Rapid evolution in response to warming does not affect the toxicity of a pollutant: Insights from experimental evolution in heated mesocosms

Abstract

While human-induced stressors such as warming and pollutants may co-occur and interact, evolutionary studies typically focus on single stressors. Rapid thermal evolution may help organisms better deal with warming, yet it remains an open question whether thermal evolution changes the toxicity of pollutants under warming. We investigated the effects of exposure to a novel pollutant (zinc oxide nanoparticles, nZnO) and 4°C warming (20°C vs. 24°C) on key life history and physiological traits of the water flea Daphnia magna, a keystone species in aquatic ecosystems. To address the role of thermal evolution, we compared these effects between clones from an experimental evolution trial where animals were kept for two years in outdoor mesocosms at ambient temperatures or ambient +4°C. The nZnO was more toxic at 20°C than at 24°C: only at 20°C, it caused reductions in early fecundity, intrinsic growth rate and metabolic activity. This was due to a higher accumulated zinc burden at 20°C than at 24°C, which was associated with an upregulation of a metallothionein gene at 20°C but not at 24°C. Clones from the heated mesocosms better dealt with warming than clones from the ambient mesocosms, indicating rapid thermal evolution. Notably, rapid thermal evolution did not change the toxicity of nZnO, neither at 20°C nor at 24°C, suggesting no pleiotropy or metabolic trade-offs were at work under the current experimental design. Evaluating whether thermal evolution influences the toxicity of pollutants is important for ecological risk assessment. It provides key information to extrapolate laboratory-derived toxicity estimates of pollutants both in space to warmer regions and in time under future global warming scenarios. In general, studying how the evolution of tolerance to one anthropogenic stressor influence tolerance to other anthropogenic stressors should get more attention in a rapidly changing world where animals increasingly face combinations of stressors.