Carassius gibelio is an extraordinary cyprinid species exhibiting both sexual and asexual reproduction. We hypothesized that parasitism selection is one of the potential mechanisms contributing to the coexistence of the two reproductive forms of C. gibelio living in the same habitat. We performed a four-year study to investigate the dynamics of parasite infection in C. gibelio. According to the Red Queen prediction, the asexual form is a target of parasite adaptation due to its low genetic variability. Both sexual and gynogenetic forms of C. gibelio exhibited similar levels of prevalence, with monogeneans being the most frequently observed parasite group. We observed the temporal dynamics of parasite infection in the last year of investigation, when both forms were more strongly parasitized. The sexual form was more parasitized by ectoparasites in the first and last years and less parasitized by nematodes in the last year when compared to the gynogenetic form. We found no trend of high parasite infection in gynogenetic mtDNA haplotypes. We conclude that Red Queen dynamics is not the mechanism driving parasite infection in sexual-gynogenetic C. gibelio over a long time scale. Alternatively, we suggest that the dynamics of parasite infection in this complex may be generated by multiple mechanisms.

Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 2 611 37 Brno Czech Republic

Institute of Vertebrate Biology Academy of Sciences of the Czech Republic v v i Květná 8 603 65 Brno Czech Republic

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Smith J. M. The Evolution of Sex. Cambridge, UK: Cambridge University Press; 1978.

Bell G. The Masterpiece of Nature: the Evolution and Genetics of Sexuality. Berkeley, Calif, USA: University of California Press; 1982.

Lamatsch D. K., Stöck M. Sperm-dependent parthenogenesis and hybridogenesis in teleost fishes. In: Schön I., Martens K., Dijk P., editors. Lost Sex. Dordrecht, Netherlands: Springer; 2009. pp. 399–432.

Allendorf F. W. Ecological and Genetic Effects of Fish Introductions: Synthesis and Recommendations. Canadian Journal of Fisheries and Aquatic Sciences. 1991;48(S1):178–181. doi: 10.1139/f91-318. DOI

Moyle P. B., Light T. Fish invasions in California: Do abiotic factors determine success? Ecology. 1996;77(6):1666–1670. doi: 10.2307/2265770. DOI

Cowx I. G. Introduction of fish species into european fresh waters: Economic successes or ecological disasters ? BFPP - Bulletin Francais de la Peche et de la Protection des Milieux Aquatiques. 1997;(344-345):57–77.

Lusk S., Lusková V., Halačka K. Prussian carp – 25 years since its natural introduction. Proceedings of the 3rd Czech Conference of Ichthyology; 1998; pp. 135–140.

Szczerbowski J. A., Banarescu P. M., Poepke H. J. The Freshwater Fishes of Europe, Cyprinidae 2, Part III, Carassius to Cyprinus. AULA-Verlag. 2002;5(3):5–41.

Lusk S., Lusková V. Invasive fish species in the Czech Republic. Proceedings of the 8th Czech Conference of Ichthyology; 2005; Czech. pp. 135–140.

García-Berthou E., Alcaraz C., Pou-Rovira Q., Zamora L., Coenders G., Feo C. Introduction pathways and establishment rates of invasive aquatic species in Europe. Canadian Journal of Fisheries and Aquatic Sciences. 2005;62(2):453–463. doi: 10.1139/f05-017. DOI

Lusk S., Baruš V., Veselý V. On the occurrence of Carassius auratus in the Morava river drainage area. Folia Zoologica. 1977;4(26):377–381.

Lusk S., Luskova V., Hanel L. Alien fish species in the Czech Republic and their impact on the native fish fauna. Folia Zoologica. 2010;59(1):57–72. doi: 10.25225/fozo.v59.i1.a9.2010. DOI

Lusk S., Koščo J., Lusková V., Halačka K., Košuth P. Alien fish species in the floodplains of the Dyje and the Bodrog rivers. Ecohydrology & Hydrobiology. 2004;4(2):199–205.

Lusk S., Baruš V., Kirka A. Current spreading and importance of the giebel (Carassius auratus gibelio Bloch) in Czechoslovakia. Czech Journal of Animal Science. 1980;25(11):871–878.

Baruš V., Oliva O. Fauna of Czech Republic and Slovak Republic, Petromyzontes and Osteichtyes . Prague, Czech Republic: Academia; 1995.

Lusková V., Halačka K., Vetešník L., Lusk S. Changes of ploidy and sexuality status of ‘Carassius auratus’ populations in the drainage area of the River Dyje (Czech Republic) Ecohydrology & Hydrobiology. 2004;4(2):165–171.

Lusková V., Lusk S., Halačka K., Vetešník L. Carassius auratus gibelio—The most successful invasive fish in waters of the Czech Republic. Russian Journal of Biological Invasions. 2010;1(3):176–180. doi: 10.1134/S2075111710030069. DOI

Vetešník L., Halačka K., Lusková V., Lusk S. Erythrocyte profile of diploid and triploid silver crucian carp (Carassius auratus) Acta Veterinaria Brno. 2006;75(2):203–207. doi: 10.2754/avb200675020203. DOI

Papoušek I. Molecular-genetic analyses of Carassius species in central Europe [Ph.D. thesis] Brno, Czech Republic: Masaryk University, Faculty of Science; 2008.

Van Valen L. A new evolutionary law. Evolutionary Theory. 1973;1:1–30.

Jaenike J. An hypothesis to account for the maintenance of sex within populations. Evolutionary Theory. 1978;3:191–194.

Lively C. M., Craddock C., Vrijenhoek R. C. Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature. 1990;344(6269):864–866. doi: 10.1038/344864a0. DOI

Lampert K. P., Fischer P., Schartl M. Major histocompatibility complex variability in the clonal Amazon molly, Poecilia formosa: Is copy number less important than genotype? Molecular Ecology. 2009;18(6):1124–1136. doi: 10.1111/j.1365-294X.2009.04097.x. PubMed DOI

Lively C. M., Dybdahl M. F. Parasite adaptation to locally common host genotypes. Nature. 2000;405(6787):679–681. doi: 10.1038/35015069. PubMed DOI

Hakoyama H., Nishimura T., Matsubara N., Iguchi K. Difference in parasite load and nonspecific immune reaction between sexual and gynogenetic forms of Carassius auratus. Biological Journal of the Linnean Society. 2001;72(3):401–407. doi: 10.1006/bijl.2000.0507. doi: 10.1111/j.1095-8312.2001.tb01326.x. DOI

Hakoyama H., Iwasa Y. Coexistence of a sexual and an unisexual form stabilized by parasites. Journal of Theoretical Biology. 2004;226(2):185–194. doi: 10.1016/j.jtbi.2003.08.012. PubMed DOI

Kotusz J., Popiolek M., Drozd P., De Gelas K., Šlechtová V., Janko K. Role of parasite load and differential habitat preferences in maintaining the coexistence of sexual and asexual competitors in fish of the Cobitis taenia hybrid complex. Biological Journal of the Linnean Society. 2014;113(1):220–235. doi: 10.1111/bij.12329. DOI

Šimková A., Košař M., Vetešník L., Vyskočilová M. MHC genes and parasitism in Carassius gibelio, a diploid-triploid fish species with dual reproduction strategies. BMC Evolutionary Biology. 2013;13, article 122 doi: 10.1186/1471-2148-13-122. PubMed DOI PMC

Šimková A., Hyršl P., Halačka K., Vetešník L. Physiological and condition-related traits in the gynogenetic-sexual Carassius auratus complex: different investments promoting the coexistence of two reproductive forms? BMC Evolutionary Biology. 2015;15, article 438 doi: 10.1186/s12862-015-0438-6. PubMed DOI PMC

Vetešník L., Halačka K., Šimková A. The effect of ploidy and temporal changes in the biochemical profile of gibel carp (Carassius gibelio): A cyprinid fish species with dual reproductive strategies. Fish Physiology and Biochemistry. 2013;39(2):171–180. doi: 10.1007/s10695-012-9688-z. PubMed DOI

Ergens R., Lom J. Causative Agents of Fish Diseases . Prague, Czech Republic: Academia; 1970.

Malmberg G. On the occurrence of Gyrodactylus on Swedish fishes. Skrifter utgivna av Sodra Sveriges Fiskeriforening. 1957:19–76.

Flajšhans M. A model approach to distinguish diploid and triploid fish by means of computer-assisted image analysis. Acta Veterinaria Brno. 1997;66(2):101–110. doi: 10.2754/avb199766020101. DOI

Halačka K., Lusková V. Polyploidy in Carassius auratus in the lower reaches of the river Dyje - determination using the size of erythrocyte nuclei. Proceedings of the 4th Czech Ichthyological Conference, Book of Abstracts; 2000; Vodňany, Czech Republic. Research Institute of Fish Culture and Hydrobiology; pp. 106–109.

Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. Dallas, Tex, USA: University of Texas South Western Medical Center; 1989.

Vetešník L., Papoušek I., Halačka K., Lusková V., Mendel J. Morphometric and genetic analysis of Carassius auratus complex from an artificial wetland in Morava River floodplain, Czech Republic. Fisheries Science. 2007;73(4):817–822. doi: 10.1111/j.1444-2906.2007.01401.x. DOI

Papoušek I., Vetešník L., Halačka K., Lusková V., Humpl M., Mendel J. Identification of natural hybrids of gibel carp Carassius auratus gibelio (Bloch) and crucian carp Carassius carassius (L.) from lower Dyje River floodplain (Czech Republic) Journal of Fish Biology. 2008;72(5):1230–1235. doi: 10.1111/j.1095-8649.2007.01783.x. DOI

Liu H., Tzeng C.-S., Teng H.-Y. Sequence variations in the mitochondrial DNA control region and their implications for the phylogeny of the Cypriniformes. Canadian Journal of Zoology. 2002;80(3):569–581. doi: 10.1139/z02-035. DOI

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution. 2013;30(12):2725–2729. doi: 10.1093/molbev/mst197. PubMed DOI PMC

Clement M., Posada D., Crandall K. A. TCS: A computer program to estimate gene genealogies. Molecular Ecology. 2000;9(10):1657–1659. doi: 10.1046/j.1365-294X.2000.01020.x. doi: 10.1046/j.1365-294x.2000.01020.x. PubMed DOI

Hamilton W. D. Sex versus Non-Sex versus Parasite. Oikos. 1980;35(2):p. 282. doi: 10.2307/3544435. DOI

Hamilton W. D., Axelrod R., Tanese R. Sexual reproduction as an adaptation to resist parasites (A review) Proceedings of the National Acadamy of Sciences of the United States of America. 1990;87(9):3566–3573. doi: 10.1073/pnas.87.9.3566. PubMed DOI PMC

Tobler M., Schlupp I. Parasites in sexual and asexual mollies (Poecilia, Poeciliidae, Teleostei): A case for the Red Queen? Biology Letters. 2005;1(2):166–168. doi: 10.1098/rsbl.2005.0305. PubMed DOI PMC

Trematode Diplostomum pseudospathaceum inducing differential immune gene expression in sexual and gynogenetic gibel carp (Carassius gibelio): parasites facilitating the coexistence of two reproductive forms of the invasive species

Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction

Uncovering the monogenean species diversity of cyprinoid fish in Iraq using an integrative approach