Hierarchical chemosensory regulation of male-male social interactions in Drosophila

Abstract

Pheromones regulate male social behaviors in Drosophila, but the identities and behavioral role(s) of these chemosensory signals, and how they interact, are incompletely understood. Here we show that (Z)-7-tricosene (7-T), a male-enriched cuticular hydrocarbon (CH) previously shown to inhibit male-male courtship, is also essential for normal levels of aggression. The opposite influences of 7-T on aggression and courtship are independent, but both require the gustatory receptor Gr32a. Surprisingly, sensitivity to 7-T is required for the aggression-promoting effect of 11-cis-vaccenyl acetate (cVA), an olfactory pheromone, but 7-T sensitivity is independent of cVA. 7-T and cVA therefore regulate aggression in a hierarchical manner. Furthermore, the increased courtship caused by depletion of male CHs is suppressed by a mutation in the olfactory receptor Or47b. Thus, male social behaviors are controlled by gustatory pheromones that promote and suppress aggression and courtship, respectively, and whose influences are dominant to olfactory pheromones that enhance these behaviors.

A Systematic Analysis of Drosophila Gustatory Receptor Gene Expression in Abdominal Neurons which Project to the Central Nervous System

“…Among the Grs observed to express in neurons apparently innervating the reproductive organs, Gr32a is required for pheromone detection (Miyamoto and Amrein, 2008;Wang et al, 2011), and Gr64c is a member of the putative sugar receptor subfamily . It is as yet unclear whether these Grs act as chemosensors for certain molecules in the reproductive organs, or if they act as sensors for completely different modalities.…”

Pheromones mediating copulation and attraction in Drosophila

“…1F). Furthermore, in an Or47b mutant (22), which has two identical independent knockout alleles, Or47b [2] and Or47b [3] (in all experiments, we used only Or47b [3] after backcrossing it to the Canton-S background to minimize genetic background effects), the responses of at4A OSNs to ML were completely abolished, whereas at4C OSNs still responded to the three fly odorants ( Fig. 1 H and I).…”

Tailless and Atrophin control Drosophila aggression by regulating neuropeptide signalling in the pars intercerebralis

“…The elucidation of the genes and neuronal circuitry that regulate aggression is key to the understanding of its mechanisms. The fruit fly Drosophila melanogaster has recently emerged as a model system to study aggression [2][3][4][5][6][7][8][9][10][11][12] . Several conserved neuromodulators have been shown to play a role in fly aggression [5][6][7] .…”

“…For example, serotonin plays a critical role in the modulation of aggression across a broad range of species but the effect is different in vertebrates and invertebrates 13,14 . In addition, fly-specific pheromonal cues have been identified that affect aggression in Drosophila [10][11][12] . What remains unclear is whether the molecular mechanisms that control aggression in flies are mechanistically conserved with those in mammals.…”