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Issue: Vol. 4093 No. 3: 23 Mar. 2016
Type: Article
Published: 2016-03-22
DOI: 10.11646/zootaxa.4093.3.5
Page range: 382–390
Abstract views: 66
PDF downloaded: 1

Multilocus phylogeny of the Asian Lance-headed pitvipers (Squamata, Viperidae, Protobothrops)

College of Life Sciences and Food Engineering, Yibin University, Yibin 644007, China
College of Life Sciences and Food Engineering, Yibin University, Yibin 644007, China
College of Life Sciences and Food Engineering, Yibin University, Yibin 644007, China
College of Life Sciences and Food Engineering, Yibin University, Yibin 644007, China
College of Life Sciences and Food Engineering, Yibin University, Yibin 644007, China
College of Life Sciences and Food Engineering, Yibin University, Yibin 644007, China
Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet St., Hanoi, Vietnam
College of Life Sciences and Food Engineering, Yibin University, Yibin 644007, China
Department of Biology, Northeastern Illinois University, Chicago, IL 60625
College of Life Sciences and Food Engineering, Yibin University, Yibin 644007, China
Reptilia Asia Bayesian distribution venomous snake systematics

Abstract

Despite the public health significance and potential applications to medical research, the evolutionary history of the Asian Lance-headed pitvipers (genus Protobothrops) remains inadequately studied. Previous research generally focused on a few selected species with no comprehensive molecular study of Protobothrops. Here, we conduct the first study to infer the phylogenetic relationships of all currently recognized species in this genus based on four mitochondrial DNA fragments and four nuclear genes. Bayesian Inference and Maximum Likelihood analyses show that within Protobothrops there are four strongly supported clades forming distinct subgroups. The first subgroup, which is sister to the other three, consists of three species, P. himalayanus, P. kaulbacki, and P. sieversorum. The second subgroup contains only P. mangshanensis. The final two subgroups, which are sister groups, include the other four and six Protobothrops species. Although our findings provide additional information on the phylogenetic relationships of the genus Protobothrops, the placement of P. dabieshanensis and P. elegans remains problematic. In addition, our molecular results indicate that P. trungkhanhensis, currently considered endemic to Vietnam, should be added to the species known from China. Our ancestral area estimation indicated that Protobothrops likely originated in southwestern China. This study improves our understanding of the evolutionary relationships among species of Asian Lance-headed pitvipers, providing a greater framework for future studies.

 

References

  1. Arevalo, E., Davis, S.K. & Sites, J.W. (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.

    http://dx.doi.org/10.1093/sysbio/43.3.387

    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, 2107–2118.

    http://dx.doi.org/10.1111/j.0014-3820.2000.tb01253.x

    Casewell, N.R., Wagstaff, S.C., Harrison, R.A., Renjifo, C. & Wüster, W. (2011). Domain loss facilitates accelerated evolution and neofunctionalization of duplicate snake venom metalloproteinase toxin genes. Molecular Biology and Evolution, 28 (9), 2637–2649.

    http://dx.doi.org/10.1093/molbev/msr091

    Che, J., Zhou, W.W., Hu, J.S., Yan, F., Papenfuss, T.J., Wake, D.B. & Zhang, Y.P. (2010) Spiny frogs (Paini) illuminate the history of the Himalayan region and Southeast Asia. Proceedings of the National Academy of Sciences, 107, 13765–13770.

    http://dx.doi.org/10.1073/pnas.1008415107

    Chen, T.B., Luo, J., Meng, Y.J., Wen, B.H. & Jiang, K. (2013). Discovery of Protobothrops maolanensis in Guangxi, with taxonomic discussion. Sichuan Journal of Zoology, 1, 116–118.

    Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415.

    http://dx.doi.org/10.1111/j.1095-8312.2005.00503.x

    Flot, J.F. (2010) SEQPHASE: a web tool for interconverting PHASE input/output files and FASTA sequence alignments. Molecular Ecology Resources, 10, 162–166.

    http://dx.doi.org/10.1111/j.1755-0998.2009.02732.x

    Groth, J.G. & Barrowclough, G.F. (1999) Basal divergences in birds and the phylogenetic utility of the nuclear RAG-1 gene. Molecular Phylogenetics and Evolution, 12, 115–123.

    http://dx.doi.org/10.1006/mpev.1998.0603

    Gumprecht, A, Tillack, F, Orlov, N.L., Captain, A. & Ryabov, S. (2004) Asian Pitvipers. Geitje Books, Berlin, 362 pp.

    Guo, P., Liu, Q., Li, C., Chen, X., Jiang, K., Wang, Y.Z. & Malhotra, A. (2011) Molecular phylogeography of Jerdon’s pitviper (Protobothrops jerdonii): importance of the uplift of the Tibetan plateau. Journal of Biogeography, 38, 2326–2336.

    http://dx.doi.org/10.1111/j.1365-2699.2011.02566.x

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

    Guo, P., Malhotra, A., Li, P.P., Creer, S. & Pook, C.E. (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. Herpetological Journal, 17, 237–246.

    Guo, P., Pang, J.F., Zhang, Y.P. & Zhao, E.M. (2006) A re-analysis of the phylogeny of the genus Protobothrops (Reptilia: Viperidae), with particular reference to the systematic position of P. xiangchengensis. Amphibia-Reptilia, 27, 433–439.

    http://dx.doi.org/10.1163/156853806778189954

    Hoge, A.R. & Romano-Hoge S.A.R.W.L. (1983) [1980/81] Notes on micro and ultrastructure of “Oberhäutschen” in Viperoidea. Memórias do Instituto Butantan, 44/45, 81–118.

    Huang, S., He, S.P., Peng, Z.G., Zhao, K. & Zhao, E.M. (2007) Molecular phylogeography of endangered sharp-snouted pitviper (Deinagkistrodon acutus; Reptilia, Viperidae) in mainland China. Molecular Phylogenetics and Evolution, 44, 942–952.

    http://dx.doi.org/10.1016/j.ympev.2007.05.019

    Huang, X., Pan, T., Han, D.M., Zhang, L., Hou, Y.X., Yu, L., Zheng, H.M. & Zhang, B.W. (2012) A new species of the genus Protobothrops (Squamata: Viperidae: Crotalinae) from the Dabie Mountains, Anhui, China. Asian Herpetological Research, 3 (3), 213–218.

    http://dx.doi.org/10.3724/SP.J.1245.2012.00213

    Knight, A. & Mindell, D.P. (1993) Substitution bias, weighting of DNA sequence evolution, and the phylogenetic position of Fea’s viper. Systematic Biology, 42, 18–31.

    http://dx.doi.org/10.1093/sysbio/42.1.18

    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.

    http://dx.doi.org/10.1016/j.ympev.2005.07.016

    Liu, Q., Myers, E.A., Zhong, G.H., Hu, J., Zhao, H. & Guo, P. (2012) Molecular evidence on the systematic position of the lance-headed pitviper Protobothrops maolanensis Yang et al. 2011. Zootaxa, 3178, 57–62.

    Malhotra, A. & Thorpe, R.S. (2004) A phylogeny of four mitochondrial gene regions suggests a revised taxonomy for Asian pitvipers (Trimeresurus and Ovophis). Molecular Phylogenetics and Evolution, 32, 83–100.

    http://dx.doi.org/10.1016/j.ympev.2004.02.008

    Nylander, J.A.A. (2004) MrModeltest v.2. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.

    Orlov, N.L., Ryabov, S.A. & Nguyen, T.T. (2009) Two new species of genera Protobothrops Hoge et Romano-Hoge, 1983 and Viridovipera Malhotra et Thorpe, 2004 (Ophidia: Viperidae: Crotalinae) from karst region in northeastern Vietnam, part I, description of a new species of Protobothrops genus. Russian Journal Herpetology, 16, 69–82.

    Pan, H.J., Chettri, B., Yang, D.D., Jiang, K., Wang, K., Zhang, L. & Vogel, G. (2013) A new species of the genus Protobothrops (Squamata: Viperidae) from southern Tibet, China and Sikkim, India. Asian Herpetological Research, 4 (2), 109–115.

    http://dx.doi.org/10.3724/SP.J.1245.2013.00109

    Parkinson, C.L., Moody, S.M. & Ahlquist, J.E. (1997) Phylogenetic relationships of the “Agkistrodon complex” based on mitochondrial DNA sequence data. In: Thorpe, R.S., Wüster, W. & Malhotra, A. (Eds.), Venomous Snakes: Ecology, Evolution and Snakebite). Clarendon Press, Oxford, pp. 63–78.

    Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer v1.6. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed 1 March 2015)

    Ree, R.H., Moore, B.R., Webb, C.O. & Donoghue, M.J. (2005) A likelihood framework for inferring the evolution of geographic range on phylogenetic trees. Evolution, 59 (11), 2299–2311.

    http://dx.doi.org/10.1554/05-172.1

    Ronquist, F., Teslenko, M., Mark, P.V.D., Ayres, D., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3), 539–542.

    http://dx.doi.org/10.1093/sysbio/sys029

    Sambrook, J. & Russell, D.W. (2002) Molecular Cloning: A Laboratory Manual, 3rd Edition. Cold Spring Harbor Laboratory Press, NY, 2100 pp.

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

    http://dx.doi.org/10.1093/bioinformatics/btl446

    Stephens, M., Smith, N.J. & Donnelly, P. (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68, 978–989.

    http://dx.doi.org/10.1086/319501

    Sun, H.L. (1997) Research of the formation, environment change on Qinghai-Xizang (Tibetan) plateau. Hunan Science and Technology Press, Changsha, 181 pp.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    http://dx.doi.org/10.1093/molbev/mst197

    Townsend, T.M., Alegre, R.E., Kelley, S.T., Wiens, J.J. & Reeder, T.W. (2008) Rapid development of multiple nuclear loci for phylogenetic analysis using genomic resources: An example from squamate reptiles. Molecular Phylogenetics and Evolution, 47, 129–142

    http://dx.doi.org/10.1016/j.ympev.2008.01.008

    Uetz, P. The Reptile Database. Available from http://www.reptile-database.org (accessed 18 December 2014)

    Wüster, W., Peppin, L., Pook, C.E. & Walker, D.E. (2008) A nesting of vipers: Phylogeny and historical biogeography of the Viperidae (Squamata: Serpentes). Molecular Phylogenetics and Evolution, 49, 445–459.

    http://dx.doi.org/10.1016/j.ympev.2008.08.019

    Yan, F., Zhou, W.W., Zhao, H.T., Yuan, Z.Y., Wang, Y.Y., Jiang, K., Jin, J.Q., Murphy, R.W., Che, J. & Zhang, Y.P. (2013) Geological events play a larger role than Pleistocene climatic fluctuations in driving the genetic structure of Quasippa boulengeri (Anura: Dicroglossidae). Molecular Ecology, 22, 1120–1133.

    http://dx.doi.org/10.1111/mec.12153

    Yang, J.H., Orlov, N.L. & Wang, Y.Y. (2011) A new species of pitviper of the genus Protobothrops from China (Squamata: Viperidae). Zootaxa, 2936, 59–68.

    Yu, Y., Harris, A.J. & He, X.J. (2010) S-DIVA (Statistical Dispersal-Vicariance Analysis): A tool for inferring biogeographic histories. Molecular Phylogenetics and Evolution, 56 (2), 848–850.

    http://dx.doi.org/10.1016/j.ympev.2010.04.011

    Yu, Y., Harris, A.J. & He, X.J. (2015). RASP (Reconstruct Ancestral State in Phylogenies) [v.1.107]. Available from: http://mnh.scu.edu.cn/soft/blog/RASP (accessed 10 June 2015)

    Zhang, D.X. & Hewitt, G.M. (1996) Nuclear integrations-challenges for mitochondrial-DNA markers. Trends in Ecology & Evolution, 11, 247–251.

    http://dx.doi.org/10.1016/0169-5347(96)10031-8

    Zhao, E.M. (2006) Snakes of China. Anhui Science and Technology Publishing House, Hefei, 372 pp.

    Zhou, W.W., Yan, F., Fu, J.Z., Wu, S.F., Murphy, R.W., Che, J. & Zhang, Y.P. (2013) River islands, refugia and genetic structuring in the endemic brown frog Rana kukunoris (Anura, Ranidae) of the Qinghai-Tibetan Plateau. Molecular Ecology, 22, 130–142.

    http://dx.doi.org/10.1111/mec.12087.