Some fruit odours sexually arouse male fruitflies. The response is mediated by olfactory neurons that are sensitive to food smells and plug into the brain's neural circuit for sexual behaviour. See Letter p.236
The smell of a delicious stew often stimulates a man's appetite, but it rarely turns him on. Male Drosophila fruitflies, however, behave differently. On page 236 of this issue, Grosjean et al.1 identify how particular odours from rotten fruit and decaying vegetables — the creatures' typical diet — act as aphrodisiacs to male fruitflies.
Males and females of many animal species produce chemical compounds that they use to find each other and to communicate their mating status. These volatile pheromones diffuse, and putative mating partners can detect them over fairly long distances. Female moths, for instance, release sex pheromones that can attract males from several kilometres away. How the nervous system perceives and interprets pheromones, and how these chemicals modify behaviours, are central questions in neurobiology.
Drosophila melanogaster is a powerful genetic model for addressing such questions. A key aspect of these flies' ecology is that they meet and mate where they feed. A series of cues from the female, including a pheromone bouquet spread on her abdomen, elicits sexual arousal in the male fly2.
Grosjean et al.1 find that odours unrelated to the female also promote male courtship behaviour. They show that phenylacetic acid and phenylacetaldehyde — two aromatic compounds found in fruits and other plants — specifically activate an olfactory receptor, IR84a, in sensory neurons on the fly nose (the antennae), thereby triggering male courtship behaviour. Indeed, when the authors removed the Ir84a gene, the mutant male flies not only couldn't smell these two odours, but also did not engage in courtship as vigorously as normal flies. Conversely, perfuming an unattractive mating partner (a dead female) with phenylacetic acid enhanced sexual appetite in the normal male, but not in the IR84a mutants.
How can sensory neurons tuned to detect food-derived odours promote sexual behaviour? Olfactory neurons connect to a brain centre called the antennal lobe, from where their projections are further parsed into smaller centres called glomeruli3. Grosjean and colleagues find that all IR84a-expressing olfactory neurons innervate the same glomerulus — one of the three glomeruli that are involved in male courtship behaviour.
Male fruitflies have a dedicated and complex neural circuit that controls most aspects of their courtship behaviour — from sensory perception to motor output4,5. The identity of this courtship circuit is governed largely by male-specific isoforms of the transcription factor Fruitless (FRUM). As it turns out, the IR84a olfactory neurons also express FRUM. What's more, they form synaptic connections in the antennal lobe with projection neurons that also express FRUM.
The projection neurons downstream of the olfactory neurons dispatch different forms of sensory information to distinct brain regions. For example, information on food odours typically reaches one place and pheromone information goes to another. Yet Grosjean et al. show that the projection neurons downstream of IR84a sensory neurons are an exception: their axonal processes intermingle tightly with other FRUM-positive projection neurons in the pheromone-processing centre of the brain (Fig. 1). In other words, the neural circuit mediating male-fly courtship is equipped with a plug-in to sense food resources that modulates the decision to court females.
How various sensory signals coming from different sources are integrated and computed in the brain into an actual decision is poorly understood. It seems, however, that the projection neurons conveying food or female-related odours connect to a unique centre that determines whether the olfactory environment is amenable to courtship. Knowledge of how this neural circuit reaches 'decisions' and how it triggers behaviours will require detailed characterization of the wiring and activity of the circuit6,7.
Regardless of how male flies integrate food odours into the decision to mate, one may wonder why they do so in the first place. Female flies do worry about where they lay their eggs, but their male counterparts usually seem to have little say in this. Or perhaps they do. Linking courtship behaviour to a food compound gives the male some sway over how his progeny will be raised. Should the levels of phenylacetic acid be limited (read: low food resources), a male might not insist on courting local females, no matter how attractive they smell, and might wait to sire progeny grown in a richer environment.
This solution — linking food odour to male reproductive behaviour — has probably evolved relatively recently. Although IR84a belongs to an ancient family of receptors, it is found only in fruitflies, and is notably absent from insect species that rely on long-range pheromones to attract mates. Thus, evolution of IR84a may have shaped the ecology of fruitflies: targeting good food may have become a proxy for finding a sexual partner, thus circumventing the need for long-range pheromones (Fig. 2).
Advertisers often exaggerate the powerful role of human pheromones and perfumes in sexual attraction. It is nonetheless remarkable that the very chemical compounds that, according to this paper1, enhance fly sexual appetite are also pleasant to humans and are used in perfumes for their sweet, floral smell. It remains to be seen to what extent environmental stimuli affect sexual behaviours in other species, including humans.
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The conserved mitochondrial genomes of Drosophila mercatorum (Diptera: Drosophilidae) with different reproductive modes and phylogenetic implications
International Journal of Biological Macromolecules (2019)