Skip to main content
SpringerLink
Log in

Recent invasion and low level of divergence between diploid and triploid forms of Carassius auratus complex in Croatia

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Carassius auratus is an invasive species in European waters, comprising a complex of diploid and polyploid forms with different modes of reproduction. However, the evolutionary history and relationships between the diploids and polyploids are still unresolved. In this study, 51.5% diploids and 48.5% triploids, including four triploid males, were discovered among the 363 individuals sampled in Croatia. We used eight microsatellite loci and mitochondrial displacement loop sequences to analyze the structure and origin of populations; and to attempt to infer the evolutionary history of the two different forms in Croatia. Microsatellite analyses revealed high allelic and clonal diversity, corroborating that high propagule vectors can compensate for the negative effects of genetic bottlenecks in successful invasive species. The absence of significant population structuring confirmed recent origin and rapid spreading of populations. No evidence was found for the existence of native European populations. Distances between individuals using both nuclear and mtDNA markers revealed the absence of substantial clustering on the ploidy level, while the split between the different ploidies on population level was only partial, suggesting that the reproductive isolation between the two forms is either of a very recent origin, or that there exists uni-, or bidirectional gene flow between the diploid and triploid forms.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abramenko MI, Nadtoka EV, Makhotkin MA, Kravchenko OV, Poltavtseva TG (2004) Distribution and cytogenetic features of triploid males of crucian carp in Azov basin. Russ J Dev Biol 35:305–315. doi:10.1023/B:RUDO.0000043825.97296.54

    Article  Google Scholar 

  • Alves MJ, Coelho MM, Collares-Pereira MJ (2001) Evolution in action through hybridization and polyploidy in an Iberian freshwater fish: a genetic review. Genetica 111:375–385. doi:10.1023/A:1013783029921

    Article  PubMed  CAS  Google Scholar 

  • Apalikova OV, Eliseikina MG, Kovaleva MY, Brykov VA (2008) Collation of data on the ploidy levels and mitochondrial DNA phylogenetic lineages in the silver crucian carp Carassius auratus gibelio from Far Eastern and Central Asian populations. Russ J Genet 44:873–880. doi:10.1134/S1022795408070168

    Article  CAS  Google Scholar 

  • Brykov VA, Apalikova OV, Eliseikina MG, Kovalev MY (2005) Mitochondrial DNA variation in diploid and triploid forms of silver crucian carp Carassius auratus gibelio. Russ J Genet 41:659–663. doi:10.1007/s11177-005-0141-6 (Translated from Genetika 41:811–816)

    Article  CAS  Google Scholar 

  • Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Mol Biol Evol 25:624–633. doi:10.1093/molbev/msm271

    Article  PubMed  CAS  Google Scholar 

  • Crow JF (1999) The odds of losing at genetic roulette. Nature 397:293–294. doi:10.1038/16789

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1993) PHYLIP (Phylogeny Inference Package) version 3.68. Distributed by the author. Department of Genetics, University of Washington, Seattle

  • Freyhof J, Lieckfeld D, Pitra C, Ludwig A (2005) Molecules and morphology: evidence for introgression of mitochondrial DNA in Dalmatian cyprinids. Mol Phyl Evol 37:347–354

    Article  CAS  Google Scholar 

  • Goldstein DB, Ruiz Linares A, Cavalli-Sforza LL, Feldman MW (1995) An evaluation of genetic distances for use with microsatellite loci. Genetics 139:463–471

    PubMed  CAS  Google Scholar 

  • Gui J-F, Zhou L (2010) Genetic basis and breeding application on clonal diversity and dual reproduction modes in polyploid Carassius auratus gibelio. Sci China Life Sci 53:409–415. doi:10.1007/s11427-010-0092-6

    Article  PubMed  Google Scholar 

  • Guldbrandtsen B, Tomiuk J, Loeschcke V (2000) POPDIST, Version 1.1.1: a program to calculate population genetic distance and identity measures. J Hered 91:178–179

    Article  PubMed  CAS  Google Scholar 

  • Guo W, Gui J-F (2008) Microsatellite marker isolation and cultured strain identification in Carassius auratus gibelio. Aquacult Int 16:497–510. doi:10.1007/s10499-007-9161-7

    Article  CAS  Google Scholar 

  • Hänfling B (2007) Understanding the establishment success of non-indigenous fishes: lessons from population genetics. J Fish Biol 71:115–135. doi:10.1111/j.1095-8649.2007.01685.x

    Article  Google Scholar 

  • Hänfling B, Bolton P, Harley M, Carvalho GR (2005) A molecular approach to detect hybridisation between crucian carp (Carassius carassius) and non-indigenous carp species (Carassius spp.) and Cyprinus carpio). Freshw Biol 50:403–417. doi:10.1111/j.1365-2427.2004.01330.x

    Article  Google Scholar 

  • Hardy OJ, Vekemans X (1999) Isolation by distance in a continuous population: reconciliation between spatial autocorrelation analysis and population genetics models. Heredity 83:145–154. doi:10.1046/j.1365-2540.1999.00558.x

    Article  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620. doi:10.1046/j.1471-8278.2002.00305.x

    Article  Google Scholar 

  • Hey J (2010) Isolation with migration models for more than two populations. Mol Biol Evol 27:905–920. doi:10.1093/molbev/msp296

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist FR (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Kajgana LJ (1996) Silver crucian carp or chiton and damages it causes by its presence on fish farms. Ribarstvo 54:131–134 (In Serbo-Croatian)

    Google Scholar 

  • Kingston SE, Adams LD, Rosel PE (2009) Testing mitochondrial sequences and anonymous nuclear markers for phylogeny reconstruction in a rapidly radiating group: molecular systematics of the Delphininae (Cetacea: Odontoceti: Delphinidae). BMC Evol Biol 9:245

    Article  PubMed  Google Scholar 

  • Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Publications Kottelat, Cornol, pp 142–147

    Google Scholar 

  • Lampert KP, Lamatsch DK, Epplen JT, Schartl M (2005) Evidence for a monophyletic origin of triploid clones of the Amazon Molly, Poecilia formosa. Evolution 59:881–889

    PubMed  CAS  Google Scholar 

  • Li F-B, Gui J-F (2008) Clonal diversity and genealogical relationships of gibel carp in four hatcheries. Anim Genet 39:28–33. doi:10.1111/j.1365-2052.2007.01671.x

    Article  PubMed  Google Scholar 

  • Liu S-J (2010) Distant hybridization leads to different ploidy fishes. Sci China Life Sci 53:416–425. doi:10.1007/s11427-010-0057-9

    Article  PubMed  Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794. doi:10.1111/j.1471-8286.2004.00770.x

    Article  Google Scholar 

  • Mezhzherin SV, Lisetskii IL (2004) The genetic structure of European goldfish Carassius auratus s. lato (Cyprinidae) in Ukrainian water bodies: an analysis of bisexual samples. Biol Bull 31:574–581 (Translated from Izv Akad Nauk Biol 6:689–697)

    Article  Google Scholar 

  • Murakami M, Matsuba C, Fujitani H (2001) The maternal origins of the triploid ginbuna (Carassius auratus langsdorfii): phylogenetic relationships within the C. auratus taxa by partial mitochondrial D-loop sequencing. Genes Genet Syst 76:25–32

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • O’Connell M, Wright JM (1997) Microsatellite DNA in fishes. Rev Fish Biol Fisher 7:331–363. doi:10.1023/A:1018443912945

    Article  Google Scholar 

  • 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 20:797–804

    Article  PubMed  Google Scholar 

  • Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Plančić J (1967) Srebrnasti karas-Carassius auratus gibelio Bloch nova vrsta naše ihtiofaune. Ribarstvo Jugoslavije 22:155–156 (In Serbo-Croatian)

    Google Scholar 

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808. doi:10.1080/10635150490522304

    Article  PubMed  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464. doi:10.1016/j.tree.2007.07.002

    Article  PubMed  Google Scholar 

  • Ronfort J, Jenczewski E, Bataillon T, Rousset F (1998) Analysis of population structure in autotetraploid species. Genetics 150:921–930

    PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Sato M, Kawamata K, Zaslavskaya N, Nakamura A, Ohta T, Nishikiori T, Brykov V, Nagashima K (2005) Development of microsatellite markers for Japanese scallop (Mizuhopecten yessoensis) and their application to a population genetic study. Mar Biotechnol 7:713–728

    Article  PubMed  CAS  Google Scholar 

  • Schlupp I (2005) The evolutionary ecology of gynogenesis. Ann Rev Ecol Evol S 36:399–417. doi:10.1146/annurev.ecolsys.36.102003.152629

    Article  Google Scholar 

  • Schories S, Lampert KP, Lamatsch DK, de León FJG, Schartl M (2007) Analysis of a possible independent origin of triploid P. formosa outside of the Río Purificación river system. Front Zool 4:13. doi:10.1186/1742-9994-4-13

    Article  PubMed  Google Scholar 

  • Slavík O, Bartoš L (2004) What are the reasons for the Prussian carp expansion in the upper Elbe River, Czech Republic. J Fish Biol 65:240–253. doi:10.1111/j.1095-8649.2004.00560.x

    Article  Google Scholar 

  • Sušnik S, Weiss S, Odak T, Delling B, Treer T, Snoj A (2007) Reticulate evolution: ancient introgression of the Adriatic brown trout mtDNA in softmouth trout Salmo obtusirostris (Teleostei: Salmonidae). Biol J Linn Soc 90:139–152

    Article  Google Scholar 

  • Takada M, Tachihara K, Kon T, Yamamoto G, Iguchi K, Miya M, Nishida M (2010) Biogeography and evolution of the Carassius auratus-complex in East Asia. BMC Evol Biol 10:7. doi:10.1186/1471-2148-10-7

    Article  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092

    Article  PubMed  CAS  Google Scholar 

  • Tang Q, Liu H, Mayden RL, Xiong B (2006) Comparison of evolutionary rates in the mitochondrial DNA cytochrome b gene and control region and their implications for phylogeny of the Cobitoidea (Teleostei: Cypriniformes). Mol Phylogenet Evol 39:347–357. doi:10.1016/j.ympev.2005.08.007

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Tomiuk J, Loeschcke V (1996) A maximum likelihood estimator of the genetic identity between polyploid species. J Theor Biol 179:51–54. doi:10.1006/jtbi.1996.0047

    Article  PubMed  CAS  Google Scholar 

  • Tóth B, Várkonyi E, Hidas A, Edviné Meleg E, Váradi L (2005) Genetic analysis of offspring from intra- and interspecific crosses of Carassius auratus gibelio by chromosome and RAPD analysis. J Fish Biol 66:784–797. doi:10.1111/j.1095-8649.2005.00644.x

    Article  Google Scholar 

  • Tsipas G, Tsiamis G, Vidalis K, Bourtzis K (2009) Genetic differentiation among Greek lake populations of Carassius gibelio and Cyprinus carpio carpio. Genetica 136:491–500. doi:10.1007/s10709-008-9331-1

    Article  PubMed  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi:10.1111/j.1471-8286.2004.00684.x

    Article  Google Scholar 

  • Vrijenhoek RC (2006) Polyploid hybrids: multiple origins of a treefrog species. Curr Biol 16:R245–R247. doi:10.1016/j.cub.2006.03.005

    Article  PubMed  CAS  Google Scholar 

  • Vuković T (1982) Sistematika riba. Slatkovodno ribarstvo. Ribozajednica & Jumena, Zagreb, 605 pp (In Serbo-Croatian)

  • Wang Z-W, Zhu H-P, Wang D, Jiang F-F, Guo W, Zhou L, Gui J-F (2011) A novel nucleo-cytoplasmic hybrid clone formed via androgenesis in polyploid gibel carp. BMC Res Notes 4(1):82. doi:10.1186/1756-0500-4-82

    Article  PubMed  Google Scholar 

  • Wei W-H, Zhang J, Zhang Y-B, Zhou L, Gui J-F (2003) Genetic heterogeneity and ploidy level analysis among different gynogenetic clones of the polyploid gibel carp. Cytometry 56:46–52. doi:10.1002/cyto.a.10077

    Article  PubMed  Google Scholar 

  • Won YJ, Hey J (2005) Divergence population genetics of chimpanzees. Mol Biol Evol 22:297–307. doi:10.1093/molbev/msi017

    Article  PubMed  CAS  Google Scholar 

  • Yi M-S, Li Y-Q, Liu J-D, Zhou L, Yu Q-X, Gui J-F (2003) Molecular cytogenetic detection of paternal chromosome fragments in allogynogenetic gibel carp, Carassius auratus gibelio Bloch. Chromosome Res 11:665–671

    Article  PubMed  CAS  Google Scholar 

  • Yue GH, David L, Orban L (2007) Mutation rate and pattern of microsatellites in common carp (Cyprinus carpio L.). Genetica 129:329–331. doi:10.1007/s10709-006-0003-8

    Article  PubMed  CAS  Google Scholar 

  • Zhou L, Wang Y, Gui J-F (2000) Genetic evidence for gonochoristic reproduction in gynogenetic silver crucian carp (Carassius auratus gibelio Bloch) as revealed by RAPD assays. J Mol Evol 51:498–506. doi:10.1007/s002390010113

    PubMed  CAS  Google Scholar 

  • Zhu H-P, Ma D-M, Gui J-F (2006) Triploid origin of the gibel carp as revealed by 5S rDNA localization and chromosome painting. Chromosome Res 14:767–776. doi:10.1007/s10577-006-1083-0

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by the earmarked fund for Modern Agro-industry Technology Research System (NYCYTX-49), the National Natural Science Foundation of China (30630050), the Doctor-Candidate Visiting Program from Graduate School of Chinese Academy of Sciences (082Z03), the Autonomous Project of State Key Laboratory of Freshwater Ecology and Biotechnology (2008FBZ15), and the Innovation Project of Institute of Hydrobiology, Chinese Academy of Sciences (075A011301, 085A021301). English-language suggestions were provided by Cori Veverka and Kevin Wender; and assistance during sampling by Ratko Štuka, Robert Plečuh, Nikica Šprem, Domagoj Ceković, Dalibor Banaj, Tomislav Majić and Vladimir Jakovlić. The authors would also like to thank the anonymous reviewers who helped improve the manuscript.

Author information

Authors and Affiliations

  1. State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Graduate School of the Chinese Academy of Sciences, 430072, Wuhan, People’s Republic of China

    Ivan Jakovlić & Jian-Fang Gui

Authors
  1. Ivan Jakovlić
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jian-Fang Gui
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jian-Fang Gui.

Appendices

Appendix 1

See Table 7.

Table 7 Number of alleles per locus and population
Full size table

Appendix 2

See Table 8.

Table 8 Genetic differentiation between pairs of populations calculated as FST (below the diagonal line) and RhoST (above the diagonal line)
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jakovlić, I., Gui, JF. Recent invasion and low level of divergence between diploid and triploid forms of Carassius auratus complex in Croatia. Genetica 139, 789–804 (2011). https://doi.org/10.1007/s10709-011-9584-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-011-9584-y

Keywords

Search

Navigation