A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone

Abstract

Insects, like many other animals, use sex pheromones to coordinate their reproductive behaviours. Volatile pheromones are detected by odorant receptors expressed in olfactory receptor neurons (ORNs). Whereas fruit odours typically activate multiple ORN classes, pheromones are thought to act through single dedicated classes of ORN. This model predicts that activation of such an ORN class should be sufficient to trigger the appropriate behavioural response. Here we show that the Drosophila melanogaster male-specific pheromone 11-cis-vaccenyl acetate (cVA) acts through the receptor Or67d to regulate both male and female mating behaviour. Mutant males that lack Or67d inappropriately court other males, whereas mutant females are less receptive to courting males. These data suggest that cVA has opposite effects in the two sexes: inhibiting mating behaviour in males but promoting mating behaviour in females. Replacing Or67d with moth pheromone receptors renders these ORNs sensitive to the corresponding moth pheromones. In such flies, moth pheromones elicit behavioural responses that mimic the normal response to cVA. Thus, activation of a single ORN class is both necessary and sufficient to mediate behavioural responses to the Drosophila sex pheromone cVA.

Dendritic Eph organizes dendrodendritic segregation in discrete olfactory map formation in Drosophila

“…In addition, the expression pattern of Eph-myc in the pupal optic lobe was consistent with the previous report (Supplemental Fig. S1D Ejima et al 2007;Kurtovic et al 2007;van der Goes van Naters and Carlson 2007;Grosjean et al 2011;Liu et al 2011;Lebreton et al 2014;Lin et al 2016). Interestingly, the expression was markedly low in the neighboring regions of the Eph-positive glomeruli (Supplemental Fig.…”

“…Among 50 glomeruli, the DA1, DL3, VA1lm, and VL2a glomeruli exhibited high Eph expression during development, holding the line against the other glomeruli by their unique function. Unlike other glomeruli, the DA1, DL3, VA1lm, and VL2a glomeruli receive inputs from the axons of ORNs (Or67d, Or65a, Or47b, and Ir84a, respectively) dedicated to sensing odors related to reproductive behavior, such as pheromones and food-derived odors promoting male courtship behaviors (Ejima et al 2007;Kurtovic et al 2007;van der Goes van Naters and Carlson 2007;Grosjean et al 2011;Liu et al 2011;Lebreton et al 2014;Lin et al 2016). Among them, Or67d, the primary neuron of the DA1 olfactory circuit, detects Drosophila male-specific pheromone 11 cis-vaccenyl acetate (cVA) and triggers sex-specific courtship behavior in both male and female flies (Kurtovic et al 2007).…”

On the scent of speciation: the chemosensory system and its role in premating isolation

“…As a result, the genomics of chemosensory systems can now help to unravel molecular features of chemoreception and to trace the mechanisms of chemical perception from molecules to behaviour (see for review in insects: Rutzler and Zwiebel, 2005;Benton, 2006;Hallem et al, 2006;mammals: Dulac and Torello, 2003;and across phyla: Mombaerts, 1999;Firestein, 2001;Matsunami and Amrein, 2003;Ache and Young, 2005). By linking chemistry and physiology at one end with ecology and evolution at the other, 'chemogenomics' provides new opportunities to dissect the genetic basis of complex behaviour (Fitzpatrick et al, 2005;Kurtovic et al, 2007) and the functional genetic variation that underlies adaptation and reproductive isolation (Moyle, 2005;Clark, 2006;Noor and Feder, 2006;Storz and Hoekstra, 2007).…”

Into the mind of a fly

“…The availability of the genome sequence of Drosophila melanogaster opened this system to rapid molecular analysis by Carlson, Dean Smith, Liqun Luo, Dickson, Richard Axel and a number of former Axel trainees, resulting in the complete description of the sequence and expression of all 62 odorant receptors and 68 taste receptors (reviewed in ref. 32), the complete map of connectivity of primary olfactory centres 33,34 , an initial view of how primary olfactory information is mapped in the higher brain 35,36 , and a comprehensive survey of ligand tuning of a majority of the odorant receptors 37 , including those tuned to pheromones 38,39 . A major effort in this growing field is to understand the underlying central mechanisms by which a fly discriminates among all the odours it is able to detect and how the circuitry underlying pheromone perception leads to stereotyped behaviours.…”