Skip to main content
SpringerLink
Log in

Genetic evolution and diversity of common carp Cyprinus carpio L.

  • Review Article
  • Published:
Central European Journal of Biology

Abstract

Knowledge of genetic variation and population structure of existing strains of both farmed and wild common carp Cyprinus carpio L. is absolutely necessary for any efficient fish management and/or conservation program. To assess genetic diversity in common carp populations, a variety of molecular markers were analyzed. Of those, microsatellites and mitochondrial DNA were most frequently used in the analysis of genetic diversity and genome evolution of common carp. Using microsatellites showed that the genome evolution in common carp exhibited two waves of rearrangements: one whole-genome duplication (12–16 million years ago) and a more recent wave of segmental duplications occurring between 2.3 and 6.8 million years ago. The genome duplication event has resulted in tetraploidy since the common carp currently harbors a substantial portion of duplicated loci in its genome and twice the number of chromosomes (n = 100–104) of most other cyprinid fishes. The variation in domesticated carp populations is significantly less than that in wild populations, which probably arises from the loss of variation due to founder effects and genetic drift. Genetic differentiation between the European carp C.c. carpio and Asian carp C.c. haematopterus is clearly evident. In Asia, two carp subspecies, C.c. haematopterus and C.c. varidivlaceus, seem to be also genetically distinct.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AFLP:

amplified fragment length polymorphism

EST:

expressed sequence tag

mtDNA:

mitochondrial DNA

PIC:

polymorphism information content

PCR:

polymerase chain reaction

RAPD:

random amplification of polymorphic DNA

RFLP:

restriction fragment length polymorphism

SNP:

single nucleotide polymorphism

References

  1. Nelson J.S., Fishes of the world, 3rd ed., John Wiley & Sons Inc., New York, 1994

    Google Scholar 

  2. Balon E.K., The oldest domesticated fishes, and the consequences of an epigenetic dichotomy in fish culture, J. Ichthyol. Aquat. Biol., 2006, 11, 47–86

    Google Scholar 

  3. Balon E.K., Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers, Aquaculture, 1995, 129, 3–48

    Article  Google Scholar 

  4. Kirpitchnikov V.S., Homologous hereditary variation and evolution of wild common carp Cyprinus carpio L, Genetika, 1967, 8, 65–72, (in Russian)

    Google Scholar 

  5. Kirpitchnikov V.S., Genetics and breeding of common carp, INRA, Paris, 1999

    Google Scholar 

  6. Kottelat M., Fishes of Laos, WHT Publication (Pty) Ltd, Colombo, Sri Lanka, 2001

    Google Scholar 

  7. Valenta M., Slechta V., Slechtova V., Kalal L., Genetic polymorphism and isoenzyme patterns of lactate dehydrogenase in tench (Tinca tinca), crician carp (Carassuis carassius) and carp (Cyprinus carpio), Anim. Blood Groups Biochem. Genet., 1977, 8, 217–230

    PubMed  CAS  Google Scholar 

  8. Danzmann R.G., Down N.E., Isozyme expression in F1 hybrids between carp and goldfish, Biochem. Genet., 1982, 20, 1–15

    Article  PubMed  CAS  Google Scholar 

  9. Zhou J., Wu Q., Wang Z., Ye Y., Genetic variation analysis within and among six varieties of common carp (Cyprinus carpio L.) in China using microsatellite markers, Genetika, 2004, 40, 1389–1393

    PubMed  Google Scholar 

  10. David L., Rosenberg N.A., Lavi U., Feldman M.W., Hillel J., Genetic diversity and population structure inferred from the partially duplicated genome of domesticated carp, Cyprinus carpio L., Genet. Sel. Evol., 2007, 39, 319–340

    Article  PubMed  Google Scholar 

  11. Li D., Kang D., Yin Q., Sun X., Liang L., Microsatellite DNA marker analysis of genetic diversity in wild common carp (Cyprinus carpio L.) populations, J. Genet. Genomics, 2007, 34, 984–993

    Article  PubMed  CAS  Google Scholar 

  12. David L., Rajasekaran P., Fang J., Hillel J., Lavi U., Polymorphism in ornamental and common carp strains (Cyprinus carpio L.) as revealed by AFLP analysis and a new set of microsatellite markers, Mol. Genet. Genomics, 2001, 266, 353–262

    Article  PubMed  CAS  Google Scholar 

  13. Kohlmann K., Gross R., Murakaeva A., Kersten P., Genetic variability and structure of common carp (Cyprinus carpio) populations throughout the distribution range inferred from allozyme, microsatellite and mitochondrial DNA markers, Aquat. Living Resour., 2003, 16, 421–431

    Article  Google Scholar 

  14. Zhou J.F., Wu Q.J., Ye Y.Z., Tong J.G., Genetic divergence between Cyprinus carpio carpio and Cyprinus carpio haematopterus as assessed by mitochondrial DNA analysis, with emphasis on origin of European domestic carp, Genetica, 2003, 119, 93–97

    Article  PubMed  CAS  Google Scholar 

  15. Ludannyi R.I., Khrisanfova G.G., Vasiév V.A., Prizenko V.K., Bogeruk, A.K., Ryskov A.P., et al., Genetic diversity and differentiation of Russian common carp (Cyprinus carpio L.) breeds inferred from RAPD markers, Genetika, 2006, 42, 1121–1129, (in Russian)

    PubMed  CAS  Google Scholar 

  16. Thai B.T., Burridge C.P., Pham T.A., Austin C.M., Using mitochondrial nucleotide sequences to investigate diversity and genealogical relationships within common carp (Cyprinus carpio L.), Anim. Genet., 2005, 36, 23–28

    Article  PubMed  CAS  Google Scholar 

  17. Mabuchi K., Senou H., Nishida M., Mitochondrial DNA analysis reveals cryptic large scale invasion of non-native genotypes of common carp (Cyprinus carpio) in Japan, Mol. Ecol., 2008, 17, 796–809

    PubMed  CAS  Google Scholar 

  18. Liu Z.Y., Cordes J.F., DNA marker technologies and their applications in aquaculture genetics, Aquaculture, 2004, 238, 1–37

    Article  CAS  Google Scholar 

  19. Crooijmans R.P.M.A., Bierbooms V.A.F., Koman J., Van der Poel J.J., Groenen, M.A.M., Microsatellite markers in common carp, Anim. Genet., 1997, 28, 129–134

    Article  CAS  Google Scholar 

  20. Aliah R.S., Takagi M., Dong S., Teoh C.T., Taniguchi, N. Isolation and inheritance of microsatellite markers in the common carp Cyprinus carpio, Fish. Sci., 1999, 65, 235–239

    CAS  Google Scholar 

  21. Wei D., Lou Y., Sun X. Isolation of microsatellite markers in the common carp, Zool. Res., 2001, 22, 238–241

    CAS  Google Scholar 

  22. Yue G.H., Ho M.Y., Orban L., Komen J., Microsatellites within genes and ESTs of common carp and their applicability in silver crucian carp, Aquaculture, 2004, 234, 85–98

    Article  CAS  Google Scholar 

  23. Sun X.-W., Hou N., Liang L.-Q., Microsatellite clones in common carp (Cyprinus carpio): rapid isolation and characteristic analysis, Mol. Ecol. Resour., 2008, 8, 1357–1359

    Article  CAS  Google Scholar 

  24. Ward R.D., Grewe P.M., Appraisal of molecular genetic techniques in fisheries, In: Carvalho G.R., Pitcher T.J. (Eds.), Molecular Genetics in Fisheries, Chapman & Hall, Great Britain, 1995

    Google Scholar 

  25. Bruford M.W., Bradley D.G., Luikart G., DNA markers reveal the complexity of livestock domestication, Nat. Rev. Genet., 2003, 4, 900–910

    Article  PubMed  CAS  Google Scholar 

  26. Chang Y.-S., Huang F.-L., Lo T.-B., The complete nucleotide sequence and gene organization of carp (Cyprinus carpio) mitochondrial genome, J. Mol. Evol., 1994, 38, 138–155

    Article  PubMed  CAS  Google Scholar 

  27. Gross R., Kohlmann K., Kersten P., PCR-RFLP analysis of the mitochondrial DNA ND- 3/4 and ND-5/6 gene polymorphisms in the European and East Asian subspecies of common carp (Cyprinus carpio L.), Aquaculture, 2002, 204, 7–516

    Article  Google Scholar 

  28. Guo X.H., Liu S.J., Liu Y., Comparative analysis of the mitochondrial DNA control region in cyprinids with different ploidy level, Aquaculture, 2003, 224, 25–38

    Article  CAS  Google Scholar 

  29. Thai B.T., Si V.N., Phan P.D., Austin, C.M., Phylogenetic evaluation of subfamily classification of the Cyprinidae focusing on Vietnamese species, Aquat. Living Resour., 2007, 20, 143–153

    Article  Google Scholar 

  30. Ohno S., Atkin N.B., Comparative DNA values and chromosome complements of eight species of fishes, Chromosoma, 1966, 18, 455–466

    Article  PubMed  CAS  Google Scholar 

  31. Ohno S., Muramoto J., Christian L., Atkin N.B., Diploid-tetraploid relationship among old world members of the fish family Cyprinidae, Chromosoma, 1967, 23, 1–19

    Article  Google Scholar 

  32. Ferris S. D., Whitt G.S., The evolution of duplicate gene expression in the carp (Cyprinus carpio), Experientia, 1977, 33, 1299–1301

    Article  CAS  Google Scholar 

  33. Engelsma M.Y., Stet R.J., Saeij J.P., Verburgvan Kemenade B.M., Differential expression and haplotypic variation of two interleukin-1 beta genes in the common carp (Cyprinus carpio L.), Cytokine, 2003, 22, 21–32

    Article  PubMed  CAS  Google Scholar 

  34. Li S., Hu W., Wang Y., Zhu Z., Cloning and expression analysis in mature individuals of two chicken GnRH (cGnRH-II) genes in common carp (Cyprinus carpio), Sci. China C Life Sci., 2004, 47, 349–358

    Article  PubMed  CAS  Google Scholar 

  35. Futami K., Zhang H., Okamoto N., Functional divergence of duplicated c-myc genes in a tetraploid fish, the common carp (Cyprinus carpio), Gene, 2005, 363, 61–66

    Article  PubMed  CAS  Google Scholar 

  36. Uyeno T., Smith G.R., Tetraploid origin of the karyotype of catostomid fishes, Science, 1972, 175, 644–646

    Article  PubMed  CAS  Google Scholar 

  37. Kirpichnikov V.S., Genetic bases of fish selection, Springer-Verlag, Berlin, 1981

    Google Scholar 

  38. Larhammar D., Risinger C., Molecular genetic aspects of tetraploidy of the common carp Cyprinus carpio, Mol. Phylogenet. Evol., 1994, 3, 59–68

    Article  PubMed  CAS  Google Scholar 

  39. David L., Blum S., Feldman M.W., Lavi U., Hillel J. Recent duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci, Mol. Biol. Evol., 2003, 20, 1425–1434

    Article  PubMed  CAS  Google Scholar 

  40. Ojima Y., Hitotsumachi S., Makino S., Cytogenetic studies in lower vertebrates. I. Preliminary report on the chromosomes of funa (Carassius auratus) and the goldfish, Proc. Jpn. Acad., 1966, 42, 62–66

    Google Scholar 

  41. Taylor J., Mahon R., Hybridization of Cyprinus carpio and Carassius auratus, the first two exotic species in the lower Laurentian Great Lakes, Environ. Biol. Fishes, 1, 1966, 205–208

    Article  Google Scholar 

  42. Ohno S., Dispensable genes, Trends Genet., 1985, 1, 160–164

    Article  CAS  Google Scholar 

  43. Polley S.D., Tiku P.E., Trueman R.T., Caddick M.X., Morozov I.Y., Cossins A.R., Differential expression of cold- and diet-specific genes encoding two carp liver delta 9-acyl-CoA desaturase isoforms, Am. J. Physiol. Regul. Integr. Comp. Physiol., 2003, 284, R41–R50

    PubMed  CAS  Google Scholar 

  44. Tiku P.E., Gracey A.Y., Macartney A.I., Beynon R.J., Cossins A.R., Cold-induced expression of delta9-desaturase in carp by transcriptional and posttranslational mechanisms, Science, 1996, 271, 815–818

    Article  PubMed  CAS  Google Scholar 

  45. Force A., Lynch M., Pickett F.B., Amores A., Yan Y.L., Postlethwait J., Preservation of duplicate genes by complementary, degenerative mutations, Genetics, 1999, 151, 1531–1545

    PubMed  CAS  Google Scholar 

  46. Liu S.J., Liu Y., Zhou G.J., The formation of tetraploid stocks of red crucian carp x common carp hybrids as an effect of interspecific hybridization, Aquaculture, 2001, 192, 171–186

    Article  Google Scholar 

  47. Wolfe K. H., Yesterday’s polyploids and the mystery of diploidization, Nat. Rev. Genet., 2001, 2, 333–341

    Article  PubMed  CAS  Google Scholar 

  48. Zhang Y., Liang L., Jiang P., Li D., Lu C., Sun X., Genome evolution trend of common carp (Cyprinus carpio L.) as revealed by the analysis of microsatellite loci in a gynogentic family, J. Genet. Genomics, 2008, 35, 97–103

    Article  PubMed  CAS  Google Scholar 

  49. Kohlmann K., Kersten P., Genetics variability of German and foreign common carp (Cyprinus carpio L.) population, Aquaculture, 1999, 173, 435–445

    Article  Google Scholar 

  50. Froufe E., Magyary I., Lehoczky I., Weiss S., mtDNA sequence data supports an Asian ancestry and single introduction of common carp into Danube basin, Fish Biol., 2002, 61, 301–314

    Article  CAS  Google Scholar 

  51. Kohlmann K., Kersten P., Flajshans M., Microsatellitebased genetic variability and differentiation of domesticated, wild and feral common carp (Cyprinus carpio L.) populations, Aquaculture, 2005, 247, 253–266

    Article  CAS  Google Scholar 

  52. Memis D., Kohlmann K., Genetic characterization of wild common carp (Cyprinus carpio L.) from Turkey, Aquaculture, 2006, 258, 257–262

    Article  CAS  Google Scholar 

  53. Zardoya R., Doadrio I., Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids, J. Mol. Evol., 1999, 49, 227–237

    Article  PubMed  CAS  Google Scholar 

  54. Hickling C., Fish culture, Faber & Faber, London, 1962

    Google Scholar 

  55. Vooren C.M., Ecological aspects of the introduction of fish species into natural habitats in Europe, with special reference to the Netherlands, J. Fish Biol., 1972, 4, 565–583

    Article  Google Scholar 

  56. Desvignes J.F., Laroche J., Durand J.D., Bouvet Y., Genetic variability in reared stocks of common carp Cyprinus carpio L. based on allozymes and microsatellites, Aquaculture, 2001, 194, 291–301

    Article  CAS  Google Scholar 

  57. Wang C.H., Li S.F., Genetic variability and relationships in mitochondrial DNA CO II gene sequence of red common carps in China, Yi Chuan Xue Bao, 2004, 31, 1226–1231, (in Chinese)

    PubMed  CAS  Google Scholar 

  58. Nguyen V.H., Ngo S.V., Vietnamese freshwater fish, cyprinid family, Agriculture Publish House, Hanoi, Vietnam, 2001

    Google Scholar 

  59. Wang C.H., Li S.F., Phylogenetic relationships of ornamental (Koi) carp, Oujiang Color carp and Long-fin carp revealed by mitochondrial DNA COII gene sequences and RAPD analysis, Aquaculture, 2004, 231, 83–91

    Article  CAS  Google Scholar 

  60. Mabuchi K., Seno, H., Suzuki T., Nishida M., Discovery of an ancient lineage of Cyprinus carpio from Lake Biwa, central Japan, based on mtDNA sequence data, with reference to possible multiple origins of koi, J. Fish Biol., 2005, 66, 1516–1528

    Article  Google Scholar 

  61. Mabuchi K., Miya M., Senou H., Suzuki T., Nishida M., Complete mitochondrial DNA sequence of the Lake Biwa wild strain of common carp (Cyprinus carpio L.): further evidence for an ancient origin, Aquaculture, 2006, 257, 68–77

    Article  CAS  Google Scholar 

  62. Jewell M.A.S., Rahman M.M., Islam M.N., Study of genetic variation in different hatchery populations of common carp (Cyprinus carpio L.) of Mymensingh district in Bangladesh using microsatellite DNA markers, J. Biosci., 2006, 14, 113–120

    Google Scholar 

  63. Mickett K., Morton C., Feng, J., Li P., Simmons M., Dunham R.A., et al., Assessing genetic diversity of domestic populations of channel catfish (Ictalurus punctatus) in Alabama using AFLP markers, Aquaculture, 2003, 228, 91–105

    Article  CAS  Google Scholar 

  64. Innes B.H., Elliott N.G., Genetic diversity in a Tasmanian hatchery population of Atlantic salmon (Salmo salar L.) compared with its Canadian progenitor population., Aquaculture Res., 2006, 37, 563–569

    Article  CAS  Google Scholar 

  65. Was A., Wenne R., Genetic differentiation in hatchery and wild sea trout (Salmo trutta) in the Southern Baltic at microsatellite loci, Aquaculture, 2002, 204, 493–506

    Article  CAS  Google Scholar 

  66. Sekino M., Hara M., Taniguchi N. Genetic diversity within and between hatchery strains of Japanese flounder Paralichthys olivaceus assessed by means of microsatellite and mitochondrial DNA sequencing analysis, Aquaculture, 2002, 213, 101–122

    Article  CAS  Google Scholar 

  67. Allendorf F.W., Phelps S., Loss genetic variation in hatchery stock of cutthroat trout, Am. Fish. Soc., 1980, 109, 537–543

    Article  Google Scholar 

  68. Thai B.T., Pham A.T., Austin C.M., Genetic diversity of common carp in Vietnam using direct sequencing and SSCP analysis of the mitochondrial DNA control region, Aquaculture, 2006, 258, 228–240

    Article  CAS  Google Scholar 

  69. Zhu Z.Y., Sun Y.H., Embryonic and genetic manipulation in fish, Cell Res., 2000, 10, 17–27

    Article  PubMed  CAS  Google Scholar 

  70. Gomelsky B., Chromosome set manipulation and sex control in common carp: a review, Aquat. Living Resour., 2003, 16, 408–415

    Article  Google Scholar 

  71. Vandeputte M., Selective breeding of quantitative traits in the common carp (Cyprinus carpio): a review, Aquat. Living Resour., 2003, 16, 399–407

    Article  Google Scholar 

  72. Komen J., Thorgaard G.H., Androgenesis, gynogenesis and the production of clones in fishes: a review, Aquaculture, 2007, 269, 150–173

    Article  Google Scholar 

  73. Murakaeva A., Kohlmann K., Kersten P., Kamilov B., Khabibullin D., Genetic characterization of wild and domesticated common carp (Cyprinus carpio L.) populations from Uzbekistan, Aquaculture, 2003, 218, 153–166

    Article  Google Scholar 

  74. Lehoczky I., Jeney J., Magyary I., Hancz C., Kohlmann K., Preliminary data on genetic variability and purity of common carp (Cyprinus carpio L.) strains kept at the live gene bank at Research Institute for Fisheries, Aquaculture and Irrigation (HAKI) Szarvas, Hungary, Aquaculture, 2005, 247, 45–49

    CAS  Google Scholar 

  75. Sun X., Liang L., A genetic linkage map of common carp (Cyprinus carpio L.) And mapping of a locus associated with cold tolerance, Aquaculture, 2007, 269, 174–186

    Article  CAS  Google Scholar 

  76. Vasemagi A., Nilsson J., Primmer C.R., Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in atlantic salmon (Salmo salar L.), Mol. Biol. Evol., 2005, 22, 1067–1076

    Article  PubMed  CAS  Google Scholar 

  77. Christoffels A., Bartfai R., Srinivasan H., Komen H., Orban L., Comparative genomics in cyprinids: common carp ESTs help the annotation of the zebrafish genome, BMC Bioinformatics, 2006, 7, Suppl. 5, S2

    Article  PubMed  CAS  Google Scholar 

  78. He C., Chen L., Simmons M., Kim S., Liu Z.J., Putative SNP discovery in interspecific hybrids of catfish by comparative EST analysis, Anim. Genet., 2003, 34, 445–448

    Article  PubMed  CAS  Google Scholar 

  79. Rasooly R.S., Henken D., Freeman, N., Tompkins L., Badman D., Briggs J., et al., Genetic and genomic tools for zebrafish research: the NIH zebrafish initiative, Dev. Dyn., 2003, 228, 490–496

    Article  PubMed  CAS  Google Scholar 

  80. Tang J., Leunissen JA, Voorrips RE, van der Linden CG, Vosman B., HaploSNPer: a web-based allele and SNP detection tool, BMC Genetics, 2008, 9, 23

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Diagnostics, National Research Center GosNIIgenetika, 113545, Moscow, Russia

    Dimitry A. Chistiakov

  2. Department of Fish Ecology, Federal Research Institute of Fisheries and Oceanography, 111394, Moscow, Russia

    Natalia V. Voronova

Authors
  1. Dimitry A. Chistiakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Natalia V. Voronova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dimitry A. Chistiakov.

About this article

Cite this article

Chistiakov, D.A., Voronova, N.V. Genetic evolution and diversity of common carp Cyprinus carpio L. . cent.eur.j.biol. 4, 304–312 (2009). https://doi.org/10.2478/s11535-009-0024-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11535-009-0024-2

Keywords

Search

Navigation