Making snails happy or not? – Evaluating the impact of antidepressant fluoxetine on the reproductive performance of a hermaphroditic freshwater snail species

Background

Fluoxetine, a commercial antidepressant, is leaking into aquatic environments. Since this compound is specifically designed to induce physiological and behavioural responses at low concentration, the impact on aquatic life is expected to be drastic. For instance, previous studies reported that external application of fluoxetine induces spawning in marine bivalves (Fong et al. 1998, Fong 1998). Thus, it is highly plausible that fluoxetine that is present in the aquatic environment affects the reproduction of molluscs. Interestingly, Fong et al. (1998) have received the Ig-Nobel award by making snails ‘happy’ with their research.

The great pond snail, Lymnaea stagnalis, provides fascinating research opportunities to evaluate the potential impacts of fluoxetine on the reproduction of aquatic life. First, this species is simultaneously hermaphroditic (i.e., male and female at the same time), like many other snails and various worms, for example. This relatively widespread reproductive system allows us to generalize the outcome of this study to other species. Second, possessing two sex functions in one body makes hermaphrodites potentially more vulnerable for induced changes in reproduction. That is, a change in one sex function could also affect other sex functions of an individual. Previous studies show that hermaphrodites change the resource allocation to male and female functions depending on their social conditions (sex allocation, Lorenzi et al. 2005; Ramm et al. 2019). Their flexibility in sex allocation could make them vulnerable for the effect of fluoxetine in the environment, since it may induce a shift in sex allocation irrespective of their social situation. Second, exposure of fluoxetine can have transgenerational effects in L. stagnalis. These snails alter the serotonin level in the uterus depending on the season in which they reproduce, in order to facilitate the adaptation of offspring for the environment (Ivashkin et al. 2015). Since fluoxetine is specifically aimed at altering the serotonin level, we can test if this compound in the environment influences the current generation, as well as future generations, of this species. Lastly, our extensive knowledge of the reproductive physiology and behaviour of L. stagnalis provides the opportunity to evaluate the impact of antidepressants in the wild.

Approach

– Exposing snails to fluoxetine (passive dosing)
– Behavioural assay (sex role choice)
– Development (investment on reproductive organs [male-, female-], embryo activity in the egg)
– Measuring reproductive performance (egg laying, sperm transfer, investment on reproductive organs)
– Life history traits (growth, maturation, survival, learning)
– Statistics

Keywords

Pharmaceutical pollution, reproductive physiology, neurotransmitter, serotonin behaviour, adaptation, sex allocation, hermaphrodites

Reference

Lorenzi MC, Sella G, Schleicherová D, Ramella L. 2005. Outcrossing hermaphroditic polychaete worms adjust their sex allocation to social conditions: Sex allocation in hermaphrodites. Journal of Evolutionary Biology 18: 1341–1347.

Ivashkin E, Khabarova MYu, Melnikova V, Nezlin LP, Kharchenko O, Voronezhskaya EE, Adameyko I. 2015. Serotonin Mediates Maternal Effects and Directs Developmental and Behavioral Changes in the Progeny of Snails. Cell Reports 12: 1144–1158.

Ramm SA, Lengerer B, Arbore R, Pjeta R, Wunderer J, Giannakara A, Berezikov E, Ladurner P, Schärer L. 2019. Sex allocation plasticity on a transcriptome scale: Socially sensitive gene expression in a simultaneous hermaphrodite. Molecular Ecology mec.15077.

Supervision

Dr. Joris M. Koene
E-mail: joris.koene@vu.nl

Dr. Yumi Nakadera
E-mail: y.nakadera@vu.nl

Prof.dr. Kees van Gestel
E-mail: kees.van.gestel@vu.nl

There is also the possibility to collaborate with Dr. Jessica Legradi (for neurotoxicity) and Prof.dr. Marja Lamoree/Prof.dr. Pim Leonards (for metabolomics).