Hybrid neurons in a microRNA mutant are putative evolutionary intermediates in insect CO2 sensory systems

Carbon dioxide ( CO2) elicits different olfactory behaviors across species. In Drosophila, neurons that detect CO2 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 CO2 neurons in the MPs. miR- 279 acts through down- regulation of the transcription factor Nerfin- 1. The ectopic neurons are hybrid cells. They express CO2 receptors and form connections characteristic of CO2 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 CO2.