Transcriptome Profile Analyses of Head Kidney in Roach (Rutilus rutilus), Common Bream (Abramis brama) and Their Hybrids: Does Infection by Monogenean Parasites in Freshwater Fish Reveal Differences in Fish Vigour among Parental Species and Their Hybrids?

SIMPLE SUMMARY: Interspecific hybrids of F1 generations have frequently been characterized by high vigour resulting from heterosis advantage. In contrast, post-F1 generations are expected to express hybrid breakdown, i.e., they suffer from low viability and survival, reproductive abnormalities or sterility and limited ecological performance. Resistance or susceptibility to parasites is one of the measures reflecting hybrid vigour. The present study aimed to analyse the experimental infection of the blood-feeding generalist parasite Paradiplozoon homoion (Monogenea) in two target fish species, Abramis brama and Rutilus rutilus, and their reciprocal F1 hybrids and backcross hybrids, and to reveal potential parasite-induced changes in their transcriptome profiles of head kidney. We hypothesized various effects of hybridization in terms of parasitism in F1 hybrids and backcross hybrids reflected by differential gene expression. The number of differentially expressed genes (DEGs) differed between fish lines with a lower number of DEGs in F1 hybrids and a higher number in backcross hybrids when compared to the parental lines, A. brama and R. rutilus. Backcross hybrids were more infected than F1 hybrids and parental lines. DEG analyses revealed the role of heme binding, erythrocyte differentiation and immunity-related processes in fish after infection by blood-feeding P. homoion. Using GO and KEGG analyses, we revealed the similarity in DEGs between two backcross generations of hybrids. This finding may indicate a potential consequence of hybrid breakdown in backcross generations. Gene expression in less parasitized F1 hybrids is in line of hybrid advantage. ABSTRACT: Hybrid generations usually face either a heterosis advantage or a breakdown, that can be expressed by the level of parasite infection in hybrid hosts. Hybrids are less infected by parasites than parental species (especially F1 generations) or more infected than parental species (especially post-F1 generations). We performed the experiment with blood-feeding gill parasite Paradiplozoon homoion (Monogenea) infecting leuciscid species, Abramis brama and Rutilus rutilus, their F1 generation and two backcross generations. Backcross generations tended to be more parasitized than parental lines and the F1 generation. The number of differentially expressed genes (DEGs) was lower in F1 hybrids and higher in backcross hybrids when compared to each of the parental lines. The main groups of DEGs were shared among lines; however, A. brama and R. rutilus differed in some of the top gene ontology (GO) terms. DEG analyses revealed the role of heme binding and erythrocyte differentiation after infection by blood-feeding P. homoion. Two backcross generations shared some of the top GO terms, representing mostly downregulated genes associated with P. homoion infection. KEGG analysis revealed the importance of disease-associated pathways; the majority of them were shared by two backcross generations. Our study revealed the most pronounced DEGs associated with blood-feeding monogeneans in backcross hybrids, potentially (but not exclusively) explainable by hybrid breakdown. The lower DEGs reported in F1 hybrids being less parasitized than backcross hybrids is in line with the hybrid advantage.