Ichthyological Research

, Volume 66, Issue 3, pp 411–416 | Cite as

Genetic population structure of the eight-barbel loach Lefua echigonia in the Ise Bay region, a single paleo-river basin in central Honshu, Japan

  • Gen ItoEmail author
  • Yasunori Koya
  • Shigeru Kitanishi
  • Tokumasa Horiike
  • Takahiko Mukai
Short Report


We examined the genetic population structure of Lefua echigonia in the Ise Bay region based on the nucleotide sequences of the mitochondrial DNA cytochrome b region. Previous phylogeographic studies reported that only the Tokai lineage is distributed in this region; however, the present study revealed that the native Kinki lineage (Kuwana sub-lineage) is also distributed here. Moreover, the Tokai lineage was separated into three sub-lineages—Ise Bay, Mikawa-Shizuoka, and Nakatsugawa—with the Ise Bay and Mikawa-Shizuoka sub-lineages further subdivided into six and two local lineages, respectively. We revealed that L. echigonia has clear geographic differentiation within a single paleo-river basin.


Nemacheilidae Cytochrome b Biogeography 



We express sincere thanks to Mr. Tomonari Asaka, Mr. Asaomi Asano, Mr. Kazuhisa Asano, Mr. Ryota Hamaguchi, Mr. Toshihiko Handa, Ms. Rina Ido, Dr. Takahiko Itai, Mr. Masaaki Kobayashi, Mr. Fumiya Komatsu, Ms. Chiaki Mineshita, Mr. Fumiyoshi Murase, Mr. Naofumi Nakanishi, Ms. Yukiko Shinkai, Mr. Go Shinkai, Ms. Miyu Suzuki, Ms. Rui Tajima, Dr. Taiga Yodo, and the Natural Environmental Division, Gifu City Government Office, for their assistance with obtaining the specimens, and to the Division of Genomics Research, Life Science Research Center, Gifu University, for their help with the DNA analysis. This work was supported by JSPS KAKENHI Grant Number 26250044 to author T. Mukai.

Supplementary material

10228_2019_683_MOESM1_ESM.tif (8.1 mb)
Supplementary material 1 (TIFF 8263 kb)
10228_2019_683_MOESM2_ESM.tif (8.1 mb)
Supplementary material 2 (TIFF 8255 kb)


  1. Alvarado Bremer JR, Zhang L (1998) A polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) assay for the discrimination of mitochondrial DNA from the Florida and Northern subspecies of largemouth bass. Am Fish Soc 127:507–511CrossRefGoogle Scholar
  2. Association of Wildlife Research and EnVision (2017) Search system of Japanese red data. Accessed 1 June 2017
  3. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  4. Avise JC (2004) Molecular markers, natural history, and evolution (2nd edn). Sinauer, SunderlandGoogle Scholar
  5. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefGoogle Scholar
  6. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973CrossRefGoogle Scholar
  7. Horikawa M, Mukai T (2007) Distribution of mitochondrial DNA haplotypes of a cyprinid fish, Biwia zezera, in the Nobi Plain, Japan. Bull Biogeogr Soc Jpn 62:29–34Google Scholar
  8. Hosoe T, Koya Y (2008) Habitat environments of Japanese eight-barbel loach, Lefua echigonia, in Gifu Prefecture, central Japan. Sci Rep Fac Educ Gif Univ (Nat Sci) 32:19–28Google Scholar
  9. Hosoya K (2013) Cobitidae. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, 3rd edn. Tokai University Press, Tokyo, pp 328–334Google Scholar
  10. Kakino W, Hujisaku M, Mizutani M Goto A (2006a) Relationships between fish and amphibian fauna and characteristic of water zone in hill-bottom valleys of upper basin of the Kokai River. Trans JSIDRE 241:123–131Google Scholar
  11. Kakino W, Mizutani M, Fujisaku M, Goto A (2006b) Influence of environmental factors on fish fauna distribution in hill-bottom valleys-case study of the upper stream of the Kokai River. Trans JSIDRE 246:1–8Google Scholar
  12. Kakioka R, Kokita T, Tabata R, Mori S, Watanabe K (2013) The origins of limnetic forms and cryptic divergence in Gnathopogon fishes (Cyprinidae) in Japan. Environ Biol Fish 96:631–644CrossRefGoogle Scholar
  13. Kawabe T (1994) Biwako no oitachi (Formation of Lake Biwa). In: Research Group for Natural History of Lake Biwa (ed) The natural history of Lake Biwa. Yasaka Shobo, Tokyo, pp 25–72Google Scholar
  14. Kitagawa T, Yoshioka M, Kashiwagi M, Okazaki T (2001) Population structure and local differentiation in the delicate loach, Niwaella delicata, as revealed by mitochondrial DNA and morphological analyses. Ichthyol Res 48:127–135CrossRefGoogle Scholar
  15. Kitanishi S, Hayakawa A, Takamura K, Nakajima J, Kawaguchi Y, Onikura N, Mukai T (2016) Phylogeography of Opsariichthys platypus in Japan based on mitochondrial DNA sequences. Ichthyol Res 63:506–518CrossRefGoogle Scholar
  16. Komiya T, Fujita-Yanagibayashi S, Watanabe K (2014) Multiple colonization of Lake Biwa by Sarcocheilichthys fishes and their population history. Environ biol Fish 97:741–755CrossRefGoogle Scholar
  17. Kottelat M (2012) Conspectus cobitidum: an inventory of the loaches of the world (Teleostei: Cypriniformes: Cobitoidei). Raffles Bull Zool Suppl 26:1–199Google Scholar
  18. 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. Mol Biol Evol 13:1242–1254CrossRefGoogle Scholar
  19. Machida H, Matsuda T, Umitsu M, Koizumi T (2006) Regional geomorphology of the Japanese Island vol 5 Geomorphology of Chubu Region. University of Tokyo Press, TokyoGoogle Scholar
  20. Mihara M, Sakai T, Nakano K, Martins LdeO, Hosoya K, Miyazaki J (2005) Phylogeography of loaches of the genus Lefua (Balitoridae, Cypriniformes) inferred from mitochondrial DNA sequences. Zool Sci 22:157–168CrossRefGoogle Scholar
  21. Mitsuo Y, Ohira M, Tsunoda H, Yuma M (2013) Movement patterns of small benthic fish in lowland headwater streams. Freshw Biol 58:2345–2354Google Scholar
  22. Miyazaki J, Hida S, Ozaki T, Tabata Y, Iwata M, Nakazawa M, Fukasawa Y, Asaka T (2017) Intraspecific relationships and variation of two Lefua species (Balitoridae, Cypriniformes) in the Tokai region, Honshu, Japan. J Water Resour Prot 9:238–253CrossRefGoogle Scholar
  23. Moriyama A (1985) Geomorphic development of the Ena and Nakatsugawa tectonic Basin, central Japan. Bull Aichi Univ Education, Nat Sci 34:1–15Google Scholar
  24. Moriyama A (2004) Submarine topography, especially the formation of caldrons and sand banks in the Ise and Mikawa Bay. Bull Aichi Univ Education, Nat Sci 53:39–56Google Scholar
  25. Mukai T, Umemura K, Takagi M (2011) First record of Paramisgurnus dabryanus accompanied with the invasion of Chinese lineage of Misgurnus anguillicaudatus in Gifu Prefecture, Japan. Bull Biogeogr Soc Jpn 66:85–92Google Scholar
  26. Nakagawa H, Seki S, Ishikawa T, Watanabe K (2016) Genetic population structure of the Japanese torrent catfish Liobagrus reinii (Amblycipitidae) inferred from mitochondrial cytochrome b variations. Ichthyol Res 63:333–346CrossRefGoogle Scholar
  27. Nakajima J, Uchiyama R (2017) Loaches of Japan -natural history and culture. Yamakei Publishers, TokyoGoogle Scholar
  28. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefGoogle Scholar
  29. Saka R, Takehana Y, Suguro N, Sakaizumi M (2003) Genetic population structure of Lefua echigonia inferred from allozymic and mitochondrial cytochrome b variations. Ichthyol Res 50:301–309CrossRefGoogle Scholar
  30. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337CrossRefGoogle Scholar
  31. Suguro N, Hosoya K (2015) Lefua echigonia Jordan & Richardson. 1907. In: Ministry of the Environment (ed) Threatened wildlife of Japan, red data book 2014, vol 4 Pisces: brackish and fresh water fishes. GYOSEI Corporation, Tokyo, pp 196–197Google Scholar
  32. Suzuki M, Kitanishi S, Yodo T, Mukai T (2016) Population genetics structure of Sarcocheilichthys variegatus variegatus in the Tokai region, Japan and invasion of a non-indigenous mitochondrial DNA lineage. Jpn J Ichthyol 63:107–118Google Scholar
  33. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version6.0. Mol Biol Evol 30: 2725–2729CrossRefGoogle Scholar
  34. Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional, and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Resour 11:914–921CrossRefGoogle Scholar
  35. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  36. Tominaga K, Watanabe K, Kakioka R, Mori S, Jeon SR (2009) Two highly divergent mitochondrial DNA lineages within Pseudogobio esocinus populations in central Honshu, Japan. Ichthyol Res 56:195–199CrossRefGoogle Scholar
  37. Tominaga K, Nakajima J, Watanabe K (2016) Cryptic divergence and phylogeography of the pike gudgeon Pseudogobio esocinus (Teleostei: Cyprinidae): a comprehensive case of freshwater phylogeography in Japan. Ichthyol Res 63:79–93CrossRefGoogle Scholar
  38. Watanabe K, Nishida M (2003) Genetic population structure of Japanese bagrid catfishes. Ichthyol Res 50:140–148CrossRefGoogle Scholar
  39. Watanabe K, Mori S (2008) Comparison of genetic population structure between two cyprinids. Hemigrammocypris rasborella and Pseudorasbora pumila subsp., in the Ise Bay basin, central Honshu, Japan. Ichthyol Res 55:309–320CrossRefGoogle Scholar
  40. Watanabe K, Kano Y, Takahashi H, Mukai T, Kakioka R, Tominaga K (2010) GEDIMAP: a database of genetic diversity for Japanese freshwater fishes. Ichthyol Res 57:107–109CrossRefGoogle Scholar
  41. Watanabe K, Mori S, Tanaka T, Kanagawa N, Itai T, Kitamura J, Suzuki N, Tominaga T, Kakioka R, Tabata R, Abe T, Tashiro Y, Hashimoto Y, Nakajima J, Onikura N (2014) Genetic population structure of Hemigrammocypris rasborella (Cyprinidae) inferred from mtDNA sequences. Ichthyol Res 61:352–360CrossRefGoogle Scholar
  42. Yoshida F, Ozaki M (2000) Late Cenozoic paleogeography of the southern Chubu District. Chisitsu News 546:21–24Google Scholar

Copyright information

© The Ichthyological Society of Japan 2019

Authors and Affiliations

  • Gen Ito
    • 1
    Email author
  • Yasunori Koya
    • 2
  • Shigeru Kitanishi
    • 3
  • Tokumasa Horiike
    • 4
  • Takahiko Mukai
    • 5
  1. 1.The United Graduate School of Agricultural ScienceGifu UniversityGifuJapan
  2. 2.Faculty of EducationGifu UniversityGifuJapan
  3. 3.Faculty of Science and TechnologyOita UniversityOitaJapan
  4. 4.Faculty of AgricultureShizuoka UniversityShizuokaJapan
  5. 5.Faculty of Regional StudiesGifu UniversityGifuJapan

Personalised recommendations