title: Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems.
abstract: To sense myriad environmental odors, animals have evolved multiple, large families of divergent olfactory receptors. How and why distinct receptor repertoires and their associated circuits are functionally and anatomically integrated is essentially unknown. We have addressed these questions through comprehensive comparative analysis of the Drosophila olfactory subsystems that express the ionotropic receptors (IRs) and odorant receptors (ORs). We identify ligands for most IR neuron classes, revealing their specificity for select amines and acids, which complements the broader tuning of ORs for esters and alcohols. IR and OR sensory neurons exhibit glomerular convergence in segregated, although interconnected, zones of the primary olfactory center, but these circuits are extensively interdigitated in higher brain regions. Consistently, behavioral responses to odors arise from an interplay between IR- and OR-dependent pathways. We integrate knowledge on the different phylogenetic and developmental properties of these receptors and circuits to propose models for the functional contributions and evolution of these distinct olfactory subsystems.
authors.affiliation: Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015 Lausanne, Switzerland.
authors.forename: Ana F
authors.initials: AF
authors.lastname: Silbering
authors.forename: Raphael
authors.initials: R
authors.lastname: Rytz
authors.forename: Yael
authors.initials: Y
authors.lastname: Grosjean
authors.forename: Liliane
authors.initials: L
authors.lastname: Abuin
authors.forename: Pavan
authors.initials: P
authors.lastname: Ramdya
authors.forename: Gregory S X E
authors.initials: GS
authors.lastname: Jefferis
authors.forename: Richard
authors.initials: R
authors.lastname: Benton
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified; D005075:Biological Evolution; D004330:Drosophila / Q000235:genetics*; D029721:Drosophila Proteins / Q000819:agonists / Q000235:genetics / Q000502:physiology*; D008024:Ligands; D018782:Maze Learning / Q000502:physiology; D009154:Mutation; D009812:Odorants; D009833:Olfactory Pathways / Q000033:anatomy & histology* / Q000254:growth & development / Q000502:physiology*; D055696:Olfactory Perception / Q000235:genetics / Q000502:physiology*; D018034:Olfactory Receptor Neurons / Q000033:anatomy & histology / Q000254:growth & development / Q000502:physiology*; D058468:Receptors, Ionotropic Glutamate / Q000819:agonists / Q000235:genetics / Q000502:physiology*; D018035:Receptors, Odorant / Q000235:genetics / Q000502:physiology
chemical_list: D029721:Drosophila Proteins; D008024:Ligands; D058468:Receptors, Ionotropic Glutamate; D018035:Receptors, Odorant; C555767:ionotropic receptor 25a, Drosophila; C555766:ionotropic receptor 8a, Drosophila