A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship

Abstract

Contact chemosensation is required for several behaviors that promote insect survival. These include evasive behaviors such as suppression of feeding on repellent compounds, known as antifeedants, and inhibition of male-to-male courtship. However, the gustatory receptors (GRs) required for responding to nonvolatile avoidance chemicals are largely unknown. Exceptions include Drosophila GR66a and GR93a, which are required to prevent ingestion of caffeine, and GR32a, which is necessary for inhibiting male-to-male courtship. However, GR32a is dispensable for normal taste. Thus, distinct GRs may function in sensing avoidance pheromones and antifeedants. Here, we describe the requirements for GR33a, which is expressed widely in gustatory receptor neurons (GRNs) that respond to aversive chemicals. Gr33a mutant flies were impaired in avoiding all nonvolatile repellents tested, ranging from quinine to denatonium, lobeline, and caffeine. Gr33a mutant males also displayed increased male-to-male courtship, implying that it functioned in the detection of a repulsive male pheromone. In contrast to the broadly required olfactory receptor (OR) OR83b, which is essential for trafficking other ORs, GR66a and GR93a are localized normally in Gr33a mutant GRNs. Thus, rather than regulating GR trafficking, GR33a may be a coreceptor required for sensing all nonvolatile repulsive chemicals, including tastants and pheromones.