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.

• Keywords
• RNA seq, asexual and sexual reproduction, differential gene expression, fish, immunity-associated pathways, invasive species, parasites,
• MeSH
• Trematode Infections * veterinary   immunology   parasitology   MeSH
• Host-Parasite Interactions immunology   MeSH
• Carps parasitology   immunology   genetics   MeSH
• Fish Diseases * immunology   parasitology   MeSH
• Gene Expression Regulation MeSH
• Reproduction immunology   MeSH
• Gene Expression Profiling MeSH
• Transcriptome MeSH
• Trematoda * physiology   MeSH
• Introduced Species * MeSH
• Animals MeSH
• Check Tag
• Female MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH

Gibel carp (Carassius gibelio) is a cyprinid fish that originated in eastern Eurasia and is considered as invasive in European freshwater ecosystems. The populations of gibel carp in Europe are mostly composed of asexually reproducing triploid females (i.e., reproducing by gynogenesis) and sexually reproducing diploid females and males. Although some cases of coexisting sexual and asexual reproductive forms are known in vertebrates, the molecular mechanisms maintaining such coexistence are still in question. Both reproduction modes are supposed to exhibit evolutionary and ecological advantages and disadvantages. To better understand the coexistence of these two reproduction strategies, we performed transcriptome profile analysis of gonad tissues (ovaries) and studied the differentially expressed reproduction-associated genes in sexual and asexual females. We used high-throughput RNA sequencing to generate transcriptomic profiles of gonadal tissues of triploid asexual females and males, diploid sexual males and females of gibel carp, as well as diploid individuals from two closely-related species, C. auratus and Cyprinus carpio. Using SNP clustering, we showed the close similarity of C. gibelio and C. auratus with a basal position of C. carpio to both Carassius species. Using transcriptome profile analyses, we showed that many genes and pathways are involved in both gynogenetic and sexual reproduction in C. gibelio; however, we also found that 1500 genes, including 100 genes involved in cell cycle control, meiosis, oogenesis, embryogenesis, fertilization, steroid hormone signaling, and biosynthesis were differently expressed in the ovaries of asexual and sexual females. We suggest that the overall downregulation of reproduction-associated pathways in asexual females, and their maintenance in sexual ones, allows the populations of C. gibelio to combine the evolutionary and ecological advantages of the two reproductive strategies. However, we showed that many sexual-reproduction-related genes are maintained and expressed in asexual females, suggesting that gynogenetic gibel carp retains the genetic toolkits for meiosis and sexual reproduction. These findings shed new light on the evolution of this asexual and sexual complex.

• Keywords
• Asexual reproduction, Carassius gibelio, Differential expression analysis, Evolution of sexual reproduction, Gynogenesis, Meiosis, Oogenesis, Reproduction, Transcriptomics,
• MeSH
• Polymorphism, Single Nucleotide MeSH
• Carps * genetics   physiology   MeSH
• Reproduction, Asexual * genetics   MeSH
• Ovary metabolism   MeSH
• Reproduction * genetics   MeSH
• Gene Expression Profiling MeSH
• Transcriptome MeSH
• Animals MeSH
• Check Tag
• Male MeSH
• Female MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH

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.

• MeSH
• Cyprinidae * genetics   parasitology   MeSH
• Genetic Variation * MeSH
• Host-Parasite Interactions genetics   MeSH
• Fish Diseases * genetics   parasitology   MeSH
• Animals MeSH
• Check Tag
• Male MeSH
• Female MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH

BACKGROUND: Carassius auratus complex is an extraordinary species complex including the diploid and polyploid forms exhibiting asexual and sexual reproduction modes. The coexistence of both forms in the same habitats is currently reported. The stable coexistence of asexual and sexual forms assumes some disadvantages for asexuals that balance the costs of sex. In our study, we hypothesized and tested the differences in physiological (including heamatological and immunological), growth-related, condition-related, and fitness-related traits between gynogenetic females and sexuals. RESULTS: Our results revealed similar growth performance in gynogenetic females and sexuals measured by body size and weight, or expressed by condition factor. The energy allocation in reproduction measured by the relative size of gonads revealed no difference between gynogenetic and sexual females; in addition, both females in spawning expressed the same estradiol levels in blood plasma. We found a gender specific trade-off between investment in reproduction and immunocompetence (measured by the spleen-somatic index). Higher aerobic performance expressed by the heart index and higher oxygen-carrying capacity were found in sexual males, with increasing values before and during spawning. Our study evidenced significantly lower aerobic performance but higher oxygen-carrying capacity per erythrocyte in gynogenetic females when compared to sexuals. IgM production differed between gynogens and sexuals of C. auratus complex. CONCLUSIONS: Our study indicates that a similar amount of energy is invested by both gynogenetic and sexual females of C. auratus complex in reproductive behaviour. We suggest that lower aerobic performance in gynogens may represent their physiological disadvantage balancing the cost of sexual reproduction. A trade-off between the number of erythrocytes and the oxygen-carrying capacity per erythrocyte in sexual males and gynogenetic females may contribute to the coexistence of gynogenetic and sexual forms. In addition, the differences in specific immunity between gynogens and sexuals may also reduce the evolutionary disadvantage of sexual reproduction. In conclusion, we propose that several mechanisms contribute to the coexistence of the gynogenetic-sexual C. auratus complex.

• MeSH
• Biological Evolution MeSH
• Diploidy MeSH
• Ecosystem MeSH
• Goldfish anatomy & histology   genetics   immunology   physiology   MeSH
• Reproduction MeSH
• Triploidy MeSH
• Aquaculture economics   MeSH
• Animals MeSH
• Check Tag
• Male MeSH
• Female MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH