Hybrid Neurons in a MicroRNA Mutant Are Putative Evolutionary Intermediates in Insect CO₂ Sensory Systems

• Published in: Science (American Association for the Advancement of Science) 2008-02, Vol.319 (5867), p.1256-1260
• Main Authors: Cayirlioglu, Pelin, Kadow, Ilona Grunwald, Zhan, Xiaoli, Okamura, Katsutomo, Suh, Greg S.B, Gunning, Dorian, Lai, Eric C, Zipursky, S. Lawrence
• Format: Article
• Language: English
• Subjects: 3' Untranslated Regions; Animals; Animals, Genetically Modified; Antennas; Biological and medical sciences; Biology; Carbon dioxide; Carbon Dioxide - analysis; Carbon Dioxide - metabolism; Drosophila; Drosophila - genetics; Drosophila - physiology; Drosophila Proteins - genetics; Drosophila Proteins - metabolism; Evolution; Fundamental and applied biological sciences. Psychology; Gene Expression Regulation; Hybrid Cells - physiology; Insect behavior; Insects; MicroRNA; MicroRNAs - genetics; MicroRNAs - metabolism; Mutation; Neurons; Neurosciences; Olfactory Receptor Neurons - cytology; Olfactory Receptor Neurons - physiology; Olfactory system and olfaction. Gustatory system and gustation; Palps; Receptors; Receptors, Cell Surface - metabolism; Ribonucleic acid; RNA; Sense Organs - physiology; Senses; Sensilla; Somesthesis and somesthetic pathways (proprioception, exteroception, nociception); interoception; electrolocation. Sensory receptors; Species Specificity; Stem cells; Transcription Factors - genetics; Transcription Factors - metabolism; Vertebrates: nervous system and sense organs
• ISSN: 0036-8075; 1095-9203
• DOI: 10.1126/science.1149483

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.