Is gynogenetic reproduction in gibel carp (Carassius gibelio) a major trait responsible for invasiveness?

Fuad, Mehedi Hasan; Vetešník, Lukáš; Šimková, Andrea Vetešníková

doi:10.25225/jvb.21049

Cited by 21 publications

(9 citation statements)

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“…The genomic incorporation of sperm-derived fragments from an exogenous species, which was reported in gynogenetic C. gibelio from aquaculture in China (27), can also favor genetic diversity in asexual lines. In C. gibelio, the combination of the advantages of gynogenetic reproduction, which allows for faster population growth (23,23), and sexual reproduction, which provides higher resistance to parasites and higher immune gene variability (29), higher aerobic performance and better immunity (123), lower metabolic rate, and lower energy intake (124), might explain the coexistence of sexual and asexual forms, and the high adaptive abilities of this species and its invasiveness in European water ecosystems. Figure 6…”

Section: Discussionmentioning

confidence: 99%

“…The gibel carp (Carassius gibelio), also known as Prussian carp, considered as a subspecies of C. auratus or a member of the C. auratus complex, is a cyprinid sh originating from eastern Eurasia that became invasive in European freshwater ecosystems during the 20th century, due to its high ecological tolerance and adaptive abilities (22,23). Gibel carp exhibits a dual mode of reproduction -sexual reproduction and gynogenesis.…”

Section: Introductionmentioning

confidence: 99%

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Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction

Jacques,

Tichopád,

Demko

et al. 2024

Preprint

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction

Jacques,

Tichopád,

Demko

et al. 2024

Preprint

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“…Wetlands such as the Ðurica pond, part of Marina, and Dubovac are ideal habitats for strictly protected species, the crucian carp Carassius carassius and the tench Tinca tinca, which are among the rarest fish species of the Danube ecosystem, not only because of the current limitation of their habitat distribution, but also because of the high abundances of allochthonous and, according to the characteristics of population biology, invasive species such as Prussian carp (Carassius gibelio) and bullhead, both brownhead and bullhead (Ameiurus nebulosus and Ameiurus melas) [29].…”

Section: Discussionmentioning

confidence: 99%

Status and Perspectives of the Ichthyofauna of the Labudovo okno Ramsar Site: An Analysis of 14 Years of Data

Nikolić

Nedić²,

Jurlina

et al. 2023

Sustainability

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Over the last 14 years, ichthyological and ecological parameters have been monitored in the Labudovo okno Ramsar site. This area is important for its biodiversity as it is home to many rare and endangered plants and animal species. A total of 3861 fish specimens were sampled and measured at six sampling sites four times during the sampling period. An analysis of biodiversity indexes, relative biomass (kg/ha), and relative annual production (kg/ha) was carried out to assess the effectiveness of existing conservation measures. The results obtained show a trend decline in biodiversity, relative biomass, and relative annual production. This indicates a biodiversity conservation problem that should be addressed through other mechanisms in addition to the principles of the Ramsar Convention.

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“…Its exceptional diversity of skills represents possible biological phenomena such as the presence of three ploidy levels—tetraploid, hexaploid, and octoploid ( Kalous and Knytl 2011 ; Xiao et al 2011 ; Knytl et al 2022 ). The alternation of sexual and asexual (gynogenetic) mode of reproduction ( Cherfas 1966 ; Przybył et al 2020 ; Fuad et al 2021 ) gives Carassius a competitive advantage in the rate of spatial expansion of asexuals. In addition, sexual reproduction should ensure higher resistance to parasites than gynogenesis due to recombination processes ( Hakoyama et al 2001 ).…”

Section: Introductionmentioning

confidence: 99%

Cytogenetic Analysis of the Fish Genus Carassius Indicates Divergence, Fission, and Segmental Duplication as Drivers of Tandem Repeat and Microchromosome Evolution

Fornaini,

Černohorská,

do Vale Martins

et al. 2024

Genome Biology and Evolution

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Fishes of the genus Carassius are useful experimental vertebrate models for study of evolutionary biology and cytogenetics. Carassius demonstrates diverse biological characteristics, such as variation in ploidy levels and chromosome numbers, and presence of microchromosomes. Carassius polyploids with ≥ 150 chromosomes have microchromosomes, but their origin, especially in European populations, is unknown. We used cytogenetics to study evolution of tandem repeats (U1 and U2 small nuclear DNAs and H3 histone) and microchromosomes in Carassius from the Czech Republic. We tested the hypotheses whether the number of tandem repeats was affected by polyploidization or divergence between species and what mechanism drives evolution of microchromosomes. Tandem repeats were found in tetraploid and hexaploid C. gibelio, tetraploid C. auratus and C. carassius in conserved numbers, with the exception of U1 snDNA in C. auratus. This conservation indicates reduction and/or loss in the number of copies per locus that may have occurred by divergence rather than polyploidization. To study evolution of microchromosomes, we used the whole microchromosome painting probe from hexaploid C. gibelio and hybridized it to tetraploid and hexaploid C. gibelio, tetraploid C. auratus and C. carassius. Our results revealed variation in the number of microchromosomes in hexaploids, indicating that the evolution of Carassius karyotype is governed by macrochromosome fissions followed by segmental duplication in pericentromeric areas. This is a potential mechanism responsible for the presence of microchromosomes in Carassius hexaploids. Differential efficacy of one or both of these mechanisms in different tetraploids could ensure variability in chromosome number in polyploids in general.

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Is gynogenetic reproduction in gibel carp (Carassius gibelio) a major trait responsible for invasiveness?

Abstract: BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses.

Cited by 21 publications

References 97 publications

Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction

Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction

Status and Perspectives of the Ichthyofauna of the Labudovo okno Ramsar Site: An Analysis of 14 Years of Data

Cytogenetic Analysis of the Fish Genus Carassius Indicates Divergence, Fission, and Segmental Duplication as Drivers of Tandem Repeat and Microchromosome Evolution

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