The benefits of coinfection: Prior exposure to trematodes decreases ranaviral disease risk in amphibians

Background/Question/Methods

Epidemiological research has traditionally focused on the interaction between a single host and pathogen, yet hosts in nature are typically infected with multiple pathogens. Moreover, there is growing evidence that coinfections can alter disease patterns underscoring the need for greater empirical attention. In particular, a central question concerns how temporal separation of infections affects the interaction between pathogens and disease outcomes. Using larval gray tree frogs (Hyla versicolor) as our model host, we explored the interaction between ranavirus (frog virus 3, FV3) and the trematode Echinostoma trivolvis. Our goal was to assess how temporal separation between ranavirus and trematode exposure influenced the infection success of each pathogen and host mortality. We conducted a 2 x 2 x 3 factorial experiment with two trematode exposure treatments (0 or 50 cercariae), two virus treatments (0 or 10⁶ plaque forming units [PFUs]), and three time points of virus addition (simultaneous with Echinostoma treatments, 5 days after exposure to Echinostoma, or 10 days after exposure to Echinostoma). We predicted that simultaneous exposure to Echinostoma and ranavirus would have minimal effects on ranavirus infection but as the temporal separation between exposures increased we predicted ranavirus infection to increase along with host mortality. 

Results/Conclusions

Trematode infection rate was similar across all treatments, with an average infection rate of 40%. Thus, ranavirus infection had no influence on trematode infection. However, ranavirus infection prevalence and load were dependent on whether trematodes were present and when trematode exposure occurred. Compared to treatments without trematodes, we observed a 13% decrease in ranavirus infection prevalence and a 32% decrease in viral loads in trematode treatments. Moreover, ranavirus prevalence and viral load both decreased by ~50% as the temporal separation between exposures increased. These results translated to reduced mortality for the hosts; mortality was 55% lower for tadpoles exposed to trematodes 10 days before virus addition compared to tadpoles simultaneously infected with both pathogens. These results suggest that prior exposure to trematodes can decrease susceptibility to ranavirus infection and mortality. While more research is necessary, trematode exposure may provide cross-reactive immunity to ranaviruses. Additionally, we demonstrate that priority effects may play an important role in structuring pathogen communities within hosts and play a role in disease outcomes. Given that environmental variation can lead to variation in pathogen exposure and the composition of pathogen communities, there is a need for more coinfection research that examines priority effects.