Open Access Open Access  Restricted Access Subscription or Fee Access
Cover Image

Phylogenetic Analysis of Old World Viperid Snakes (Serpentes, Viperidae) Based on Skeletal Morphology

P. B. Snetkov, N. L. Orlov

Abstract


The system of the family Viperidae remains controversial despite the fact that numerous studies had place during last years. The results of different analyses most of which are based on molecular data are conflicting. We conducted the phylogenetic analysis including 39 osteological characters and 31 species of Old World viperid snakes. According to these results, genera Azemiops and Causus do not belong to subfamily Viperinae, so their separation into distinct subfamilies is supported. The validity of subfamily Azemiopinae is confirmed by molecular data. The common primitive character of Azemiops and Causus is joining of the prefrontals to the lateral parts of the frontals, while in the true vipers (Viperinae) the prefrontals join to the anterior margins of the frontals and the contact between these bones nearly reaches the midline of the skull. This type of articulation and the particular shape of the prefrontal can be added to the diagnosis of subfamily Viperinae (without Azemiops and Causus). One more result of our analysis is that the most basal form among true vipers is genus Cerastes. Other true vipers are divided into two groups. Inside the first group, including genera Atheris, Bitis, Echis, and Vipera, the genera Atheris and Bitis form a clade what is consistent with results of some molecular studies. The second group includes genera Daboia, Macrovipera, Montivipera, and Pseudocerastes. In subfamily Crotalinae the clade including genera Calloselasma and Hypnale is strongly supported, that confirms the results of many molecular studies. Protobothrops mangshanensis is close to two other species of genus Protobothrops that is not in conflict with referring P. mangshanensis (originally Zhaoermia mangshanensis) to this genus.

Keywords


Viperidae; true vipers; pitvipers; phylogeny; osteological phylogenetic analysis

Full Text:

PDF

References


Alencar L. R. V., Quental T. B., Grazziotin F. G., Alfaro M. L., Martins M., Venzon M., and Zaher H. (2016), “Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates,” Mol. Phylogen. Evol., 105, 50 – 62.

Ananjeva N. B., Orlov N. L., Chalikov R. G., Darevskij I. S., Ryabov S. A., and Barabanov A. V. (2006), Atlas of reptiles of North Eurasia [in Russian], Zoological Institute Russian Academy of Sciences, St. Petersburg.

Ashe J. S. and Marx H. (1988), “Phylogeny of the viperine snakes (Viperinae): Part II. Cladistic analysis and major lineages,” Fieldiana Zool., 52, 1 – 23.

Cadle J. E. (1992), “Phylogenetic relationships among vipers: immunological evidence,” in: Campbell J. A. and Brodie E. D. Jr. (eds.), Biology of the pitvipers, Tyler, Texas, pp. 41 – 48.

Castoe T. A. and Parkinson C. L. (2006), “Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes),” Mol. Phylogen. Evol., 39, 91 – 110.

Creer S., Pook C. E., Malhotra A., and Thorpe R. S. (2006), “Optimal intron analysis in the Trimeresurus radiation of Asian pitvipers,” Syst. Biol., 55(1), 57 – 72.

David P. and Ineich I. (1999), “Les serpents venimeux du monde: systématique et repartition,” Dumérilia, 3, 3 – 499.

David P., Vogel G., and Dubois A. (2011), “On the need to follow rigorously the Rules of the Code for the subsequent designation of a nucleospecies (type species) for a nominal genus which lacked one: the case of the nominal genus Trimeresurus Lacépède, 1804 (Reptilia: Squamata: Viperidae),” Zootaxa, 2992, 1 – 51.

Goloboff P. (1999), NONA (No Name) Version 2, Published by the author, San Miguel de Tucumán, Argentina. Available online at www.cladistics.org.

Grismer L. L., Grismer J. L., and McGuire J. A. (2006), “A new species of pitviper of the genus Popeia (Squamata: Viperidae) from Pulau Tioman, Pahang, West Malaysia,” Zootaxa, 1305, 1 – 19.

Groombridge B. C. (1980), A Phyletic Analysis of Viperine Snakes. Unpublished Ph.D. Thesis, City of London Polytechnic, London.

Groombridge B. C. (1986), “Phyletic relationships among viperine snakes,” in: Roček Z. (ed.), Studies in Herpetology, Charles University, Prague, pp. 219 – 222.

Gumprecht A., Tillack F., Orlov N. L., Captain A., and Ryabov S. (2004), Asian Pitvipers. 1st Edition, Geitje Books, Berlin.

Guo P., Jadin R. C., Malhotra A., and Li C. (2010), “An investigation of cranial evolution of Asian pitvipers (Serpentes: Crotalinae) with comments on phylogenetic position of Peltopelor macrolepis,” Acta Zool., 91, 402 – 407.

Guo P., Malhotra A., Li P. P., Creer S., and Pook C. E. (2009a), “An evaluation of the systematic value of skull morphology in the Trimeresurus radiation (Serpentes: Viperidae: Crotalinae) of Asian pitvipers,” J. Zool. Syst. Evol. Res., 47(4), 378 – 384.

Guo P., Malhotra A., Li C., Creer S., Pook C., and Wen T. (2009b), “Systematics of the Protobothrops jerdonii complex (Serpentes, Viperidae, Crotalinae) inferred from morphometric data and molecular phylogeny,” Herpetol. J., 19, 85 – 96.

Guo P., Malhotra A., Li P. P., Pook C. E., and Creer S. (2007), “New evidence on the phylogenetic position of the poorly known Asian pitviper Protobothrops kaulbacki (Serpentes: Viperidae: Crotalinae) with a redescription of the species and a revision of the genus Protobothrops,” Herpetol. J., 17, 237 – 246.

Guo P. and Wang Y. (2011), “A new genus and species of cryptic Asian green pitviper (Serpentes: Viperidae: Crotalinae) from southwest China,” Zootaxa, 2918, 1 – 14.

Guo P. and Zhao E.-M. (2006), “Comparison of skull morphology in nine Asian pit vipers (Serpentes: Crotalinae),” Herpetol. J., 16, 305 – 313.

Herrman H. W. (1990), Albumin-immunulogische Untersuchungen zur Phylogenie der Paläarktischen Großvipern (Reptilia: Serpentes: Viperidae). Diploma Thesis, University of Marburg, Germany.

Herrman H. W. (1995), Zur Phylogenie afrikanischer Vipern (Reptilia: Serpentes: Viperidae). Ph.D. Thesis, University of Marburg, Germany.

Herrman H. W. and Joger U. (1995), “Molecular data on the phylogeny of African vipers — preliminary results,” in: Llorento A., Mantori A., Santos X., and Carretero M. A. (eds.), Sci. Herpetol. Salamanca, Associacion Herpetologica Española), pp. 92 – 97.

Herrman H. W. and Joger U. (1997), “Evolution of viperine snakes,” in: Thorpe R. S., Wüster W., Malhotra A. (eds.), Venomous Snakes: Ecology, Evolution And Snake Bite. Symp. Zool. Soc. London, Vol. 70, Oxford University Press, Oxford, pp. 43 – 61.

Herrman H. W., Joger U., Lenk P., and Wink M. (1999), “Morphological and molecular phylogenies of viperines: conflicting evidence?” Kaupia Darmst. Beitr. Naturgesch., 8, 21 – 30.

Herrman H. W., Joger U., and Nilson G. (1992a), “Molecular phylogeny and systematic of viperine snakes. I. General phylogeny of European vipers,” in: Korsos Z., Kiss I. (eds.), Proc. of the 6th Gen. Ord. Meeting of the Soc. Eur. Herpetol., Hungary Natural History Museum, Budapest, pp. 219 – 224.

Herrman H. W., Joger U., and Nilson G. (1992b), “Phylogeny and systematic of viperine snakes. III: resurrection of the genus Macrovipera (Reuss, 1927) as suggested by biochemical evidence,” Amphibia–Reptilia, 13(4), 375 – 392.

Hoge A. R. and Romano-Hoge S. A. L. (1980), “Poisonous snakes of the world. I. Checklist of the pitvipers. Viperoidea, Viperidae, Crotalinae,” Mem. Inst. Butantan, 42/43, 179 – 309.

Ineich I. and Tellier J. M. (1992), “Un glande supralabile à débouché externe chez le genre Echis (Reptilia, Viperidae), cas unique chez les serpents,” C.R. Acad. Sci. Paris, 315(3), 49 – 53.

Jadin R. C., Smith E. N., and Campbell J. (2011), “Unravelling a tangle of Mexican serpents: a systematic revision of highland pitvipers,” Zool. J. Linn. Soc., 163, 943 – 958.

Joger U. and Courage K. (1999), “Are palearctic “rattlesnakes” (Echis and Cerastes) monophyletic?” Kaupia Darmst. Beitr. Naturgesch., 8, 65 – 81.

Liem K. F., Marx H., and Rabb G. R. (1971), “The viperid snake Azemiops: Its comparative cephalic anatomy and phylogenetic position in relation to Viperinae and Crotalinae,” Fieldiana Zool., 59, 1 – 126.

Malhorta A., Roger S., Thorpe M., and Stuart B. L. (2011), “Two new species of pitviper of the genus Cryptelytrops Cope 1860 (Squamata: Viperidae: Crotalinae) from Southeast Asia,” Zootaxa, 2757, 1 – 23.

Malhotra A. and Thorpe R. S. (2000), “A phylogeny of the Trimeresurus group of pitvipers: new evidence from a mitochondrial gene tree,” Mol. Phylogen. Evol., 16, 199 – 211.

Malhotra A. and Thorpe R. S. (2004), “A phylogeny of four mitochondrial gene regions suggests a revised taxonomy for Asian pit vipers (Trimeresurus and Ovophis),” Mol. Phylogen. Evol., 32, 83 – 100.

Mallow D., Ludwig D., and Nilson G. (2003), True Vipers: Natural History and Toxinology of Old World Vipers, Krieger Publishing Company, Malabar, Florida.

Marx H., Ashe J. S., and Watrous L. E. (1988), “Phylogeny of the viperine snakes (Viperinae): Part I. Character analysis,” Fieldiana Zool., 51, 1 – 16.

Marx H. and Rabb G. B. (1965), “Relationships and zoogeography of the viperine snakes (Family Viperidae),” Fieldiana Zool., 44, 161 – 206.

McDiarmid R. W., Campbell J. A., and Touré T. S. A. (1999), Snake Species of the World. A Taxonomic and Geographic Reference. Vol. 1, Herpetol. League.

Nixon K. C. (1999), WinClada Version 1.0000, Published by the author, Ithaca, New York. Available online at www.cladistics.org.

Orlov N. L., Ananjeva N. B., Barabanov A. A., Ryabov S. A., and Khalikov R. G. (2002), “Diversity of vipers (Azemiopinae, Crotalinae) in East, Southeast, and South Asia: annotated checklist and natural history data (Reptilia: Squamata: Serpentes: Viperidae),” Faun. Abh. Mus. Tierk. Dresden, 23, 177 – 218.

Orlov N. L., Ryabov S. A., and Nguyen T. T. (2013), “On the Taxonomy and the Distribution of the Genus Azemiops Boulenger, 1888: Description of a new species,” Russ. J. Herpetol., 20(2), 110 – 128.

Parker H. W. and Grandison A. G. C. (1977), Snakes: a Natural History, Cornell Univ. Press, Ithaca, NY.

Pyron R. A., Burbrink F. T., Colli J. R., Montes de Oca A. N., Vitt L. J., Kuczynski C. A., and Wiens J. J. (2011), “The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees,” Mol. Phylogen. Evol., 58, 329 – 342.

Sanders K. L., Malhotra A., and Thorpe R. S. (2004), “Ecological diversification in a group of Indomalayan pitvipers (Trimeresurus): convergence in taxonomically important traits has implications for species identification,” J. Evol. Biol., 17, 721 – 731.

Tu M.-C., Wang H.-Y., Tsai M.-P., Toda M., Lee W.-J., Zhang F.-J., and Ota H. (2000), “Phylogeny, taxonomy and biogeography of the Oriental pitvipers of the genus Trimeresurus (Reptilia: Viperidae: Crotalinae): a molecular perspective,” Zool. Sci., 17, 1147 – 1157.

Tuniev B. S., Orlov N. L., Ananjeva N. B., and Agasyan A. L. (2009), Snakes of Caucasus: Taxonomic Diversity, Distribution, Conservation [in Russian], KMK, St. Petersburg – Moscow.

Uetz P. and Hoљek J. (eds.) (2016), The Reptile Database, http://www.reptile-database.org, accessed 19 August 2016.

Vidal N. and Lecointre G. (1998), “Weighting and congruence: a case study based on three mitochondrial genes in pitvipers,” Mol. Phylogen. Evol., 9(3), 366 – 374.

Wüster W., Peppin L., Pook C. E., and Walker D. E. (2008), “Nesting of vipers: phylogeny and historical biogeography of the Viperidae (Squamata: Serpentes),” Mol. Phylogen. Evol., 49, 445 – 459.

Ziegler T., Herrmann H. W., David P., Orlov N. L., and Pauwels O. S. G. (2000) “Triceratolepidophis sieversorum, a new genus and species of pitviper (Reptilia: Serpentes: Viperidae: Crotalinae) from Vietnam,” Russ. J. Herpetol., 7(3), 199 – 214.

Zug G. R., Laurie J. V., and Caldwell J. P. (2001), Herpetology. An Introductional Biology of Amphibians and Reptiles, Acad. Press, San Diego, California.


Refbacks

  • There are currently no refbacks.