Rockefeller University researchers have found that male fruit flies of the species Drosophila erecta will not court at all unless they are surrounded by the smell of fermenting fruit, according to Mirage News. The study, published in the journal Nature, describes how the insects' brains combine food odor with the sight of other flies to switch on sexual behavior. The work was led by first author Philipp Brand, a former postdoctoral researcher in the Laboratory of Neurophysiology and Behavior who now leads a research group at the Max Planck Institute for Brain Research in Frankfurt, with lab head Vanessa Ruta.
Why it matters
Most laboratory work on fruit fly courtship has observed single pairs of flies in bare enclosures. Those conditions leave out the sensory world the insects actually inhabit, where mating happens among large groups gathered on a piece of rotting fruit. The new findings suggest that courtship cannot be understood apart from the environment in which it occurs.
Ruta said the study shows an emerging principle: that courtship is shaped by ecological and social context and cannot be separated from it. She added that people are highly sensitive to social context in how they respond to others, so it is not surprising that other animals have evolved to do the same. Mirage News reports that the results also show how the neural activity behind mating is triggered.
A tale of two species
Brand, an evolutionary biologist who did extensive fieldwork in Central America during his doctorate, designed the experiments to bring more of the natural setting into the lab. The team built large chambers with a central patch of apple cider vinegar on agar, standing in for a piece of fermenting fruit, and varied whether males were alone or in groups and whether the vinegar scent was present.
The species responded very differently. Males of Drosophila melanogaster and several close relatives explored the arena and mated with females whether or not the odor was there. Male D. erecta, by contrast, largely stayed put when the scent was absent, showing little interest in their surroundings or in other flies. With the vinegar aroma present, their behavior changed completely: they gathered on the food patch and repeatedly approached nearby flies, male or female, until they found a mate. More than 90 percent of D. erecta matings took place on the vinegar patch, while D. melanogaster mated in a more spread-out pattern.
Brand described the scene as a vigorous interaction among all the flies once food is present, adding that it looks chaotic because everyone is interacting with everyone. Males also courted more energetically in larger groups than when alone with a single female, suggesting that the movement of nearby flies raised their arousal. The constant motion changed what each male saw, enlarging the share of his visual field filled by other flies and increasing the visual motion across his retina.
A conserved circuit with an extra switch
To see what was happening in the brain, the researchers placed males in a virtual reality system built in Ruta's lab. A fly walks on an air-supported ball and can turn or move forward and backward in place while its brain activity is recorded.
Earlier work from the lab had identified a neural circuit in a higher brain region, shared among several close relatives of D. melanogaster, that involves P1 interneurons and LC10a visual neurons and coordinates visually guided pursuit during courtship. The same circuit was active during D. erecta mating behavior, but with a difference: the P1 and LC10a neurons fired only when food odor was present, Brand said.
According to Mirage News, that heightened visual response draws males toward other flies, a kind of social foraging that leads them to the crowded food patch. The crowding then increases visual motion, which further raises arousal, forming a feedback loop. Ruta noted that such loops produce the collective behaviors seen in schools of fish, flocks of birds or swarms of locusts, and that these normally nonsocial creatures are strongly influenced by the presence of others.
Brand said that while D. erecta shares the same conserved neural circuitry as its close relatives, it is unique among them in requiring an additional environmental input, the aroma of food, to activate the neurons that promote sexual arousal. Without that scent, he said, the males are completely uninterested in mating, unlike its close cousins.
The paper adds to a growing body of work on how animals integrate sensory cues from their surroundings rather than responding to a single trigger. For D. erecta, the combination of a specific food odor, the sight of moving companions and a crowded surface appears to be what turns a quiet male into a courting one.
What to watch: whether follow-up studies identify the specific olfactory pathways that gate the P1 and LC10a circuit, and whether similar environment-dependent switches turn up in other species studied outside stripped-down lab settings.
