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Introduction: Parasite-mediated selection is considered one of the potential mechanisms contributing to the coexistence of asexual-sexual complexes. Gibel carp (Carassius gibelio), an invasive fish species in Europe, often forms populations composed of gynogenetic and sexual specimens. Methods: The experimental infection was induced in gynogenetic and sexual gibel carp using eye-fluke Diplostomum pseudospathaceum (Trematoda), and the transcriptome profile of the spleen as a major immune organ in fish was analyzed to reveal the differentially expressed immunity-associated genes related to D. pseudospathaceum infection differing between gynogenetic and sexual gibel carp. Results: High parasite infection was found in gynogenetic fish when compared to genetically diverse sexuals. Although metacercariae of D. pseudospathaceum are situated in an immune-privileged organ, our results show that eye trematodes may induce a host immune response. We found differential gene expression induced by eye-fluke infection, with various impacts on gynogenetic and sexual hosts, documenting for the majority of DEGs upregulation in sexuals, and downregulation in asexuals. Differences in gene regulation between gynogenetic and sexual gibel carp were evidenced in many immunity-associated genes. GO analyses revealed the importance of genes assigned to the GO terms: immune function, the Notch signaling pathway, MAP kinase tyrosine/threonine/phosphatase activity, and chemokine receptor activity. KEGG analyses revealed the importance of the genes involved in 12 immunity-associated pathways - specifically, FoxO signaling, adipocytokine signaling, TGF-beta signaling, apoptosis, Notch signaling, C-type lectin receptor signaling, efferocytosis, intestinal immune network for IgA production, insulin signaling, virion - human immunodeficiency virus, Toll-like receptor signaling, and phosphatidylinositol signaling system. Discussion: Our study indicates the limited potential of asexual fish to cope with higher parasite infection (likely a loss of capacity to induce an effective immune response) and highlights the important role of molecular mechanisms associated with immunity for the coexistence of gynogenetic and sexual gibel carp, potentially contributing to its invasiveness. [ABSTRACT FROM AUTHOR]

The coexistence of sexual and asexual lineages is rarely documented in vertebrates. Various ecological and evolutionary mechanisms have been proposed to explain their stable coexistence. Gibel carp (Carassius gibelio), a highly invasive freshwater fish in Europe, is one such example of a sexual and asexual vertebrate, combining gynogenesis (sperm-dependent parthenogenesis) and sexual reproduction. In this study, we focused on vigour-related traits in gynogenetic and sexual forms of gibel carp coexisting in the same habitat, to reveal whether there is a link between parasite load and vigour-related traits reflecting the potential advantage of one reproductive form over another, which may eventually facilitate the obligatory coexistence of sperm-dependent gynogenetic females with sexual males. Using physiological parameters (indexes of somatic condition, energetic condition, and reproductive performance; glucose levels; and erythrocytes-related variables), diploid sexual males, diploid sexual females, and triploid gynogenetic females were found to be differentiated from one another. However, based on immune variables representing innate immunity, specific immunity, and index of immunocompetence, mostly sexual males were found to be weakly differentiated from both groups of females. We revealed different patterns of interactions between parasite abundance and immune variables between sexual and gynogenetic forms. Using parasite assemblage composition, different relationships between parasite assemblage and immunity or physiology in sexual males and sexual females were evidenced, potentially related to male reproduction biology. In contrast, gynogenetic females exhibited the advantage that parasite assemblage composition did not affect their immunity or physiology. Our study suggests that reproduction mode-associated costs of physiology and immunity may facilitate the coexistence of the asexual-sexual complex. We highlight that multiple ecological processes and evolutionary mechanisms contribute to the coexistence of asexual and sexual gibel carp. [ABSTRACT FROM AUTHOR]