Explaining interspecific variation in host infection and disease: Experimental evidence that immunosuppression increases trematode infection success in amphibian hosts

Background/Question/Methods

Within natural communities, hosts exhibit tremendous variation in patterns of infection and pathology. While some of these effects can be explained through differences in behavior, exposure, and developmental phenology, the relative contributions of these factors in relation to immune function are rarely quantified. In amphibians, the trematode Ribeiroia ondatrae causes debilitating malformations and mortality in a range of host species. However, individual host species vary considerably in their susceptibility to infection. For instance, Hyla versicolor are largely resistant to Ribeiroia infection even relative to other hylids, yet the source of this resistance remains unknown. We tested the role of antimicrobial peptides (AMPs) and corticosterone, an immunosuppressant, in explaining interspecific variation in short- and long-term infections within amphibians. To evaluate the role AMPs, we (a) extracted AMPs from larval P. regilla and H. versicolor and tested their effects on Ribeiroia cercariae over 24-hours and (b) exposed P. regilla and H. versicolor to Ribeiroia using hosts that were either un-manipulated, AMP deficient, or had the other species’ AMPs added. To evaluate the effects of immunosuppression, we treated H. versicolor tadpoles with either corticosterone, ethanol (vehicle control), or nothing (blank control) and exposed them to 30 Ribeiroia, 30 Echinostoma, and 30 Alaria cercariae. 

Results/Conclusions

Our results didn’t indicate a significant role of AMPs in controlling trematode responses. Cercarial survival was unaffected by exposure to amphibian AMPs, and there were no significant differences in Ribeiroia infection intensity among unmanipulated, AMP deficient, and foreign AMP treated tadpoles for both H. versicolor and P. regilla. At 4 days post-exposure, we found that tadpoles treated with corticosterone were infected with 62 times more Ribeiroia, 2.4 times more Echinostoma, and 1.9 times more Alaria than control tadpoles. Treatment with ethanol as a vehicle control didn’t affect parasite infectivity or persistance. Ten days after discontinuing corticosterone, tadpoles in the immunosuppressed treatment had reduced infection intensities of all three parasites. Compared to 4 days post-exposure, Ribeiroia infection was reduced to 6%, Echinosotma infection was reduced to 37%, and Alaria infection was reduced to 44%. Control tadpoles also exhibited a decrease in infection from four to fourteen days post-exposure, likely reflecting parasite mortality from host immunity. Together, these results suggest that, although AMPs aren’t responsible, elements of host immunity play an important role in parasite infectivity and subsequent persistence within infected hosts and that variation in infection among host and parasite species can be explained, in part, by variation in immune activity.