Abstract
We describe a new species of egg-eating sea snake, Aipysurus mosaicus sp. nov., from northern Australia and southernNew Guinea. This species was previously considered to be an allopatric population of A. eydouxii, which occursthroughout the Sunda Shelf and in New Guinea. Molecular analyses reveal these two species to be sister lineages withfixed nucleotide substitutions at three independent mitochondrial and nuclear loci, and a deep phylogenetic divergenceexceeding that of all other sampled species pairs in Aipysurus. Aipysurus mosaicus sp. nov. is also distinguished from A.eydouxii by morphological characters relating to scalation (e.g. number of ventral scales), colour pattern (e.g. number andshape of transverse body bands), internal soft anatomy (e.g. position of heart in relation to ventral scales), and skeletalmorphology (e.g. shape of nasal and caudal neural spines). Additional sampling is needed to clarify the extent ofgeographic contact between A. eydouxii and the new species in New Guinea where they appear to be sympatric. It is likelythat the boundaries between these taxa will be mirrored in other coastal sea snakes with ranges spanning the deep watersof the Timor Trench; discovery of such cryptic species will have important implications for conservation of this highly diverse but relatively poorly studied group of marine vertebrates.References
Alcala, A.C. (1986) Amphibians and Reptiles. Guide to Philippine flora and fauna, 10, 1–195.
Arévalo, E., Davis, S.K. & Sites, J. (1994) Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in Central Mexico. Systematic Biology, 43, 387–418.
Bertozzi, T., Sanders, K.L., Sistrom, M.J. & Gardner, M.G. Anonymous nuclear loci in non-model organisms: making the most of high throughput genome surveys. Bioinformatics doi:10.1093/bioinformatics/bts284.
Bleeker, P. (1858) 17. No title. Natuurwetenschappelijk Tijdschrift Voor Nederlandsch - Indië, 16, 49–50.
Boulenger, G. A. (1896) Catalogue of the snakes in the British Museum (Natural History). III Containing the Colubridae (Opistoglyphae and Proteroglyphae) Amblycephalidae and Viperidae. British Museum of Natural History, London, 727 pp.
Brown, J.M., Hedtke, S.M., Lemmon, A.R., Lemmon & E.M. (2010) When Trees Grow Too Long: Investigating the Causes of Highly Inaccurate Bayesian Branch-Length Estimates. Systematic Biology, 59, 145–161. doi10.1093/sysbio/syp081.
Burbrink, F.T., Lawson, R. & Slowinski, J.P. (2000) Mitochondrial DNA Phylogeography of the polytypic North American Rat Snake (Elaphe obsoleta): A critique of the subspecies concept. Evolution, 54, 2107–2118.
Cogger, H. (2007) Marine snakes. In Tzioumis, V. & Keable, S. (Eds), Description of key species groups in the east marine region. Australian Museum, 80–94.
Cogger, H.G. (1975) Sea Snakes of Australia and New Guinea. In Dunson, W.A. (Ed.) The Biology of Sea Snakes. University Park Press, Baltimore London & Tokyo, 59–139.
Cogger, H.G. (1992) Reptiles and Amphibians of Australia. Reed International Books, Chatswood New South Wales and Cornell University Press, New York., 775.
Cogger, H.G., Cameron, E.E. & Cogger, H.M. (1983) Hydrophiidae. In Zoological catalogue of Australia. Amphibia and Reptilia. Government Publishing Service, Canberra: Australian, 241–256.
David, P. & Ineich, I. (1999) Les serpents venimeux du monde: systématique et répartition. Dumerilia (Paris), 3, 3–499.
Drummond, A.J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T. & Wilson, A. (2010) Geneious v5.0.4 Available from http://www.geneious.com.
Dunson, W.A. & Minton, S.A. (1978) Diversity, Distribution, and Ecology of Philippine Marine Snakes (Reptilia, Serpentes). Journal of Herpetology, 12, 281–286.
Felsenstein, J. (1989) PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics, 5, 164–166.
Flower, S.S. (1899) Notes on a Second Collection of Reptiles made in the Malay Peninsula and Siam, from November 1896 to September 1898, with a List of the Species recorded from those Countries. Proceedings of the Zoological Society of London, 67, 600–697.
Fry, G.C., Milton, D.A. & Wassenberg, T.J. (2001) The reproductive biology and diet of sea snake bycatch of prawn trawling in northern Australia: characteristics important for assessing the impacts on populations. Pacific conservation biology, 7, 55–73.
Glodek, G.S. & Voris, H.K. (1982) Marine Snake Diets: Prey Composition, Diversity and Overlap. Copeia, 1982, 661–666.
Golay, P., Smith, H.M., Broadley, D.G., Dixon, J. R., McCarthy, C., Rage, J.C., Schätti, B. & Toriba, M. (1993) Endoglyphs and other major venomous snakes of the world. A checklist. Herpetological Data Centre, Azemiops, Geneva, 478 pp.
Gray, J.E. (1849) Catalogue of the Specimens of Snakes in the Collection of the British Museum. Printed by order of the Trustees, 125 pp.
Greer, A.E. (1997) The biology and evolution of Australian snakes. Surrey Beatty and Sons Sydney New South Wales, Australia, 358 pp.
Günther, A.C.L.G. (1864) The reptiles of British India. Ray Society, London, 452 pp.
Hall, R. (2009). Southeast Asia’s changing palaeogeography. Blumea, 54, 148–161.
Heatwole, H. (1975) Sea snakes of the Gulf of Carpentaria. In Dunson, W.A. (Ed), The Biology of Sea Snakes. London & Tokyo, Baltimore, 145–149.
Heatwole, H. (1999) Sea Snakes. University of New South Wales Press, Sydney, 148 pp.
Heatwole, H. & Cogger, H.G. (1994) Sea snakes of Australia. In: Gopalakrishnakone, P. (Ed), Sea snake toxinology. Singapore University Press, Singapore, 167–205.
Heled, J. & Drummond, A. (2010) Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution, 27, 570–580.
Herre, A.W.C.T. (1942) Notes on Philippine Sea-Snakes. Copeia, 1942, 7–9.
Kass, R.E. & Raftery, A.E. (1995) Bayes factors. Journal of the American Statistical Association, 90, 773–795.
Kharin, V.E. (1981) A review of sea snakes of the genus Aipysurus (Serpentes: Hydrophiidae). Zoologicheskii Zhurnal, 60, 257–254.
Kharin, V.E. (2005) A check-list of sea snakes (Serpentes: Laticaudidae, Hydrophiidae) of the World Ocean. Tinro, 140, 71–89.
Kharin, V. & Hallermann, J. (2009) Annotated catalogue of sea kraits (Laticaudidae) and sea snakes (Hydrophiidae) of the herpetological collection of the Zoological Museum, University of Hamburg. Mitteilungen aus dem Hamburgischen zoologische Museum und Institut, 106, 51–67.
Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Paabo, 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 of the United States of America, 86, 6196–6200.
Krefft, G., Scott, H. & Forde, H. (1869) The Snakes of Australia: An Illustrated and Descriptive Catalogue of All the Known Species. T. Richards, Government Printer, 100 pp.
Lemen, C.A. & Voris, H.K. (1981) A Comparison of Reproductive Strategies Among Marine Snakes. The Journal of Animal Ecology, 50, 89–101.
Leviton, A.E., Gibbs, R.H., Heal, E. & Dawson, C.E. (1985) Standards in Herpetology and Ichthyology Part I. Standard Symbolic Codes for Institutional Rescource Collections in Herpetology and Ichthyology. Copeia, 1985, 802–832.
Li, M., Fry, B.G. & Kini, R.M. (2005a) Eggs-Only Diet: Its Implications for the Toxin Profile Changes and Ecology of the Marbled Sea Snake (Aipysurus eydouxii). Journal of Molecular Evolution, 60, 81–89.
Li, M., Fry, B.G. & Kini, R.M. (2005b) Putting the Brakes on Snake Venom Evolution: The Unique Molecular Evolutionary Patterns of Aipysurus eydouxii (Marbled Sea Snake) Phospholipase A2 Toxins. Molecular Biology and Evolution, 22, 934–941.
Librado, P. & Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452 doi: 10.1093/bioinformatics/btp187.
Lim, B.L. & Sawai, Y. (1976) In Ohsaka, A., Hayashi, K. & Sawai, Y. (Eds), Ecology and distribution of some sea snakes in Peninsular Malaysia. Animal, plant and microbial toxins, New York, 515–520.
Limpus, C.J. (1975) In Dunson, W.A. (Ed), Coastal sea snakes of subtropical Queensland waters (230 to 280 south latitude). The Biology of Sea Snakes. University Park Press, London & Tokyo, 174–182.
Lukoschek, V. & Keogh, J.S. (2006) Molecular phylogeny of sea snakes reveals a rapidly diverged adaptive radiation. Biological Journal of the Linnean Society, 89, 523–539.
Lukoschek, V., Keogh, J.S. & Avise, J.C. (2011) Evaluating Fossil Calibrations for Dating Phylogenies in Light of Rates of Molecular Evolution: A Comparison of Three Approaches. Systematic Biology, doi: 10.1093/sysbio/syr075.
Masters, B.C., Fan, V. & Ross, H.A. (2011) Species delimitation—a geneious plugin for the exploration of species boundaries. Molecular Ecology Resources, 11, 154–157
MacPherson, J. (1933) Freshwater Snakes and Sea Snakes. The Australasian Nurses Journal, 31, 100–103.
McCarthy, C.J. & Warrell, D. (1991) A collection of sea snakes from Thailand with new records of Hydrophis belcheri (Gray). Bulletin of Natural History Museum (zoology), London, 57, 161–166.
Minton, S.A. (1975) Geographic distribution of sea snakes. In Dunson, W.A. (Ed), The Biology of Sea Snakes. London & Tokyo, Baltimore, 21–31.
Murphy, J.C., Cox, M.J. & Voris, H.K. (1999) A key to the sea snakes in the Gulf of Thailand. Natural History Bulletin of the Siam Society, 47, 95–108.
Nylander, J.A.A. (2004) MRMODELTEST v2.2. Program Distributed by the Author. Evolutionary Biology Centre, Uppsala University.
Ovenden, J.R., Kashiwagi, T., Broderick, D., Giles, J. & Salini, J. (2009) The extent of population genetic subdivision differs among four co-distributed shark species in the Indo-Australian archipelago. BMC Evolutionary Biology, 9(1), 40.
Porter, R., Irwin, S., Irwin, T. & Rodrigues, K. (1997) Records of marine snake species from The Hey-embley and Mission Rivers far North Queensland. Herpetofauna (Sydney), 27, 2–7.
Rambaut A. & Drummond, A.J. (2007) Tracer v1.4, Available from http://beast.bio.ed.ac.uk/Tracer
Rasmussen, A.R. (1989) An analysis of Hydrophis ornatus (Gray), H. lamberti Smith, and H. inornatus (Gray)(Hydrophiidae, Serpentes) based on samples from various localities, with remarks on feeding and breeding biology of H. ornatus. Amphibia-Reptilia, 10, 397–417.
Rasmussen, A.R. (1993) The status of the Persian Gulf Sea Snake Hydrophis lapemoides (Gray, 1849) (Serpentes, Hydrophiidae). Bulletin of Natural History Museum (zoology), London, 59, 97–105.
Rasmussen, A.R. (1997) Systematics of sea snakes: A critical review. Symposium of the Zoological Society of London, 70, 15–30.
Rasmussen, A.R. (2002) Phylogenetic analysis of the "true" aquatic elapid snakes Hydrophiinae (sensu Smith et al. 1977) indicating two independent radiations into water. Steenstrupia, 27, 47–63.
Rasmussen, A.R., Murphy, J.C., Ompi, M., Gibbons, J.W. & Uetz, P. (2011) Marine Reptiles. PLos One, 6, 1–12.
Redfield, J.A., Holmes, J.C. & Holms, R.D. (1978) Sea snakes of the eastern Gulf of Carpentaria. Australian Journal of Marine and Freshwater Research, 29, 325–334.
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. doi:10.1093/bioinformatics/btg180
Sanders, K.L., Lee, M.S.Y., Leys, R., Foster, R. & Keogh, J.S. (2008) Molecular phylogeny and divergence dates for Australasian elapids and sea snakes (hydrophiinae): evidence from seven genes for rapid evolutionary radiations. Journal of Evolutionary Biology, 21, 682–695.
Sanders, K.L., Mumpuni & Lee, M.S.Y. (2010) Uncoupling ecological innovation and speciation in sea snakes (Elapidae, Hydrophiinae, Hydrophiini). Journal of Evolutionary Biology, 23, 2685–2695.
Schmidt, P. (1852) Beiträge zur ferneren Kenntniss der Meerschlangen. Abhandlungen aus dem Gebiete der Naturwissenschaften, 2, 69–86.
Smith, L.A. (1974) The sea snakes of Western Australia (Serpentes: Elapidae, Hydrophiinae), with a description of a new subspecies. Record of the Western Australian Museum, 3, 93–110.
Smith, M.A. (1926) Monograph of the sea-snakes (Hydrophiidae). Printed by order of the Trustees of the British museum (Natural History) London, 130 pp.
Smith, M.A. (1943) The fauna of British India, Ceylon and Burma. Reptilia and Amphibia Taylor & Francis, London, 1–583 pp.
Stephens, M. & Donnelly, P. (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetics, 73, 1162–1169.
Stephens, M., Smith, N. & Donnelly, P. (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68, 978–989.
Stuebing, R.B. (1991). A checklist of the snakes of Borneo. Raffles Bulletin of Zoology, 39, 323–362.
Swofford, D.L. (2002) PAUP* 4.0: phylogenetic analysis using parsimony (*and other methods). Beta version 4.0b4a. Sinauer Associates, Sunderland, MA
Taylor, E.H. (1922) The snakes of the Philippine Islands. Bureau of Printing, Manila, 555 pp.
Taylor, E.H. (1965) The serpentes of Thailand and adjacent waters. University of Kansas Science Bulletin, 9, 609–1096.
Thomas, R.A. (1976) Dorsal scale row formulae in snakes. Copeia, 1976, 837–841.
Voris, H.K. (1966) Fish Eggs as the Apparent Sole Food Item for a Genus of Sea Snake, Emydocephalus (Krefft). Ecology, 47, 152–154.
Voris, H.K. (1977) A phylogeny of the sea snakes (Hydrophiidae). Fieldiana Zoology, 70, 79–166.
Wall, F. (1909) A monograph of the sea snakes. Memoirs of the Asiatic Society of Bengal, 2, 169–251.
Ward, T.M. (2000) Factors affecting the catch rates and relative abundance of sea snakes in the by-catch of trawlers targeting tiger and endeavour prawns on the northern Australian continental shelf. Marine and Freshwater Research, 51, 155–164.
Wells, R.W. (2007) Some taxonomic and nomenclatural considerations on the class Reptilia in Australia. The sea snakes of Australia. An introduction to the members of the families Hydrophiidae and Laticaudidae in Australia, with a new familial and generic arrangement. Australian Biodiversity Record, 8, 1–124.
Wells, R.W. & Wellington, C.R. (1983) A synopsis of the class Reptilia in Australia. Australian. Journal of Herpetology, 1, 73–129.
Zwickl, D.J. (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D., University of Texas at Austin.