Adaptive plastic responses to metal contamination in a multistress context: a field experiment in fish

Wild populations often differ in their tolerance to environmental stressors, but intraspecific variability is rarely taken into account in ecotoxicology. In addition, plastic responses to multiple stressors have rarely been investigated in realistic field conditions. In this study, we compared the responses to metal contamination of gudgeon populations (Gobio occitaniae) differing in their past chronic exposure to metal contamination, using a reciprocal transplant experiment and an immune challenge mimicking a parasite attack to test for potential effects of multiple stressors across biological levels. We measured fish survival and traits involved in metal bioaccumulation, oxidative stress, immunity, cell apoptosis, and energy management to decipher underpinning physiological mechanisms across biological levels (i.e., gene expression, cell, organism). Fish from the two replicate High Contamination sites had higher survival when transferred into contaminated sites, suggesting a local adaptation to the contaminated site, possibly explained by higher levels of detoxification and antioxidant capacity but with potential higher apoptosis costs compared to their naïve counterparts. We found no evidence of co- or maladaptation to the immune stressor, suggesting no specific costs to face pathogens. In the emerging field of evolutionary ecotoxicology, this study underlines the need to consider intraspecific variability to better understand the effects of pollution in heterogeneous populations.