This blog post is provided by Dr Upama Aich and tells the #StoryBehindThePaper for the paper “Long-term effects of widespread pharmaceutical pollution on trade-offs between behavioural, life-history, and reproductive traits in fish“. The study, led by Dr Upama Aich from the Monash University School of Biological Sciences and Assistant Professor Giovanni Polverino from the University of Tuscia, was recently published in the Journal of Animal Ecology. Upama, Gio and colleagues studied the effects of Prozac on male guppies and found that low doses of fluoxetine had stronger negative effects on male guppies’ physiology and behaviour than high levels, disrupting their pace-of-life syndrome and potentially impacting reproductive success.
Have you ever wondered what happens to the medications we take once they leave our bodies? The drugs that help millions of people manage their mental health can have unintended consequences for aquatic life when they find their way into our waterways. Our recent study, published in the Journal of Animal Ecology, explores how chronic exposure to fluoxetine, a commonly used antidepressant, shapes the lives of male guppies (Poecilia reticulata) over multiple generations (Fig. 1).
Diving into the Study
Fluoxetine, also known as Prozac, is used in the treatment of depression and obsessive-compulsive disorder. It is one of the most commonly prescribed psychotherapeutic drugs worldwide and is found in many water systems due to its widespread use and incomplete removal during wastewater treatment. Using an indoor mesocosm system, we set out to understand how long-term exposure to this pharmaceutical (5 years, overlapping 15 generations) influences the life-history, behaviour, and reproductive traits of guppies. Guppies are often used in ecological studies due to their well-known biology, ease of care, and vibrant colouration in males (Fig. 2).
We studied male fish from three different treatment groups that were exposed to no fluoxetine, low fluoxetine, and high fluoxetine for five years across multiple generations.
Our study focused on understanding how fluoxetine exposure affects guppies’ life history and behavioural traits, particularly in relation to the pace-of-life syndrome (POLS)—a concept that links an organism’s life history traits with its behaviour and physiology (Fig. 3).
Key Findings
Our research uncovered several key insights:
1. Dose-Dependent Mean Effects on Behaviour and Physiology:
Low treatment of fluoxetine had stronger effects on individuals than the higher dose. Such dose-dependent relationships are well-reported in the literature and could result from several different mechanisms (see the discussion section for details). Specifically, we found that low fluoxetine exposure reduced male body condition and increased gonopodium size, indicating a potential trade-off in the investment of key traits that facilitate male mating success. Low concentrations also decreased sperm motility in males. As female guppies mate with many different males (polyandry), reduced sperm motility can lead to decreased fertilisation success in males under polluted conditions. (Video).
2. Individual-Level Responses:
Interestingly, fluoxetine exposure reduced within-individual variability in male activity and refuge use behaviour. A lower flexibility in behaviour can put a fish at an increased risk of perishing in a changing and increasingly polluted world. However, behavioural tactics that are more consistent over time may improve male efficiency in mating success, especially when their sperm quality is compromised.
3. Shifting Trait Correlations:
The most intriguing discovery was the reshaping of trait correlations—i.e., the pace-of-life syndrome. Fluoxetine exposure altered between-individual correlations in 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 between-individual correlations (e.g., activity and gonopodium size). Such shifts in POLS have the potential to impact the diversity of life strategies and their evolution in guppy populations (Fig. 4).
Broader Implications
The presence of pharmaceuticals like fluoxetine in aquatic systems is a growing environmental issue. The disruption of the pace-of-life syndrome by fluoxetine highlights the complex and far-reaching effects of pharmaceutical pollutants on aquatic ecosystems that were previously unknown. The observed reduction in sperm motility and behavioural flexibility in guppies could have cascading effects throughout the food web, potentially leading to broader ecological consequences. Future research should delve deeper into the long-term evolutionary consequences of chronic pollutant exposure and explore mitigation strategies to safeguard aquatic biodiversity (Fig. 5).
Read the paper
Read the full paper here: Aich, U., Polverino, G., YazdanParast, F., Melo, G. C., Tan, H., Howells, J., Nosrati, R., &Wong, B. B. M. (2024). Long-term effects of widespreadpharmaceutical pollution on trade-offs between behavioural,life-history and reproductive traits in fish. Journal of AnimalEcology, 00, 1–16. https://doi.org/10.1111/1365-2656.14152
Animal Ecology in Focus 