Neuroethology of Olfaction in Drosophila Evolution and Specialization

In insects olfaction is a primary sensory modality. As a result changes in the animal’s ecology are often paralleled by modifications in the olfactory system. Using a comparative approach between the generalist Drosophila melanogaster and its sibling specialist D. sechellia, I looked at the coding properties of the olfactory system. Using electrophysiology, neuroanatomy, and behavioral assays we demonstrate how the olfactory system of adults of specialist fruitfly Drosophila sechellia has evolved to accommodate its unique preference for Morinda citrifolia fruit. We show that the fly has expanded the number of one antennal sensillum type inhabited by two neurons sensitive to Morinda volatiles. The numerical increased has caused the formation of a macro glomerular complex tuned to fruit volatiles. Accordingly, the olfactory preference of the species for these odors and combinations thereof has radically changed. We subsequently show that also larvae of this species changed their olfactory preference. With such a simple olfactory circuitry, consisting of only 21 olfactory neurons, the identification of the factor underlying the switch is especially promising. Finally, we looked what olfactory information is conveyed to the brain of the fruitfly via an evolutionarily old olfactory subsystem, that of coeloconic sensory neurons. These neurons express ionotropic receptors (Irs) instead of conventional olfactory receptors (Ors), and natural ligand for this set of receptors have been poorly investigated. We identified three new ligands biologically active for coeloconic neurons, and investigate the significance of these compounds in odor coding and in fly attraction.