Sex-specific effect of long-term fluoxetine exposure on inhibitory control in guppies (Poecilia reticulata)

Environmental contamination with psychoactive drugs poses a serious hazard to wildlife. However, the long-term effects of these bioactive pollutants on animal cognition, a key fitness-enhancing trait, remain unknown. For five years, we exposed multiple generations of guppies (Poecilia reticulata) to environmentally relevant concentrations (0 ng/L, 30 ng/L, 300 ng/L) of the common antidepressant and ubiquitous freshwater pollutant fluoxetine. We aimed to investigate potential transgenerational effects of fluoxetine by comparing an unexposed control population to two exposed populations 10 months after fluoxetine addition was halted. We used a well-established inhibitory control assay to quantify guppies’ cognition, and we measured a key personality trait, ‘boldness’. There was a sex-specific, non-monotonic effect of fluoxetine on cognition. Females in both fluoxetine-exposed groups had significantly lower inhibitory control than unexposed females. By contrast, fluoxetine-exposed males did not differ in their cognitive ability from control (i.e., unexposed) treatment males, but males from the high-concentration treatment had greater inhibitory control than those from the low-concentration treatment. Males from the high-concentration treatment were marginally bolder than those from the low-concentration treatment. Our results are the first evidence that long-term fluoxetine exposure affects inhibitory control in non-humans and highlight the importance of considering the cognitive and legacy impacts of psychoactive pollution on wildlife.