Abstract
Insect olfactory receptor (Or) genes are large, rapidly evolving gene families of considerable interest for evolutionary studies. They determine the responses of sensory neurons which mediate critical behaviours and ecological adaptations. We investigated the evolution across the genus Drosophila of a subfamily of Or genes largely responsible for the perception of ecologically relevant aliphatic esters; products of yeast fermentation and fruits. Odour responses were recorded from eight classes of olfactory receptor neurons known to express this Or subfamily in D. melanogaster and from homologous sensilla in seven other species. Despite the fact that these species have diverged over an estimated 40 million years, we find that odour specificity is largely maintained in seven of the eight species. In contrast, we observe extensive changes in most neurons of the outgroup species D. virilis, and in two neurons across the entire genus. Some neurons show small shifts in specificity, whilst some dramatic changes correlate with gene duplication or loss. An olfactory receptor neuron response similarity tree did not match an Or sequence similarity tree, but by aligning Or proteins of likely functional equivalence we identify residues that may be relevant for odour specificity. This will inform future structure–function studies of Drosophila Ors.
Similar content being viewed by others
Abbreviations
- ORN:
-
Olfactory receptor neuron
- Or:
-
Olfactory receptor
- PCR:
-
Polymerase chain reaction
References
Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:e20
Bohbot J, Pitts RJ, Kwon HW, Rützler M, Robertson HM, Zwiebel LJ (2007) Molecular characterization of the Aedes aegypti odorant receptor gene family. Insect Mol Biol 16:525–537
Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327–338
Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535–1547
de Bruyne M, Clyne PJ, Carlson JR (1999) Odor coding in a model olfactory organ: the Drosophila maxillary palp. J Neurosci 19:4520–4532
de Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552
Dekker T, Ibba I, Siju KP, Stensmyr MC, Hansson BS (2006) Olfactory shifts parallel superspecialism for toxic fruit in Drosophila melanogaster sibling, D. sechellia. Curr Biol 16:101–109
Dobritsa AA, van Naters W, Warr CG, Steinbrecht RA, Carlson JR (2003) Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37:827–841
Engsontia P, Sanderson AP, Cobb M, Walden KK, Robertson HM, Brown S (2008) The red flour beetle’s large nose: an expanded odorant receptor gene family in Tribolium castaneum. Insect Biochem Mol Biol 38:387–397
Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548–1553
Gardiner A, Barker D, Butlin RK, Jordan WC, Ritchie MG (2008) Drosophila chemoreceptor gene evolution: selection, specialization and genome size. Mol Ecol 17:1648–1657
Gardiner A, Butlin RK, Jordan WC, Ritchie MG (2009) Sites of evolutionary divergence differ between olfactory and gustatory receptors of Drosophila. Biol Lett 5:244–247
Guo S, Kim J (2007) Molecular evolution of Drosophila odorant receptor genes. Mol Biol Evol 24:1198–1207
Guo S, Kim J (2009) Dissecting the molecular mechanism of Drosophila odorant receptors through activity modeling and comparative analysis. Proteins 78:381–399. doi:10.1002/prot.22556
Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125:143–160
Helfand SL, Carlson JR (1989) Isolation and characterization of an olfactory mutant in Drosophila with a chemically specific defect. Proc Natl Acad Sci USA 86:2908–2912
Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631
Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Chrystal MA, Cravchik A, Collins FH, Robertson HM, Zwiebel LJ (2002) G protein-coupled receptors in Anopheles gambiae. Science 298:176–178
Kato A, Touhara K (2009) Mammalian olfactory receptors: pharmacology, G protein coupling and desensitization. Cell Mol Life Sci 66:3743–3753. doi:10.1007/s00018-009-0111-6
Kreher SA, Mathew D, Kim J, Carlson JR (2008) Translation of sensory input into behavioral output via an olfactory system. Neuron 59:110–124
Markow TA, O’Grady PM (2005) Evolutionary genetics of reproductive behavior in Drosophila: connecting the dots. Annu Rev Genet 39:263–291
McBride CS, Arguello JR (2007) Five Drosophila genomes reveal non neutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics 177:1395–1416
Nozawa M, Nei M (2007) Evolutionary dynamics of olfactory receptor genes in Drosophila species. Proc Natl Acad Sci USA 104:7122–7127
Olsson SB, Linn CE Jr, Roelofs WL (2006) The chemosensory basis for behavioral divergence involved in sympatric host shifts. I. Characterizing olfactory receptor neuron classes responding to key host volatiles. J Com Physiol A Neuroethol Sens Neural Behav Physiol 192:279–288
Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 16:1395–1403
Russo CAM, Takezaki N, Nei M (1995) Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol 12:391–404
Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006 (Epub 2008 Apr 13)
Schawaroch V (2002) Phylogeny of a paradigm lineage the Drosophila melanogaster species group (Diptera: Drosophilidae). Biol J Linean Soc 76:21–37
Semmelhack JL, Wang JW (2009) Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 459:218–223
Smadja C, Peng SHI, Butlin RK, Robertson HM (2009) Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. Mol Biol Evol 26:2073–2086
Smart R, Kiely A, Beale M, Vargas E, Carraher C, Kralicek AV, Christie DL, Chen C, Newcomb RD, Warr CG (2008) Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem Mol Biol 38:770–780
Stensmyr MC, Dekker T, Hansson BS (2003) Evolution of the olfactory code in the Drosophila melanogaster subgroup. Proc Biol Sci 270:2333–2340
Stranden M, Liblikas I, König WA, Almaas TJ, Borg-Karlson AK, Mustaparta H (2003) (−)-Germacrene D receptor neurones in three species of heliothine moths: structure-activity relationships. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189:563–577
Tunstall NE, Sirey T, Newcomb RD, Warr CG (2007) Selective pressures on Drosophila chemosensory receptor genes. J Mol Evol 64:628–636
Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725–736
Wanner KW, Anderson AR, Trowell SC, Theilmann DA, Robertson HM, Newcomb RD (2007) Female-biased expression of odourant receptor genes in the adult antennae of the silkworm, Bombyx mori. Insect Mol Biol 16:107–119
Wicher D, Schäfer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452:1007–1011
Acknowledgments
We thank Rebecca Hallas (Ary Hoffmann lab) and Rob Good (Charles Robin lab) from the University of Melbourne for D. ananassae and D. serrata stocks. We also thank Jyotika Taneja (Monash University) for maintaining fly stocks and Stephen Trowell (CSIRO Entomology, Canberra) for comments on the manuscript. We thank two anonymous reviewers for their helpful suggestions for improvements to the manuscript. This work was funded by a grant from the Collaboration fund of CSIRO’s Food Futures Flagship, Australia. All experiments comply with “principles of animal care”, publication No. 86-23, revised 1985 of the National Institute of Health, and also with the current laws of Australia
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
de Bruyne, M., Smart, R., Zammit, E. et al. Functional and molecular evolution of olfactory neurons and receptors for aliphatic esters across the Drosophila genus. J Comp Physiol A 196, 97–109 (2010). https://doi.org/10.1007/s00359-009-0496-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-009-0496-6