Ichthyological Research

, Volume 65, Issue 3, pp 383–397 | Cite as

Comparative phylogeography of diadromous and freshwater daces of the genus Tribolodon (Cyprinidae)

  • Katsutoshi Watanabe
  • Harumi Sakai
  • Takeshi Sanada
  • Mutsumi Nishida
Full Paper


Far Eastern daces, genus Tribolodon (Cyprinidae), are thought to have diversified and developed unique diadromous life histories under changing conditions in the Sea of Japan and the surrounding environment. To examine the relationships between life history traits, distribution, and genetic population structures, we conducted a comparative phylogeographic analysis using partial mtDNA sequence data from samples collected over almost the full ranges of all four Tribolodon species. Phylogenetic analyses revealed several intraspecific haplotype groups that differentiated in the early Pleistocene to the Pliocene with or without geographic overlaps. A time-calibrated phylogeny suggested that the relatively smaller geographic ranges of the strictly freshwater species, T. sachalinensis and T. nakamurai, were explained not by the recent origins of these species, but by their limited dispersal abilities and smaller historical population sizes. The wider-ranging diadromous species, T. brandtii and T. hakonensis, exhibited similar major phylogeographic structures in their distributions, but the chronological order and timing of formation of this structure largely differed between the two species. In addition to those differences, the overlapping patterns of the differentiated intraspecific lineages in these species suggest dynamic, but somewhat restricted dispersal during the Plio-Pleistocene. Tribolodon hakonensis, one of the most widespread species of East Asian freshwater fishes, included both common and unique phylogeographic patterns compared to other fish species; the unique patterns (i.e., its wide range across freshwater biogeographic boundaries like the sea and mountains) would reflect its ecological features as a remarkable generalist inhabiting lakes, upper and lower reaches of rivers, and even coastal areas.


Freshwater fish Mitochondrial DNA (mtDNA) Far East Asia Central Highland Diadromy 



We thank S. Amano, A. Goto, R. Kakioka, H. Kato, K. Katsura, H. Kohno, K. Iguchi, S.-R. Jeon, T. Kaneko, S. N. Safronov, H. Sugiyama, R. Tabata, Y. Takahashi, T. Tokuhara, V. V. Tsuiger, G. Yamamoto, Y. Yamazaki, and A. Zama for their help in the collection of specimens. This study was partially supported by the Sumitomo Foundation and JSPS KAKENHI (No. 06041004, 09041138, 21370035, 26291079, 26250044, and 17H03720).

Supplementary material

10228_2018_624_MOESM1_ESM.docx (75 kb)
Supplementary material 1 (DOCX 74 kb)
10228_2018_624_MOESM2_ESM.pdf (105 kb)
Supplementary material 2 (PDF 106 kb)
10228_2018_624_MOESM3_ESM.pdf (273 kb)
Supplementary material 3 (PDF 274 kb)
10228_2018_624_MOESM4_ESM.pdf (473 kb)
Supplementary material 4 (PDF 473 kb)


  1. Aoyagi H (1957) General notes on the freshwater fishes of the Japanese Archipelago. Taishukan, TokyoGoogle Scholar
  2. Aoyama J, Watanabe S, Ishikawa S, Nishida M, Tsukamoto K (2000) Are morphological characters distinctive enough to discriminate between two species of freshwater eels, Anguilla celebesensis and A. interioris? Ichthyol Res 47:157–161Google Scholar
  3. Atsumi K, Nomoto K, Machida Y, Ichimura M, Koizumi I (2017) No reduction of hatching rates among F1 hybrids of naturally hybridizing three Far Eastern daces, genus Tribolodon (Cypriniformes, Cyprinidae). Ichthyol Res.
  4. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  5. Avise JC, Arnold J, Ball RM Jr, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Interspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522Google Scholar
  6. Berra TM (2001) Freshwater fish distribution. Academic Press, San DiegoGoogle Scholar
  7. Brykov VA, Polyakova NE, Semina AV (2011) Phylogeographic analysis reveals two periods of divergence in large scaled redfin Tribolodon hakonensis (Pisces, Cyprinidae). Russ J Genet 47:1324–1332Google Scholar
  8. Brykov VA, Polyakova NE, Semina AV (2013) Comparative analysis of mitochondrial DNA variation in four species of Far Eastern redfins of the genus Tribolodon (Pisces, Cyprinidae). Russ J Genet 49:310–319Google Scholar
  9. Burridge CP, Craw D, Waters JM (2006) River capture, range expansion, and cladogenesis: the genetic signature of freshwater vicariance. Evolution 60:1038–1049Google Scholar
  10. Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Mol Biol Evol 25:624–633Google Scholar
  11. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660Google Scholar
  12. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772Google Scholar
  13. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214Google Scholar
  14. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710Google Scholar
  15. Emerson BC, Gillespie RG (2008) Phylogenetic analysis of community assembly and structure over space and time. Trends Ecol Evol 23:619–630Google Scholar
  16. Ferreira MA, Suchard MA (2008). Bayesian analysis of elapsed times in continuous-time Markov chains. Can J Stat 36:355–368Google Scholar
  17. Gudkov PK, Polyakova NE, Semina AV, Nazarkin MV (2010) Comparative morphological analysis of big scaled redfin Tribolodon hakonensis Günther, 1877 (Cyprinidae, Cypriniformes) from Sakhalin and Southern Primorye. J Ichthyol 50:740–744Google Scholar
  18. Higuchi M, Goto A (1996) Genetic evidence supporting the existence of two distinct species in the genus Gasterosteus around Japan. Environ Biol Fishes 47:1–16Google Scholar
  19. Iijima A, Tada R (1990) Evolution of Tertiary sedimentary basins of Japan in reference to opening of the Japan Sea. J Fac Sci, Univ Tokyo Sec 2: Geol Mineral Geogr Geophys 22:121–171Google Scholar
  20. Imai C, Sakai H, Arai T (2008) Otolith Sr:Ca of an endangered cyprinid Tribolodon nakamurai indicating absence of sea-migrating traits. J Nat Fish Univ 57:137–141Google Scholar
  21. Imoto JM, Saitoh K, Sasaki T, Yonezawa T, Adachi J, Kartavtsev YP, Miya M, Nishida M, Hanzawa N (2013) Phylogeny and biogeography of highly diverged freshwater fish species (Leuciscinae, Cyprinidae, Teleostei) inferred from mitochondrial genome analysis. Gene 514:112–124Google Scholar
  22. Jolivet L, Tamaki K, Fournier M (1994) Japan Sea, opening history and mechanism: a synthesis. J Geophys Res 99:22237–22259Google Scholar
  23. Kaneko T, Hasegawa S, Uchida K, Ogasawara T, Oyagi A, Hirano T (1999) Acid tolerance of Japanese dace (a cyprinid teleost) in Lake Osorezan, a remarkable acid lake. Zool Sci 16:871–877Google Scholar
  24. Kartavtsev YF, Sviridov VV, Hanzawa N, Sasaki T (2002) Genetic divergence of Far-Eastern dace species belonging to the genus Tribolodon (Pisces, Cyprinidae) and closely related taxa. Russ J Genet 38:1285–1297Google Scholar
  25. Kawabe T (1994) Biwako no oitachi (Formation of Lake Biwa). In: Research Group for Natural History of Lake Biwa (ed) Biwako no shizenshi (The natural history of Lake Biwa). Yasaka Shobo, Tokyo, pp 24–72Google Scholar
  26. 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 48:127–135Google Scholar
  27. Kitamura A (2010) Formation and paleoenvironment of the Japanese Archipelago. In: Watanabe K, Takahashi H (eds) Tansuigyorui chiri no shizenshi (Natural history of freshwater fish geography). Hokkaido University Press, Sapporo, pp 13–28Google Scholar
  28. Kitamura A, Kimoto K (2006) History of the inflow of the warm Tsushima Current into the Sea of Japan between 3.5 and 0.8 Ma. Palaeogeogr Palaeoclimatol Palaeoecol 236:355–366Google Scholar
  29. Kitano J, Mori S, Peichel CL (2007) Phenotypic divergence and reproductive isolation between sympatric forms of Japanese threespine sticklebacks. Biol J Linn Soc 91:671–685Google Scholar
  30. Kitaura J, Wada K, Nishida M (1998) Molecular phylogeny and evolution of unique mud-using territorial behavior in ocypodid crabs (Crustacea: Brachyura: Ocypodidae). Mol Biol Evol 15:626–637Google Scholar
  31. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874Google Scholar
  32. Lindberg GU (1972) Large-scale fluctuations of sea level in the quaternary period: hypothesis based on biogeographic evidence. Nauka, LeningradGoogle Scholar
  33. MacDonald G (2003) Biogeography: introduction to space, time and life. WileyGoogle Scholar
  34. McDowall RM (2001) Diadromy, diversity and divergence: implications for speciation processes in fishes. Fish Fish 2:278–285Google Scholar
  35. McDowall RM (2008) Diadromy, history and ecology: a question of scale. Hydrobiologia 602:5–14Google Scholar
  36. Mizuno N (1987) Formation of freshwater fish fauna in Japan. In: Mizuno N, Goto A (eds) Freshwater fishes of Japan: their distribution, variation and speciation. Tokai University Press, TokyoGoogle Scholar
  37. Myers GS (1949) Salt tolerance of fresh-water fish groups in relation to zoogeographical problems. Bijdr Dierkd 28:315–322Google Scholar
  38. Nakagawa H (2014) Contribution of environmental and spatial factors to the structure of stream fish assemblages at different spatial scales. Ecol Freshw Fish 23:208–223Google Scholar
  39. Nakamura M (1969) Cyprinid fishes of Japan: studies on the life history of cyprinid fishes of Japan. Research Institute for Natural Resources, TokyoGoogle Scholar
  40. Nishimura S (1974) Nihon-kai no seiritsu (Formation of the Sea of Japan). Tsukiji-Shokan, TokyoGoogle Scholar
  41. Palumbi S, Martin A, Romano S, McMillian WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Univ Hawaii, HonoluluGoogle Scholar
  42. Polyakova NE, Semina AV, Brykov VA (2015) Analysis of mtDNA and nuclear markers points to homoploid hybrid origin of the new species of Far Eastern redfins of the genus Tribolodon (Pisces, Cyprinidae). Russ J Genet 51:1075–1087Google Scholar
  43. Rambaut A (2016) FigTree Version 1.4.3. software/figtree/. Accessed 23 March 2017
  44. Rambaut A, Drummond AJ, Suchard M (2013) Tracer version 1.6. Accessed 23 March 2017
  45. Ryazanova IN, Polyakova NE (2012) Differentiation of large scaled redfin Tribolodon hakonensis (Pisces, Cyprinidae) in the Russian part of the range as inferred from the data of karyological analysis and PCR RFLP analysis of mitochondrial DNA. Russ J Genet 48:199–207Google Scholar
  46. Saitoh K, Sado T, Mayden RL, Hanzawa N, Nakamura K, Nishida M, Miya M (2006) Mitogenomic evolution and interrelationships of the Cypriniformes (Actinopterygii: Ostariophysi): the first evidence toward resolution of higher-level relationships of the World’s largest freshwater fish clade based on 59 whole mitogenome sequences. J Mol Evol 63:826–841Google Scholar
  47. Sakai H (1995) Life-history and genetic divergence in three species of Tribolodon (Cyprinidae). Mem Fac Fish Hokkaido Univ 42:1–98Google Scholar
  48. Sakai H, Amano S (2014) A new subspecies of anadromous Far Eastern dace, Tribolodon brandtii maruta subsp. nov. (Teleostei, Cyprinidae) from Japan. Bull Natl Mus Nat Sci Ser A 40:219–229Google Scholar
  49. Sakai H, Hamada K (1985) Electrophoretic discrimination of Tribolodon species (Cyprinidae) and the occurrence of their hybrids. Jpn J Ichthyol 32:216–224Google Scholar
  50. Sakai H, Imai C (2002) Otolith Sr:Ca ratios of the freshwater and anadromous cyprinid genus Tribolodon. Ichthyol Res 52:182–184Google Scholar
  51. Sakai H, Goto A, Jeon SR (2002) Speciation and dispersal of Tribolodon species (Pisces, Cyprinidae) around the Sea of Japan. Zool Sci 19:1291–1303Google Scholar
  52. Sakai H, Ito Y, Shedko SV, Safronov SN, Frolov SV, Chereshnev IA, Jeon SR, Goto A (2006) Phylogenetic and taxonomic relationships of Northern Far Eastern phoxinin minnows, Phoxinus and Rhynchocypris (Pisces, Cyprinidae), as inferred from allozyme and mitochondrial 16S rRNA sequence analyses. Zool Sci 23:323–331Google Scholar
  53. Sasaki T, Kartavtsev YP, Chiba SN, Uematsu T, Sviridov VV, Hanzawa N (2007) Genetic divergence and phylogenetic independence of Far Eastern species in subfamily Leuciscinae (Pisces: Cyprinidae) inferred from mitochondrial DNA analyses. Genes Genet Syst 82:329–340Google Scholar
  54. Semina AV, Polyakova NE, Brykov VA (2006) Genetic analysis identifies a cryptic species of Far Eastern daces of the genus Tribolodon. Doklady Biol Sci 407:173–175Google Scholar
  55. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313Google Scholar
  56. Tabata R, Kakioka R, Tominaga K, Komiya T, Watanabe K (2016) Phylogeny and historical demography of endemic fishes in Lake Biwa: the ancient lake as a promoter of evolution and diversification of freshwater fishes in western Japan. Ecol Evol 6:2601–2623Google Scholar
  57. Tada R (1994) Paleoceanographic evolution of the Japan Sea. Palaeogeogr Palaeoclimatol Palaeoecol 108: 487–508Google Scholar
  58. Takahashi H, Møller PR, Shedko SV, Ramatulla T, Joen SR, Zhang CG, Sideleva VG, Takata K, Sakai H, Goto A, Nishida M (2016) Species phylogeny and diversification process of Northeast Asian Pungitius revealed by AFLP and mtDNA markers. Mol Phylogenet Evol 99:44–52Google Scholar
  59. Templeton AR (2006) Population genetics and microevolutionary theory. WileyGoogle Scholar
  60. Templeton AR, Sing CF (1993) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics 134:659–669Google Scholar
  61. Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) Barcoding Australia’s fish species. Philos Trans R Soc Lond B Biol Sci. 360:1847–1857Google Scholar
  62. Watanabe K (2012) Faunal structure of Japanese freshwater fishes and its artificial disturbance. Environ Biol Fishes 94:533–547Google Scholar
  63. Watanabe K, Takahashi H (2010) Tansuigyorui chiri no shizenshi (Natural history of freshwater fish geography). Hokkaido University Press, SapporoGoogle Scholar
  64. Watanabe K, Iguchi K, Hosoya K, Nishida M (2000) Phylogenetic relationships of the Japanese minnows, Pseudorasbora (Cyprinidae), as inferred from mitochondrial 16S rRNA gene sequences. Ichthyol Res 47:43–50Google Scholar
  65. 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 57:107–109Google Scholar
  66. Watanabe K, Tominaga K, Nakajima J, Kakioka R, Tabata R (2016) Japanese freshwater fishes: biogeography and cryptic diversity. In: M. Motokawa and H. Kajihara (eds) Species diversity of animals in Japan, diversity and commonality in animals. Springer, Tokyo, pp 183–227Google Scholar
  67. Yamamoto S, Morita K, Kitano S, Watanabe K, Koizumi I, Maekawa K, Takamura K (2004) Phylogeography of white-spotted charr (Salvelinus leucomaenis) inferred from mitochondrial DNA sequences. Zool Sci 21:229–240Google Scholar
  68. Yokoyama T (1988) Seinan Nihon no Shizenshi (Natural history of southwestern Japan). Sanwa- shobo, TokyoGoogle Scholar
  69. Yokoyama R, Goto A (2005) Evolutionary history of freshwater sculpins, genus Cottus (Teleostei; Cottidae) and related taxa, as inferred from mitochondrial DNA phylogeny. Mol Phylogenet Evol 36:654–668Google Scholar
  70. Yonekura N, Kaizuka S, Nogami M, Chinzai K (2001) Regional geomorphology of the Japanese Islands, vol 1. Introduction to Japanese geomorphology. University of Tokyo Press, TokyoGoogle Scholar
  71. Zardoya R, Doadrio I (1999) Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids. J Mol Evol 49:227–237Google Scholar

Copyright information

© The Ichthyological Society of Japan 2018

Authors and Affiliations

  1. 1.Department of Zoology, Division of Biological Sciences, Graduate School of ScienceKyoto UniversityKyotoJapan
  2. 2.Department of Applied AquabiologyNational Fisheries UniversityShimonosekiJapan
  3. 3.Department of Marine BioscienceFukui Prefectural UniversityObamaJapan
  4. 4.University of the RyukyusOkinawaJapan
  5. 5.Fukami Elementary SchoolYamatoJapan

Personalised recommendations