Population-level variation in infection outcomes not influenced by pesticide exposure in larval wood frogs (Rana sylvatica)

There is increasing evidence that populations of non-target wildlife species can evolve tolerance to pesticides. As ecosystems become increasingly exposed to chemical contaminants globally, it is important to consider not only the immediate consequences of contaminant exposure but also the potential costs associated with evolved responses. Theory predicts there may be trade-offs, including increased susceptibility to parasites, associated with evolved pesticide tolerance. It remains unclear, however, how environmental context (i.e. presence/absence of pesticides in the contemporary environment) interacts with evolved pesticide tolerance levels to influence infection outcomes. Several studies have demonstrated that wood frog (Rana sylvatica) populations close to agriculture, where frequent exposure to pesticides is more likely, show higher baseline tolerance to pesticides than do populations far from agriculture. Using eight wood frog populations from across an agricultural gradient, we explored patterns of variation in susceptibility to parasites associated with a population's proximity to agriculture (a proxy for pesticide tolerance), and how these patterns are influenced by experimental exposure of tadpoles to the insecticide carbaryl. We did this by first placing tadpoles in an environment containing the pesticide carbaryl (1 mg/L) or in a pesticide-free control environment for 5 days, and subsequently exposing tadpoles to trematodes (Echinostoma trivolvis) or ranavirus (frog virus 3). We found that variation in trematode susceptibility was related to the tadpole populations' proximity to agriculture. Individuals from populations located close to agriculture were modestly more susceptible to trematode infections than individuals from populations farther from agriculture. Ranavirus susceptibility was not associated with proximity to agriculture. Surprisingly, exposure to carbaryl increased the survival rates of tadpoles infected with ranavirus. There were no other significant effects of carbaryl exposure on the measured disease outcomes. This study provides evidence for a potential trade-off between trematode resistance and putative pesticide tolerance. We show that host populations can vary significantly in their susceptibility to pathogens, but that pesticide exposure does not always increase parasite susceptibility or uniformly exacerbate disease outcomes. Further research is needed to determine how genetic variation among populations impact susceptibility to parasites, and if these patterns of susceptibility are consistent across space and time.

Automated summary

Evidence suggests that populations of non-target wildlife species can develop tolerance to pesticides, with those closer to agriculture showing higher baseline tolerance. Exposure to pesticides may affect susceptibility to parasites in wood frog populations, but does not consistently increase parasite susceptibility or worsen disease outcomes. Further research is needed to understand how genetic variation impacts susceptibility to parasites and if these patterns remain consistent over time and space.