Abstract
Most West Indian snakes of the family Dipsadidae belong to the Subfamily Xenodontinae and Tribe Alsophiini. As recognized here, alsophiine snakes are exclusively West Indian and comprise 43 species distributed throughout the region. These snakes are slender and typically fast-moving (active foraging), diurnal species often called racers. For the last four decades, their classification into six genera was based on a study utilizing hemipenial and external morphology and which concluded that their biogeographic history involved multiple colonizations from the mainland. Although subsequent studies have mostly disagreed with that phylogeny and taxonomy, no major changes in the classification have been proposed until now. Here we present a DNA sequence analysis of five mitochondrial genes and one nuclear gene in 35 species and subspecies of alsophiines. Our results are more consistent with geography than previous classifications based on morphology, and support a reclassification of the species of alsophiines into seven named and three new genera: Alsophis Fitzinger (Lesser Antilles), Arrhyton Günther (Cuba), Borikenophis Hedges & Vidal gen. nov. (Puerto Rican Bank and nearby islands), Caraiba Zaher et al. (Cuba), Cubophis Hedges & Vidal gen. nov. (primarily Cuba but extending throughout the western Caribbean and Bahamas Bank), Haitiophis Hedges & Vidal gen. nov. (Hispaniola), Hypsirhynchus Günther (Hispaniola and Jamaica), Ialtris Cope (Hispaniola), Magliophis Zaher et al. (Puerto Rican Bank), and Uromacer Duméril & Bibron (Hispaniola). Several subspecies are recognized as full species. Three subtribes are recognized within the tribe Alsophiini Fitzinger: Alsophiina Fitzinger (for Alsophis, Borikenophis, Caraiba, Cubophis, Haitiophis, Hypsirhynchus, Ialtris, and Magliophis), Arrhytonina Hedges & Vidal subtribus nov. (for Arrhyton), and Uromacerina Hedges & Vidal subtribus nov. (for Uromacer). Divergence time estimates based on the molecular data indicate a relatively recent (~17–13 million years ago, Ma) origin for alsophiines. A single species apparently dispersed from South America, probably colonizing Hispaniola or Cuba and then later (13–0 Ma) there was dispersal to other islands and subsequent adaptive radiation, mostly in the Pliocene (5.3–1.8 Ma) and Pleistocene (1.8–0.01 Ma). More evidence will be needed to resolve all relationships among the genera and species groups and further details of their biogeographic history.References
Augé, M. & Rage, J.-C. (2000) Les Squamates (Reptilia) du Miocène moyen de Sansan. Mémoires du Muséum National d’Histoire Naturelle, 183, 263–313.
Barbour, T., & Ramsden, C.T. (1919) The Herpetology of Cuba. Memoirs of the Museum of Comparative Zoology, 47, 71–213.
Bibron, G. (1840) Plate 27. In: de la Sagra, R., Historia física, politica y natural de la Isla de Cuba. Arthus Bertrand, Paris.
Boulenger, G.A. (1893) Catalogue of snakes in the British Museum (Natural History). Vol. 1, Longmans and Company, London, 448 pp.
Breuil, M. (2002) Histoire naturelle des amphibiens et reptiles terrestres de l’archipel Guadeloupéen. Muséum National d’Histoire Naturelle, Paris, 339 pp.
Burbrink, F.T. & Pyron, R.A. (2008) The taming of the skew: Estimating proper confidence intervals for divergence dates. Systematic Biology, 57, 317–328.
Burbrink, F.T., Lawson, R. & Slowinski, J.B. (2000) Mitochondrial DNA phylogeography of the polytypic North American ratsnake (Elaphe obsoleta): a critique of the subspecies concept. Evolution, 54, 2107–2118.
Cadle, J.E. (1984) Molecular systematics of xenodontine colubrid snakes: I. South American xenodontines. Herpetologica, 40, 8–20.
Cadle, J.E. (1985) The Neotropical colubrid snake fauna: lineage components and biogeography. Systematic Zoology, 34, 1–20.
Cadle, J.E. & Greene, H.W. (1993) Phylogenetic patterns, biogeography, and the ecological structure of Neotropical snake assemblages. In: Ricklefs, R.E. & Schluter, D. (Eds.), Species diversity in ecological communities: historical and geographical perspectives. University of Chicago Press, Chicago, pp. 281–293.
Carlquist, S. (1965) Island life. A natural history of the islands of the World. Natural History Press, Garden City, New York, 451 pp.
Cochran, D.M. (1941) The herpetology of Hispaniola. Bulletin of the U.S. National Museum, 177, 1–398.
Cope, E.D. (1862 [1863]) Synopsis of the species of Holcosus and Ameiva, with diagnoses of new West Indian and South American Colubridae. Proceedings of the Academy of Natural Sciences, Philadelphia, 14, 60–82.
Crother, B.I. (1999) Phylogenetic relationships among West Indian xenodontine snakes (Serpentes; Colubridae) with comments on the phylogeny of some mainland xenodontines. Contemporary Herpetology, 1999, 1–21. Available: http://www.contemporaryherpetology.org/ch/1999/2/index.htm
Crother, B.I. & Hillis, D.M. (1995) Nuclear ribosomal DNA restriction sites, phylogenetic information, and the phylogeny of some xenodontine (Colubridae) snakes. Journal of Herpetology, 29, 316–320.
De Queiroz, A., Lawson, R. & Lemos-Espinal, J.A. (2002) Phylogenetic relationships of North American garter snakes (Thamnophis) based on four mitochondrial genes: how much DNA sequence is enough? Molecular Phylogenetics and Evolution, 22, 315–329.
Donovan, S.K. (2002) A karst of thousands: Jamaica’s limestone scenery. Geology Today, 18, 143–151.
Dowling, H.G. (1975) A provisional classification of snakes. In: Dowling, H.G. (Ed.), 1974 yearbook of herpetology. Herpetological Information Search Systems, The American Museum of Natural History, New York, pp. 167–170.
Duméril, A.M.C., & Bibron, G. (1853) Prodrome de la classification des reptiles ophidiens. Mémoires de l'Académie des Sciences de l'Institut de France, 23, 478.
Dunn, E.R. (1932) The colubrid snakes of the Greater Antilles. Copeia, 1932, 89–92.
Fitzinger, L. (1843) Systema reptilium. Braumüller et Seidel Bibliopolas, Wien, 106 pp.
Forstner, M.R.J., Davis, S.K. & Arévalo, E. (1995) Support for the hypothesis of anguimorph ancestry for the suborder Serpentes from phylogenetic analysis of mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 4, 93–102.
Gosse, P.H. (1851) A Naturalist’s Sojurn in Jamaica. Longman, Brown, Green and Longmans, London. 508 pp.
Grant, C. (1940) The herpetology of the Cayman Islands. Bulletin of the Institute of Jamaica, 2, 1–65.
Grant, C., Smith, H.M., & Alayo, P. (1959) The status of the snakes of the genus Arrhyton in Cuba. Herpetologica, 15, 129–133.
Günther, A. (1858) Catalogue of colubrine snakes of the British Museum. British Museum, London, 281 pp.
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.
Hass, C.A., Maxson, L.R. & Hedges, S.B. (2001) Relationships and divergence times of West Indian amphibians and reptiles: insights from albumin immunology. In: Woods, C.A. & Sergile, F.E. (Eds.), Biogeography of the West Indies: patterns and perspectives. CRC Press, Boca Raton, Florida, pp. 157–174.
Hedges, S.B. (1994) Molecular evidence for the origin of birds. Proceedings of the National Academy of Sciences USA, 91, 2621–2624.
Hedges, S.B. (1996a) Historical biogeography of West Indian vertebrates. Annual Review of Ecology and Systematics, 27, 163–196.
Hedges, S.B. (1996b) The origin of West Indian amphibians and reptiles. In: Powell, R. & Henderson, R.W. (Eds.), Contributions to West Indian herpetology: a tribute to Albert Schwartz. Society for the Study of Amphibians and Reptiles. Ithaca, New York, pp. 95–128.
Hedges, S.B. (2001) Caribbean biogeography: an outline. In: Woods, C.A. & Sergile, F.E. (Eds.), Biogeography of the West Indies: Patterns and Perspectives. CRC Press, Boca Raton, Florida, pp. 15–33.
Hedges, S.B. (2002) Morphological variation and the definition of species in the snake genus Tropidophis (Tropidophiidae). Bulletin of Natural History Museum (London), Zoology Series, 68, 83–90.
Hedges, S.B. (2006) Paleogeography of the Antilles and origin of West Indian terrestrial vertebrates. Annals of the Missouri Botanical Garden, 93, 231–244.
Hedges, S.B. & Garrido, O.H. (1992) Cuban snakes of the genus Arrhyton: two new species and a reconsideration of A. redimitum Cope. Herpetologica, 48, 168–177.
Hedges, S.B., Hass, C.A. & Maxson, L.R. (1992) Caribbean biogeography: molecular evidence for dispersal in West Indian terrestrial vertebrates. Proceedings of the National Academy of Sciences USA, 89, 1909–1913.
Heinicke, M.P., Duellman, W.E. & Hedges, S.B. (2007) Major Caribbean and Central American frog faunas originated by oceanic dispersal. Proceedings of the National Academy of Sciences USA, 104, 10092–10097.
Henderson, R.W. (1984) The diets of Hispaniolan colubrid snakes. 1. Introduction and prey genera. Oecologia, 62, 234–239.
Henderson, R.W. (1990) A new subspecies of Alsophis antiguae (Parker) from Great Bird Island (Antigua), Lesser Antilles. Caribbean Journal of Science, 25, 119–122.
Henderson, R.W. (1992) Consequences of predator introductions and habitat destruction on amphibians and reptiles in the post-Columbus West Indies. Caribbean Journal of Science. 28, 1–10.
Henderson, R.W. & Powell, R. (1996) Alsophis ater. Catalogue of American Amphibians and Reptiles, 633, 1–2.
Henderson, R.W. & Powell, R. (1996) Alsophis sanctaecrucis. Catalogue of American Amphibians and Reptiles, 634, 1–2.
Henderson, R.W., Powell, R., Daltry, J.C. & Day, M.L. (1996) Alsophis antiguae. Catalogue of American Amphibians and Reptiles, 632, 1–3.
Henderson, R.W. & Sajdak, R.A. (1996) Diets of West Indian racers (Colubridae: Alsophis): Composition and biogeographic implications. In: Powell, R. & Henderson, R.W. (Eds.), Contributions to West Indian herpetology: a tribute to Albert Schwartz. Society for the Study of Amphibians and Reptiles. Ithaca, New York, pp. 327–338.
Henderson, R.W., Schwartz, A. & Noeskehallin, T.A. (1987) Food habits of three colubrid tree snakes (Genus Uromacer) on Hispaniola. Herpetologica, 43, 241–248.
Horn, H.S. (1969) Polymorphism and evolution of the Hispaniola snake genus Uromacer (Colubridae). Breviora, Museum of Comparative Zoology, 324, 1–23.
Hower, L.M. & Hedges, S.B. (2003) Molecular phylogeny and biogeography of West Indian teiid lizards of the genus Ameiva. Caribbean Journal of Science, 39, 298–306.
Iturralde-Vinent, M.A. & MacPhee, R.D.E. (1999) Paleogeography of the Caribbean region: implications for Cenozoic biogeography. Bulletin of the American Museum of Natural History, 238, 1–95.
IUCN (2008) IUCN Redlist of Threatened Species. Available from: http://www.iucnredlist.org/ (accessed 21 December 2008)
Knight, A. & Mindell, D.P. (1994) On the phylogenetic relationships of Colubrinae, Elapidae and Viperidae and the evolution of front fanged venom systems in snakes. Copeia, 1994, 1–9.
Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Pääbo, S., Villablanca, F.X. & Wilson, A.C. (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences USA, 86, 6196–6200.
Kumazawa, Y., Ota, H., Nishida, M. & Ozawa, T. (1996) Gene rearrangements in snake mitochondrial genomes: highly concerted evolution of control-region-like sequences duplicated and inserted into a tRNA gene cluster. Molecular Biology and Evolution, 13, 1242–1254.
Lazell, J.D., Jr. (1967) Wiederentdeckung von zwei angeblich ausgestorbenen Schlangenarten der westindischen Inseln. Salamandra, 3, 91–97.
Lynn, W. G., & Grant, C. (1940) The Herpetology of Jamaica. Bulletin of the Institute of Jamaica, Science Series, 1, 1–148.
Maglio, V.J. (1970) West Indian xenodontine colubrid snakes: their probable origin, phylogeny, and zoogeography. Bulletin of the Museum of Comparative Zoology, 141, 1–54.
Mitchell, S.F. (2004) Lithostratigraphy and palaeogeography of the White Limestone Group. Cainozoic Research, 3, 5–30.
Myers, C.W. (1973) A new genus for Andean snakes related to Lygophis boursieri and a new species (Colubridae). American Museum Novitates, 2522, 1–37.
Palumbi, S.R., Martin, A., Romano, S., Mcmillan, W.O., Stice, L. & Grabowski, G. (1991) The simple fool’s guide to P.C.R., Univ. of Hawaii Press, Honolulu, 43 pp.
Parker, H.W. (1933) Some amphibians and reptiles from the Lesser Antilles. Annals of the Magazine of Natural History, 11, 151–158.
Peters, W.C.H. (1863) Uber einige neue oder weniger bekannte Schlangenarten des zoologischen Museums zu Berlin. Monatsbericht Königlich Preussischen Akademie der Wissenschaften zu Berlin, 1863, 272–289.
Philippe, H. (1993) MUST2000: a computer package of management utilities for sequences and trees. Nucleic Acids Research, 21, 5264–5272.
Pinou, T., Vicario, S., Marschner, M. & Caccone, A. (2004) Relict snakes of North America and their relationships within caenophidia, using likelihood-based Bayesian methods on mitochondrial sequences. Molecular Phylogenetics and Evolution, 32, 563–574.
Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818.
Powell, R. & Henderson, R.W. (1994) Ialtris. Catalogue of American Amphibians and Reptiles, 590, 1–2.
Powell, R. & Henderson, R.W. (1998) Alsophis anomalus. Catalogue of American Amphibians and Reptiles, 659, 1–2.
Powell, R. & Henderson, R.W. (1998) Alsophis melanichnus. Catalogue of American Amphibians and Reptiles, 660, 1–2.
Powell, R., Henderson, R.W., Adler, K. & Dundee, H.A. (1996) An annotated checklist of West Indian amphibians and reptiles. In: Powell, R. & Henderson, R.W. (Eds.), Contributions to West Indian Herpetology: a tribute to Albert Schwartz. Society for the Study of Amphibians and Reptiles, S.S.A.R., Ithaca, New York, pp. 51–93.
Reinhardt, J. & Lütken, C.F. (1862) Bidrag tii det vestindiske Öriges og navnligen tii de dansk-vestindiske Oers Herpetologie. Vidensk. Meddel. Naturhist. For. Kjöbenhavn, 153–291.
Ronquist, F. & Huelsenbeck, J.P. (2003) Mr Bayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
Rosen, D.E. (1975) A vicariance model of Caribbean biogeography. Systematic Zoology, 24, 431–464.
Ruibal, R. (2003) Introduction. In: Barbour, T. & C.T. Ramsden, The herpetology of Cuba. Facsimile Reprints in Herpetology, Society for the Study of Amphibians and Reptiles, Ithaca, New York, pp. iii–vii.
Schlegel, H. (1837) Essai sur la physionomie des serpens. Kips et van Stockum, La Haye, The Netherlands, 606 pp.
Schmidt, K.P. (1926) The amphibians and reptiles of Mona Island, West Indies. Field Museum Natural History Series, 12, 149–163.
Schwartz, A. (1966) Snakes of the genus Alsophis in Puerto Rico and the Virgin Islands. Studies on the Fauna of Curacao and Other Caribbean Islands, 90, 177–227.
Schwartz, A. (1967) A review of the genus Dromicus in Puerto Rico and the Virgin Islands. Stahlia, 9, 1–14.
Schwartz, A. (1970) A systematic review of Uromacer catesbyi Schlegel (Serpentes, Colubridae). Tulane Studies in Zoology and Botany, 16, 131–149.
Schwartz, A. (1971) A systematic review of the Hispaniolan snake genus Hypsirhynchus. Studies on the Fauna of Curacao and Other Caribbean Islands, 128, 63–94.
Schwartz, A. (1976) Variation in the Hispaniola colubrid snake Uromacer frenatus Günther (Reptilia, Serpentes, Colubridae). Journal of Herpetology, 10, 319–327.
Schwartz, A. & Garrido, O.H. (1981) A review of the Cuban members of the genus Arrhyton (Reptilia, Serpentes, Colubridae). Annals of the Carnegie Museum of Natural History, 50, 207–230.
Schwartz, A. & Henderson, R.W. (1991) Amphibians and reptiles of the West Indies: descriptions, distributions, and natural history. University of Florida Press, Gainesville, 720 pp.
Schwartz, A., & Rossman, D.A. (1976) A review of the Hispaniolan colubrid snake genus Ialtris. Studies on the Fauna of Curacao and Other Caribbean Islands, 50, 76–102.
Schwartz, A. & Thomas, R. (1965) The Genus Darlingtonia (Serpentes) in Hispaniola including a new subspecies from the Dominican Republic. Breviora, 229, 1–10.
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.
Thomas, R., Henderson, R.W., Powell, R. & Rodríguez, P.G. (2007) Alsophis anomalus (Hispaniolan Brown Racer). Herpetological Review, 38, 338–339.
Thomas, R.A. (1997) Galapagos terrestrial snakes: biogeography and systematics. Herpetological Natural History 5, 19–40.
Thorne, J.L. & Kishino, H. (2002) Divergence time and evolutionary rate estimation with multilocus data. Systematic Biology, 51, 689–702.
Uetz, P., Goll, J. & Hallerman, J. (2008) The TIGR Reptile Database. Available: http://www.reptile-database.org/ (Accessed: August 4, 2008).
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 snakes inferred from four nuclear and mitochondrial genes. Comptes Rendus Biologies, 325, 977–985.
Vidal, N. & Hedges, S.B. (2002b) Higher-level relationships of caenophidian snakes inferred from four nuclear and mitochondrial genes. Comptes Rendus Biologies, 325, 987–995.
Vidal, N. & Hedges, S.B. (2005) The phylogeny of squamate reptiles (lizards, snakes, and amphisbaenians) inferred from nine nuclear protein-coding genes. Comptes Rendus Biologies, 328, 1000–1008.
Vidal, N., Kindl, S.G., Wong, A. & Hedges, S.B. (2000) Phylogenetic relationships of xenodontine snakes inferred from 12S and 16S ribosomal RNA sequences, Molecular Phylogenetics and Evolution, 14, 389–402.
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, New York, pp. 390–397.
Wiens, J.J., Brandley, M.C. & Reeder, T.W. (2006) Why does a trait evolve multiple times within a clade? Repeated evolution of snakelike body form in squamate reptiles. Evolution, 60, 123–141.
Winnepenninckx, B., Backeljau, T. & Dewachter, R. (1993) Extraction of high molecular weight DNA from molluscs. Trends in Genetics, 9, 407.
Yang, Z. & Yoder, A.D. (2003) Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene loci and calibration points, with application to a radiation of cute-looking mouse lemur species. Systematic Biology, 52, 705–716.
Yang, Z. (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS, 13, 555–556.
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.
Zaher, H., Grazziotin, F.G., Cadle, J.E., Murphy, R.W., Moura-Leite, J.C. & Bonatto, S.L. (2009) Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South America xenodontines: a revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia, 49,115–153.