Evolved pesticide tolerance influences susceptibility to parasites in amphibians

Abstract

Because ecosystems throughout the globe are contaminated with pesticides, there is a need to understand how natural populations cope with pesticides and the implications for ecological interactions. From an evolutionary perspective, there is evidence that pesticide tolerance can be achieved via two mechanisms: selection for constitutive tolerance over multiple generations or by inducing tolerance within a single generation via phenotypic plasticity. While both mechanisms can allow organisms to persist in contaminated environments, they might result in different performance trade‐offs including population susceptibility to parasites. We have identified 15 wood frog populations that exist along a gradient from close to agriculture and high, constitutive pesticide tolerance to far from agriculture and inducible pesticide tolerance. Using these populations, we investigated the relationship between evolutionary responses to the common insecticide carbaryl and host susceptibility to the trematode Echinoparyphium lineage 3 and ranavirus using laboratory exposure assays. For Echinoparyphium, we discovered that wood frog populations living closer to agriculture with high, constitutive tolerance experienced lower loads than populations living far from agriculture with inducible pesticide tolerance. For ranavirus, we found no relationship between the mechanism of evolved pesticide tolerance and survival, but populations living closer to agriculture with high, constitutive tolerance experienced higher viral loads than populations far from agriculture with inducible tolerance. Land use and mechanisms of evolved pesticide tolerance were associated with susceptibility to parasites, but the direction of the relationship is dependent on the type of parasite, underscoring the complexity between land use and disease outcomes. Collectively, our results demonstrate that evolved pesticide tolerance can indirectly influence host–parasite interactions and underscores the importance of including evolutionary processes in ecotoxicological studies.

Evaluating the fitness consequences of plasticity in tolerance to pesticides

“…These results corroborate previous studies demonstrating the presence of phenotypic costs of tolerance, such as reduced fecundity or survival of tolerant individuals in pesticide‐free environments (Baucom & Mauricio, 2004; Semlitsch et al, 2000). Beyond life history trade‐offs (e.g., survival and reproduction), high tolerance to pesticides has been linked with reduced tolerance to biotic stressors, such as parasites (Hua et al, 2017; Jansen, Stoks, Coors, Doorslaer, & Meester, 2011). Additionally, these findings are coherent with observations from Hua et al (2015), where high plasticity in tolerance was most common in environments where pesticide exposure was likely infrequent or absent (i.e., far from agriculture).…”

Evolutionary toxicology: Toward a unified understanding of life's response to toxic chemicals

“…However, the authors also show that adaptation to a pesticide can bear costs, as indicated by increased viral loads following exposure to ranavirus. This work from Hua et al (2017) highlights the need to consider multiple stressors in evolutionary ecotoxicological inquiry and reminds us of the value of studying nontarget species in agricultural contexts, where most of our knowledge about evolution has been limited largely to studies of pest species. Another important takeaway from Hua et al (2017) is that community context matters when assessing the evolutionary impacts of contaminants on a given organism, a point seldom considered in community ecotoxicology.…”

“…Attempting to understand this capacity of evolution is a recurrent theme in the papers appearing in this special issue (see especially Whitehead et al 2017). Our ability to gain this understanding will surely improve as we broaden our assessment of evolutionary toxicology beyond the scope of pesticide resistance, and focus on increasingly diverse contexts where nontarget organisms are impacted by the use and distribution of toxic chemicals in the environment (e.g., Hua et al 2017;Whitehead, Clark, Reid, Hahn, & Nacci, et al 2017). Indeed, numerous observations of phenotypic and molecular changes have now been described in wild populations exposed to industrial age chemicals.…”

“…In Hua et al (2017), recently evolved pesticide tolerance in an amphibian is shown to influence its susceptibility to parasites.…”

“…Thus, Hua et al (2017) bring a much needed community perspective to evolutionary toxicology. This special issue also provides insights into how the application of evolutionary principles in ecotoxicology can strengthen both predictions and conclusions.…”