. doi: 10.1111/bij.12129. DOI

Alekperov AM, Loginov AA. Essays on biology of the reptiles of Abşeron. Proceedings of the Azerbaijan State University. Series Biological. 1953;5:106–127.

Ananjeva NB, Orlov NL, Khalikov RG, Darevsky IS, Ryabov SA, Barabanov AV. The reptiles of Northern Eurasia. Taxonomic diversity, distribution, conservation status. 2006. Zoological Institute, Russian Academy of Sciences. Series Faunistica no. 47, Pensoft.

Arakelyan MS, Danielyan FD, Corti C, Sindaco R, Leviton AE. Herpetofauna of Armenia and Nagorno-Karabakh. Contribution to herpetology. Vol. 27. Salt Lake City: SSAR; 2011. p. 149.

Asher A, Asher TM. The peoples of Ararat. Charleston: BookSurge Publishing; 2009. p. 336.

Avise JC. Phylogeography: the history and formation of species. Cambridge: Harvard University Press; 2000.

Baker RJ, Bradley RD. Speciation in mammals and the genetic species concept. Journal of Mammalogy. 2006;87(4):643–662. doi: 10.1644/06-mamm-f-038r2.1. PubMed DOI PMC

Baran İ, Ilgaz Ç, Avcı A, Kumlutaş Y, Olgun K. Türkiye Amfibi ve Sürüngenleri. Ankara: Tübitak; 2012.

Blain H-A. Amphibians and Squamata Reptiles from Azokh 1/Chapter 9. Azokh Cave and the Transcaucasian Corridor. In: Fernández-Jalvo Y, King T, Yepiskoposyan L, Andrews P, editors. Series Vertebrate Paleobiology and Paleoanthropology. Dordrecht: Springer Science+Media; 2016. pp. 191–210.

Blain H-A, Agustí J, Lordkipanidze D, Rook L, Delfino M. Paleoclimatic and paleoenvironmental context of the Early Pleistocene hominins from Dmanisi (Georgia, Lesser Caucasus) inferred from the herpetofaunal assemblage. Quaternary Science Reviews. 2014;105:136–150. doi: 10.1016/j.quascirev.2014.10.004. DOI

Böhme W, Ščerbak NN. Elaphe quatuorlineata (Lacépède, 1789)—Vierstreifennatter. In: Böhme W, editor. Handbuch der Reptilien und Amphibien Europas. Band 3/I. Schlangen (Serpentes) I (Typhlopidae, Boidae, Colubridae 1: Colubrinae) Wiesbaden: AULA—Verlag; 1993. pp. 373–396.

Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ. BEAST 2: a software platform for Bayesian evolutionary analysis. PLOS Computational Biology. 2014;10:e1003537. doi: 10.1371/journal.pcbi.1003537. PubMed DOI PMC

Boulenger GA. Catalogue of the snakes in the British Museum. V. II, containing the conclusion of the Colubridae aglyphae. London: British Museum Natural History; 1894. 382, + 25 figs, 20 pls.

Bunyatova S. The reptiles of caucasian major within Azerbaijan. Proceedings of International Caucasian Forestry Symposium; 24–26 October 2013; Artvin. 2013. pp. 611–616.

Bunyatova SN, Akhmedov SB, Dzhafarov AR. Ekologicheskyi analiz gerpetofauny (Testudinidae: Sauria: Serpentes) Talysha (An ecological analysis of the herpetofauna (Testudinidae: Sauria: Serpentes) of Talysh). Trudy Samarskogo nauchno-issledovatelskogo tsentra Rossiyiskoyi akademii nauk. Proceedings of the Samara Scientific Center of Russian Academy of Sciences. 2012;14:144–149.

Burbrink FT, Lawson R. How and when did Old World rat snakes disperse into the New World? Molecular Phylogenetics and Evolution. 2007;43(1):173–189. doi: 10.1016/j.ympev.2006.09.009. PubMed DOI

Chen X, Lemmon AR, Lemmon EM, Pyron AR, Burbrink FT. Using phylogenomics to understand the link between biogeographic origins and regional diversification in ratsnakes. Molecular Phylogenetics and Evolution. 2017;111:206–218. doi: 10.1016/j.ympev.2017.03.017. PubMed DOI

Clark RJ, Clark ED. Report on a collection of amphibians and reptiles from Turkey. Occasional Papers of the California Academy of Sciences. 1973;104:1–62.

Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Molecular Ecology. 2000;9(10):1657–1659. doi: 10.1046/j.1365-294x.2000.01020.x. PubMed DOI

Davis PH. Distribution patterns in Anatolia with particular reference to endemism. In: Davis PH, editor. Plant Life of South-West Asia. Edinburgh: Botanical Society of Edinburgh; 1971. pp. 15–27.

Dubois A, Nemésio A. Does nomenclatural availability of nomina of new species or subspecies require the deposition of vouchers in collections? Zootaxa. 2007;1409:1–22.

Ezard T, Fujisawa T, Barraclough T. SPLITS: species’ limits by threshold statistics. R package version 1https://rdrr.io/rforge/splits/ 2009

Fišer C, Robinson CT, Malard F. Cryptic species as a window into the paradigm shift of the species concept. Molecular Ecology. 2018;27(3):613–635. doi: 10.1111/mec.14486. PubMed DOI

Flärdh B. Herpetofaunan pa Mount Ararat. Snoken. Journal of National Swedish Herpetological Association. 1983;13:31–38.

Flot JF. Seqphase: a web tool for interconverting phase input/output files and fasta sequence alignments. Molecular Ecology Resources. 2010;10(1):162–166. doi: 10.1111/j.1755-0998.2009.02732.x. PubMed DOI

Fraser DJ, Bernatchez L. Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology. 2001;10(12):2741–2752. PubMed

Fritz U, Ayaz D, Buschbom J, Kami HG, Mazanaeva LF, Aloufi AA, Auer M, Rifai L, Šilić T, Hundsdörfer AK. Go east: phylogeographies of Mauremys caspica and M. rivulata—discordance of morphology, mitochondrial and nuclear genomic markers and rare hybridization. Journal of Evolutionary Biology. 2008;21:527–540. PubMed

Guicking D, Joger U, Wink M. Cryptic diversity in a Eurasian water snake (Natrix tessellata, Serpentes: Colubridae): evidence from mitochondrial sequence data and nuclear ISSR-PCR fingerprinting. Organisms, Diversity, and Evolution. 2009;9(3):201–214.

Gvoždík V, Jandzik D, Cordos B, Rehák I, Kotlík P. A mitochondrial DNA phylogeny of the endangered vipers of the Vipera ursinii complex. Molecular Phylogenetics and Evolution. 2012;62(3):1019–1024. doi: 10.1016/j.ympev.2011.12.001. PubMed DOI

Gvoždík V, Jandzik D, Lymberakis P, Jablonski D, Moravec J. Slow worm, Anguis fragilis (Reptilia: Anguidae) as a species complex: genetic structure reveals deep divergences. Molecular Phylogenetics and Evolution. 2010;55(2):460–472. doi: 10.1016/j.ympev.2010.01.007. PubMed DOI

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

Helfenberger N. Phylogenetic relationships of Old World ratsnakes based on visceral organ topography, osteology, and allozyme variation. Russian Journal of Herpetology. 2001;8:1–62.

Huang S, Ding L, Burbrink FT, Yang J, Huang J, Ling C, Chen X, Zhang Y. A new species of the genus Elaphe (Squamata: Colubridae) from Zoige County, Sichuan, China. Asian Herpetological Research. 2012;3(1):38–45. doi: 10.3724/SP.J.1245.2012.00038. DOI

Iljashenko VYu, Shatalkin AI, Kuvaev AV, Komendatov AYu, Britaev TA, Kosyan AR, Pavlov DS, Shilin NI, Ananjeva NB, Tuniyev BS, Semenov DV, Syroechkovsky EE, Morozov VV, Mischenko AL, Rozhnov VV, Poyarkov AD. Rare and endangered animals of Russia. Materials to the Red Data Book of Russian Federation. Moscow: Company of scientific publications “KMK”; 2018. p. 112.

Jablonski D, Soltys K, Simonov E. Complete mitochondrial genome of the Four-lined snake, Elaphe quatuorlineata (Bonnaterre, 1790) Mitochondrial DNA Part B—Resources. 2019;4(1):897–898. doi: 10.1080/23802359.2019.1573121. DOI

Jandzik D, Avcı A, Gvoždík V. Incongruence between taxonomy and genetics: three divergent lineages within two subspecies of the rare Transcaucasian rat snake (Zamenis hohenackeri) Amphibia-Reptilia. 2013;34(4):579–584. doi: 10.1163/15685381-00002911. DOI

Jandzik D, Jablonski D, Zinenko O, Kukushkin OV, Moravec J, Gvoždík V. Pleistocene extinctions and recent expansions in an anguid lizard of the genus Pseudopus. Zoologica Scripta. 2018;47(1):21–32.

Kahle R-D, García N, Kostopoulos DS, Lacombat F, Lister AM, Mazza PPA, Spassov N, Titov VV. Western Palaearctic palaeoenvironmental conditions during the Early and early Middle Pleistocene inferred from large mammal communities, and implications for hominin dispersal in Europe. Quaternary Science Reviews. 2011;30:1368–1395. doi: 10.1016/j.quascirev.2010.07.020. DOI

Kapli P, Botoni D, Ilgaz Ç, Kumlutaş Y, Avci A, Rastegar-Pouyani N, Fathinia B, Lymberakis P, Ahmadzadeh F, Poulakakis N. Molecular phylogeny and historical biogeography of the Anatolian lizard Apathya (Squamata, Lacertidae) Molecular Phylogenetics and Evolution. 2013;66(3):992–1001. doi: 10.1016/j.ympev.2012.12.002. PubMed DOI

Kapli P, Lutteropp S, Zhang J, Kobert K, Pavlidis P, Stamatakis A, Flouri T. Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. biorxiv preprint. 2016063875 PubMed PMC

Kornilios P. Polytomies, signal and noise: revisiting the mitochondrial phylogeny and phylogeography of the Eurasian blindsnake species complex (Typhlopidae, Squamata) Zoologica Scripta. 2017;46(6):665–674.

Kornilios P, Ilgaz Ç, Kumlutaş Y, Lymberakis P, Moravec J, Sindaco R, Rastegar-Pouyani N, Afroosheh M, Giokas S, Fraguedakis-Tsolis S, Chondropoulos B. Neogene climatic oscillations shape the biogeography and evolutionary history of the Eurasian blindsnake. Molecular Phylogenetics and Evolution. 2012;62(3):856–873. doi: 10.1016/j.ympev.2011.11.035. PubMed DOI

Kornilios P, Ilgaz Ç, Kumlutaş Y, Giokas S, Fraguedakis-Tsolis S, Chondropoulos B. The role of Anatolian refugia in herpetofaunal diversity: an mtDNA analysis of Typhlops vermicularis Merrem, 1820 (Squamata, Typhlopidae) Amphibia-Reptilia. 2011;32(3):351–363. doi: 10.1163/017353711X579858. DOI

Kornilios P, Thanou E, Lymberakis P, Sindaco R, Liuzzi C, Giokas S. Mitochondrial phylogeography, intraspecific diversity and phenotypic convergence in the four-lined snake (Reptilia, Squamata) Zoologica Scripta. 2014;43(2):149–160.

Kotsakiozi P, Jablonski D, Ilgaz Ç, Kumlutaş Y, Avcı A, Meiri S, Itescu Y, Kukushkin OV, Gvoždík V, Scillitani G, Roussos S, Jandzik D, Kasapidis P, Lymberakis P, Poulakakis P. Multilocus phylogeny and coalescent species delimitation in Kotschy’s gecko, Mediodactylus kotschyi: hidden diversity and cryptic species. Molecular Phylogenetics and Evolution. 2018;125:177–187. PubMed

Krijgsman W, Tesakov A, Yanina T, Lazarev S, Danukalova G, Van Baak CGC, Agustí J, Alçiçek MC, Aliyeva E, Bista D, Bruch A, Büyükmeriç Y, Bukhsianidze M, Flecker R, Frolov P, Hoyle TM, Jorissen EL, Kirscher U, Koriche SA, Kroonenberg SB, Lordkipanidze D, Oms O, Rausch L, Singarayer J, Stoica M, Van de Velde S, Titov VV, Wesselingh FP. Quaternary time scales for the Pontocaspian domain: Interbasinal connectivity and faunal evolution. Earth-Science Reviews. 2018;188:1–40. doi: 10.1016/j.earscirev.2018.10.013. DOI

Kropachev II, Shiryaev KA, Thien NT, Orlov NL. New record of Protobothropos cf. maolanensis in Northeastern Vietnam, with data on its morphology and biology. Russian Journal of Herpetology. 2015;22:93–102.

Kyriazi P, Poulakakis N, Parmakelis A, Crochet PA, Moravec J, Rastegar-Pouyani N, Tsigenopoulos CS, Magoulas A, Mylonas M, Lymberakis P. Mitochondrial DNA reveals the genealogical history of the snake-eyed lizards (Ophisops elegans and O. occidentalis) (Sauria: Lacertidae) Molecular Phylogenetics and Evolution. 2008;49(3):795–805. doi: 10.1016/j.ympev.2008.08.021. PubMed DOI

Lanfear R, Calcott B, Ho SYW, Guindon S. Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution. 2012;29(6):1695–1701. doi: 10.1093/molbev/mss020. PubMed DOI

Lenk P, Joger U, Wink M. Phylogenetic relationships among European ratsnakes of the genus Elaphe Fitzinger based on mitochondrial DNA sequence comparisons. Amphibia-Reptilia. 2001;22(3):329–339. doi: 10.1163/156853801317050124. DOI

Li E, Feng D, Yan P, Xue H, Chen J, Wu XB. The complete mitochondrial genome of Oocatochus rufodorsatus (Reptilia, Serpentes, Colubridae) Mitochondrial DNA. 2014;25(6):449–450. doi: 10.3109/19401736.2013.814116. PubMed DOI

Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25(11):1451–1452. doi: 10.1093/bioinformatics/btp187. PubMed DOI

Lymberakis P, Poulakakis N. Three continents claiming an archipelago: the evolution of Aegean’s herpetofaunal diversity. Diversity. 2010;2(2):233–255. doi: 10.3390/d2020233. DOI

Marzahn E, Mayer W, Joger U, Ilgaz Ç, Jablonski D, Kindler C, Kumlutaş U, Nistri A, Schneeweiss N, Vamberger M, Žagar A, Fritz U. Phylogeography of the Lacerta viridis complex: mitochondrial and nuclear markers provide taxonomic insights. Journal of Zoological Systematics and Evolutionary Research. 2016;54(2):85–105. doi: 10.1111/jzs.12115. DOI

Mazanaeva LF, Askenderov AD. Landscape-zonal distribution of amphibians and reptiles in the Intermontane Daghestan. Bulletin of Daghestan Scientific Center. 2014;54:53–58.

Mazanaeva LF, Tuniyev BS. Zoogeograficheskij analiz gerpetofauny Dagestana. Sovremennaya gerpetologiya. 2011;11:55–76.

Mizsei E, Jablonski D, Roussos SA, Dimaki M, Ioannidis Y, Nilson G, Nagy ZT. Nuclear markers support the mitochondrial phylogeny of Vipera ursinii–renardi complex (Squamata: Viperidae) and species status for the Greek meadow viper. Zootaxa. 2017;4227:75–88. doi: 10.11646/zootaxa.4227.1.4. PubMed DOI

Musilová R, Zavadil V, Marková S, Kotlík P. Relics of the Europe’s warm past: Phylogeography of the Aesculapian snake. Molecular Phylogenetics and Evolution. 2011;57:1245–1252. PubMed

Muskhelishvili TA. Presmykayuschiesya vostochnoyi Gruzii (Reptiles of the eastern Georgia) Tbilisi: Metsniereba; 1970. p. 244.

Nagy ZT, Lawson R, Joger U, Wink M. Molecular systematics of racers, whipsnakes and relatives (Reptilia: Colubridae) using molecular and nuclear markers. Journal of Zoological Systematics and Evolutionary Research. 2004;42(3):223–233. doi: 10.1111/j.1439-0469.2004.00249.x. DOI

Nagy ZT, Bellaagh M, Wink M, Paunović A, Korsós Z. Phylogeography of the Caspian whipsnake in Europe with emphasis on the westernmost populations. Amphibia-Reptilia. 2010;31(4):455–461. doi: 10.1163/017353710x518397. DOI

Najafov Dj, Hashimov R, Isgenderov T. Distribution and ecology of snakes (Reptilia, Ophidia) on the Absheron Peninsula. Bulletin of Moscow State Open University, Series Natural Sciences. 2013;1:13–16.

Nilson G, Andrén C, Flärdh B. Vipera albizona, a new mountain viper from central Turkey, with comments on isolating effects of the Anatolian “Diagonal”. Amphibia-Reptilia. 1990;11(3):285–294. doi: 10.1163/156853890x00203. DOI

Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP. Sequence-Based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology. 2006;55(4):595–609. doi: 10.1080/10635150600852011. PubMed DOI

Psonis N, Antoniou A, Karameta E, Leaché AD, Kotsakiozi P, Darriba D, Kozlov A, Stamatakis A, Poursanidis D, Kukushkin O, Jablonski D, Crnobrnja-Isailović J, Gherghel I, Lymberakis P, Poulakakis N. Resolving complex phylogeographic patterns in the Balkan Peninsula using closely related wall-lizard species as a model system. Molecular Phylogenetics and Evolution. 2018;125:100–115. doi: 10.1016/j.ympev.2018.03.021. PubMed DOI

R Development Core Team . R: a language and environment for statistical computing. Vienna: The R Foundation for Statistical Computing; 2019.

Rambaut A, Suchard MA, Xie W, Drummond A. Tracer 1.6. 2013. http://beast.bio.ed.ac.uk/Tracer. [1 February 2018]. http://beast.bio.ed.ac.uk/Tracer

Ratnikov VYu. Trudy nauchno-issledovatelskogo instituta geologii Voronezhskogo gosudarstvennogo universiteta (Proceedings of the Institute of Geology of the Voronezh State University) Voronezh: Publishing House of the Voronezh State University; 2002. Pozdnekayinozoyiskie zemnovodnye i scheshuyichatye presmykayuschiesya Vostochno-Evropeyiskoi ravniny (Late Cenozoic Amphibians and Squamate Reptiles of the East European Plain) p. 138.

Ratnikov VYu. Nekotorye soobrazheniya o formoobrazovanii i dinamike arealov u zemnovodnykh i presmykayuschihsya Evropy v pleistocene (Some arguments about speciation and distribution ranges dymamics at European amphibians and reptiles during Pleistocene) Amurskyi Zoologicheskyi Zhurnal (Amurian Zoological Journal) 2014;6:308–316.

Ratnikov VYu. Scheshuyichatye presmykayuschiesya iz verkhnepleistocenovykh otlozhenyi peschery Emine-Bair-Khosar v Krymu (Squamate reptiles from Upper Pleistocene deposites of the cave Emine-Bair-Khosar in the Crimea); (Biospeleology of the Caucasus and others regions of Russia) Biospeleologiya Kavkaza i drugikh rayionov Rossii: Proceedings of All-Russian Conference of Young Scientists; 3–4 December, 2015; Moscow, Kostroma: Kostromskoyi Publishing House; 2015. pp. 64–65.

Red Data book of Kazakhstan (Krаsnaya kniga Kazakhstana) Zhivotnye (Animals). Part 1. Pozvonochnye (Vertebates) Vol. 1. Almaty: Konzhyk; 1996. p. 324.

Red Data book of Turkmenistan (Krasnaya kniga Turkmenistana) Bespozvonochnye i pozvonochnye zhivotnye. Invertebrate and vertebrate animals. Vol. 1. Ashkhabad: Ylym; 1999. p. 370.

Red Data book of Ukraine. Animal Kingdom (Chervona kniga Ukrayiny. Tvarynnyi svit) Kiev. Ukrayins’ka entsiklopediya imeni M. P. Bazhana (“Ukrainskaya encyclopedia imeni M.P Bazhana”) 1994. p. 457.

Redcozubov OI. Neogenovye reptilii Moldovy (Neogene reptiles of Moldova) 1991. p. 20. Synopsis of PhD Research Theses. Palaeontological Institute of Academy of Sciences of the USSR.

Redcozubov OI. Razvitie fauny reptilyi v neogene na territorii respubliki Moldova. Paleoekologicheskie, biostratigraficheskie aspekty (Development of the reptiles fauna in Neogene at the territory of Republic of Moldova. Palaeoecological, biostratigraphic aspects). Sovremennye problemy zoologii i ekologii (Current Challenges of Zoology and Ecology): Proceedings of International Scientific-Memorial Conference Dedicated to 120th Anniversary of Birthday of prof. I. I Puzanov; 22–25 April, 2005; Odessa: Phoenix; 2005. pp. 222–224.

Ronquist F, Teslenko M, Van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology. 2012;61(3):539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

Safaei-Mahroo B, Ghaffari H, Fahimi H, Broomand S, Yazdanian M, Najafi Majd E, Hosseinian Yousefkhani SS, Rezazadeh E, Hosseinzadeh MS, Nasrabadi R, Rajabizadeh M, Mashayekhi M, Motesharei A, Naderi A, Kazemi SM. The herpetofauna of Iran: checklist of taxonomy, distribution and conservation status. Asian Herpetological Research. 2015;6:257–290.

Sahlean TC, Strugariu A, Dincă PC, Chişamera G, Stanciu CR, Zamifresku SR, Gherghel I, Moraru VE. Morphological characteristics of the elusive blotched snake (Elaphe sauromates) at its northwestern range limit (Romania) Turkish Journal of Zoology. 2016;40(1):136–140.

Schulz K-D. Eine Monographie der schlangengattung Elaphe Fitzinger. Wurselen: Bushmaster Publications; 1996. p. 460.

Şensoy S, Demircan M, Ulupinar U, Balta İ. Climate of Turkey. Web site of Turkish state meteorological serviсe. 2016. http://www.mgm.gov.tr/files/en-us/climateofturkey.pdf http://www.mgm.gov.tr/files/en-us/climateofturkey.pdf

Sillero N, Campos J, Bonardi A, Corti C, Creemers R, Crochet P-A, Crnobrnja Isailovic J, Denoël M, Ficetola GF, Gonçalves J, Kuzmin S, Lymberakis P, De Pous P, Rodríguez A, Sindaco R, Speybroeck J, Toxopeus B, Vieites DR, Vences M. Updated distribution and biogeography of amphibians and reptiles of Europe. Amphibia-Reptilia. 2014;35(1):1–31. doi: 10.1163/15685381-00002935. DOI

Simpson GG. The species concept. Evolution. 1951;5:285–298.

Sindaco R, Jeremčenko VK. The reptiles of the Western Palearctic. 1. Annotated checklist and distributional atlas of the turtles, crocodiles, amphisbaenians and lizards of Europe, North Africa, Middle East and Central Asia. Latina: Edizioni Belvedere; 2008. p. 579.

Sindaco R, Venchi A, Carpaneto GM, Bologna MA. The reptiles of Anatolia: a checklist and zoogeographical analysis. Biogeographia—The Journal of Integrative Biogeography. 2000;21:441–554. doi: 10.21426/b6110017. DOI

Sindaco R, Venchi A, Grieco C. The reptiles of the Western Palearctic 2. Annotated checklist and distributional Atlas of the snakes of Europe, North Africa, the Middle East and Central Asia, with an update to the vol. 1. Latina: Societas Herpetologica Italica, Via Adige; 2013.

Skourtanioti E, Kapli P, Ilgaz Ç, Kumlutaş Y, Avci A, Ahmadzadeh F, Crnobrnja-Isailović J, Gherghel I, Lymberakis P, Poulakakis N. A reinvestigation of phylogeny and divergence times of the Ablepharus kitaibelii species complex (Sauria, Scincidae) based on mtDNA and nuDNA genes. Molecular Phylogenetics and Evolution. 2016;103:199–214. doi: 10.1016/j.ympev.2016.07.005. PubMed DOI

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC

Stephens M, Smith NJ, Donnelly P. A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics. 2001;68(4):978–989. doi: 10.1086/319501. PubMed DOI PMC

Strauch A. Die Schlangen des Russischen Reichs, in systematischer und zoogeographischer Beziehung. Mémoires de l’Académie impériale des sciences de St. Pétersbourg. Series 721; 1873. pp. 1–288.

Stümpel N, Rajabizadeh M, Avcı A, Wüster W, Joger U. Phylogeny and diversification of mountain vipers (Montivipera, Nilson et al., 2001) triggered by multiple Plio–Pleistocene refugia and high-mountain topography in the Near and Middle East. Molecular Phylogenetics and Evolution. 2016;101:336–351. doi: 10.1016/j.ympev.2016.04.025. PubMed DOI

Szyndlar Z. Fossil snakes form Poland. Acta Zoologica Cracoviensia. 1984;28:1–156.

Szyndlar Z. A review of Neogene and Quaternary snakes of central and eastern Europe. Part I: Scolecophidia, Boidae, Colubridae. Estudios Geológicos. 1991;47(1):103–126.

Tamar K, Šmíd J, Göçmen B, Meiri S, Carranza S. An integrative systematic revision and biogeography of Rhynchocalamus snakes (Reptilia, Colubridae) with a description of a new species from Israel. PeerJ. 2016;4:e2769. doi: 10.7717/peerj.2769. PubMed DOI PMC

Tiedemann F, Häupl M. Ein weiterer Nachweis von Elaphe quatuorlineata aus Syrien. Salamandra. 1978;14(4):212–214.

Tuniyev BS. On the Mediterranean influence on the formation of herpetofauna of the Caucasian isthmus and its main xerophylous refugia. Russian Journal of Herpetology. 1995;2(2):95–119.

Tuniyev BS, Orlov NL, Ananjeva NB, Agasyan AL. St. Petersburg-Moscow: KMK Scientific Press Ltd; 2009. Snakes of the Caucasus: taxonomic diversity, distribution, conservation.

Tuniyev BS, Tuniyev SB, Avcı A, Ilgaz Ç. Gerpetologicheskie issledovanija v vostochnoj i severo-vostochnoj Turcii. Sovremennaya gerpetologiya. 2014;14:44–53.

Utiger U, Helfenberger N, Schätti B, Schmidt C, Ruf M, Ziswiler V. Molecular systematics and phylogeny of Old World and New World ratsnakes, Elaphe auct., and related genera (Reptilia, Squamata, Colubridae) Russian Journal of Herpetology. 2002;9(2):105–124.

Venczel M. Quaternary snakes of Bihor (Romania) Oradea: Editura Muzeului Tării Crişurilor; 2000. p. 144.

Venczel M, Şen S. Pleistocene amphibians and reptiles from Emirkaya-2, Turkey. Herpetological Journal. 1994;4:159–165.

Venczel M, Várdai G. The genus Elaphe in the Carpathian basin: fossil record. Nymphaea (Folia Naturae Bihariae) 2000;28:65–82.

Wallach V, Williams KL, Boundy J. Snakes of the World. A catalogue of living and extinct species. London, New York: CRC Press, Taylor & Francis Group; 2014. p. 1227.

Wiley EO. The evolutionary species concept reconsidered. Systematic Zoology. 1978;27(1):17–26. doi: 10.2307/2412809. DOI

Zinner H. Contributions to the herpetofauna of Mount Hermon. No III. Elaphe quatuorlineata (Ophidia: Colubridae) Israel Journal of Zoology. 1972;21:123–127.

Zhang J, Kapli P, Pavlidis P, Stamatakis A. A general species delimitation method with applications to phylogenetic placements. Bioinformatics. 2013;29(22):2869–2876. doi: 10.1093/bioinformatics/btt499. PubMed DOI PMC