A gustatory receptor paralog controls rapid warmth avoidance in Drosophila

Behavioral responses to temperature are critical for survival, and animals from insects to humans show strong preferences for specific temperatures(1, 2). Preferred temperature selection promotes avoidance of adverse thermal environments in the short-term and maintenance of optimal body temperatures over the long-term(1, 2), but its molecular and cellular basis is largely unknown. Recent studies have yielded conflicting views of thermal preference in Drosophila, attributing importance to either internal(3) or peripheral(4) warmth sensors. Here we reconcile these views by demonstrating that thermal preference is not a singular response, but involves multiple systems relevant in different contexts. We previously found that the Transient Receptor Potential (TRP) channel TRPA1 acts internally to control the slowly developing preference response of flies exposed to a shallow thermal gradient(3). Here we find that the rapid response of flies exposed to a steep warmth gradient does not require TRPA1; rather, the Gustatory receptor (Gr) Gr28b(D) drives this behavior via peripheral thermosensors. Grs are a large gene family widely studied in insect gustation and olfaction and implicated in host-seeking by insect disease vectors(5–7), but not previously implicated in thermosensation. At the molecular level, Gr28b(D) misexpression confers thermosensitivity upon diverse cell types, suggesting it is a warmth sensor. These data reveal a new type of thermosensory molecule and uncover a functional distinction between peripheral and internal warmth sensors in this tiny ectotherm reminiscent of thermoregulatory systems in larger, endothermic animals(2). The use of multiple, distinct molecules to respond to a given temperature, as observed here, may facilitate independent tuning of an animal’s distinct thermosensory responses.