Carbon dioxide (CO 2 ) elicits different olfactory behaviors across species. In Drosophila, neurons that detect CO 2 are located in the antenna, form connections in a ventral glomerulus in the antennal lobe, and mediate avoidance. By contrast, in the mosquito these neurons are in the maxillary palps (MPs), connect to medial sites, and promote attraction. We found in Drosophila that loss of a microRNA, miR-279, leads to formation of CO 2 neurons in the MPs. miR-279 acts through downregulation of the transcription factor Nerfin-1. The ectopic neurons are hybrid cells. They express CO 2 receptors and form connections characteristic of CO 2 neurons, while exhibiting wiring and receptor characteristics of MP olfactory receptor neurons (ORNs). We propose that this hybrid ORN reveals a cellular intermediate in the evolution of species-specific behaviors elicited by CO 2 .In insects, both the position of CO 2 neurons and the behavior elicited by CO 2 differ among species. For example, olfactory detection of CO 2 through neurons positioned in or around the mouthparts of an insect, such as maxillary palps (MPs) and labial palps, correlates with feedingrelated behaviors. Indeed, in some blood-feeding insects such as mosquitoes and tsetse flies, these neurons are harbored in the MPs and are important in locating hosts via plumes of CO 2 that they emit (1-3). The hawkmoth, Manduca sexta, monitors nectar profitability of newly opened Datura wrightii flowers through CO 2 receptor neurons located in their labial palps (4,5). In these examples, CO 2 acts as an attractant. Conversely, in Drosophila CO 2 is a component of a stress-induced odor that triggers avoidance behavior (6). This repellent response is driven by antennal neurons expressing the CO 2 receptor complex 8). How did these diverse behavioral responses to CO 2 arise during insect evolution? We propose that this diversity emerged through multiple steps, including changes in cellular position (arising from elimination of CO 2 neurons in one appendage and generation of these neurons in another) and changes in circuitry.In the course of a genetic screen for mutants disrupting the organization of the olfactory system, we isolated a mutant (S0962−07) that resulted in the formation of ectopic Gr21a-expressing §To whom correspondence should be addressed.
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