Food odour enhances male flies’ attractiveness

When female flies smell their favorite food, they become more receptive to courting males

“A way to someone’s heart is through their stomach” is a popular saying. But it is not only in humans that romance and a good dinner seem to go together well. In the vinegar fly Drosophila melanogaster, scientists from the Max Planck Institute for Chemical Ecology in Jena have now even identified the respective underlying neuronal mechanism in the fly’s brain. If vinegar is nearby, male flies are perceived as more attractive and the receptivity of virgin females towards courting males is increased.

Vinegar odour boosts the perception of a male sex pheromone in the brain of unmated female Drosophila melanogaster flies, as a team of scientists from the Department of Evolutionary Neuroethology has now discovered. The researchers were able to identify the underlying neuronal mechanism in the brain of Drosophila flies. Previous experiments had revealed that the male pheromone cis-vaccenyl acetate activates the glomerulus DA1 in the brains of female flies. Glomeruli are spherical functional units in the antennal lobe, the olfactory centre in the fly brain. “We were able to show in our study that vinegar odour enhances the reactions of female flies to the male sex pheromone significantly. Both odours together intensify the activation of DA1,” explains Silke Sachse, head of the “Olfactory Coding” research group. The scientists observed this effect only in unmated virgin flies; it was absent in males and mated females.

Analyzing the underlying neural mechanisms, the neurobiologists were able to elucidate how the odour signals were processed in the fly brain and determine which brain areas were activated. They used functional imaging techniques to monitor and visualize brain activity induced by the sex pheromone, by vinegar, and by both odours together.

Transgenic fly lines were crucial for the experiments. In these flies, selected electrical synapses -- connections between specific classes of nerve cells -- had been silenced. The various lines helped researchers pinpoint the neurons involved in signal transfer and to precisely locate the neuronal site of the interaction of two odours. “We were able to show that the enhanced activation of the glomerulus DA1 is mediated by a so-called “lateral excitation” in a particular class of neurons. Different neighbouring glomeruli in the brain respond to the odour of vinegar, and the excitation from those glomeruli is transmitted to DA1 via electrical synapses,” says first author, Sudeshna Das, who came to the Max Planck Institute as a fellow from the Alexander von Humboldt Foundation. The male sex pheromone, in contrast to the vinegar, activates DA1 directly through the specialized olfactory receptor Or67d. Thus both odours activate the same olfactory glomerulus, just through different neuronal pathways. Together, the scents evoke an enhanced behavioural response in virgin females, increasing their willingness to mate.

From an ecological perspective, this mechanism is extremely important, because it accelerates mating when sufficient food is available for the females and for their offspring. “We were surprised that this strong response enhancement of the pheromone response by vinegar is completely absent in mated female flies. However, after discovering the behavioural relevance for courtship we realized that this effect only makes sense in virgin females,” says Silke Sachse.

The increased willingness to mate in the presence of sufficient food is important with respect to reproductive success, which is probably why this rare synergistic interaction between the responses to two different odours has evolved. “A synergistic interaction of two odours is extremely rare and has hardly been observed so far. The more general rule is that different odours rather inhibit each other and lead to mixture inhibition which allows the olfactory system not to become saturated when more than one odour is perceived,” Silke Sachse emphasizes.

The results have also further ecological relevance: “In nature, female flies only perceive little amounts of the male sex pheromone. From an evolutionary point of view it seems useful that they evolved a mechanism which enhances the effect of the pheromone without the males having to release higher concentrations. If you consider that Drosophila flies have a pretty short life span during which they are constantly threatened by predators, infections or toxic food, accelerated mating and reproduction is very important for their survival,” says Sudeshna Das.