Ichthyological Research

, Volume 55, Issue 4, pp 309–320 | Cite as

Comparison of genetic population structure between two cyprinids, Hemigrammocypris rasborella and Pseudorasbora pumila subsp., in the Ise Bay basin, central Honshu, Japan

  • Katsutoshi Watanabe
  • Seiichi Mori
Full Paper


Two small cyprinid fishes, Hemigrammocypris rasborella and Pseudorasbora pumila subsp. (sensu Nakamura 1963), inhabit similar habitats and often occur sympatrically in the Ise Bay basin, central Honshu Island, Japan. Their genetic population structures were revealed, using sequence data from the mitochondrial cytochrome b gene, and then compared. Hemigrammocypris rasborella populations in the Ise Bay area formed a monophyletic group that has been isolated from eastern (Tenryu River) and western (Lake Biwa–Yodo River) populations at least for several hundred thousand years. Pseudorasbora pumila subsp., endemic to the Ise Bay area, was estimated to have become isolated from its sister subspecies, P. p. pumila, about 5 million years ago. Both H. rasborella and P. pumila subsp. had centers of genetic diversity around the Okazaki Plain in the eastern part of the basin and showed trans-bay distribution of haplotypes or haplotype groups. Their common population structure was explained by geological features in the Ise Bay area, in which a large paleo-river system developed in regression periods, suggesting gene flow among populations of each species in the mid to lower reaches of the paleo-river. Based on the estimated expansion or divergence time, however, not all populations experienced gene flow during the Last Glacial. In contrast to the maintenance of high genetic diversity in H. rasborella, almost all populations of P. pumila subsp. have lost mitochondrial DNA genetic diversity. This implies that effective population size of P. pumila subsp. tended to be smaller, probably because of differences in reproductive ecology, even though the two species have been exposed to similar environmental changes. For conservation of the two species, genetic and adaptive differentiation among local populations should be considered, and attention should be paid to inbreeding depression, especially in P. pumila subsp.


Mitochondrial DNA (mtDNA) Cytochrome b (cytbMismatch distribution Nested clade phylogeographic analysis (NCPA) 



We express sincere thanks to M. Nishida and N. Nagata for their valuable advice during this study, to R. Kakioka for assistance with experiments, and to Y. Fujii, K. Hosoya, K. Iguchi, T. Itai, N. Kanagawa, K. Kawamura, and J. Kitamura for providing fish samples. This study was partially supported by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science, and Technology, Japan (no. 18570086, Biodiversity Research of the 21st Century COE: A14, and “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem” of the GCOE) and by the Foundation of River and Watershed Environment Management (“Beautifying and Greening the Riverside Environment”).


  1. Akada J, Yodo T (2006) Geographical and between-habitat variations in the body shape of Hemigrammocypris rasborella. Jpn J Ichthyol 53:175–179Google 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 47:157–161CrossRefGoogle Scholar
  3. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  4. Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Mol Ecol 7:431–452CrossRefGoogle Scholar
  5. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedCrossRefGoogle Scholar
  6. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. TREE 15:290–295PubMedGoogle Scholar
  7. Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864PubMedCrossRefGoogle Scholar
  8. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1:47–50Google Scholar
  9. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, LondonGoogle Scholar
  10. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913PubMedCrossRefGoogle Scholar
  11. Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568PubMedCrossRefGoogle Scholar
  12. Japan Ministry of the Environment (2003) Threatened wildlife of Japan, Red data book. 2nd edn. Japan Wildlife Research Center, TokyoGoogle Scholar
  13. 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
  14. Kawamura K (2006) Pseudorasbora pumila subsp. sensu Nakamura, 1969. In: Natural Environment Division, Department of Environment and Forestry, Mie Prefecture (ed) Red data book of Mie Prefecture 2005, Animals. Mie Prefecture Environmental Conservation Agency, Tsu, p 142Google Scholar
  15. Konishi M, Takata K (2004) Isolation and characterization of polymorphic microsatellite DNA markers in topmouth gudgeon, Pseudorasbora (Teleostei: Cyprinidae). Mol Ecol Notes 4:64–66CrossRefGoogle Scholar
  16. Maehata M (1997) Ushimotsugo, Pseudorasbora pumila subspecies. In: Nagata Y, Hosoya K (eds) Circumstances in endangered Japanese freshwater fishes and their protection. Midori Shobo, Tokyo, pp 114–121Google Scholar
  17. Mizuno S (2006) Hemigrammocypris rasborella Fowler, 1910. In: Natural Environment Division, Department of Environment and Forestry, Mie Prefecture (ed) Red data book of Mie Prefecture 2005, Animals. Mie Prefecture Environmental Conservation Agency, Tsu, p 147Google Scholar
  18. Moriyama A (2004) Submarine topography, especially the formation of caldrons and sand banks in the Ise and Mikawa Bay. Bull Aichi Univ Education, Natural Sci 53:39–56Google Scholar
  19. Nakamura M (1963) Keys to the freshwater fishes of Japan—fully illustrated in colors. Hokuryukan, TokyoGoogle Scholar
  20. Nakamura M (1969) Cyprinid fishes of Japan—studies on the life history of cyprinid fishes of Japan. Res Inst Nat Res Spec Pub 4, TokyoGoogle Scholar
  21. Near TJ, Kassler TW, Koppelman JB, Dillman CB, Philipp DP (2003) Speciation in North American black basses Micropterus. Evolution 57:1610–1621PubMedGoogle Scholar
  22. Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273PubMedCrossRefGoogle Scholar
  23. Ohnaka T, Sasaki H, Nagai K, Numachi K (1999) Marked monomorphism at the D-loop region of mtDNA in an endangered species Pseudorasbora pumila subsp. sensu Nakamura (1963). Nippon Suisan Gakkaishi 65:1005–1009Google Scholar
  24. Ota Y, Naruse T, Tanaka S, Ikada A (2004) Regional geomorphology of the Japanese Islands, vol 6. Geomorphology of Kinki, Chugoku and Shikoku. University of Tokyo Press, TokyoGoogle Scholar
  25. Palumbi S, Martin A, Romano S, McMillian WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Univ Hawaii, HonoluluGoogle Scholar
  26. Posada D, Crandall KA, Templeton AR (2000) GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488PubMedCrossRefGoogle Scholar
  27. Rocha-Olivares A, Rosenblatt RH, Vetter RD (1999) Molecular evolution, systematics, and zoogeography of the rockfish subgenus Sebastomus (Sebastes, Scorpaenidae) based on mitochondrial cytochrome band control region sequences. Mol Phylogenet Evol 11:441–458PubMedCrossRefGoogle Scholar
  28. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  29. Schneider S, Excoffier L (1999) Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089PubMedGoogle Scholar
  30. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4b10a. Sinauer Associates, SunderlandGoogle Scholar
  31. Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464PubMedCrossRefGoogle Scholar
  32. Takeuchi A (1999) Pliocene and later vicissitude of stress field and tectonics in the Hoku-Shin-Etsu district, central Japan. Earth Monthly 21:583–588Google Scholar
  33. Tanaka T, Yamashina Y, Miura Y (2001) Population fluctuation of the cyprinid fish, Hemigrammocypris rasborella, in an irrigation pond. Bulletin of Kansai Organization for Nature Conservation 23:99–107Google Scholar
  34. Templeton AR (1998) Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7:381–397PubMedCrossRefGoogle Scholar
  35. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633PubMedGoogle Scholar
  36. Templeton AR, Sing CF (1993) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. IV. Nested analyses with cladogram uncertainty and recombination. Genetics 134:659–669PubMedGoogle Scholar
  37. Uchiyama R (1989) Ushimotsugo, Pseudorasbora pumila subsp. In: Kawanabe H, Mizuno N (eds) Freshwater fishes of Japan. Yama-Kei Publishers, Tokyo, pp 308–309Google Scholar
  38. Ueda K (1989) Phytogeography of Tokai Hilly land element I. Definition. Acta Phytotax Geobot 40:190–202Google Scholar
  39. Watanabe K (1998) Parsimony analysis of the distribution pattern of Japanese primary freshwater fishes, and its application to the distribution of the bagrid catfishes. Ichthyol Res 45:259–270CrossRefGoogle Scholar
  40. 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 47:43–50CrossRefGoogle Scholar
  41. Watanabe K, Mori S, Nishida M (2003) Genetic relationships and origin of two geographic groups of the freshwater threespine stickleback, ‘Hariyo’. Zool Sci 20:265–274PubMedCrossRefGoogle Scholar
  42. Yokoyama T (1988) Seinan Nihon no Shizenshi (natural history of southwestern Japan). Sanwa-shobo, KyotoGoogle Scholar
  43. 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
  44. Yoshida F (1992) Geologic development of the Setouchi Geologic Province since Early Miocene—with special reference to the first and second Setouchi Inland Sea times. Bull Geol Surv Jpn 43:43–67Google Scholar
  45. Zardoya R, Doadrio I (1999) Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids. J Mol Evol 49:227–237PubMedCrossRefGoogle Scholar

Copyright information

© The Ichthyological Society of Japan 2008

Authors and Affiliations

  1. 1.Department of Zoology, Division of Biological Science, Graduate School of ScienceKyoto UniversitySakyo-ku, KyotoJapan
  2. 2.Biological LaboratoryGifu Keizai UniversityOgaki, GifuJapan

Personalised recommendations