An olfactory receptor for food-derived odours promotes male courtship in Drosophila

Abstract

Many animals attract mating partners through the release of volatile sex pheromones, which can convey information on the species, gender and receptivity of the sender to induce innate courtship and mating behaviours by the receiver. Male Drosophila melanogaster fruitflies display stereotyped reproductive behaviours towards females, and these behaviours are controlled by the neural circuitry expressing male-specific isoforms of the transcription factor Fruitless (FRU(M)). However, the volatile pheromone ligands, receptors and olfactory sensory neurons (OSNs) that promote male courtship have not been identified in this important model organism. Here we describe a novel courtship function of Ionotropic receptor 84a (IR84a), which is a member of the chemosensory ionotropic glutamate receptor family, in a previously uncharacterized population of FRU(M)-positive OSNs. IR84a-expressing neurons are activated not by fly-derived chemicals but by the aromatic odours phenylacetic acid and phenylacetaldehyde, which are widely found in fruit and other plant tissues that serve as food sources and oviposition sites for drosophilid flies. Mutation of Ir84a abolishes both odour-evoked and spontaneous electrophysiological activity in these neurons and markedly reduces male courtship behaviour. Conversely, male courtship is increased--in an IR84a-dependent manner--in the presence of phenylacetic acid but not in the presence of another fruit odour that does not activate IR84a. Interneurons downstream of IR84a-expressing OSNs innervate a pheromone-processing centre in the brain. Whereas IR84a orthologues and phenylacetic-acid-responsive neurons are present in diverse drosophilid species, IR84a is absent from insects that rely on long-range sex pheromones. Our results suggest a model in which IR84a couples food presence to the activation of the fru(M) courtship circuitry in fruitflies. These findings reveal an unusual but effective evolutionary solution to coordinate feeding and oviposition site selection with reproductive behaviours through a specific sensory pathway.

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).…”

The use of the sex pheromone as an evolutionary solution to food source selection in caterpillars

“…However, no aggregation behaviour has been reported for S. littoralis larvae. Very recently, the detection of food-derived odours has been shown to promote male courtship in D. melanogaster 22 . Similarly, it is possible that the detection of the sex pheromone promotes food search in caterpillars.…”

Testing <em>Drosophila</em> Olfaction with a Y-maze Assay

“…Use this control strain to backcross every other stock necessary for later steps. This backcrossing step is typically represented by at least 5 successive crosses of a single virgin female (to allow possible crossing-over between homologous chromosomes) to 2-3 isogenic reference males 5 . Rather use brief cooling on ice.…”

“…These tests include multimodal assays such as courtship tests where various sensory modalities, including olfaction, are important to elicit male courtship 3 . Other assays have also been developed to tackle the role of odorants more specifically; these include T-mazes, Y-mazes, trap assays, four-field arenas and wind-tunnels 4,5,6,7,8 .…”