Evolution of tolerance to chlorpyrifos causes cross-tolerance to another organophosphate and a carbamate, but reduces tolerance to a neonicotinoid and a pharmaceutical.

Abstract Exposure to pesticides is a major stressor in freshwater ecosystems. While populations can evolve tolerance to pesticides and thereby ensure their persistence in contaminated environments, this may have important consequences for their sensitivity to other pollutants. Indeed, tolerance to one pollutant may both increase (as a cost of tolerance) or decrease (cross-tolerance) the sensitivity to other pollutants. Despite the increasing concern of pharmaceuticals in waterbodies, no patterns of pesticide-induced (cross-)tolerance have been studied. We conducted 48 h acute toxicity assays with a range of concentrations of different pollutants to determine how the evolution of tolerance to the insecticide chlorpyrifos affects the sensitivity to other pesticides and a pharmaceutical in the water flea Daphnia magna, a keystone zooplankton species in aquatic food webs. We capitalized on an experimental evolution trial with chlorpyrifos, hence could unambiguously identify any patterns in increased tolerance or sensitivity to the other pollutants as a direct result of the evolution of tolerance to chlorpyrifos. We found that evolution of tolerance to chlorpyrifos conferred cross-tolerance to another organophosphate, namely malathion (mean change in EC50,48h: factor 3.1), and to the carbamate carbaryl (factor 1.7), confirming that a shared mode of action favours the evolution of cross-tolerance. While the evolution of tolerance to chlorpyrifos did not affect the sensitivity to the pyrethroid esfenvalerate, it increased the sensitivity to the neonicotinoid imidacloprid as shown by the decrease in EC50,48h (factor 0.6). Notably, we demonstrated for the first time that the evolution of tolerance to a pesticide increased the sensitivity to a pharmaceutical, namely fluoxetine (decrease in EC50,48h with factor 0.7), thereby identifying an overlooked cost of tolerance to a pesticide. Given the increasing exposure to pesticides and pharmaceuticals, our results highlight that considering cross-tolerance and costs of tolerance is crucial in risk assessment of both pesticides and pharmaceuticals in aquatic ecosystems.