BACKGROUND: The gibel carp is a fish species with dual reproduction modes, gynogenesis and sexual reproduction, coexisting in mixed diploid-polyploid populations. Following the Red Queen (RQ) assumption, asexual organisms are, due to their low genetic diversity, targets for parasite adaptation. Because MHC polymorphism is maintained by selection from parasites and sexual selection, MHC genes are considered as a suitable candidate for testing the RQ hypothesis. In this study, we investigated MHC variability and the selection pressure acting on MHC genes in sexual diploids and asexual triploids. In addition, we tested whether the asexual form of gibel carp suffers from higher parasite loads than the sexual form. RESULTS: At the population level, genotype and allelic diversity of MHC were reduced in gynogenetic triploids when compared to sexual diploids. Different patterns in positively selected sites (PSS) between gynogens and sexual gibel carp were also found. A weak difference in parasite species richness was found between sexual fish and gynogens. However, two common clones of gynogens were significantly more parasitized than sexual diploids or other gynogens with rare MHC genotypes. At the individual level, the higher number of alleles was not associated with higher parasitism in either sexual diploids or gynogens. CONCLUSIONS: The differences in MHC diversity between gynogenetic triploids and sexual diploids are in accordance with the hypothesis of sexually-mediated selection increasing MHC diversity and fulfil a prerequisite of the Red Queen hypothesis. The different patterns in PSS between gynogens and sexual gibel carp also suggest the potential role of sexual selection and supports parasite-mediated selection maintaining MHC diversity. We showed that the most common MHC genotypes of gynogenetic triploids are the target of parasite selection. Our results suggest that the MHC genotype in gibel carp is more important than allelic number for immunocompetence.

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

Zobrazit více v PubMed

Mee JA, Rowe L. A comparison of parasite loads on asexual and sexual Phoxinus (Pisces: Cyprinidae) Can J Zoolog. 2006;84:808–816. doi: 10.1139/z06-064. DOI

Tobler M, Schlupp I. Differential susceptibility to food stress in neonates of sexual and asexual mollies (Poecilia, Poeciliidae) Evol Ecol. 2010;24:39–47. doi: 10.1007/s10682-008-9288-7. 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. Biol J Linn Soc. 2001;72:401–407. doi: 10.1111/j.1095-8312.2001.tb01326.x. DOI

Maynard Smith J. The Evolution of Sex. Cambridge: Cambridge University Press; 1978.

Bell G. The masterpiece of nature: the evolution and genetics of sexuality. Berkeley: University of California Press; 1982.

Lynch M, Burger R, Butcher D, Gabriel W. The mutational meltdown in asexual populations. J Hered. 1993;84:339–344. PubMed

Ching B, Jamieson S, Heath JW, Heath DD, Hubberstey A. Transcriptional differences between triploid and diploid Chinook salmon (Oncorhynchus tshawytscha) during live Vibrio anguillarum challenge. Heredity. 2010;104:224–234. doi: 10.1038/hdy.2009.108. PubMed DOI

Hamilton WD, Axelrod R, Tanese R. Sexual reproduction as an adaption to resist parasites (a review) P Natl Acad Sci USA. 1990;87:3566–3573. doi: 10.1073/pnas.87.9.3566. PubMed DOI PMC

Weeks SC. A reevaluation of the Red Queen model for the maintenance of sex in a clonal-sexual fish complex (Poeciliidae: Poeciliopsis) Can J Fish Aquat Sci. 1996;53:1157–1164.

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

Kokko H, Heubel KU, Rankin DJ. How populations persist when asexuality requires sex: the spatial dynamics of coping with sperm parasites. Proc R Soc B. 2008;275:817–825. doi: 10.1098/rspb.2007.1199. PubMed DOI PMC

Van Valen L. A new evolutionary law. Evol Theor. 1973;1:1–30.

Jaenike J. An hypothesis to account for the maitenance of sex within populations. Evol Theor. 1978;3:191–194.

Hamilton WD. Sex versus non-sex versus parasite. Oikos. 1980;35:282–290. doi: 10.2307/3544435. DOI

Seger J, Hamilton WD. In: The Evolution of Sex. Michod RE, Levin BR, editor. Sunderland, MA: Sinauer Associates; 1988. Parasites and sex; pp. 176–193.

Lively CM, Craddock C, Vrijenhoek RC. Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature. 1990;344:864–867. doi: 10.1038/344864a0. DOI

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

Klein J. The Natural History of the Major Histocompatibility Complex. New York: John Wiley; 1986.

Klein J, Figueroa F. Evolution of MHC. CRC Cr Rev Imunol. 1986;6:295–386. PubMed

Hughes AL, Nei M. Maintenance of MHC polymorphism. Nature. 1992;355:402–403. PubMed

Penn DJ, Potts WK. The evolution of mating preferences and major histocompatibility complex genes. Am Nat. 1999;153:145–164. doi: 10.1086/303166. PubMed DOI

Schaschl H, Tobler M, Plath M, Penn DJ, Schlupp I. Polymorphic MHC loci in an asexual fish, the amazon molly (Poecilia formosa; Poeciliidae) Mol Ecol. 2008;17:5220–5230. doi: 10.1111/j.1365-294X.2008.03997.x. PubMed DOI

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

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

Peňáz M, Ráb P, Prokeš M. Cytological analysis, gynogenesis and early development of Carassius auratus gibelio. Acta Sc Nat Brno. 1979;13:1–33.

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) Ecohydrol Hydrobiol. 2004;4:165–171.

Vetemaa M, Eschbaum R, Albert A, Saat T. Distribution, sex ration and growth of Carassius gibelio (Bloch) in coastal and inland water of Estonia (north-eastern Baltic Sea) J Appl Ichthyol. 2005;21:287–294. doi: 10.1111/j.1439-0426.2005.00680.x. DOI

Liasko R, Koulish A, Pogrebniak A, Papiggioti O, Taranenko L, Leonardos I. Influence of environmental parameters on growth pattern and population structure of Carassius auratus gibelio in Eastern Ukraine. Hydrobiologia. 2011;658:317–328. doi: 10.1007/s10750-010-0502-6. DOI

Takada M, Tachihara K. Comparisons of age, growth, and maturity between male and female, and diploid and triploid individuals in Carassius auratus from Okinawajima Island, Japan. Aquat Conserv - Mar Freshwat Ecosyst. 2009;19:806–814. doi: 10.1002/aqc.1032. DOI

Rylková K, Kalous L, Šlechtová V, Bohlen J. Many branches, one root: First evidence for a monophyly of the morphologically highly diverse goldfish (Carassius auratus) Aquaculture. 2010;302:36–41. doi: 10.1016/j.aquaculture.2010.02.003. DOI

Moravec F. Checklist of the metazoan parasites of fishes of the Czech Republic and the Slovak Republic (1873–2000) Prague: Academia; 2001.

Klein J, O’Huigin C. C: MHC polymorphism and parasites. Philos Trans R Soc Lond B. 1994;346:351–358. doi: 10.1098/rstb.1994.0152. PubMed DOI

Shamsi S, Jalali B, Meshgi MA. Infection with Dactylogyrus spp. among introduced cyprinid fishes and their geographical distribution in Iran. Iran J Vet Res. 2009;10:70–74.

Wang GX, Jiang DX, Li J, Han J, Liu YT, Liu XL. Anthelmintic activity of steroidal saponins from Dioscorea zingiberensis C. H. Wright against Dactylogyrus intermedius (Monogenea) in goldfish (Carassius auratus) Parasitol Res. 2010;107:1365–1371. doi: 10.1007/s00436-010-2010-z. PubMed DOI

Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature. 1993;364:33–39. doi: 10.1038/364033a0. PubMed DOI

Seifertová M, Šimková A. Structure, diversity and evolutionary patterns of expressed MHC class IIB genes in chub (Squalius cephalus), a cyprinid fish species from Europe. Immunogenetics. 2011;63:167–181. doi: 10.1007/s00251-010-0495-3. PubMed DOI

Ottová E, Šimková A, Morand S. The role of major histocompatibility complex diversity in vigour of fish males (Abramis brama L.) and parasite selection. Biol J Linn Soc. 2007;90:525–538. doi: 10.1111/j.1095-8312.2007.00743.x. DOI

Kruiswijk CP, Hermsen T, Fujiki K, Dixon B, Savelkoul HFJ, Stet RJM. Analysis of genomic and expressed major histocompatibility class Ia and class II genes in a hexaploid Lake Tana African ‘large’ barb individual (Barbus intermedius) Immunogenetics. 2004;55:770–781. doi: 10.1007/s00251-003-0635-0. PubMed DOI

Rakus KL, Wiegertjes GF, Jurecka P, Walker PD, Pilarczyk A, Irnazarov I. Major histocompatibility (MH) class IIB gene polymorphism influences disease resistance of common carp (Cyprinus carpio L.) Aquaculture. 2009;288:44–50. doi: 10.1016/j.aquaculture.2008.11.016. DOI

Radtkey RR, Becker B, Miller RD, Riblet R, Case TJ. Variation and evolution of class I Mhc in sexual and parthenogenetic geckos. P Roy Soc B-Biol Sci. 1996;263:1023–1032. doi: 10.1098/rspb.1996.0151. PubMed DOI

Abdelmonem AA, Metwally MM, Hussein HS, Elsheikha HM. Gross and microscopic pathological changes associated with parasitic infection in European eel (Anguilla anguilla, Linnaeus 1758) Parasitol Res. 2006;106:463–469. PubMed

Cable J, van Oosterhout C. The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. Int J Parasitol. 2007;37:1449–1458. doi: 10.1016/j.ijpara.2007.04.013. PubMed DOI

Nowak MA, Tarczy-Hornoch K, Austyn JM. The optimal number of major histocompatibility complex molecules in an individual. P Natl Acad Sci USA. 1992;89:10896–10899. doi: 10.1073/pnas.89.22.10896. PubMed DOI PMC

Wegner KM, Reusch TBH, Kalbe M. Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evolution Biol. 2003;16:224–232. doi: 10.1046/j.1420-9101.2003.00519.x. PubMed DOI

Hakoyama H, Iwasa Y. Coexistence of a sexual and an unisexual form stabilized by parasites. J Theor Biol. 2004;226:185–194. doi: 10.1016/j.jtbi.2003.08.012. PubMed DOI

Schlupp I. Mate choice and the Amazon Molly: how sexuality and unisexuality can coexist. J Heridity. 2010;101:S55–S61. doi: 10.1093/jhered/esq015. PubMed DOI

Janko K, Eisner J. Sperm-dependent parthenogens delay the spatial expansion of their sexual hosts. J Theor Biol. 2009;261:431–440. doi: 10.1016/j.jtbi.2009.08.012. PubMed DOI

Jokela J, Dybdahl MF, Lively CM. The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. Am Nat. 2009;174:S43–S53. doi: 10.1086/599080. PubMed DOI

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

Kanagawa T. Bias and artifacts in multitemplate polymerase chain reactions (PCR) J Biosci Bioeng. 2003;96:317–323. PubMed

Lenz TL, Becker S. Simple approach to reduce PCR artefact formation leads to reliable genotyping of MHC and other highly polymorphic loci - Implications for evolutionary analysis. Gene. 2008;427:117–123. doi: 10.1016/j.gene.2008.09.013. PubMed DOI

Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid S. 1999;41:95–98.

Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–4680. doi: 10.1093/nar/22.22.4673. PubMed DOI PMC

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–2739. doi: 10.1093/molbev/msr121. PubMed DOI PMC

Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986;3:418–426. PubMed

Jukes TH, Cantor CR. In: Mammalian Protein Metabolism. Munro HN, editor. New York: Academic Press; 1969. Evolution of protein molecules; pp. 21–132.

Posada D, Crandall KA. Modeltest: Testing the model of DNA substitution. Bioinformatics. 1998;14:817–818. doi: 10.1093/bioinformatics/14.9.817. PubMed DOI

Swofford DL. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates; 2003.

Yang ZH. PAML4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586–1591. doi: 10.1093/molbev/msm088. PubMed DOI

Ergens R, Lom J. Causative agents of fish diseases. Prague: Academia; 1970. (In Czech)

Magurran AE. Ecological diversity and its measurement. London: Croom Helm; 1983.

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

Diversity of MHC IIB genes and parasitism in hybrids of evolutionarily divergent cyprinoid species indicate heterosis advantage

A Long Temporal Study of Parasitism in Asexual-Sexual Populations of Carassius gibelio: Does the Parasite Infection Support Coevolutionary Red Queen Dynamics?

Physiological and condition-related traits in the gynogenetic-sexual Carassius auratus complex: different investments promoting the coexistence of two reproductive forms?