Meeting a threat of the Anthropocene: Taste avoidance of metal ions by Drosophila

Abstract

The Anthropocene Epoch poses a critical challenge for organisms: they must cope with new threats at a rapid rate. These threats include toxic chemical compounds released into the environment by human activities. Here, we examine elevated concentrations of heavy metal ions as an example of anthropogenic stressors. We find that the fruit fly Drosophila avoids nine metal ions when present at elevated concentrations that the flies experienced rarely, if ever, until the Anthropocene. We characterize the avoidance of feeding and egg laying on metal ions, and we identify receptors, neurons, and taste organs that contribute to this avoidance. Different subsets of taste receptors, including members of both Ir (Ionotropic receptor) and Gr (Gustatory receptor) families contribute to the avoidance of different metal ions. We find that metal ions activate certain bitter-sensing neurons and inhibit sugar-sensing neurons. Some behavioral responses are mediated largely through neurons of the pharynx. Feeding avoidance remains stable over 10 generations of exposure to copper and zinc ions. Some responses to metal ions are conserved across diverse dipteran species, including the mosquito Aedes albopictus. Our results suggest mechanisms that may be essential to insects as they face challenges from environmental changes in the Anthropocene.