Advertisement

Ichthyological Research

, Volume 57, Issue 3, pp 215–222 | Cite as

Genetic constitution and phylogenetic relationships of Japanese crucian carps (Carassius)

  • Gunji Yamamoto
  • Mikumi Takada
  • Kei’ichiro Iguchi
  • Mutsumi NishidaEmail author
Full Paper

Abstract

The genetic constitution and phylogenetic relationships among the proposed species and subspecies of the crucian carp complex in Japan (Carassius cuvieri, C. auratus subspp. 1 and 2, C. a. grandoculis, C. a. buergeri, and C. a. langsdorfii) were investigated based on analyses of the partial nucleotide sequences of the mitochondrial DNA control region and amplified fragment length polymorphisms of nuclear DNA. Our results demonstrate that C. cuvieri and C. auratus are different entities. However, although several distinct lineages were observed for C. auratus, none corresponded to the proposed subspecies. Moreover, the five subspecies of C. auratus were not necessarily separated genetically from each other. Triploid fish, which are currently classified as a single subspecies (C. a. langsdorfii) but are sometimes treated as an independent species, fell into various clades along with diploid individuals of other subspecies that have the same or similar mitochondrial haplotypes. This suggests that gynogenetic triploid crucian carps distributed throughout the Japanese Archipelago have polyphyletic maternal origins. Our results indicate that Japanese crucian carps are a much more complex assemblage than previously believed.

Keywords

Carassius auratus Mitochondrial DNA Nuclear DNA AFLP Triploid 

Notes

Acknowledgments

We thank K. Watanabe and S. Ishikawa for their kind suggestions. We are grateful to K. Nakayama, Y. Fujioka, H. Hakoyama, K. Katsura, N. Watanabe, S. Ito, N. Mastubara, Y. Niimura, Y. Yamashina, R. Yoshida, and M. Noguchi for their help in obtaining specimens, and T. Ohkawa for his assistance with the phylogenetic analysis during the initial phase of this study. We also thank the editor and two reviewers for their valuable comments about earlier versions of this manuscript.

References

  1. Albertson RC, Markert JA, Danley PD, Kocher TD (1999) Phylogeny of a rapidly evolving clade: the chiclid fishes of Lake Malawi, East Africa. Proc Natl Acad Sci USA 96:5107–5110CrossRefPubMedGoogle Scholar
  2. Avise JC, Quattro JM, Vrijenhoek RC (1992) Molecular clones within organismal clones: mitochondrial DNA phylogenies and the evolutionary histories of unisexual vertebrates. Evol Biol 26:225–246Google Scholar
  3. Chang YS, Huang FI, Lo TB (1994) The complete nucleotide sequence and gene organization of carp (Cyprinus carpio) mitochondrial genome. J Mol Evol 38:138–155CrossRefPubMedGoogle Scholar
  4. Dong S, Taniguchi N (1996) Clonal nature of offsprings of Ginbuna Carassius langsdorfii by RAPD-PCR and isozyme patterns. Nippon Suisan Gakkaishi 62:891–896Google Scholar
  5. Eschmeyer WN (2008). Catalog of fishes, online version. http://research.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Accessed April 2009
  6. Hosoya K (2002) Cyprinidae. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, English edn. Tokai University Press, Tokyo, pp 253–271Google Scholar
  7. Iguchi K, Tanimura Y, Nishida M (1997) Sequence divergence in the mtDNA control region of amphidromous and landlocked forms of ayu. Fish Sci 63:901–905Google Scholar
  8. Iguchi K, Yamamoto G, Matsubara N, Nishida M (2003) Morphological and genetic analysis of fish of a Carassius complex (Cyprinidae) in Lake Kasumigaura with reference to the taxonomic status of two all-female triploid morphs. Biol J Linn Soc Lond 79:351–357CrossRefGoogle Scholar
  9. Jukes TH, Cantor CH (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York, pp 21–132Google Scholar
  10. Kalous L, Šlechtová JR, Bohlen J, Petrtý M, Švátora M (2007) First European record of Carassius langsdorfii from the Elbe basin. J Fish Biol 70:132–138CrossRefGoogle Scholar
  11. Kawanabe H, Mizuno N (1989) Fishes in river and lake. Part I. Hoikusha, OsakaGoogle Scholar
  12. Kobayasi H (1971) A cytological study on gynogenesis of the triploid ginbuna (Carassius auratus langsdorfii). Zool Mag 80:316–322Google Scholar
  13. Kobayasi H (1976) A cytological study on the maturation division in the oogenic process of the triploid Ginbuna (Carassius auratus langsdorfii). Jpn J Ichthyol 22:234–240Google Scholar
  14. Kobayasi H (1982) The distribution of polyploid funa. Jpn Women’s Univ J Home Econ Dep 29:145–161Google Scholar
  15. Kobayasi H, Ochi H (1972) Chromosome studies of the hybrids, ginbuna (Carassius auratus langsdorfii) × kinbuna (C. auratus subsp.), and ginbuna × loach (Misgurnus anguillicaudatus). Zool Mag 81:67–71Google Scholar
  16. Kobayasi H, Kawashima Y, Takeuchi N (1970) Comparative chromosome studies in the genus Carassius, especially with a finding of polyploidy in the ginbuna (C. auratus langsdorfii). Jpn J Ichthyol 17:153–160Google Scholar
  17. Komiyama T, Kobayashi H, Tateno Y, Inoko H, Gojobori T, Ikeo K (2009) An evolutionary origin and selection process of goldfish. Gene 430:5–11CrossRefPubMedGoogle Scholar
  18. Mada Y, Umino T, Arai K (2001) Genetic evidence of gynogenetic reproduction and clonal nature of triploid and tetraploid cyprinid fish Carassius langsdorfii collected from the Kami-dokanbori moat in the Imperial Palace. Nippon Suisan Gakkai Shi 67:217–221Google Scholar
  19. Meyer A (1993) Evolution of mitochondrial DNA in fishes. Biochem Mol Biol Fish 2:1–38Google Scholar
  20. Miyadi D, Kawanabe H, Mizuno N (1976) Colored illustrations of the freshwater fishes of Japan (new edition). Hoikusha, OsakaGoogle Scholar
  21. Murakami M, Fujitani H (1997) Polyploid-specific DNA sequences from triploid ginbuna (Japanese silver crucian carp, Carassius auratus langsdorfi). Genes Genet Syst 72:107–113CrossRefPubMedGoogle Scholar
  22. Murakami M, Matsuba C, Fujitani H (2001) The maternal origins of the triploid ginbuna (Carassius auratus langsdorfi): phylogenetic relationships within the C. auratus taxa by partial mitochondrial D-loop sequencing. Gen Genet Syst 76:25–32CrossRefGoogle Scholar
  23. Murakami M, Matsuba C, Fujitani H (2002) Characterization of DNA markers isolated from the gynogenetic triploid ginbuna (Carassius auratus langsdorfi) by representational difference analysis. Aquaculture 208:59–68CrossRefGoogle Scholar
  24. Nakamura M (1969) Cyprinid fishes of Japan—studies on the life history of cyprinid fishes of Japan. Research Institute for Natural Resources, TokyoGoogle Scholar
  25. Nishida M, Ohkawa T, Iwata Y (1998) Methods of analysis of genetic population structure with mitochondrial DNA markers. Fish Genet Breed Sci 26:81–100Google Scholar
  26. Ohara K, Dong S, Taniguchi N (1999) High proportion of heterozygotes in microsatellite DNA loci of wild clonal silver crucian carp, Carassius langsdorfii. Zool Sci 16:909–913CrossRefGoogle Scholar
  27. Ohara K, Ariyoshi T, Sumida E, Sitizyo K, Taniguchi N (2000) Natural hybridization between diploid crucian carp species and genetic independence of triploid crucian carp elucidated by DNA markers. Zool Sci 17:357–364PubMedGoogle Scholar
  28. Ohara K, Ariyoshi T, Sumida E, Taniguchi N (2003) Clonal diversity in the Japanese silver crucian carp, Carassius langsdorfii inferred from genetic markers. Zool Sci 20:797–804CrossRefPubMedGoogle Scholar
  29. Onozato H, Torisawa M, Kusama M (1983) Distribution of the gynogenetic polyploid crucian carp, Carassius auratus langsdorfii in Hokkaido, Japan. Jpn J Ichthyol 30:184–190Google Scholar
  30. Sakai H, Iguchi K, Yamazaki Y, Sideleva VG, Goto A (2009) Morphological and mtDNA sequence studies on three crucian carp (Carassius: Cyprinidae) including a new stock from the Ob River system, Kazakhstan. J Fish Biol 74:1756–1773CrossRefGoogle Scholar
  31. Shimizu Y, Oshiro T, Sakaizumi M (1993) Electrophoretic studies of diploid, triploid, and tetraploid forms of the Japanese silver crucian carp, Carassius auratus langsdorfii. Jpn J Ichthyol 40:65–75Google Scholar
  32. Swofford DL (1999) PAUP*: phylogenetic analysis using parsimony (*and other methods), ver. 4.0b. Sinauer Associates, SunderlandGoogle Scholar
  33. Taniguchi N (1982) Carassius fishes in the western part of Japan featuring the okinbuna. Freshw Fish 8:59–68Google Scholar
  34. Taniguchi N (2001) Carassius. In: Kawanabe H, Mizuno N, Hosoya K (eds) Freshwater fishes of Japan. Yama-kei, Tokyo, pp 339–353Google Scholar
  35. Templeton A (1994) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and apes. Evolution 37:221–244CrossRefGoogle Scholar
  36. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedGoogle Scholar
  37. Umino T, Arai K, Maeda K, Zhang Q, Sakae K, Niwase I, Nakagawa H (1997) Natural clones detected by multilocus DNA fingerprinting in gynogenetic triploid ginbuna Carassius langsdorfii in Kurose River, Hiroshima. Fish Sci 63:147–148Google Scholar
  38. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Paleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414CrossRefPubMedGoogle Scholar
  39. Yamashita M, Jiang J, Onozato H, Nakanishi T, Nagahama Y (1993) A tripolar spindle formed at meiosis I assures the retention of the original ploidy in the gynogenetic triploid crucian carp, ginbuna Carassius auratus langsdorfii. Dev Growth Differ 35:631–636CrossRefGoogle Scholar
  40. Zhang Q, Arai K (1996) Flow cytometry for DNA contents of somatic cells and spermatozoa in the progeny of natural tetraploid loach. Fish Sci 62:870–877Google Scholar

Copyright information

© The Ichthyological Society of Japan 2010

Authors and Affiliations

  • Gunji Yamamoto
    • 1
  • Mikumi Takada
    • 1
  • Kei’ichiro Iguchi
    • 2
  • Mutsumi Nishida
    • 1
    Email author
  1. 1.Department of Marine Bioscience, Ocean Research InstituteThe University of TokyoTokyoJapan
  2. 2.National Research Institute of Fisheries ScienceNaganoJapan

Personalised recommendations