Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 1945 No. 1: 28 Nov. 2008
Type: Article
Published: 2008-11-28
DOI: 10.11646/zootaxa.1945.1.3
Page range: 51–66
Abstract views: 73
PDF downloaded: 1

Dissecting the major African snake radiation: a molecular phylogeny of the Lamprophiidae Fitzinger (Serpentes, Caenophidia)

UMR 7138, Systématique, Evolution, Adaptation, Département Systématique et Evolution, C. P. 26, Muséum National d’Histoire Naturelle, 43 Rue Cuvier, Paris 75005, France
Bayworld, P.O. Box 13147, Humewood 6013, South Africa
Royal Belgian Institute of Natural Sciences, Rue Vautier 29, B-1000 Brussels, Belgium Smithsonian Institution, Center for Conservation Education and Sustainability, B.P. 48, Gamba, Gabon
Department of Biology, 208 Mueller Laboratory, Pennsylvania State University, University Park, PA 16802-5301 USA
Biodiversity Foundation for Africa, P.O. Box FM 730, Bulawayo, Zimbabwe
Institute of Pharmacy and Molecular Biotechnology, University of Heidelberg, INF 364, D-69120 Heidelberg, Germany
Centre national de séquençage, Genoscope, 2 rue Gaston-Crémieux, CP5706, 91057 Evry cedex, France
Staatliches Naturhistorisches Museum, Pockelsstr. 10, 38106 Braunschweig, Germany
Royal Belgian Institute of Natural Sciences, Rue Vautier 29, B-1000 Brussels, Belgium
Reptilia Alethinophidia Atractaspidinae c-mos cytochrome b Dromophis Elapoidea Gonionotophis Hormonotus Lamprophiinae Lamprophis Lycodonomorphus Lycognathophis Mehelya Micrelaps ND4 Oxyrhabdium Psammophiinae Psammophis

Abstract

The Elapoidea includes the Elapidae and a large (~60 genera, 280 sp.) and mostly African (including Madagascar) radiation termed Lamprophiidae by Vidal et al. (2007), that includes at least four major groups: the psammophiines, atractaspidines, lamprophiines and pseudoxyrhophiines. In this work, we reviewed the recent taxonomic history of the lamprophiids, and built a data set including two nuclear protein-coding genes (c-mos and RAG2), two mitochondrial rRNA genes (12S and 16S rRNA) and two mitochondrial protein-coding genes (cytochrome b and ND4) for 85 species belonging to 45 genera (thus representing about 75% of the generic diversity and 30% of the specific diversity of the radiation), in order to clarify the phylogenetic relationships of this large and neglected group at the subfamilial and generic levels. To this aim, 480 new sequences were produced. The vast majority of the investigated genera fall into four main monophyletic clusters, that correspond to the four subfamilies mentioned above, although the content of atractaspidines, lamprophiines and pseudoxyrhophiines is revised. We confirm the polyphyly of the genus Stenophis, and the relegation of the genus name Dromophis to the synonymy of the genus name Psammophis. Gonionotophis brussauxi is nested within Mehelya. The genus Lamprophis Fitzinger, 1843 is paraphyletic with respect to Lycodonomorphus Fitzinger, 1843. Lamprophis swazicus is the sister-group to Hormonotus modestus, and may warrant generic recognition. Molecular data do not support the traditional placement of Micrelaps within the Atractaspidinae, but its phylogenetic position, along with that of Oxyrhabdium (previously considered to belong to the Xenodermatidae), requires additional molecular data and they are both treated as Elapoidea incertae sedis. The interrelationships of Psammophiinae, Atractaspidinae, Lamprophiinae, Pseudoxyrhophiinae, Prosymna (13 sp.), Pseudaspis (1 sp.) and Pythonodipsas (1 sp.), Buhoma (2 species), and Psammodynastes (1 sp.) remain unresolved. Finally, the genus Lycognathophis, endemic to the Seychelles, does not belong to the African radiation, but to the Natricidae.

References

  1. Alfaro, M.E., Karns, D.R., Voris, H.K., Brock, C.D. & Stuart, B.L. (2008). Phylogeny, evolutionary history, and biogeography of Oriental-Australian rear-fanged water snakes (Colubroidea: Homalopsidae) inferred from mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution, 46, 576–593.

    Bourquin, O. (1991). A new genus and species of snake from the Natal Drakensberg, South Africa. Annals of the Transvaal Museum, 35, 199–203.

    Branch, W.R. (1998). A field guide to the snakes and other reptiles of Southern Africa, revised edition. Struik Publishing, Cape Town.

    Brandstätter, F. (1995). Eine Revision der Gattung Psammophis mit Berücksichtigung der Schwestergattungen innerhalb der Tribus Psammophiini (Colubridae: Lycodontinae). Teil 1: Die Gattungen und Arten der Tribus Psammophiini. Teil 2: Rasterelektronenmikroskopische Untersuchungen zur Schuppenultrastruktur bei den Arten der Tribus Psammophiini mit besonderer Berücksichtigung der Arten der Gattung Psammophis. Mathematik und Naturwissenschaften. Universität des Saarlandes, Saarbrücken, 480 pp.

    Broadley, D.G. (1966). The herpetology of South-East Africa. Unpublished PhD. Thesis, University of Natal.

    Broadley, D.G. (1990). FitzSimons' Snakes of Southern Africa (Revised Edition). 387pp. 84 colour pl. + Addendum. Parklands: Jonathan Ball & Ad. Donker.

    Broadley, D.G. (1996). A revision of the genus Lycophidion (Serpentes: Colubridae) in southern Africa. Syntarsus, 3, 1–33.

    Broadley, D.G. (2005). Book review: The Amphibians and Reptiles of the Western Sahara by P. Geniez. J. A. Mateo, M. Geniez & J. Pether. African Journal of Herpetology, 54, 103–104.

    Broadley, D.G. (2007). On the status of Simocephalus riggenbachi Sternfeld 1910. African Journal of Herpetology, 56, 171-173.

    Cadle, J.E. (1994). The colubrid radiation in Africa (Serpentes: Colubridae): phylogenetic relationships and evolutionary patterns based on immunological data. Zoological Journal of the Linnean Society, 110, 103–140.

    Cadle, J.E. & Ineich, I. (2008). Nomenclatural status of the Malagasy snake genus Bibilava Glaw, Nagy, Franzen, and Vences, 2007: Resurrection of Thamnosophis Jan and designation of a lectotype for Leptophis lateralis Duméril, Bibron, and Duméril (Serpentes: Colubridae). Herpetological Review, 39, 285–288.

    de Queiroz, A., Lawson, R. & Lemos-Espinal, J.A. (2002). Phylogenetic relationships of North American garter snakes: how much DNA is enough? Molecular Phylogenetics and Evolution, 22, 315–329.

    Dowling, H.G. & Duellman, W.D. (1978). Systematic Herpetology: a synopsis of families and higher categories. Herpetological Information Search Systems, New York.

    Dowling, H.G., Hass, C.A., Hedges, S.B. & Highton, R. (1996). Snake relationships revealed by slow-evolving proteins: a preliminary survey. Journal of Zoology (London), 240, 1–28.

    Fry, B.G., Scheib, H., van de Weerd, L., Young, B., McNaughtan, J., Ryan Ramjan, S.F., Vidal, N., Poelmann, R.E. & Norman, J.A. (2008). Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes. Molecular and Cellular Proteomics, 7, 215–246.

    Glaw, F, Nagy, Z.T. & Vences, M. (2007a). Phylogenetic relationships and classification of the Malagasy pseudoxyrhophiine snake genera Geodipsas and Compsophis based on morphological and molecular data. Zootaxa, 1517, 53–62.

    Glaw, F., Nagy, Z.T., Franzen, M. & Vences, M. (2007b). Molecular phylogeny and systematics of the pseudoxyrhophiine snake genus Liopholidophis (Reptilia, Colubridae): evolution of its exceptional sexual dimorphism and descriptions of new taxa. Zoologica Scripta, 36, 291–300.

    Hall, T.A. (1999). Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    Kelly, C.R., Barker, N.P. & Villet, M.H. (2003). Phylogenetics of advanced snakes (Caenophidia) based on four mitochondrial genes. Systematic Biology, 52, 439–459.

    Kelly, C.M.R., 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, 1045–1060.

    Kelly, C.M.R., Barker, N.P. & Villet, M.H. Phylogeny, biogeography and classification of the snake superfamily Elapoidea: a rapid radiation in the late Eocene. Cladistics, in press.

    Keogh, J.S. (1998). Molecular phylogeny of elapid snakes and a consideration of their biogeographic history. Biological Journal of the Linnean Society, 63, 177–203.

    Lawson, R., Slowinski, J.B., Crother, B.I. & Burbrink, F.T. (2005). Phylogeny of the Colubroidea (Serpentes): new evidence from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 37, 581–601.

    McDowell, S.B. (1968). Affinities of the snakes usually called Elaps lacteus and E. dorsalis. Journal of the Linnean Society (Zoology), 47, 561–578.

    McDowell, S.B. (1986). The architecture of the corner of the mouth of colubroid snakes. Journal of Herpetology, 20, 349–403.

    Nagy, Z.T., Joger, U., Wink, M., Glaw, F. & Vences, M. 2003. Multiple colonization of Madagascar and Socotra by colubrid snakes: evidence from nuclear and mitochondrial gene phylogenies. Proceedings of the Royal Society, London: Biological Sciences, 270, 2613–2621.

    Nagy, Z.T., Vidal, N., Vences, M., Branch, W.R., Pauwels, O.S.G., Wink, M. & Joger, U. (2005). Molecular systematics of African Colubroidea (Squamata: Serpentes). In: B.A. Huber, Sinclair, B.J. & Lampe, K.H. (Eds.), African biodiversity: molecules, organisms, ecosystems. Springer Verlag, Bonn, pp. 221–228.

    Palumbi, S.R., Martin, A., Romano, S., McMillan, W.O., Stice, L. & Grabowski, G. (1991). The simple fool’s guide to PCR, Version 2.0. University of Hawaii.

    Philippe, H. (1993). MUST2000: a computer package of management utilities for sequences and trees. Nucleic Acids Research, 21, 5264–5272.

    Posada, D. & Crandall, K.A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818.

    Rasmussen, J.B. (2002). A review of the African members of the genus Micrelaps Boettger 1880 (Serpentes Atractaspididae). Tropical Zoology, 15, 71–87.

    Ronquist, F. & Huelsenbeck, J.P. (2003). Mr Bayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.

    Shine, R., Branch, W.R., Harlow, P.S., Webb, J.K. & Shine, T. (2006). Biology of burrowing asps (Atractaspididae) from Southern Africa. Copeia, 2006, 103–115.

    Spawls, S. & Branch, W.R. (1995). Dangerous snakes of Africa. Blanford Press, London, 192 pp.

    Stamatakis, A. (2006). RAxML-VI-HPC: Maximum Likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.

    Stamatakis, A., Hoover, P. & Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML Web-Servers. Systematic Biology, 57, 758–771.

    Swofford, D.L. (2002). PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4b10. Sunderland, Massachusetts: Sinauer Associates.

    Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

    Uetz, P., Goll, J. & Hallerman, J. (2008). The TIGR Reptile Database. Available: http://www.reptile-database.org/ (Accessed: August 4, 2008).

    Underwood, G. & Kochva, E. (1993). On the affinities of the burrowing asps Atractaspis (Serpentes: Atractaspididae). Zoological Journal of the Linnean Society, 107, 3–64.

    Vidal, N. (2002). Colubroid systematics: evidence for an early appearance of the venom apparatus followed by extensive evolutionary tinkering. Journal of Toxicology–Toxin Reviews, 21, 21–41.

    Vidal, N. & Hedges, S.B. (2002a). Higher-level relationships of caenophidian snakes inferred from four nuclear and mitochondrial genes. Comptes Rendus Biologies, 325, 987–995.

    Vidal, N. & Hedges, S.B. (2002b). Higher-level relationships of snakes inferred from four nuclear and mitochondrial genes. Comptes Rendus Biologies, 325, 977–985.

    Vidal, N & Hedges, S.B. (2004). Molecular evidence for a terrestrial origin of snakes. Proc. R. Soc. Lond. B (Suppl.), 271, 226–229.

    Vidal, N., Delmas, A.-S., David, P., Cruaud, C., Couloux, A. & Hedges, S.B. (2007). The phylogeny and classification of caenophidian snakes inferred from seven nuclear protein-coding genes. Comptes Rendus Biologies, 330, 182–187.

    Vidal, N., Rage, J.C., Couloux, A. & Hedges, S.B (2009). Snakes (Serpentes). In: Hedges, S.B. & Kumar, S. (Eds.), The Timetree of life. Oxford University Press, pp. 390–397.

    Vonk, F.J., Admiraal, J.F., Jackson, K., Reshef, R., de Bakker, M.A.G., Vandershoot, K., van den Berge, I., van Atten, M., Burgerhout, E., Beck, A., Mirtschin, P.J., Kochva, E., Witte, F., Fry, B.G., Woods, A.E & Richardson, M.K. (2008). Evolutionary origin and development of snake fangs. Nature, 454, 630–633.

    Williams, K.L. & Wallach, V. (1989). Snakes of the world. Volume 1. Synopsis of snake generic names. Krieger, Malabar, Florida. I–viii, 1–234.

    Winnepenninckx, B., Backeljau, T. & Dewachter, R. (1993). Extraction of high molecular weight DNA from molluscs. Trends in Genetics, 9, 407.

    Witte de, G.F. & Laurent, R. (1947). Révision d’un groupe de Colubridae Africains. Genres Calamelaps, Miodon, Aparallactus et formes affines. Mémoires du Musée Royal d’Histoire Naturelle de Belgique, 2nd série, 29, 1–133.

    Zaher, H. (1999). Hemipenial morphology of the South American xenodontine snakes, with a proposal for a monophyletic Xenodontinae and a reappraisal of colubroid hemipenes. Bulletin of the American Museum of Natural History, 240, 1–168.