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Type: Article
Published: 2023-08-30
Page range: 201-236
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Taxonomic reassessment of salamanders (genus Hynobius) from Tsushima Islands, Japan, with a resurrection of Hynobius tagoi Dunn, 1923 (Amphibia: Caudata)

1Graduate School of Human and Environmental Studies; Kyoto University; Yoshida Nihonmatsu; Sakyo-ku; Kyoto 606-8501; JAPAN. Present affiliation: Akita Prefectural Office; Sanno 4-1-1; Akita 010-8570; JAPAN.
Graduate School of Human and Environmental Studies; Kyoto University; Yoshida Nihonmatsu; Sakyo-ku; Kyoto 606-8501; JAPAN. Graduate School of Global Environmental Studies; Kyoto University; Yoshida Honmachi; Sakyo-ku; Kyoto 606-8501; JAPAN.
Graduate School of Human and Environmental Studies; Kyoto University; Yoshida Nihonmatsu; Sakyo-ku; Kyoto 606-8501; JAPAN.
Graduate School of Global Environmental Studies; Kyoto University; Yoshida Honmachi; Sakyo-ku; Kyoto 606-8501; JAPAN.
Faculty of Agriculture and Life Science; Hirosaki University; Bunkyo-cho 3; Hirosaki; Aomori 036-8561; JAPAN.
Amphibia egg-sac Hynobius nebulosus H. tsuensis Kyushu microsatellite neotype nuclear DNA

Abstract

To clarify the taxonomic status of salamanders from Tsushima Islands, Japan, we examined two species of salamanders, Hynobius tsuensis and Hynobius sp. from Tsushima Islands, and compared them with H. nebulosus from Kyushu. We found that the three taxa differ from each other in nuclear DNA, adult morphology, and egg-sac shape, and consider them to be independent species. Based on the investigation of type specimens of the synonyms, we identified Hynobius sp. as H. tagoi Dunn, 1923 and redescribe it herein. Also, we designate a neotype for H. tsuensis and redescribe H. tsuensis. The distribution areas of the two species partly overlap but they were distinguishable by their body colorations: H. tsuensis has uniformly blackish tail sides and a distinct yellow stripe on the upper tail edge; whereas H. tagoi has brown tail sides with numerous dark stippling and without a distinct yellow stripe on the upper tail edge.

 

References

  1. Abe, Y. (1922) On Ambystomidae from Japan. Zoological Magazine, 34, 328–332.
  2. AmphibiaWeb (2023) Available from: https://amphibiaweb.org/lists/Hynobiidae.shtml (accessed 28 February 2023)
  3. Aoki, G., Matsui, M. & Nishikawa, K. (2013) Mitochondrial cytochrome b phylogeny and historical biogeography of the Tohoku salamander, Hynobius lichenatus (Amphibia, Caudata). Zoological Science, 30, 167–173. https://doi.org/10.2108/zsj.30.167
  4. Dunn, E.R. (1923a) New species of Hynobius from Japan. Proceedings of the California Academy of Sciences, 4th Series, 12, 27–29.
  5. Dunn, E.R. (1923b) The salamanders of the family Hynobiidae. Proceedings of the American Academy of Arts and Sciences, 58, 445–523. https://doi.org/10.2307/20026019
  6. Dunn, O.J. (1964) Multiple comparisons using rank sums. Technometrics, 6, 241–252. https://doi.org/10.1080/00401706.1964.10490181
  7. Earl, D.A. & vonHoldt, B.M. (2012) STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7
  8. Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
  9. Hammer, Ø., Harper, D.A. & Ryan, P.D. (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4, 1–9.
  10. Hara, S. & Nishikawa, K. (2020) Intraspecific variation in the external and skeletal morphology of Hynobius setouchi Matsui, Okawa, Tanabe et Misawa, 2019 (Amphibia: Urodela: Hynobiidae). Zoological Science, 37, 346–357. https://doi.org/10.2108/zs190155
  11. Hasegawa, M., Kishino, H. & Yano, T. (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22, 160–174. https://doi.org/10.1007/BF02101694
  12. 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. https://doi.org/10.1126/science.1065889
  13. Ito, J., Baba, A., Niwa, K. & Nishikawa, K. (2023) A note on underground egg sacs of the Tsushima salamander, Hynobius tsuensis (Caudata: Hynobiidae). Herpetology Notes, 16, 211–212.
  14. Iwasawa, H. & Yamashita, K. (1991) Normal stages of development of a hynobiid salamander, Hynobius nigrescens Stejneger. Japanese Journal of Herpetology, 14, 39–62. https://doi.org/10.5358/hsj1972.14.2_39
  15. Jakobsson, M. & Rosenberg, N.A. (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23, 1801–1806. https://doi.org/10.1093/bioinformatics/btm233
  16. Kanamori, S., Nishikawa, K., Matsui, M. & Tanabe, S. (2022) A new species of lotic breeding salamander (Amphibia, Caudata, Hynobiidae) from Shikoku, Japan. PeerJ, 10, e13891. https://doi.org/10.7717/peerj.13891
  17. Kramer, C.Y. (1956) Extension of multiple range tests to group means with unequal numbers of replications. Biometrics, 12, 307–310. https://doi.org/10.2307/3001469
  18. Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874. https://doi.org/10.1093/molbev/msw054
  19. Lee, B.H., Kim, J.Y., Song, S., Hur, J.M., Cho, J.Y. & Park, Y.C. (2011) The complete mitochondrial genome sequence of the Kori salamander Hynobius yangi (Caudata: Hynobiidae). Mitochondrial DNA, 22, 168–170. https://doi.org/10.3109/19401736.2011.636437
  20. Matsui, M., Misawa, Y. & Nishikawa, K. (2009) Morphological variation in a Japanese salamander, Hynobius kimurae (Amphibia, Caudata). Zoological Science, 26, 87–95. https://doi.org/10.2108/zsj.26.87
  21. Matsui, M., Misawa, Y., Nishikawa, K. & Shimada, T. (2017) A new species of lentic breeding salamander (Amphibia, Caudata) from central Japan. Current Herpetology, 36, 116–126. https://doi.org/10.5358/hsj.36.116
  22. Matsui, M., Okawa, H., Nishikawa, K., Aoki, G., Eto, K., Yoshikawa, N., Tanabe, S., Misawa, Y. & Tominaga, A. (2019) Systematics of the widely distributed Japanese clouded salamander, Hynobius nebulosus (Amphibia: Caudata: Hynobiidae), and its closest relatives. Current Herpetology, 38, 32–90. https://doi.org/10.5358/hsj.38.32
  23. 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. https://doi.org/10.1016/j.ympev.2006.11.031
  24. Matsui, M., Tominaga, A., Liu, W.Z. & Tanaka-Ueno, T. (2008a) Reduced genetic variation in the Japanese giant salamander, Andrias japonicus (Amphibia: Caudata). Molecular Phylogenetics and Evolution, 49, 318–326. https://doi.org/10.1016/j.ympev.2008.07.020
  25. Matsui, M., Yoshikawa, N., Tominaga, A., Sato, T., Takenaka, S., Tanabe, S., Nishikawa, K. & Nakabayashi, S. (2008b) Phylogenetic relationships of two Salamandrella species as revealed by mitochondrial DNA and allozyme variation (Amphibia: Caudata: Hynobiidae). Molecular Phylogenetics and Evolution, 48, 84–93. https://doi.org/10.1016/j.ympev.2008.04.010
  26. Ministry of the Environment Government of Japan (2020) Red List of Ministry of the Environment Government of Japan, 2020. Available from: https://www.env.go.jp/content/900515981.pdf (accessed 23 April 2023)
  27. Misawa, Y. (1989) The method of counting costal grooves. In: Matsui, M., Hikida, T. & Goris, R.C. (Eds.), Current Herpetology in East Asia. Herpetological Society of Japan, Kyoto, pp. 129–134.
  28. Mori, T. (1928) On amphibians and reptiles of Quelpart Island. Chosen Natural History Society Journal, 6, 47–52.
  29. Nagaoka, S. (2001) Northern and Central Part of Kyushu Island: Tsushima Island and Tsushima Strait. In: Machida, Y., Ohta, Y., Kawana, T., Moriwaki, H. & Nagaoka, S. (Eds.), The Topography of Japan. 7. Kyushu Island and Nansei Islands. University of Tokyo Press, Tokyo, pp. 106–109.
  30. Nagasaki Prefecture (2022) Prefectural Red List of Nagasaki, 2022. Available from: https://www.pref.nagasaki.jp/shared/uploads/2022/03/1648644060-2.pdf (accessed 23 April 2023)
  31. Naito, J.I. & Kambayashi, C. (2022) Distribution pattern of Shikoku clawed salamander, Onychodactylus kinneburi, in the Western Chugoku Mountains. Biogeography, 24, 79–83. https://doi.org/10.11358/biogeo.24.79
  32. Nakamura, K. & Uéno, S.-I. (1963) Japanese Reptiles and Amphibians in Colour. Hoikusha, Osaka, 214 pp.
  33. Nishikawa, K. (2009) The first specimen of Karsenia koreana (Caudata: Plethodontidae) collected 34 years before its description. Current Herpetology, 28, 27–28. https://doi.org/10.3105/018.028.0104
  34. Nishikawa, K., Jiang, J.P., Matsui, M., Mo, Y.M., Chen, X.H., Kim, J.B., Tominaga, A. & Yoshikawa, N. (2010) Invalidity of Hynobius yunanicus and molecular phylogeny of Hynobius salamander from continental China (Urodela, Hynobiidae). Zootaxa, 2426 (1), 65–67. https://doi.org/10.11646/zootaxa.2426.1.5
  35. Nishikawa, K. & Matsui, M. (2014) Three new species of the salamander genus Hynobius (Amphibia, Urodela, Hynobiidae) from Kyushu, Japan. Zootaxa, 3852 (2), 203–226. https://doi.org/10.11646/zootaxa.3852.2.3
  36. Nishikawa, K., Matsui, M., Tanabe, S. & Sato, S. (2007) Morphological and allozymic variation in Hynobius boulengeri and H. stejnegeri (Amphibia: Urodela: Hynobiidae). Zoological Science, 24, 752–766. https://doi.org/10.2108/zsj.24.752
  37. Niwa, K., Kuro-o, M. & Nishikawa, K. (2021) Discovery of two lineages of Hynobius tsuensis (Amphibia, Caudata) endemic to Tsushima Island, Japan. Zoological Science, 38, 259–266. https://doi.org/10.2108/zs200149
  38. Niwa, K., Yoshikawa, N., Nishikawa, K. & Matsui, M. (2022a) Development of eight microsatellite markers for the Tsushima salamander, Hynobius tsuensis, and its close relatives (Amphibia: Caudata) with preliminary analysis of genetic differentiation. Current Herpetology, 41, 125–131. https://doi.org/10.5358/hsj.41.125
  39. Niwa, K., Tran, D.V. & Nishikawa, K. (2022b) Differentiated historical demography and ecological niche forming present distribution and genetic structure in coexisting two salamanders (Amphibia, Urodela, Hynobiidae) in a small island, Japan. PeerJ, 10, e13202. https://doi.org/10.7717/peerj.13202
  40. Okada, Y. (1934) A contribution toward a check list of the Urodeles of Japan. Copeia, 1, 16–19. https://doi.org/10.2307/1436428
  41. Okada, Y. (1935) Summary of taxonomy and distribution of Japanese salamanders. Zoological Magazine, 47, 575–588.
  42. Oyama, J. (1930) Hynobius tagoi and Hynobius tsuensis. Bulletin of the Biogeographical Society of Japan, 2, 21–35. https://doi.org/10.2307/1436476
  43. Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959. https://doi.org/10.1093/genetics/155.2.945
  44. Rambaut, A., Suchard, M., Xie, W. & Drummond, A. (2014) Tracer. Version 1.6. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. [program]
  45. Raymond, M. & Rousset, F. (1995) An exact test for population differentiation. Evolution, 49, 1280–1283. https://doi.org/10.2307/2410454
  46. Rice, W.R. (1989) Analyzing tables of statistical tests. Evolution, 43, 223–225. https://doi.org/10.2307/2409177
  47. Ronquist, F., Teslenko, M., Mark, P., Ayres, D.L., Darling, A., Höhna, 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, 539–542. https://doi.org/10.1093/sysbio/sys029
  48. Rosenberg, N.A. (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137–138. https://doi.org/10.1046/j.1471-8286.2003.00566.x
  49. Rousset, F. (2008) GENEPOP’007: A complete reimplementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8, 103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
  50. Sato, I. (1934) Taxonomical study of the salamanders of the nebulosus group, with special reference to the morphology of the skull. Zoological Magazine, 46, 214–224.
  51. Sato, I. (1937) A synopsis of the family Hynobiidae of Japan. Bulletin of the Biogeographical Society of Japan, 7, 31–45.
  52. Sato, I. (1943) A Monograph of the Tailed Batrachians of Japan. Nippon Shuppan-sha, Osaka, 520 pp.
  53. Sparreboom, M. (2014) Salamanders of the Old World. KNNV Publishing, Zeist, 431 pp. https://doi.org/10.1163/9789004285620_017
  54. Stejneger, L. (1907) Herpetology of Japan and adjacent territory. Bulletin of the United States National Museum, 58, 1–577. https://doi.org/10.5479/si.03629236.58.i
  55. Sugawara, H., Watabe, T., Yoshikawa, T. & Nagano, M. (2018) Morphological and molecular analyses of Hynobius dunni reveal a new species from Shikoku, Japan. Herpetologica, 74, 159–168. https://doi.org/10.1655/Herpetologica-D-17-00002.1
  56. Sugawara, H., Iwata, T., Yamashita, H. & Nagano, M. (2021) Taxonomic reassessment of the Izumo lineage of Hynobius utsunomiyaorum: Description of a new species from Chugoku, Japan. Animals, 11, 2187. https://doi.org/10.3390/ani11082187
  57. Sugawara, H., Naito, J., Iwata, T. & Nagano, M. (2022a) Molecular phylogenetic and morphological problems of the Aki salamander Hynobius akiensis: description of two new species from Chugoku, Japan. Bulletin of the Kanagawa Prefectural Museum (Natural Science), 51, 35–46. https://doi.org/10.32225/bkpmnh.2022.51_35
  58. Sugawara, H., Fujitani, T., Seguchi, S., Sawahata, T. & Nagano, M. (2022b) Taxonomic re-examination of the Yamato salamander Hynobius vandenburghi: description of a new species from Central Honshu, Japan. Bulletin of the Kanagawa Prefectural Museum (Natural Science), 51, 47–59. https://doi.org/10.32225/bkpmnh.2022.51_47
  59. Sugawara, H., Tahara, Y., Nakazono, S., Matsukoji, T. & Nagano, M. (2022c) Taxonomic revision of the Yamaguchi salamander Hynobius bakan: Description of two new species from Chugoku and Kyushu, Japan. Science Report of the Yokosuka City Museum, 69, 1–17.
  60. Suk, H.Y., Kim, D.Y., Cha, S. & Min, M.S. (2019) The complete mitochondrial genome information of Hynobius unisacculus (Amphibia, Caudata, Hynobiidae) and the phylogenetic implication. Mitochondrial DNA Part B, 4, 3705–3706. https://doi.org/10.1080/23802359.2019.1679680
  61. Suyama, Y. & Matsuki, Y. (2015) MIG-seq: An effective PCR-based method for genome-wide single-nucleotide polymorphism genotyping using the next-generation sequencing platform. Scientific Reports, 5, 16963. https://doi.org/10.1038/srep16963
  62. Tago, K. (1904) A topic of salamanders. Zoological Magazine, 16, 41–46.
  63. Tago, K. (1907) Study of salamanders from Japan. Zoological Magazine, 19, 229–248.
  64. Tanabe, A.S. (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Molecular Ecology Resources, 11, 914–921. https://doi.org/10.1111/j.1755-0998.2011.03021.x
  65. Tavaré, S. (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. In: Miura, R.M. (Ed.) Some Mathematical Questions in Biology: DNA Sequence Analysis. American Mathematical Society, Providence, Rhode Island, pp. 57–86.
  66. Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680. https://doi.org/10.1093/nar/22.22.4673
  67. Tominaga, A., Matsui, M. & Nishikawa, K. (2019a) Two new species of lotic breeding salamanders (Amphibia, Caudata, Hynobiidae) from western Japan. Zootaxa, 4550 (4), 525–544. https://doi.org/10.11646/zootaxa.4550.4.3
  68. Tominaga, A., Matsui, M., Tanabe, S. & Nishikawa, K. (2019b) A revision of Hynobius stejnegeri, a lotic breeding salamander from western Japan, with a description of three new species (Amphibia, Caudata, Hynobiidae). Zootaxa, 4651 (3), 401–433. https://doi.org/10.11646/zootaxa.4651.3.1
  69. Tukey, J.W. (1953) The problem of multiple comparisons. Mimeographed monograph.
  70. Yoshikawa, N. & Matsui, M. (2014) Two new salamanders of the genus Onychodactylus from eastern Honshu, Japan (Amphibia, Caudata, Hynobiidae). Zootaxa, 3866 (1), 53–78. https://doi.org/10.11646/zootaxa.3866.1.3
  71. Yoshikawa, N. & Matsui, M. (2022) A new salamander of the genus Onychodactylus from central Honshu, Japan (Amphibia, Caudata, Hynobiidae). Current Herpetology, 41, 82–100. https://doi.org/10.5358/hsj.41.82
  72. Yoshikawa, N., Matsui, M. & Inoue-Murayama, M. (2013) Characterization of nineteen microsatellite markers for the Japanese clouded salamander, Hynobius nebulosus, using the NGS. Conservation Genetics Resources, 5, 603–605. https://doi.org/10.1007/s12686-013-9861-4
  73. Zharkikh, A. (1994) Estimation of evolutionary distances between nucleotide sequences. Journal of Molecular Evolution, 39, 315–329. https://doi.org/10.1007/BF00160155