Molecular Logic and Evolution of Bitter Taste in Drosophila

Taste systems detect a vast diversity of toxins, which are perceived as bitter. When a species adapts to a new environment, its taste system must adapt to detect new death threats. We deleted each of six commonly expressed bitter gustatory receptors (Grs) from Drosophila melanogaster. Systematic analysis revealed that requirements for these Grs differed for the same tastant in different neurons and for different tastants in the same neuron. Responses to some tastants in some neurons required four Grs, including Gr39a. Deletions also produced increased or novel responses, supporting a model of Gr-Gr inhibitory interactions. Coexpression of four Grs conferred several bitter responses to a sugar neuron. We then examined bitter coding in three other Drosophila species. We found major evolutionary shifts. One shift depended on the concerted activity of seven Grs. This work shows how the complex logic of bitter coding provides the capacity to detect innumerable hazards and the flexibility to adapt to new ones.