Long-term effects of widespread pharmaceutical pollution on trade-offs between behavioural, life-history, and reproductive traits in fish

In our rapidly changing world, understanding how species respond to shifting conditions is of paramount importance. Pharmaceutical pollutants—ubiquitous in aquatic ecosystems globally—are a major ecological concern. Yet their impacts on animal behaviour, life history, and reproductive investment remain poorly understood, especially in the context of intraspecific variation in ecologically important traits that facilitate species’ adaptive capacities. We test whether a widespread pharmaceutical pollutant, fluoxetine (Prozac), disrupts the trade-off between individual-level (co)variation in behavioural, life history, and reproductive traits of wildlife. To do so, we exposed the progeny of wild-caught guppies (<i>Poecilia reticulata</i>) to environmentally realistic levels of fluoxetine for five years, across multiple generations. We used 12 independent laboratory populations and repeatedly quantified activity and risk-taking behaviour of male guppies, capturing both mean behaviours and variation within and among individuals across exposure treatments. We also measured key life-history traits (body condition, colouration, and gonopodium size) and assessed post-copulatory sperm traits (sperm vitality, number, and velocity) that are known to be under strong sexual selection in polyandrous species. Intraspecific (co)variation of these traits was analysed using a comprehensive, multivariate statistical approach. At the population level, fluoxetine had a dose-specific (mean) effect on the life history and sperm traits of guppies: pollutant exposure improved male body condition and increased gonopodium size, but reduced sperm velocity. At the individual level, fluoxetine reduced the behavioural plasticity of guppies by eroding their within-individual variation in both activity and risk-taking behaviour. Fluoxetine also altered among-individual correlations between pace-of-life syndrome traits: it triggered the emergence of correlations between behavioural and life-history traits (e.g., activity and body condition) and between life-history and sperm traits (e.g., gonopodium size and sperm vitality), but collapsed other among-individual correlations (e.g.,  activity and gonopodium size). Our results reveal that chronic exposure to global pollutants can affect phenotypic traits at both population and individual levels, and even alter individual-level correlations among such traits in a dose-specific manner. Our work highlights the need to integrate individual-level analyses and test behaviour in association with life-history and reproductive traits to fully understand how animals adjust to human-induced environmental change.