MHC genes and parasitism in Carassius gibelio, a diploid-triploid fish species with dual reproduction strategies

Abstract

BackgroundThe 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.ResultsAt 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.ConclusionsThe 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.

Infection Dynamics in Coexisting Sexual and Asexual Host Populations: Support for the Red Queen Hypothesis

“…Second, parasites can exhibit a high degree of genetic specificity for infection (Rauch et al 2006;Dybdahl et al 2008;Wegner et al 2008;Wilfert and Schmid-Hempel 2008;Duneau et al 2011;Luijckx et al 2011Luijckx et al , 2013, which is a necessary condition for parasite-mediated selection against common genotype. Third, parasite-mediated selection against common clones has been observed in laboratory experiments (Koskella and Lively 2009) as well as in the field for a wide Infection in Sexual and Asexual Hosts S23 range of taxa (Antonovics and Ellstrand 1984;Kelley et al 1988;Lively et al 1990;Chaboudez and Burdon 1995;Dybdahl and Lively 1998;Lively and Dybdahl 2000;Michiels et al 2001;Jokela et al 2009;Wolinska and Spaak 2009;Šimková et al 2013). Fourth, time-shift experiments (wherein hosts are exposed to parasites that were "frozen" from different time periods) have shown that parasites rapidly track common host genotypes in a variety of microbes, plants, and animals (Buckling and Rainey 2002;Decaestecker et al 2007;Koskella and Lively 2009;Thrall et al 2012;Koskella 2013Koskella , 2014.…”

Role of parasite load and differential habitat preferences in maintaining the coexistence of sexual and asexual competitors in fish of theCobitis taeniahybrid complex

“…A prerequisite for the RQ model is high virulence of a pathogen (Lively, ); however, it was proven recently that an assemblage of parasites (without a highly pathogenic one) may also drive the coexistence of sexual and gynogenetic strains along with the expectations of the RQH (e.g. the Carassius gibelio asexual complex; Šimková et al ., ). As shown theoretically, to maintain sexual reproduction, the virulence must not be extremely high (resulting in castration or death) (Lively, ).…”

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

“…Using parasite infection level as a measure of non-specific immunity, Hakoyama et al [ 52 ] found the gynogenetic form to be more susceptible to parasite disease. However, Šimková et al [ 27 ] focused on the MHC genotyping of gynogenetic and sexual specimens from the selected mixed population. They showed that infection by highly specific gill ectoparasites ( Dactylogyrus ) is higher in the most common MHC genotypes of gynogens when compared to rare MHC genotypes of gynogens or highly variable MHC genotypes of sexuals, suggesting a co-evolutionary arms-race between host immunity and parasite virulence.…”

“…Our study provides the first investigation of physiological and immune parameters in gynogenetic-sexual C. auratus complex. In addition to the limited ability of the gynogenetic form to escape parasitism as a potential mechanism promoting the coexistence of gynogenetic-sexual C. auratus complex [ 27 ], we hypothesized that the different investments in condition-, growth- and fitness-related traits may represent another mechanism contributing to the coexistence of gynogenetic and sexual forms of this complex. However, both gynogenetic and sexual forms of C. auratus complex showed comparable growth performance.…”

“…A parasitological survey of a mixed population of Prussian carp showed the weakened immunocompetence of triploid gynogenetic females (especially of the most common triploid major histocompatibility complex (MHC) genotype) measured by parasite load, i.e. the level of infection by gill monogenean parasites, when compared to that in diploid sexuals [ 27 ]. In addition, differential gene expression in fully-grown oocytes between gynogenetic and sexual forms of Prussian carp was recorded, suggesting different responses and behaviours of the oocytes towards sperm [ 28 ].…”