Pose tracking software and computational tools were used to break down the complex choreography of interacting flies. Courtesy of Ruta lab/The Rockefeller University.
For fruit flies, finding the right mate is all about the right song. Now, research shows that male flies don't just try to impress their valentine by serenading her with song-they also go to great lengths to drown out the competition. By jamming their rivals' love songs with high-frequency wing flicks, male fruit flies boost the chances that they'll win the female over.
The new study, published in Cell, explains how the fruit fly brain coordinates courtship and aggressive competition-a framework which could ultimately help scientists understand how humans flexibly adapt their behavior to different social contexts and interactions. The results also suggest that mating decisions in flies are just as highly influenced by interactions between males as by female preference-something that had not been appreciated in previous studies of individual male-female pairs.
"It turns out that mating success is not just about whether a male fly is the most vigorous in his courtship," says Vanessa Ruta, head of the Laboratory of Neurophysiology and Behavior. "It is also whether he can successfully interweave courtship and aggression from moment to moment to achieve a competitive advantage over other males."
Catching courtship in action
In most previous research on how tiny Drosophila melanogaster fruit flies mate, researchers observed one male and one female together. This has led to insights into how a male fly's song makes a female receptive to mating. But Ruta and her colleagues suspected these experiments didn't fully reflect the true nature of fly courtship.
"In the wild, flies choose mates in the context of a really complex social landscape. Lots of flies congregate on a piece of rotting fruit and there will likely be many males pursuing a female," says Ruta. "In the past, that kind of interplay has not been captured in lab experiments."
Ruta's team, led by former Rockefeller graduate students Tom Hindmarsh Sten and Rufei Li-both now postdoctoral research fellows at Stanford University-set up experiments with two male fruit flies vying for one female. They used pose-tracking software and computational tools to unpack the complex interplay and feedback between these three individuals.
Typically, female flies are much less likely to mate with wingless males, who are mute and cannot produce songs. However, when the team put both a wingless male and a winged male with a female, the female sometimes mated with the wingless fly-typically when he was close to her while the winged fly was singing. The experiment suggested that the quality of an individual fly's song was not as important as the mere presence of song.
"It showed that the female isn't actually making a choice based on who has the most perfect song," says Li. "The wingless male can sneak in while the winged male is singing, and the female is just as receptive". Wingless males therefore can exploit the song of a rival-a literal wing man, as it were.
Blocking the competition
But the team observed something else when two winged males, both able to sing, were competing for a mate. When one male began to sing near the female, the other male started rapidly flicking his wings, producing a distinct high-frequency buzz-different than a mating song.
Through studies of the female fly's brain, along with observations of her behavior during playback of recordings of mating songs and wing flicks, the researchers discovered that the noise of the wing-flicks disrupted the ability of the female to perceive clear courtship songs. While courtship songs activated a set of neurons known to encourage mating, the noise from wing flick activated opposing neurons that block her receptivity.
"These vibrations actually jam the auditory system of the female fly so they can't hear the nearby rival male," says Hindmarsh Sten.
Together, these data challenge the long-held assumption that females make all the mating decisions based on a male's courtship performance. Instead, male flies balance two behaviors: singing a courtship song to the female to make her receptive to mating and performing wing flicks towards a competitor when he is attempting to sing, in order to subvert his courtship. Mating success is shaped by an ongoing battle between males, with female choice being influenced by which male successfully outmaneuvered his rivals.
The neuroscience of social competition
To better understand how males coordinate these behaviors, the researchers recorded neural activity as males sang the courtship song or flicked.
In male flies, neurons associated with courtship were activated when the flies saw a small, moving object resembling a potential mate. However, specific neurons that evoke aggression were turned on when the flies heard another male's mating song. Importantly, both courtship and aggression-promoting neurons could be active at the same time, explaining how males rapidly switch between courtship and aggression without stopping either behavior entirely.
When males were genetically engineered so that their aggression-promoting neurons were silenced, males stopped performing wing flicks, even in the presence of other males. However, they continued to court females, indicating that these two behaviors are controlled by separate but interacting sets of brain cells.
Similar brain mechanisms likely exist in humans, where we constantly balance cooperation and competition-not just in romantic interactions, but every time we adapt our behavior to our social partners, the researchers say.
"The details of what is happening in the brain to let flies shape these opposing behaviors likely has parallels to other systems," says Ruta.
