Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 3626 No. 1: 12 Mar. 2013
Type: Articles
Published: 2013-03-12
DOI: 10.11646/zootaxa.3626.1.3
Page range: 77–93
Abstract views: 52
PDF downloaded: 1

Molecular phylogenetic reconstruction of the endemic Asian salamander family Hynobiidae (Amphibia, Caudata)

Department of Biology, University of Kentucky, 101 Thomas Hunt Morgan Building, Lexington, KY, 40506-0225
Genomics, Department of Biology, Merritt College, 1250 Campus Drive, Oakland, CA 94619 Museum of Vertebrate Zoology, 3101 Valley Life Science Building, University of California, Berkeley, CA 94720
Graduate School of Human and Environmental Studies, Kyoto University, Kyoto 606-8501, Japan
Smithsonian Institution, National Museum of Natural History, 4210 Silver Hill Rd., MRC 534, Suitland, MD 20746
Amphibia Caudata

Abstract

The salamander family Hynobiidae contains over 50 species and has been the subject of a number of molecular phylo-genetic investigations aimed at reconstructing branches across the entire family. In general, studies using the greatest amount of sequence data have used reduced taxon sampling, while the study with the greatest taxon sampling has used a limited sequence data set. Here, we provide insights into the phylogenetic history of the Hynobiidae using both dense taxon sampling and a large mitochondrial DNA sequence data set. We report exclusive new mitochondrial DNA data of 2566 aligned bases (with 151 excluded sites, of included sites 1157 are variable with 957 parsimony informative). This is sampled from two genic regions encoding a 12S–16S region (the 3’ end of 12S rRNA, tRNAVAl, and the 5’ end of 16S rRNA), and a ND2–COI region (ND2, tRNATrp, tRNAAla, tRNAAsn, the origin for light strand replication—OL, tRNACys, tRNATyr, and the 5’ end of COI). Analyses using parsimony, Bayesian, and maximum likelihood optimality criteria produce similar phylogenetic trees, with discordant branches generally receiving low levels of branch support. Monophyly of the Hynobiidae is strongly supported across all analyses, as is the sister relationship and deep divergence between the genus Onychodactylus with all remaining hynobiids. Within this latter grouping our phylogenetic results identify six clades that are relatively divergent from one another, but for which there is minimal support for their phy-logenetic placement. This includes the genus Batrachuperus, the genus Hynobius, the genus Pachyhynobius, the genus Salamandrella, a clade containing the genera Ranodon and Paradactylodon, and a clade containing the genera Liua and Pseudohynobius. This latter clade receives low bootstrap support in the parsimony analysis, but is consistent across all three analytical methods. Our results also clarify a number of well-supported relationships within the larger Batrachu-perus and Hynobius clades. While the relationships identified in this study do much to clarify the phylogenetic history of the Hynobiidae, the poor resolution among major hynobiid clades, and the contrast of mtDNA-derived relationships with recent phylogenetic results from a small number of nuclear genes, highlights the need for continued phylogenetic study with larger numbers of nuclear loci.

References

  1. Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H. L., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J. H., Staden, R., & Young, I. G. (1981). Sequence and organization of the human mitochondrial genome. Nature, 290, 457–465.
    http://dx.doi.org/10.1038/290457a0

    Angelier, J., Bergerat, F., Chu, H.-T., & Lee, T.-Q. (1990) Tectonic analyses and the evolution of a curved collision belt: The Hsüehshan Range, northern Taiwan. in Geodynamic Evolution of the Eastern Eurasian Margin (Angelier, J., ed.). Tectonophysics, 183, 77–96.

    Braun, E. L. & Kimball, R. T. (2002) Examining basal avian divergences with mitochondrial sequences: model complexity, taxon sampling, and sequence length. Systematic Biology, 51, 614–625.
    http://dx.doi.org/10.1080/10635150290102294

    DeBry, R. W. (2005) The systematic component of phylogenetic error as a function of taxonomic sampling under parsimony. Systematic Biology, 54, 432–440.
    http://dx.doi.org/10.1080/10635150590946745

    Drummond, A. J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.

    Fu, J. Z., Wang, Y. Z., Zeng, X. M., Liu, Z. J. & Zheng, Y. C. (2001) Genetic diversity of eastern Batrachuperus (Caudata: Hynobiidae). Copeia, 1100–1107.
    http://dx.doi.org/10.1643/0045-8511(2001)001[1100:GDOEBC]2.0.CO;2

    Gutell, R. R. & Fox, G. E. (1988) A compilation of large subunit RNA sequences presented in a structural format. Nucleic Acids Research, 16 Suppl, r175–269.
    http://dx.doi.org/10.1093/nar/16.suppl.r175

    Heath, T. A., Zwickl, D. J., Kim, J. & Hillis, D. M. (2008) Taxon sampling affects inferences of macroevolutionary processes from phylogenetic trees. Systematic Biology, 57, 160–166.
    http://dx.doi.org/10.1080/10635150701884640http://dx.doi.org/10.1080/10635150701884640

    Hickson, R. E., Simon, C., Cooper, A., Spicer, G. S., Sullivan, J. & Penny, D. (1996) Conserved sequence motifs, alignment, and secondary structure for the third domain of animal 12S rRNA. Molecular Biology and Evolution, 13, 150–169.
    http://dx.doi.org/10.1093/oxfordjournals.molbev.a025552

    Hillis, D. M., Pollock, D. D., McGuire, J. A. & Zwickl, D. J. (2003) Is sparse taxon sampling a problem for phylogenetic inference? Systematic Biology, 52, 124–126.
    http://dx.doi.org/10.1080/10635150390132911

    Huelsenbeck, J. P., Ronquist, F., Nielsen, R. & Bollback, J. P. (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310–2314.
    http://dx.doi.org/10.1126/science.1065889

    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.
    http://dx.doi.org/10.1073/pnas.86.16.6196

    Kolaczkowski, B. & Thornton, J. W. (2007) Effects of branch length uncertainty on Bayesian posterior probabilities for phylogenetic hypotheses. Molecular Biology and Evolution, 24, 2108–2118.

    Kumazawa, Y. & Nishida, M. (1993) Sequence evolution of mitochondrial transfer RNA genes and deep-branch animal phylogenetics. Journal of Molecular Evolution, 37, 380–398.
    http://dx.doi.org/10.1007/BF00178868

    Lee, J.-C., Angelier, J., & Chu, H.-T. (1997) Polyphase history and kinematics of a complex major fault zone in the northern Taiwan mountain belt: The Lishan fault. in An Introduction to Active Collision in Taiwan (Lallemand, S. E., & Tsien, H.-H., eds.). Tectonophysics, 274, 97–115.

    Macey, J. R. & Verma, A. (1997) Homology in phylogenetic analysis: alignment of transfer RNA genes and the phylogenetic position of snakes. Molecular Phylogenetics and Evolution, 7, 272–279.
    http://dx.doi.org/10.1006/mpev.1997.0379

    Macey, J. R., Larson, A., Ananjeva, N. B., Fang, Z. L. & Papenfuss, T. J. (1997a) Two novel gene orders and the role of light-strand replication in rearrangement of the vertebrate mitochondrial genome. Molecular Biology and Evolution, 14, 91–104.
    http://dx.doi.org/10.1093/oxfordjournals.molbev.a025706

    Macey, J. R., Larson, A., Ananjeva, N. B. & Papenfuss, T. J. (1997b) Replication slippage may cause parallel evolution in the secondary structures of mitochondrial transfer RNAs. Molecular Biology and Evolution, 14, 30–39.
    http://dx.doi.org/10.1093/oxfordjournals.molbev.a025699

    Macey, J. R., Larson, A., Ananjeva, N. B. & Papenfuss, T. J. (1997c) Evolutionary shifts in three major structural features of the mitochondrial genome among iguanian lizards. Journal of Molecular Evolution, 44, 660–674.
    http://dx.doi.org/10.1007/PL00006190

    Macey, J. R., Wang, Y., Ananjeva, N. B., Larson, A., & Papenfuss, T. J. (1999) Vicariant patterns of fragmentation among gekkonid lizards of the genus Teratoscincus produced by the Indian Collision: A molecular phylogenetic perspective and an area cladogram for Central Asia. Molecular Phylogenetics and Evolution, 12, 320–332.
    http://dx.doi.org/10.1006/mpev.1999.0641

    Macey, J. R., Schulte II, J. A., Larson, A., Ananjeva, N. B., Wang, Y., Pethiyagoda, R., Rastegar-Pouyani, N., & Papenfuss, T. J. (2000) Evaluating trans-Tethys migration: An example using acrodont lizard phylogenetics. Systematic Biology, 49, 233–256.
    http://dx.doi.org/10.1093/sysbio/49.2.233

    Maddison, W. P. & Maddison, D. R. (2000) MacClade4: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, MA.

    Maniatis, T. E., Fritsch, F. & Sambrook, J. (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Matsui, M., Iwasawa, H., Takahashi, H., Hayashi, T. & Kumakura, M. (1992) Invalid Specific Status of Hynobius-Sadoensis Sato: Electrophoretic Evidence (Amphibia, Caudata). Journal of Herpetology, 26, 308–315.
    http://dx.doi.org/10.2307/1564886

    Matsui, M., Kokuryo, Y., Misawa, Y. & Nishikawa, K. (2004) A new species of salamander of the genus Hynobius from central Honshu, Japan (Amphibia, Urodela). Zoological Science, 21, 661–669.
    http://dx.doi.org/10.2108/zsj.21.661

    Matsui, M., Misawa, Y., Nishikawa, K. & Tanabe, S. (2000) Allozymic variation of Hynobius kimurae Dunn (Amphibia, Caudata). Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology, 125, 115–125.
    http://dx.doi.org/10.1016/S0305-0491(99)00154-6

    Matsui, M., Nishikawa, K., Misawa, Y. & Tanabe, S. (2007) Systematic relationships of Hynobius okiensis among Japanese salamanders (Amphibia: Caudata). Zoological Science, 24, 746–751.
    http://dx.doi.org/10.2108/zsj.24.746

    Matsui, M., Nishikawa, K., Tanabe, S. & Misawa, Y. (2001) Systematic status of Hynobius tokyoensis (Amphibia: Urodela) from Aichi Prefecture, Japan: a biochemical survey. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology, 130, 181–189.
    http://dx.doi.org/10.1016/S1096-4959(01)00424-9

    Matsui, M., Nishikawa, K., Utsunomiya, T. & Tanabe, S. (2006) Geographic allozyme variation in the Japanese clouded salamander, Hynobius nebulosus (Amphibia: Urodela). Biological Journal of the Linnean Society, 89, 311–330.
    http://dx.doi.org/10.1111/j.1095-8312.2006.00676.x

    Matsui, M., Tominaga, A., Hayashi, T., Misawa, Y. & Tanabe, S. (2007) Phylogenetic relationships and phylogeography of Hynobius tokyoensis (Amphibia: Caudata) using complete sequences of cytochrome b and control region genes of mitochondrial DNA. Molecular Phylogenetics and Evolution, 44, 204–216.
    http://dx.doi.org/10.1016/j.ympev.2006.11.031

    McIntrye, A., Moore, T. C., Andersen, B., Balsam, W., Bé, A., Brunner, C., Cooley, J., Crowley, T., Denton, G., Gardner, J., Geitzenauer, K., Hays, J. D., Hutson, W., Imbrie, J., Irwing, G., Kellogg, T., Kennett, J., Kipp, N., Kukla, G., Kukla, H., Lozano, J., Luz, B., Mangion, S., Matthews, R. K., Mayewski, P., Molfino, B., Ninkovich, D., Opdyke, N., Prell, W., Robertson, J., Ruddiman, W. F., Sachs, H., Saito, T., Shackleton, N., Thierstein, H., & Thompson, P. (1976) The surface of the ice-age earth. Science, 191, 1131–1137.
    http://dx.doi.org/10.1126/science.191.4232.1131

    Nishihara, H., Okada, N. & Hasegawa, M. (2007) Rooting the eutherian tree: the power and pitfalls of phylogenomics. Genome Biology, 8, R199.

    Nishikawa, K., Matsui, M. & Tanabe, S. (2005) Biochemical phylogenetics and historical biogeography of Hynobius boulengeri and H. stejnegeri (Amphibia: Caudata) from the Kyushu region, Japan. Herpetologica, 61, 54–62.
    http://dx.doi.org/10.1655/03-89

    Nishikawa, K., Matsui, M., Tanabe, S. & Sato, S. (2001) Geographic enzyme variation in a Japanese salamander, Hynobius boulengeri Thompson (Amphibia: Caudata). Herpetologica, 57, 281–294.

    Nishikawa, K., Matsui, M., Tanabe, S. & Sato, S. (2007) Morphological and allozymic variation in Hynobius boulengeri and H. steinegeri (Amphibia: Urodela: Hynobiidae). Zoological Science, 24, 752–766.
    http://dx.doi.org/10.2108/zsj.24.752

    Peng, R., Zhang, P., Xiong, J. L., Gu, H. J., Zeng, X. M. & Zou, F. D. (2010) Rediscovery of Protohynobius puxiongensis (Caudata: Hynobiidae) and its phylogenetic position based on complete mitochondrial genomes. Molecular Phylogenetics and Evolution, 56, 252–258.
    http://dx.doi.org/10.1016/j.ympev.2009.12.011

    Pollock, D. D., Zwickl, D. J., McGuire, J. A. & Hillis, D. M. (2002) Increased taxon sampling is advantageous for phylogenetic inference. Systematic Biology, 51, 664–671.
    http://dx.doi.org/10.1080/10635150290102357

    Posada, D. & Crandall, K. A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817–818.
    http://dx.doi.org/10.1093/bioinformatics/14.9.817

    Pyron, R. A. & Wiens, J. J. (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution, 61, 543–583.
    http://dx.doi.org/10.1016/j.ympev.2011.06.012

    Rambaut, A. & Drummond, A. J. (2007) Tracer v1.5, Available from http://beast.bio.ed.ac.uk/Tracer

    Roelants, K., Gower, D. J., Wilkinson, M., Loader, S. P., Biju, S. D., Guillaume, K., Moriau, L. & Bossuyt, F. (2007) Global patterns of diversification in the history of modern amphibians. Proceedings of the National Academy of Sciences of the United States of America, 104, 887–892.
     http://dx.doi.org/10.1073/pnas.0608378104

    Ronquist, F. & Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.http://dx.doi.org/10.1093/bioinformatics/btg180

    Samuels, A. K., Weisrock, D. W., Smith, J. J., France, K. J., Walker, J. A., Putta, S. & Voss, S. R. (2005) Transcriptional and phylogenetic analysis of five complete ambystomatid salamander mitochondrial genomes. Gene, 349, 43–53.
    http://dx.doi.org/10.1016/j.gene.2004.12.037

    Soltis, D. E., Albert, V. A., Savolainen, V., Hilu, K., Qiu, Y. L., Chase, M. W., Farris, J. S., Stefanovic, S., Rice, D. W., Palmer, J. D. & Soltis, P. S. (2004) Genome-scale data, angiosperm relationships, and 'ending incongruence': a cautionary tale in phylogenetics. Trends in Plant Science, 9, 477–483.
    http://dx.doi.org/10.1016/j.tplants.2004.08.008

    Sorenson, M. D. (1999) TreeRot, version 2. Boston University, Boston, MA.

    Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology, 57, 758–771.
    http://dx.doi.org/10.1080/10635150802429642

    Stamatakis, A., Ludwig, T. & Meier, H. (2005) RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics, 21, 456–463.
    http://dx.doi.org/10.1093/bioinformatics/bti191

    Stefanovic, S., Rice, D. W. & Palmer, J. D. (2004) Long branch attraction, taxon sampling, and the earliest angiosperms: Amborella or monocots? BMC Evolutionary Biology, 4, 35. http://dx.doi.org/10.1186/1471-2148-4-35

    Swofford, D. L. (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, Massachusettes.

    Titus, T. A. & Larson, A. (1995) A molecular phylogenetic perspective on the evolutionary radiation of the salamander family Salamandridae. Systematic Biology, 44, 125–151.
    http://dx.doi.org/10.2307/2413703

    Tominaga, A., Matsui, M., Nishikawa, K. & Sato, S. (2003) Occurrence of two types of Hynobius naevius in northern Kyushu, Japan (Amphibia: Urodela). Zoological Science, 20, 1467–1476.
    http://dx.doi.org/10.2108/zsj.20.1467

    Tominaga, A., Matsui, M., Nishikawa, K. & Tanabe, S. (2005) Phylogenetic relationships of Hynobius naevius as revealed by mitochondrial 12S and 16S rRNA genes (Amphibia: Caudata). Zoological Science, 22, 1434–1434.

    Tominaga, A., Matsui, M., Nishikawa, K. & Tanabe, S. (2006) Phylogenetic relationships of Hynobius naevius (Amphibia: Caudata) as revealed by mitochondrial 12S and 16S rRNA genes. Molecular Phylogenetics and Evolution, 38, 677–684.http://dx.doi.org/10.1016/j.ympev.2005.10.014

    Van de Peer, Y., Van den Broeck, I., De Rijk, P. & De Wachter, R. (1994) Database on the structure of small ribosomal subunit RNA. Nucleic Acids Research, 22, 3488–3494.
    http://dx.doi.org/10.1093/nar/22.17.3488

    Weisrock, D. W., Harmon, L. J. & Larson, A. (2005) Resolving deep phylogenetic relationships in salamanders: analyses of mitochondrial and nuclear genomic data. Systematic Biology, 54, 758–777.http://dx.doi.org/10.1080/10635150500234641

    Wiens, J., Bonett, R. & Chippindale, P. (2005) Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships. Systematic Biology, 54, 91–110.
    http://dx.doi.org/10.1080/10635150590906037

    Zeng, X. M., Fu, J. Z., Chen, L. Q., Tian, Y. Z. & Chen, X. H. (2006) Cryptic species and systematics of the hynobiid salamanders of the Liua-Pseudohynobius complex: molecular and phylogenetic perspectives. Biochemical Systematics and Ecology, 34, 467–477.
    http://dx.doi.org/10.1016/j.bse.2006.01.006

    Zhang, P., Chen, Y., Zhou, H., Liu, Y., Wang, X., Papenfuss, T., Wake, D. & Qu, L. (2006) Phylogeny, evolution, and biogeography of Asiatic Salamanders (Hynobiidae). Proceedings of the National Academy of Sciences of the United States of America, 103, 7360–7365.
    http://dx.doi.org/10.1073/pnas.0602325103

    Zheng, Y., Peng, R., Kuro-o, M. & Zeng, X. (2011) Exploring patterns and extent of bias in estimating divergence time from mitochondrial DNA sequence data in a particular lineage: a case study of salamanders (order Caudata). Molecular Biology and Evolution, 28, 2521–2535.
    http://dx.doi.org/10.1093/molbev/msr072

    Zwickl, D. J. & Hillis, D. M. (2002) Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology, 51, 588–598.
    http://dx.doi.org/10.1080/10635150290102339

    Zwickl, D. & Holder, M. (2004) Model parameterization, prior distributions, and the general time-reversible model in Bayesian phylogenetics. Systematic Biology, 53, 877–888.