Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2018-02-15
Page range: 301–346
Abstract views: 85
PDF downloaded: 2

Taxonomic revision of Israeli snakes belonging to the Platyceps rhodorachis species complex (Reptilia: Squamata: Colubridae)

School of Zoology, Tel-Aviv University, Tel-Aviv 6997801, Israel The Steinhardt Museum of Natural History, Tel-Aviv University, Tel-Aviv 6997801, Israel
School of Zoology, Tel-Aviv University, Tel-Aviv 6997801, Israel
School of Zoology, Tel-Aviv University, Tel-Aviv 6997801, Israel The Steinhardt Museum of Natural History, Tel-Aviv University, Tel-Aviv 6997801, Israel
School of Zoology, Tel-Aviv University, Tel-Aviv 6997801, Israel The Steinhardt Museum of Natural History, Tel-Aviv University, Tel-Aviv 6997801, Israel
Reptilia Platyceps saharicus Israel Middle East systematics mtDNA morphology

Abstract

The Platyceps rhodorachis species complex encompasses a widespread group of morphologically similar colubrid snakes. The number and identities of species from this complex in Israel have recently been debated. Studies from the previous decade concluded that there are two species in Israel and its vicinity (compared with one previously recognized), but their identity remained contested. We estimated the number of species and their taxonomic identity using morphological and molecular data. We found some evidence for clinal variation in many of the characters used to differentiate the species, and a great overlap in traits of putative species. Genetic data revealed very low sequence divergence, with all putative species being paraphyletic. Platyceps rogersi emerged as genetically closer to Platyceps saharicus rather than to its putative conspecific, P. karelini. The phylogenetic and taxonomic results thus indicate that the Israeli populations of the P. rhodorachis complex all belong to a single species, Platyceps saharicus (Schätti & McCarthy 2004).

 

References

  1. Amr, Z.S. & Disi, A.M. (2011) Systematics, distribution and ecology of the snakes of Jordan. Vertebrate Zoology, 61 (2), 179–266.

    Anderson, J. (1871) A list of the reptilian accession to the Indian Museum, Calcutta, from 1865 to 1870, with a description of some new species. Journal of the Asiatic Society of Bengal, 40 (2), 12–39.

    Anderson, J. (1895) On a collection of reptiles and batrachians made by Colonel Yerbury at Aden and its neighbourhood. Proceedings of the Zoological Society of London, 1895 (3), 635–663.

    Arnold, T.W. (2010) Uninformative parameters and model selection using Akaike's Information Criterion. Journal of Wildlife Management, 74 (6), 1175–1178.
    https://doi.org/10.1111/j.1937-2817.2010.tb01236.x

    Arbel, A. (Ed.) (1984) Plants & animals of the land of Israel, An Illustrated Encyclopedia. Volume 5. Reptiles & amphibians. Society for the Protection of Nature & Ministry of Defence Publishing House, Jerusalem, 244 pp. [in Hebrew]

    Bar, A. & Haimovitch, G. (2013) A field guide to reptiles and amphibians of Israel. Pazbar Publishing house, 249 pp. [in Hebrew]

    Barash, A. & Hoofien, J.H. (1961) Reptiles of Israel. Hakibbutz Hameuchad Publishing House, Tel Aviv, 179 pp. [in Hebrew]

    Bodenheimer, F.S. (1935) Animal life in Palestine. L. Mayer, Jerusalem, 506 pp.

    Bodenheimer, F.S. (1953) Animal Life in the Land of Israel. Dvir Publishing House, Or Yehuda, 436 pp. [in Hebrew]

    Boulenger, G.A. (1893) Catalogue of the Snakes in the British Museum. Volume I. Trustees of The British Museum (Natural History), London, xiii + 448 pp.

    Bouskila, A. & Amitai, P. (2001) A Handbook of the Reptiles and Amphibians of Israel. Keter Publishing House Limited, Jerusalem, 345 pp. [in Hebrew]

    Bryson, R.W., Murphy, R.W., Lathrop, A. & Lazcano‐Villareal, D. (2011) Evolutionary drivers of phylogeographical diversity in the highlands of Mexico: a case study of the Crotalus triseriatus species group of montane rattlesnakes. Journal of Biogeography, 38 (4), 697–710.
    https://doi.org/10.1111/j.1365-2699.2010.02431.x

    Burbrink, F.T., Lawson, R. & Slowinski, J.B. (2000) Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept. Evolution, 54 (6), 2107–2118.
    https://doi.org/10.1111/j.0014-3820.2000.tb01253.x

    Calder, W.A. (1984) Size, function and life history. Harvard University Press, Cambridge, 448 pp.

    Cox, N., Chanson, J. & Stuart, S. (Compilers) (2006) The status and distribution of reptiles and amphibians of the Mediterranean Basin. IUCN, Gland & Cambridge, v + 42 pp.

    Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature methods, 9 (8), 772–772.
    https://doi.org/10.1038/nmeth.2109

    Disi, A., Modry, D.,‎ Necas, P. & Rifai L. (2001) Amphibians and reptiles of the Hashemite Kingdom of Jordan: an atlas and field guide. Vol. 9. Chimaira, Frankfurt, 408 pp.

    Dowling, H.G. (1950) Studies of the black swamp snake, Seminatrix pygaea (Cope) with description of two new subspecies. Miscellaneous Publications from the Museum of Zoology University of Michigan, 76, 1–38.

    Dowling, H.G. (1951) A proposed standard system of counting ventrals in snakes. British Journal of Herpetology, 1, 97–99.

    Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC evolutionary biology, 7 (1), 214.
    https://doi.org/10.1186/1471-2148-7-214

    Edwards, S., Vanhooydonck, B., Herrel, A., Measey, G.J. & Tolley, K.A. (2012) Convergent evolution associated with habitat decouples phenotype from phylogeny in a clade of lizards. PloS ONE, 7 (12), e51636.
    https://doi.org/10.1371/journal.pone.0051636

    Ewert, M.A. (1985) Biology of the Reptilia. Vol. 14. Development A. John Wiley & Sons, New York, xii + 763 pp.

    Feldman, A. & Meiri, S. (2013) Length–mass allometry in snakes. Biological Journal of the Linnean Society, 108 (1), 161–172.
    https://doi.org/10.1111/j.1095-8312.2012.02001.x

    Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39 (4), 783–791.
    https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

    Geniez, P. & Gauthier, Y. (2008) On the distribution of Platyceps saharicus (Reptilia: Colubridae) in the Sahara. Salamandra, 44 (4), 179–180.

    Geniez, P. (2015) Serpents d’Europe, d’Afrique du Nord et du Moyen-Orient. Delachaux et Niestlé, Lausanne, 380 pp.

    Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J. & Lopez, R. (2010) A new bioinformatics analysis tools framework at EMBL–EBI. Nucleic acids research, 38, W695–W699.
    https://doi.org/10.1093/nar/gkq313

    Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic biology, 52 (5), 696–704.
    https://doi.org/10.1080/10635150390235520

    Günther, A. (1865) Report on a collection of reptiles and fishes from Palestine. Proceedings of the Zoological Society of London, 1864, 488–493.

    Günther, A. (1878) Specimens of reptiles presented by Captain Burton to the British Museum. In: Burton, R. (Ed.), The Gold Mines of Midian and the ruined Midianite cities. C. Kegan Paul & Co., London, xvi + 395 pp.

    Harris, D.J. (2002) Reassessment of comparative genetic distance in reptiles from the mitochondrial cytochrome b gene. Herpetological Journal, 12 (2), 85–87.

    Helbig, A.J., Knox, A.G., Parkin, D.T., Sangster, G. & Collinson, M. (2002) Guidelines for assigning species rank. Ibis, 144 (3), 518–525.
    https://doi.org/10.1046/j.1474-919X.2002.00091.x

    Henderson, R.W. (1997) A taxonomic review of the Corallus hortulanus complex of Neotropical tree boas. Caribbean Journal of Science, 33, 198–221.

    Huelsenbeck, J.P. & Rannala, B. (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic biology, 53 (6), 904–913.
    https://doi.org/10.1080/10635150490522629

    Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17 (8), 754–755.
    https://doi.org/10.1093/bioinformatics/17.8.754

    Inger, R.F. & Clark, P.J. (1943) Partition of the genus Coluber. Copeia, 1943 (3), 141–145.
    https://doi.org/10.2307/1438603

    Kelly, C.M., Barker, N.P., Villet, M.H., Broadley, D.G. & Branch, W.R. (2008) The snake family Psammophiidae (Reptilia: Serpentes): phylogenetics and species delimitation in the African sand snakes (Psammophis Boie, 1825) and allied genera. Molecular Phylogenetics and Evolution, 47 (3), 1045–1060.
    https://doi.org/10.1016/j.ympev.2008.03.025

    Kramer, E. & Schnurrenberger, H. (1963) Systematik, Verbreitung und Ökologie der Libyschen Schlangen. Revue Suisse de Zoologie, 70 (3), 453–568.
    https://doi.org/10.5962/bhl.part.75250

    Laszlo, J. (1975) Probing as a practical method of sex recognition in snakes. International Zoo Yearbook, 15 (1), 178–179.
    https://doi.org/10.1111/j.1748-1090.1975.tb01393.x

    Lindell, L.E., Forsman, A. & Merilä, J. (1993) Variation in number of ventral scales in snakes: effects on body size, growth rate and survival in the adder, Vipera berus. Journal of Zoology, 230 (1), 101–115.
    https://doi.org/10.1111/j.1469-7998.1993.tb02675.x

    Mallet, J. (1995) A species definition for the modern synthesis. Trends in Ecology & Evolution, 10 (7), 294–299.
    https://doi.org/10.1016/0169-5347(95)90031-4

    Manier, M.K. (2004) Geographic variation in the long‐nosed snake, Rhinocheilus lecontei (Colubridae): beyond the subspecies debate. Biological Journal of the Linnean Society, 83 (1), 65–85.
    https://doi.org/10.1111/j.1095-8312.2004.00373.x

    Mayr, E. (1942) Systematics and the origin of species from the viewpoint of a zoologist. Columbia University Press, New York, xiv + 334 pp.

    McDiarmid, R.W., Foster, M.S., Guyer, C., Gibbons, J.W. & Chernoff, N. (2012) Reptile biodiversity: standard methods for inventory and monitoring. University of California Press, Berkeley, xii + 424 pp.

    Mendelson III, J.R., Barclay, M.V., Geiser, M. & Streicher, J.W. (2016) The taxonomic status of Bufo intermedius Günther, 1858: forensic entomology confirms what was long suspected from morphology. Copeia, 104 (3), 697–701.
    https://doi.org/10.1643/CH-16-422

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

    Nylander, J.A., Wilgenbusch, J.C., Warren, D.L. & Swofford, D.L. (2007) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics, 24 (4), 581–583.
    https://doi.org/10.1093/bioinformatics/btm388

    Olden, J.D., Lawler, J.J. & Poff, N.L. (2008) Machine learning methods without tears: a primer for ecologists. The Quarterly review of biology, 83 (2), 171–193.
    https://doi.org/10.1086/587826

    Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V., Underwood, E.C., D'amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C. & Loucks, C.J. (2001) Terrestrial Ecoregions of the World: A New Map of Life on Earth: A new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioScience, 51 (11), 933–938.
    https://doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2

    Osgood, D.W. (1978) Effects of temperature on the development of meristic characters in Natrix fasciata. Copeia, 1978, 33–47.
    https://doi.org/10.2307/1443819

    Perry, G. (2012) On the Appropriate Names for Snakes Usually Identified as Coluber rhodorachis (Jan, 1865) or Why Ecologists Should Approach the Forest of Taxonomy with Great Care. IRCF Reptiles & Amphibians, 19 (20), 90–100.

    Peters, H.R. (1983) The ecological implications of body size. Cambridge University Press, New York, 329 pp.
    https://doi.org/10.1017/CBO9780511608551

    Pincheira-Donoso, D. & Meiri, S. (2013) An intercontinental analysis of climate-driven body size clines in reptiles: no support for patterns, no signals of processes. Evolutionary Biology, 40, 562–578.
    https://doi.org/10.1007/s11692-013-9232-9

    Pyron, R.A., Burbrink, F.T. & Wiens, J.J. (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13 (1), 93.
    https://doi.org/10.1186/1471-2148-13-93

    R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: https://www.r-project.org/ (accessed 10 January 2018)

    Razzetti, E., Faiman, R. & Werner, Y.L. (2007) Directional asymmetry and correlation of tail injury with left-side dominance occur in Serpentes (Sauropsida). Zoomorphology, 126 (1), 31–43.
    https://doi.org/10.1007/s00435-007-0028-2

    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572–1574.
    https://doi.org/10.1093/bioinformatics/btg180

    Sanders, K.L. Rasmussen, A.R., Elmberg, J., Silva, A., Guinea, M.L. & Lee, M.S. (2013) Recent rapid speciation and ecomorph divergence in Indo‐Australian sea snakes. Molecular ecology, 22 (10), 2742–2759.
    https://doi.org/10.1111/mec.12291

    Schätti, B. & McCarthy, C. (2004) Saharo-Arabian racers of the Platyceps rhodorachis complex: description of a new species (Reptilia: Squamata: Colubrinae). Revue suisse de Zoologie, 111 (4), 691–705.
    https://doi.org/10.5962/bhl.part.80263

    Schätti, B., Tillack, F. & Kucharzewski, C. (2014) Platyceps rhodorachis (Jan, 1863)–a study of the racer genus Platyceps BLYTH, 1860 east of the Tigris (Reptilia: Squamata: Colubridae). Vertebrate Zoology, 64, 297–405.

    Schätti, B. & Utiger, U. (2001) Hemerophis, a new genus for Zamenis socotrae Günther, and a contribution to the phylogeny of Old World racers, whip snakes, and related genera (Reptilia: Squamata: Colubrinae). Revue suisse de Zoologie, 108 (4), 919–948.
    https://doi.org/10.5962/bhl.part.80170

    Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J. & Thompson, J.D. (2011) Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Molecular systems biology, 7 (1), 539.
    https://doi.org/10.1038/msb.2011.75

    Silvestro, D. & Michalak, I. (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution, 12 (4), 335–337.
    https://doi.org/10.1007/s13127-011-0056-0

    Sindaco, R., Venchi, A. & Grieco, C. (2013) The Reptiles of the western Palearctic. 2. Annotated checklist and distributional atlas of the snakes of Europe, North Africa. Middle East and Central Asia. Edizioni Belvedere, Latina, 543 pp.

    The reptiles of the Western Palearctic, vol. 2. Annotated checklist and distributional atlas of the snakes of Europe, North Africa, Middle East and Central Asia. Belvedere, Latina, Italy.

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

    Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular biology and evolution, 28 (10), 2731–2739.
    https://doi.org/10.1093/molbev/msr121

    Tristram, H.B. (1884) The survey of Western Palestine: the fauna and flora of Palestine. Committee of the Palestine Exploration Fund, London, xxii + 455 pp.
    https://doi.org/10.5962/bhl.title.7594

    Uetz, P. (2018) The Reptile Database. Available from: http://www.reptile-database.org/ (accessed 10 January 2018)

    Werner, F. (1910) Neue oder seltenere Reptilien des Musée Royal d’Histoire Naturelle de Belgique in Brüssel. Zoologische Jahrbuecher Abteilung fuer Systematik Oekologie und Geographie der Tiere, 28, 263–288.
    https://doi.org/10.5962/bhl.part.17594

    Werner, Y.L. (1988) Herpetofaunal survey of Israel (1950-85), with comments on Sinai and Jordan and on zoogeographical heterogeneity. Monographiae biologicae, 62, 355–388.

    Werner, Y.L. (1995) A guide to the reptiles and amphibians of Israel. Nature Reserves Authority—Yefe-Nof Library, Jerusalem, 86 pp.

    Werner, Y.L. (1998) The desert herpetofauna in and near Israel: a personal review of advances (1986–1997), with new data (Amphibia; Reptilia). Faunistische Abhandlungen Staatliches Museum für Tierkunde Dresden, 21, 149–161.

    Werner, Y.L. (2016) Reptile life in the land of Israel, with comments on adjacent regions. Chimaira, Frankfurt, 494 pp.

    Wheeler, B. & Torchiano, M. (2016) lmPerm: Permutation Tests for Linear Models, R package version 2.1.0. Available from: https://CRAN.R-project.org/package=lmPerm (accessed 10 January 2018)

    Wiens, J.J. & Servedio, M.R. (2000) Species delimitation in systematics: inferring diagnostic differences between species. Proceedings of the Royal Society of London B: Biological Sciences, 267 (1444), 631–636.
    https://doi.org/10.1098/rspb.2000.1049