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Heterosis versus breakdown in cyprinid hybrids associated with SVCV infection revealed by transcriptome profile analysis of head kidney

ABSTRACT: Whilst the hybrids of F1 generations usually experience heterosis for fitness-related traits (including the resistance to parasites), post-F1 generations, due to Dobzhansky–Muller genetic incompatibilities, express numerous disadvantageous traits (including susceptibility to parasites). Genetic disruption in hybrids may also result from the broken system of cyto-nuclear coadaptation. Maternal backcrosses (each parent having with the same mtDNA of parents) and paternal backcrosses (each parent having with different mtDNA of parents) have the same nuclear genetic compositions, but differ in cytoplasmic genetic elements, affecting their viability and survival. Spring viraemia of the carp virus (SVCV), a disease with a serious economic impact in aquacultures, affects almost exclusively cyprinids, primarily common carp, and causes high mortality, whilst gibel carp is a less susceptible species. Our study was focused on the transcriptome profile analysis of head kidney to reveal differential gene expression in highly susceptible common carp, weakly susceptible gibel carp, and hybrid lines, hypothetizing that the patterns of differential gene expression will reflect hybrid heterosis in F1 generations and hybrid breakdown in backcrosses and F2 generations. We expected the differences in differential gene expression between maternal and paternal backcrosses to be in line with the hypothesis of broken cyto-nuclear coadaptation.

ORGANISM(S): Carassius gibelio Carassius gibelio x Cyprinus carpio 'xingguonensis' Cyprinus carpio

PROVIDER: GSE240031 | GEO | 2023/09/12

REPOSITORIES: GEO

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Project description: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. In the present study, 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. 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. 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.

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Heterosis versus breakdown in cyprinid hybrids associated with SVCV infection revealed by transcriptome profile analysis of head kidney

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