title: Evolution of Acid-Sensing Olfactory Circuits in Drosophilids.
abstract: Animals adapt their behaviors to specific ecological niches, but the genetic and cellular basis of nervous system evolution is poorly understood. We have compared the olfactory circuits of the specialist Drosophila sechellia-which feeds exclusively on Morinda citrifolia fruit-with its generalist cousins D. melanogaster and D. simulans. We show that D. sechellia exhibits derived odor-evoked attraction and physiological sensitivity to the abundant Morinda volatile hexanoic acid and characterize how the responsible sensory receptor (the variant ionotropic glutamate receptor IR75b) and attraction-mediating circuit have evolved. A single amino acid change in IR75b is sufficient to recode it as a hexanoic acid detector. Expanded representation of this sensory pathway in the brain relies on additional changes in the IR75b promoter and trans-acting loci. By contrast, higher-order circuit adaptations are not apparent, suggesting conserved central processing. Our work links olfactory ecology to structural and regulatory genetic changes influencing nervous system anatomy and function.
authors.affiliation: Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015 Lausanne, Switzerland.
authors.forename: Lucia L
authors.initials: LL
authors.lastname: Prieto-Godino
authors.affiliation: Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015 Lausanne, Switzerland.
authors.forename: Raphael
authors.initials: R
authors.lastname: Rytz
authors.affiliation: Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015 Lausanne, Switzerland.
authors.forename: Steeve
authors.initials: S
authors.lastname: Cruchet
authors.affiliation: Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015 Lausanne, Switzerland.
authors.forename: Benoîte
authors.initials: B
authors.lastname: Bargeton
authors.affiliation: Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015 Lausanne, Switzerland.
authors.forename: Liliane
authors.initials: L
authors.lastname: Abuin
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.affiliation: Laboratory of Neurophysiology and Behavior, The Rockefeller University, New York, NY 10065, USA.
authors.forename: Vanessa
authors.initials: V
authors.lastname: Ruta
authors.affiliation: Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland; Swiss Institute of Bioinformatics, CH-1015 Lausanne, Switzerland.
authors.forename: Matteo
authors.initials: M
authors.lastname: Dal Peraro
authors.affiliation: Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015 Lausanne, Switzerland. Electronic address: Richard.Benton@unil.ch.
authors.forename: Richard
authors.initials: R
authors.lastname: Benton
mesh_terms: D000818:Animals; D005075:Biological Evolution; D002208:Caproates / Q000378:metabolism*; D004330:Drosophila; D029721:Drosophila Proteins / Q000235:genetics* / Q000378:metabolism; D004331:Drosophila melanogaster; D000067636:Drosophila simulans; D019143:Evolution, Molecular; D005638:Fruit; D032066:Morinda / Q000737:chemistry; D009154:Mutation; D009474:Neurons / Q000378:metabolism*; D009812:Odorants; D058468:Receptors, Ionotropic Glutamate / Q000235:genetics* / Q000378:metabolism; D018035:Receptors, Odorant / Q000235:genetics* / Q000378:metabolism; D012903:Smell / Q000235:genetics*
chemical_list: D002208:Caproates; D029721:Drosophila Proteins; C000621447:IR75b protein, Drosophila; D058468:Receptors, Ionotropic Glutamate; D018035:Receptors, Odorant; C037652:hexanoic acid
keywords: Drosophila melanogaster; Drosophila sechellia; adaptation; behavior; evolution; ionotropic glutamate receptor; neural circuit; neuron; odorant receptor; olfaction