Competent Non-Native Alternative Host Reduces Infection Success in a Generalist Parasite

Successful parasite proliferation depends on eco-evolutionarily stable host-parasite relationships, which may be disrupted by the introduction of non-native alternative hosts, particularly in the case of the generalist parasites adapted to multiple host species. Here, we experimentally analysed how the addition of a non-native alternative host affects the infection success of a larval generalist trematode, Diplostomum pseudospathaceum. We assessed parasite abundance, the proportion of successfully established metacercariae, and host-dependent parasite growth in the principal (Abramis brama), the native alternative (Rutilus rutilus), and the non-native alternative (Lepomis gibbosus) fish intermediate hosts. Across all experiments, A. brama showed the highest susceptibility to D. pseudospathaceum, with significantly lower abundances in both alternative hosts. This supports the view that evolutionary compatibility and host-parasite coadaptation in generalists play a more decisive role in shaping infection patterns than ecological factors such as host abundance or encounter rates. Multi-host experiments revealed a significant reduction in the proportion of successfully established metacercariae, particularly in combinations of native hosts with non-native L. gibbosus, indicating a dilution effect. Moreover, L. gibbosus exhibited a pronounced response to infection, developing stronger cataract than native hosts. Cataract formation was also more likely at lower infection intensities, indicating a lower threshold for pathology in the non-native host without a shared evolutionary history with the parasite, compared to long-term coexisting hosts. Metacercariae differed subtly yet significantly in size and organ dimensions among host species, demonstrating that host identity can affect larval morphology. Overall, our results demonstrate that the presence of alternative hosts, especially the non-native ones, can reduce parasite transmission through encounter dilution and suboptimal infection, even when those hosts are susceptible, confirming that dilution effects are not restricted to non-competent or resistant hosts.