Monogeneans in intergeneric hybrids of leuciscid fish: Is parasite infection driven by hybrid heterosis, genetic incompatibilities, or host-parasite coevolutionary interactions?

Abstract

Background: Several hypotheses have been proposed to explain parasite infection in parental species and their hybrids. Hybrid heterosis is generally applied to explain the advantage for F1 generations of hybrids exhibiting a lower level of parasite infection when compared to parental species. Post-F1 generations often suffer from genetic incompatibilities potentially reflected in the higher level of parasite infection when compared to parental species. However, the presence of specific parasites in an associated host is also limited by close coevolutionary genetic host-parasite associations. This study focused on monogenean parasites closely associated with two leuciscid fish species-common bream and roach-with the aim of comparing the level of monogenean infection between parental species and hybrids representing two F1 generations with different mtDNA and two backcross generations with different cyto-nuclear compositions.

Results: Monogenean infection in F1 generations of hybrids was lower when compared to parental species, in line with the hybrid heterosis hypothesis. Monogenean infection in backcross generations exhibited similarities with the parental species whose genes contributed more to the backcross genotype. The distribution of monogeneans associated with one or the other parental species showed the same asymmetry with a higher proportion of roach-associated monogeneans in both F1 generations and backcross generation with roach in the paternal position. A higher proportion of common bream-associated monogeneans was found in backcross generation with common bream in the paternal position.

Conclusions: Our study indicated that cyto-nuclear incompatibilities in hybrids do not induce higher monogenean infection in backcross generations when compared to parental species. However, as backcross hybrids with a higher proportion of the genes of one parental taxon also exhibited high level of this parental taxon-associated parasites, host-parasite coevolutionary interactions seem to play an obvious role in determining the level of infection of host-specific monogeneans in hybrids.

Keywords: Freshwater fish; Genetic incompatibilities; Host specificity; Host-parasite coevolution; Hybrid heterosis; Hybrids; Monogeneans.