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Issue: Vol. 4471 No. 1: 4 Sept. 2018
Type: Article
Published: 2018-09-04
DOI: 10.11646/zootaxa.4471.1.6
Page range: 137–153
Abstract views: 188
PDF downloaded: 2

A new subspecies of Zamenis hohenackeri (Strauch, 1873) (Serpentes: Colubridae) based on morphological and molecular data

Helmholtz Centre for Environmental Research, Permoserstrasse 15, 04318 Leipzig, Germany
Institute of Development, Ecology, Conservation and Cooperation, Via G. Tomasi di Lampedusa 33, 00144 Rome, Italy.
An Kuckum 5a, 52146 Würselen, Germany.
College of Education Thurgau, 8280 Kreuzlingen, Switzerland.
Department of Biology, Zoology Section, Ege University, Faculty of Science, TR 35100 Bornova-Izmir, Turkey.
Zoological Research Museum Alexander Koenig, Leibniz Institute for Animal Biodiversity, Adenauerallee 160, 53113 Bonn, Germany.
Reptilia Anatolia colour pattern Colubridae phylogeography Transcaucasian rat snake Leopard snake

Abstract

Based on morphological characteristics, two subspecies of the Transcaucasian rat snake (Zamenis hohenackeri) are currently recognized, namely Z. h. tauricus and Z. h. hohenackeri. Both subspecies are repeatedly considered to be conspecific colour morphs, or have even been confused with Z. situla. Although, few studies involved the Transcaucasian rat snake in a phylogenetic approach, none has so far led to any taxonomic changes. We assessed the intraspecific morphological variation and phylogeographic relationships among specimens from different locations across its updated distribution. Our molecular (1191 bp mtDNA, 565 bp nuDNA) and morphological data provide sufficient evidence to support three distinct lineages within the Z. hohenackeri complex with a different arrangement compared to a previous study. These represent the subspecies Z. h. hohenackeri, Z. h. tauricus, and a lineage from southwestern Turkey which is described as a new subspecies. Aspects of historical biogeography and conservation status are briefly discussed.

 

References

  1. Afrasiab, S.R. & Mohamad, S.I. (2011) First record of the rat snake, Zamenis hohenackeri (Strauch, 1873), from north-eastern Iraq with notes on other colubrid snakes. Zoology in the Middle East, 54, 19–22.
    https://doi.org/10.1080/09397140.2011.10648877

    Arakeylan, M.S., Danielyan, F.D., Corti, C., Sindaco, R. & Leviton, A.E. (2011) Herpetofauna of Armenia and Nagorno-Karabakh. Society for the Study of Amphibians and Reptiles Publications, Oxford/Ohio, 149 pp.

    Baran, I. (1978) Some rare species of snakes from Turkey. Annalen des Naturhistorischen Museums in Wien, 81, 261–265.

    Bischoff, W. (1993) Elaphe hohenackeri (Strauch, 1873)—Transkaukasische Kletternatter. In: Böhme, W. (Ed.), Handbuch der Reptilien und Amphibien Europas. Aula-Verlag, Wiesbaden, pp. 317–329.

    Brauch, H.G., Liotta, P.H., Marquina, A., Rogers, P.F. & Selim, M.E.-S. (2003) Security and Environment in the Mediterranean. Conceptualising Security and Environmental Conflicts: Springer, 1137 pp.
    https://doi.org/10.1007/978-3-642-55854-2

    Burbrink, F.T. & Lawson, R. (2007) How and when did Old World ratsnakes disperse into the New World? Molecular Phylogenetics and Evolution, 43, 173–189.
    https://doi.org/10.1016/j.ympev.2006.09.009

    Çine, A., Doğan, U., Yıldırım, C., Akçar, N., Ivy-Ochs, S., Alfimov, V., Kubik , P.W. & Schlüchter, C. (2015) Quaternary uplift rates of the Central Anatolian Plateau, Turkey: insights from cosmogenic isochron-burial nuclide dating of the Kizilirmak River terraces. Quaternary Science Reviews, 107, 81–97.
    https://doi.org/10.1016/j.quascirev.2014.10.007

    Clement, M., Snell, Q., Walke, P., Posada, D. & Crandall, K. (2002) TCS: estimating gene genealogies. Proceedings of the 16th International Parallel and Distributed Processing Symposium, 2, 184.
    https://doi.org/10.1109/IPDPS.2002.1016585

    Cosentino, D., Schildgen, T. F., Cipollari, P., Faranda, C., Gliozzi, E., Hudackova, N., Lucifora, S. & Strecker, M.R. (2012) Late Miocene surface uplift of the southern margin of the Central Anatolian Plateau, Central Taurides, Turkey. Geological Society of America Bulletin, 124, 133–145.
    https://doi.org/10.1130/B30466.1

    Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
    https://doi.org/10.1186/1471-2148-7-214

    Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.
    https://doi.org/10.1093/molbev/mss075

    Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.
    https://doi.org/10.1093/nar/gkh340

    Flot, J.F. (2010) SeqPHASE: a web tool for interconverting PHASE input/ output files and FASTA sequence alignments. Molecular Ecology Ressources, 10, 162–166.
    https://doi.org/10.1111/j.1755-0998.2009.02732.x

    Franzen, M., Bussmann, M., Kordges, K. & Thiesmeier, B. (2008) Die Amphibien und Reptilien der Südwest-Türkei. Laurenti-Verlag, Bielefeld, 328 pp.

    Göçmen, B., Mebert, K., Karış, M., Oğuz, M.A. & Ursenbacher, S. (2017) A new population and subspecies of the critically endangered Anatolian meadow viper Vipera anatolica Eiselt and Baran, 1970 in eastern Antalya province. Amphibia-Reptilia, 38, 289–305.
    https://doi.org/10.1163/15685381-00003111

    Holman, J.A. (2000) Fossil Snakes of North America. Origin, Evolution, Distribution, Paleoecology. Indiana University Press, Indianapolis, 376 pp.

    Hraoui-Bloquet, S., Sadek, R., Tok, V., Ugurtas, I. H., Sevinç, M., Werner, Y., et al. (2009) Zamenis hohenackeri. The IUCN Red List of Threatened Species 2009.
    https://doi.org/10.2305/IUCN.UK.2009.RLTS.T157251A5060528.en

    Ivanov, M. (1997) Hadi evropského kenozoika (The Snakes of the European Cenozoic). Unpublished Ph.D. thesis, Masaryk University, Brno, 217 pp.

    Ivanov, M. (2002) The oldest known Miocene snake fauna from Central Europe: Merkur-North locality, Czech Republic. Acta Palaeontologica Polonica, 47, 513–534.

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

    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.
    https://doi.org/10.1093/bioinformatics/bts199

    Koressaar, T. & Remm, M. (2007) Enhancements and modifications of primer design program Primer3 Bioinformatics, 23, 1289–1291.

    Kumlutaş, Y., Öz, M., Tunc, M. R., Kaska, Y., Özdemir, A. & Düşen, S. (2004) On snake species of the western Taurus Range, Turkey. Natura Croatica, 13, 19–33.

    Kyriazi, P., Kornilios, P., Nagy, Z.T., Poulakakis, N., Kumlutas, Y., Ilgaz, C., Avcı, A., Göçmen, B. & Lymberakis, P. (2013) Comparative phylogeography reveals distinct colonization patterns of Cretan snakes. Journal of Biogeography, 40, 1143–1155.
    https://doi.org/10.1111/jbi.12057

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

    Lanfear, R., Calcott, B., Kainer, D., Mayer, C. & Stamatakis, A. (2014) Selecting optimal partitioning schemes for phylogenomic datasets. BMC Evolutionary Biology, 14, 82.
    https://doi.org/10.1186/1471-2148-14-82

    Leigh, J.W. & Bryant, D. (2015) PopART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110–1116.
    https://doi.org/10.1111/2041-210X.12410

    Mebert, K., Göçmen, B., Karış, M., İğci, N. & Ursenbacher, S. (2016) The valley of four viper species and a highland of dwarfs: Fieldwork on threatened vipers in northeastern Turkey. International Reptile Conservation Foundation Reptiles and Amphibians, 23, 1–9.

    Müller, L. (1939) Bemerkungen über einige von Herrn Fr. Fuss in der Umgebung von Akschehir, Anatolien, gesammelte Schlangen. I, und II. Zoologischer Anzeiger Leipzig, 127, 83–95.

    Nikolskij, A.M. (1916) Fauna Rossii i sopredelnykh stran. Presmykajuszczijasja.Tom II. Ophidia [Fauna of Russia and adjacent countries. Reptiles. Vol. II. Ophidia]. Akademii Nauk, Petrograd [St. Petersburg], III + 349 + 1 pp.

    Nilson, G. & Andrén, C. (1984) A taxonomic account of the Iranian Ratsnakes of the Elaphe longissima species-group. Amphibia-Reptilia, 5, 157–171.
    https://doi.org/10.1163/156853884X-005-02-10

    RDevelopmentCoreTeam (2017) R: A language and environment for statistical computing. In. R Foundation for Statistical Computing, Vienna, Austria. Available from: https://www.R-project.org (accessed 19 July 2018)

    Şafak, Ü., Kelling, G., Gökçen, N.S. & Gürbüz, K. (2005) The mid-Cenozoic succession and evolution of the Mut basin, southern Turkey, and its regional significance. Sedimentary Geology, 173, 121–150.
    https://doi.org/10.1016/j.sedgeo.2004.03.012

    Salvi, D., Mendes, J., Carranza, S. & Harris, D.J. (2018) Evolution, biogeography and systematics of the western Palaearctic Zamenis ratsnakes. Zoologica Scripta, 47 (4), 441–461. [first published 17 June 2018]
    https://doi.org/10.1111/zsc.12295

    Schätti, B. & Baran, I. (1988) Bemerkung zur Verbreitung von Elaphe hohenackeri (STRAUCH, 1873) und Vipera xanthina (GRAY, 1849) in Süd-Anatolien (Serpentes: Colubridae, Viperidae). Salamandra, 24, 306–309.

    Schemmel, F., Mikes, T., Rojay, B. & Mulch, A. (2013) The impact of topography on isotopes in precipitation across the Central Anatolian Plateau (Turkey). American Journal of Science, 313, 61–80.
    https://doi.org/10.2475/02.2013.01

    Schulz, K.-D. (1996) A monograph of the colubrid snakes of the genus Elaphe Fitzinger. Koeltz Scientific Books, Havlickuv, iii + 439 pp.

    Schulz, K.-D. (2013) An annotated and illustrated checklist of Old World ratsnakes. In: Schulz, K.-D. (Ed.), Old World Ratsnakes. A Collection of Papers. Bushmaster Publications, Berg SG, pp. 17–268.

    Stamatakis, A. (2014) RAxML Version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.
    https://doi.org/10.1093/bioinformatics/btu033

    Stephens, M., Smith, N.J. & Donnelly, P. (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68, 978–989.
    https://doi.org/10.1086/319501

    Stephens, M. & Scheet, P. (2005). Accounting for decay of linkage disequilibrium in haplotype inference and missing data imputation. American Journal of Human Genetics, 76, 449–462.
    https://doi.org/10.1086/428594

    Strauch, A. (1873) Die Schlangen des Russischen Reichs, in systematischer und zoogeographischer Beziehung. Mémoires de l'Académie impériale des sciences de St. Pétersbourg, Série 7, 21.

    Stümpel, N., Rajabizadeh, M., Avcı, A., Wüster, W. & Joger, U. (2016) 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, 101, 336–351.
    https://doi.org/10.1016/j.ympev.2016.04.025

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
    https://doi.org/10.1093/molbev/mst197

    Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M. & Rozen, S.G. (2012) Primer3 - new capabilities and interfaces. Nucleic Acids Research, 40, e115.
    https://doi.org/10.1093/nar/gks596

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

    Van Buuren, S. & Groothuis-Oudshoorn, K. (2011) mice: Multivariate imputation by chained equations in R. Journal of Statistical Software, 45, 1–67.
    https://doi.org/10.18637/jss.v045.i03

    Werner, F. J. M. (1898) I. Wissenschaftliche Mittheilungen. 1. Über einige neue Reptilien und einen neuen Frosch aus dem cilicischen Taurus. Zoologischer Anzeiger, 21(555), 217–223.

    Xia, X. & Lemey, P. (2009) Assessing substitution saturation with DAMBE In: Salemi, M. & Vandamme, A.-M. (Eds.), The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny. Cambridge University Press, Cambridge, pp. 615–630.
    https://doi.org/10.1017/CBO9780511819049.022

    Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution, 26, 1–7.
    https://doi.org/10.1016/S1055-7903(02)00326-3

    Zheng, Y. & Wiens, J.J. (2016) Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Molecular Phylogenetics and Evolution, 94, 537–547.
    https://doi.org/10.1016/j.ympev.2015.10.009