When a male fruit fly encounters a prospective mate, he initiates courtship by following her around and gently tapping her with his leg. If she seems interested, he serenades her with a love song. Singing is followed by more intimate acts that sometimes lead to successful mating.
Now Stanford University scientists have discovered that this elaborate courtship behavior is actually choreographed by a cluster of nerve cells embedded in the central nervous system of the male fly. When these cells fail to function properly, the courtship ritual breaks down and the male is transformed from a suave Casanova into a clumsy brute that tries to force himself on unwilling females.
These findings, published in the July 29 edition of the journal Nature, may eventually help scientists understand how the brain orchestrates sexual behavior in a variety of species - from flies to reptiles to humans, according to the researchers.
"The fruit fly is a model organism whose basic cellular functions are very similar to what they are in people," said Bruce S. Baker, the Dr. Morris Herzstein Professor in Biology at Stanford and co-author of the Nature study. "It wouldn't surprise me to learn that human sexual behaviors also have underneath them a basic circuitry in the nervous system that mediates attraction and mating."
Casanova to caveman
In the Nature study, Baker and Stanford graduate student Devanand S. Manoli focused on a gene known as fruitless - one of approximately 13,000 genes in the DNA of the common fruit fly, Drosophila melanogaster.
Baker and several colleagues had previously discovered that fruitless was the master gene that controlled sexual behavior in male flies. "We found that the fruitless gene was responsible for building the neuronal circuitry for male courtship," Baker said. "This circuit, which is built into the fly's brain and ventral nerve cord, is comprised of about 1,500 neurons - roughly one percent of the total number of nerve cells in a fruit fly."
In the Nature paper, Manoli and Baker showed that 60 of those cells carried out the crucial task of coordinating the steps of the courtship ritual. When those cells didn't function properly, the male was unlikely to successfully mate, the researchers found.
"Drosophila male courtship is a complex, innate sequence of stereotyped behaviors that are programmed into the male during development," Baker explained. "The fly isn't taught anything. In fact, he's ready to mate 24 hours after he emerges from the pupa."
The courtship ritual consists of six steps carried out in a specific order. First, the male senses the presence of the female and follows her. Then he taps the female with his foreleg, which triggers pheromone cues. The male then extends a wing and vibrates it, producing a species-specific courtship song. The fourth step involves licking the female's genitalia with his proboscis, followed by attempted copulation (step five) and copulation (step six).
"A normal male completes the first three steps in about two minutes," Baker said. "That's followed by about two minutes of licking before he first attempts copulation." Copulation itself lasts another 20 minutes.
"But when we interfere with the functioning of those 60 nerve cells, the male essentially skips the tapping step and attempts to do everything else at once: He tries to copulate, lick her genitalia and play her a love song simultaneously. So what normally takes a total of four minutes is reduced to just 10 seconds - and that doesn't work very well."
While some mating did occur during the experiment, the mutant males failed to achieve their ultimate goal - reproductive success.
"The mutants did copulate, but it never resulted in fertilization, because they would consistently mis-transfer their sperm and other seminal contents," Baker said. "It also took them longer to achieve copulation than normal males. That may well be because, for successful copulation, it's female willingness that drives the whole thing. We can well assume that, when the mutant males behave in this way, they are doing things that the female does not find attractive."
Removing the network of nerve cells had other deleterious consequences, Baker noted.
"In normal courtship, to anthropomorphize it, the flies are polite," he said. "Normal males show what we refer to as 'deference' - once one male starts courting a female, the other male leaves the couple alone for at least a while, postponing his own courtship. But what happens when we put several mutant males together with a female? All the males go after her at the same time."
As an example, Baker pointed to a videotape shot during the experiment in which a female fly is frantically pursued by a half-dozen out-of-control mutants.
"Our study shows that there is an identifiable set of cells, a place in the central nervous system, that serves to coordinate each of the subroutines that make up a behavior - licking, tapping and so forth," Baker said.
"There's been some debate about whether the courtship ritual is really made up of subroutines or whether it's one continuum," he added. "What we found is that while interfering with the neural network changes the sequence, the individual subroutines - such as licking and singing - are still there. This suggests very strongly that these subroutines are somehow built into the nervous system itself."
The evolution of courtship
"Another interesting suggestion from our work is that, while rapid mating and multiple male courtship are very abnormal for Drosophila, such behaviors are the norm in other insect species," Baker observed. "This raises the possibility that there is an ancestral neuronal circuit for courtship that's common to many species, and that the very different courtship behaviors we see throughout the animal kingdom may have come about by relatively minor changes in this circuit."
Although a fruit fly is only a fraction of the size of a human being, Baker noted that both species are strikingly similar in their genetic makeup.
"The list is endless of the ways that people and flies are fundamentally similar," he explained. "For example, most major developmental genes that build the body plan and various organ systems are the same in people and flies."
Could the genes that control sexuality in flies also play a role in directing human sexuality?
"If you look at the basics of fly behavior, you find an innate ability to recognize somebody who is the right species and is the right sex," Baker said. "You tap them and get their attention, you play them a love song and so on. So the basic rudiments are pretty similar to what people do to get successful mating and produce an offspring.
"Of course, the actual way that's manifested in humans - whether you go to a rock concert or to the opera - is entirely cultural and based on your upbringing. But a basic drive to reproduce and a basic reproductive strategy may be there. The tough job for geneticists is figuring out the pieces of the machinery that actually bring these behaviors about."
This work was supported by the Medical Scientist Training Program in the Stanford School of Medicine and by the National Institutes of Health.
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