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Reproduction-associated and sex determining genes expressed differently in testes of genotypic and temperature-induced males of gibel carp (Carassius gibelio): the molecular mechanisms underlying the reproductive plasticity and invasiveness

ABSTRACT: Sex in vertebrates is commonly determined by genotype and in some cases by environmental conditions, such as temperature. A few vertebrate species display intermediate conditions of sex determination, combining sex chromosomes with an effect of temperature. This phenomenon is known for the gibel carp (Carassius gibelio), an invasive cyprinid fish species, whose abilities to adapt and colonize new environments is linked with the combination of sexual and asexual reproduction. In this study, the gonad transcriptomes were compared between genotypic males and temperature-induced males of C. gibelio. We specifically focused on the meiosis-related and reproduction-associated genes. Many genes and pathways of cell cycle control and meiosis, male differentiation and spermatogenesis were common to genotypic and temperature-induced males of gibel carp. However, the underrepresentation of several GO terms and KEGG pathways related to reproduction and spermatogenesis in genotypic males suggests lower reproductive abilities of temperature-induced males. Our study highlights the differential transcription regulation of key genes related to male sex differentiation, steroid hormone regulation, meiosis, spermatogenesis and sperm-egg interaction including the genes associated with sperm fertilization, motility and sperm flagellum function. Especially, induced males strongly overexpressed hsd17b2 and slightly overexpressed the meiotic gene mnd1, while genotypic males overexpressed sox8a and cyp19a1a, as well as the crucial fertilization gene izumo. These findings contribute to the understanding of the molecular mechanisms underlying the reproductive plasticity and invasiveness of C. gibelio in Europe. Our study highlighs the role of males, whose appearance was crucial for the transition from asexual to sexual reproduction in this species. Our findings contribute to the understanding of the molecular mechanisms underlying the reproductive plasticity and invasiveness of C. gibelio in Europe.

ORGANISM(S): Carassius gibelio

PROVIDER: GSE285878 | GEO | 2025/12/10

REPOSITORIES: GEO

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Project description: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, allow for their stable coexistence, integrating the evolutionary and ecological advantages and disadvantages of the two reproductive forms. 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.

Project description:Background The Pacific oyster Crassostrea gigas (Mollusca, Lophotrochozoa) is an alternative and irregular protandrous hermaphrodite. Little is known about the genetic and phenotypic bases of sex determinism in oysters, and little more about the molecular pathways regulating reproduction. We have recently developed and validated a microarray containing 31,918 oligomers (Dheilly et al., 2011) representing the oyster transcriptome. The application of this microarray to the study of mollusks gametogenesis should provide a better understanding of the key factors involved in sex differentiation and the regulation of oyster reproduction. Results Expression of the 31,918 ESTs was studied in gonads of oysters cultured along the French Atlantic coasts over a yearly reproductive cycle. Principal component analysis and hierarchical clustering first showed a significant divergence in gene expression patterns of males and females beginning when gonial mitosis started. Early expressed male-specific genes included bindin and female-specific genes included foxL2, a pancreatic lipase related protein, cd63 and vitellogenin. ANOVA analysis of the data further revealed 2482 genes differentially expressed during the course of males and/or females gametogenesis. The expression of 434 genes could be localized in either germ cells or somatic cells of the gonad by comparing the transcriptome of gonads to the transcriptomes of striped oocytes and somatic tissues. Analysis of the annotated genes revealed conserved molecular mechanisms between mollusks and mammals. Genes involved in chromatin condensation, DNA replication and repair, mitosis and meiosis regulation, transcription, translation and apoptosis were expressed in both male and female gonads. Additional lists of genes more specifically involved in either spermatogenesis (meiotic phase, in spermatozoids and mature sperm formation and in flagella structure and movement) or oogenesis (female sex differentiation, transcriptional regulation, cell cycle regulation and oocytes maturation) were also generated. Conclusions Our study provides novel insight into spermatogenesis and oogenesis in an alternative hermaphrodite bivalve, the Pacific oyster C. gigas. We identified genes opening new perspectives for functional studies of the signaling pathways implicated in gonad differentiation and development.

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Reproduction-associated and sex determining genes expressed differently in testes of genotypic and temperature-induced males of gibel carp (Carassius gibelio): the molecular mechanisms underlying the reproductive plasticity and invasiveness

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