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Genetic evolution and diversity of common carp Cyprinus carpio L.

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

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

© 2009 Versita Warsaw. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. (CC BY-NC-ND 3.0)

Citation Information: Open Life Sciences. Volume 4, Issue 3, Pages 304–312, ISSN (Online) 2391-5412, DOI: 10.2478/s11535-009-0024-2, July 2009

Publication History

Published Online:
2009-07-26

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.

Keywords: Common carp; Microsatellites; Mitochondrial DNA markers; Genome evolution; Genetic diversity; Population

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

  • [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

  • [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 http://dx.doi.org/10.1016/0044-8486(94)00227-F

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

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

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

  • [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

  • [8] Danzmann R.G., Down N.E., Isozyme expression in F1 hybrids between carp and goldfish, Biochem. Genet., 1982, 20, 1–15 http://dx.doi.org/10.1007/BF00484931

  • [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

  • [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 http://dx.doi.org/10.1186/1297-9686-39-3-319

  • [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 http://dx.doi.org/10.1016/S1673-8527(07)60111-8

  • [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 http://dx.doi.org/10.1007/s004380100569

  • [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 http://dx.doi.org/10.1016/S0990-7440(03)00082-2

  • [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 http://dx.doi.org/10.1023/A:1024421001015

  • [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)

  • [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 http://dx.doi.org/10.1111/j.1365-2052.2004.01215.x

  • [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

  • [18] Liu Z.Y., Cordes J.F., DNA marker technologies and their applications in aquaculture genetics, Aquaculture, 2004, 238, 1–37 http://dx.doi.org/10.1016/j.aquaculture.2004.05.027

  • [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 http://dx.doi.org/10.1111/j.1365-2052.1997.00097.x

  • [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

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

  • [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 http://dx.doi.org/10.1016/j.aquaculture.2003.12.021

  • [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 http://dx.doi.org/10.1111/j.1755-0998.2008.02305.x

  • [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

  • [25] Bruford M.W., Bradley D.G., Luikart G., DNA markers reveal the complexity of livestock domestication, Nat. Rev. Genet., 2003, 4, 900–910 http://dx.doi.org/10.1038/nrg1203

  • [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 http://dx.doi.org/10.1007/BF00166161

  • [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 http://dx.doi.org/10.1016/S0044-8486(01)00836-5

  • [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 http://dx.doi.org/10.1016/S0044-8486(03)00168-6

  • [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 http://dx.doi.org/10.1051/alr:2007025

  • [30] Ohno S., Atkin N.B., Comparative DNA values and chromosome complements of eight species of fishes, Chromosoma, 1966, 18, 455–466 http://dx.doi.org/10.1007/BF00332549

  • [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 http://dx.doi.org/10.1007/BF00293307

  • [32] Ferris S. D., Whitt G.S., The evolution of duplicate gene expression in the carp (Cyprinus carpio), Experientia, 1977, 33, 1299–1301 http://dx.doi.org/10.1007/BF01920144

  • [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 http://dx.doi.org/10.1016/S1043-4666(03)00102-9

  • [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 http://dx.doi.org/10.1360/03yc0117

  • [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 http://dx.doi.org/10.1016/j.gene.2005.06.041

  • [36] Uyeno T., Smith G.R., Tetraploid origin of the karyotype of catostomid fishes, Science, 1972, 175, 644–646 http://dx.doi.org/10.1126/science.175.4022.644

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

  • [38] Larhammar D., Risinger C., Molecular genetic aspects of tetraploidy of the common carp Cyprinus carpio, Mol. Phylogenet. Evol., 1994, 3, 59–68 http://dx.doi.org/10.1006/mpev.1994.1007

  • [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 http://dx.doi.org/10.1093/molbev/msg173

  • [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

  • [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 http://dx.doi.org/10.1007/BF00000412

  • [42] Ohno S., Dispensable genes, Trends Genet., 1985, 1, 160–164 http://dx.doi.org/10.1016/0168-9525(85)90070-8

  • [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

  • [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 http://dx.doi.org/10.1126/science.271.5250.815

  • [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

  • [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 http://dx.doi.org/10.1016/S0044-8486(00)00451-8

  • [47] Wolfe K. H., Yesterday’s polyploids and the mystery of diploidization, Nat. Rev. Genet., 2001, 2, 333–341 http://dx.doi.org/10.1038/35072009

  • [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 http://dx.doi.org/10.1016/S1673-8527(08)60015-6

  • [49] Kohlmann K., Kersten P., Genetics variability of German and foreign common carp (Cyprinus carpio L.) population, Aquaculture, 1999, 173, 435–445 http://dx.doi.org/10.1016/S0044-8486(98)00474-8

  • [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 http://dx.doi.org/10.1111/j.1095-8649.2002.tb01756.x

  • [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 http://dx.doi.org/10.1016/j.aquaculture.2005.02.024

  • [52] Memis D., Kohlmann K., Genetic characterization of wild common carp (Cyprinus carpio L.) from Turkey, Aquaculture, 2006, 258, 257–262 http://dx.doi.org/10.1016/j.aquaculture.2006.03.041

  • [53] Zardoya R., Doadrio I., Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids, J. Mol. Evol., 1999, 49, 227–237 http://dx.doi.org/10.1007/PL00006545

  • [54] Hickling C., Fish culture, Faber & Faber, London, 1962

  • [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 http://dx.doi.org/10.1111/j.1095-8649.1972.tb05702.x

  • [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 http://dx.doi.org/10.1016/S0044-8486(00)00534-2

  • [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)

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

  • [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 http://dx.doi.org/10.1016/j.aquaculture.2003.10.040

  • [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 http://dx.doi.org/10.1111/j.0022-1112.2005.00676.x

  • [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 http://dx.doi.org/10.1016/j.aquaculture.2006.03.040

  • [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

  • [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 http://dx.doi.org/10.1016/S0044-8486(03)00311-9

  • [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 http://dx.doi.org/10.1111/j.1365-2109.2006.01463.x

  • [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 http://dx.doi.org/10.1016/S0044-8486(01)00835-3

  • [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 http://dx.doi.org/10.1016/S0044-8486(01)00885-7

  • [67] Allendorf F.W., Phelps S., Loss genetic variation in hatchery stock of cutthroat trout, Am. Fish. Soc., 1980, 109, 537–543 http://dx.doi.org/10.1577/1548-8659(1980)109<537:LOGVIA>2.0.CO;2

  • [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 http://dx.doi.org/10.1016/j.aquaculture.2006.03.025

  • [69] Zhu Z.Y., Sun Y.H., Embryonic and genetic manipulation in fish, Cell Res., 2000, 10, 17–27 http://dx.doi.org/10.1038/sj.cr.7290032

  • [70] Gomelsky B., Chromosome set manipulation and sex control in common carp: a review, Aquat. Living Resour., 2003, 16, 408–415 http://dx.doi.org/10.1016/S0990-7440(03)00085-8

  • [71] Vandeputte M., Selective breeding of quantitative traits in the common carp (Cyprinus carpio): a review, Aquat. Living Resour., 2003, 16, 399–407 http://dx.doi.org/10.1016/S0990-7440(03)00056-1

  • [72] Komen J., Thorgaard G.H., Androgenesis, gynogenesis and the production of clones in fishes: a review, Aquaculture, 2007, 269, 150–173 http://dx.doi.org/10.1016/j.aquaculture.2007.05.009

  • [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 http://dx.doi.org/10.1016/S0044-8486(03)00005-X

  • [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

  • [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 http://dx.doi.org/10.1016/j.aquaculture.2007.05.017

  • [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 http://dx.doi.org/10.1093/molbev/msi093

  • [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 http://dx.doi.org/10.1186/1471-2105-7-S5-S2

  • [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 http://dx.doi.org/10.1046/j.0268-9146.2003.01054.x

  • [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 http://dx.doi.org/10.1002/dvdy.10366

  • [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 http://dx.doi.org/10.1186/1471-2156-9-23

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