Drosophila Sensory Neuroethology

Animals, like humans, need to perceive their surroundings via their senses in order to make sensible behavioral decisions, reproduce successfully, and survive. Animals are equipped with audition, vision, thermosensation, hygrosensation, mechanosensation, magnetoception, gustation, and olfaction, which detects physical and chemical changes in their habitats. Among these senses, olfaction is likely the most ancient sensory modality. Insects, the most abundant and successful group of the animal kingdom, predominantly use olfaction to find food, mates, breeding sites, and to avoid dangers. Moreover, hygrosensation is vital for insects to find a suitable habitat and to avoid risks of dehydration. Our understanding of the molecular, neuronal, and morphological organization of the insect olfactory system is today substantial, in large parts thanks to Drosophila melanogaster (vinegar fly) and the wealth of sophisticated genetic tools available in this classic model system. Our knowledge regarding the functional and molecular basis of insect hygrosensation, is, however, limited.
In this thesis, I show that the vinegar fly olfactory system do not detect odor molecules randomly, but capture and process specific odors associated with needs and dangers. I demonstrate how the olfactory system cope with toxic and harmful matters in the natural habitat and I identify an olfactory circuit that mediates repellency towards phenol, which is produced by pathogenic bacteria, predominantly present in carnivore feces. Furthermore, I show that flies have an innate and species-specific ability to find suitable humidity levels, related to their native habitat. Vinegar flies can sense humidity changes in their environment through a trio of ionotropic receptors expressed in the sacculus of the antennae. Although D. melanogaster is known as a generalist, I show that wild populations of D. melanogaster from a mopane forest within the potential ancestral habitat have a strong breeding preference towards marula fruit. This fruit is seasonally abundant, native to Southern Africa, and is presumably the ancestral host of the vinegar fly. I also argue that marula drove the D. melanogaster to become a human commensal.
In summary, the research presented in my thesis enhances our understanding of how the olfactory system operates, the behavior of wild flies, and introduces the genetic and neural basis underlying humidity sensation in insects. These findings might lead us to better strategies for controlling insect pests, as well as human disease vectors.