Insights into the Influence of Natural Retinoic Acids on Imposex Induction in Female Marine Gastropods in the Coastal Environment

Conventionally, development of imposex, i.e., superimposition of male sexual characteristics on females, in marine neogastropods has been solely linked to exposure to synthetic organotin compounds, such as triphenyltin (TPT), in the marine environment. Here, our experimental results show that marine cyanobacteria can produce retinoic acids (RAs) and their oxidative metabolites 4-oxo-RAs, and the most commonly distributed RA, i.e., all-trans-RA, can also trigger expression of genes related to imposex in female whelks Reishia clavigera after chronic exposure of 60 days. Both estimated concentrations of TPT and RAs and 4-oxo-RAs in seawater are positively associated with the Vas Deferens Sequence Index (VDSI) in female whelks collected from various sites along the coast of Hong Kong; the concentration of TPT explains 28% of the total variation of VDSI, while the total concentrations of RAs and 4-oxo-RAs contributed to 14% of the variation based on separate regression analyses. Our discoveries have implications on the cause and magnitude of imposex in marine neogastropods, calling for more research in ecotoxicology of natural RAs and 4-oxo-RAs in the marine environment in the future.