The Delicate Dance of Dominance: How the Fruit Fly Brain Controls Threat Displays
Limbs evolved as a means of locomotion. From the primitive rotating flagella of bacteria to the wings of flies and even our own legs, animals use these appendages to travel to find food or mates, or escape predators. But in countless species across the animal kingdom, limbs are repurposed to create elaborate social displays: Paradise birds fan out their wings and hop around in courtship dances, while crabs wave their claws to communicate to potential mating partners. As humans, we use our limbs to dance, gesture while talking, wield tools, and conduct a remarkable diversity of behaviors. How does the brain control and coordinate its body parts for such distinct purposes?
A new study from Caltech neuroscientists has discovered how social behaviors—specifically aggressive displays of intimidation—are wired in the brain of the fruit fly Drosophila melanogaster, a commonly used model organism. The team discovered two brain "modules" that are connected to the wings and to the legs, respectively, that govern the animal's threat displays.
The research was led by Caltech graduate student Shuo Cao and conducted in the laboratory of David Anderson, the Seymour Benzer Professor of Biology, Leadership Chair and director of the Tianqiao and Chrissy Chen Institute for Neuroscience at Caltech, and a Howard Hughes Medical Institute Investigator. A paper describing the work appears on October 15 in the journal Current Biology.
Male Drosophila exhibit four specific behaviors when trying to intimidate other fruit flies with threat displays. A fly will leap forward in rapid, stuttering bursts of activity; throw up its wings at a 45-degree angle to form a V; repeatedly turn to face the recipient of its aggression; and pump its wings forward in a movement too fast for the human eye to see. Altogether, it's not dissimilar from the actions of an aggressive man who puffs up his chest and throws out his arms in a show of intimidation.
The flies will not conduct these behaviors unless confronted with another male fly.
In 2018, the Anderson lab discovered that a tiny patch of fly brain cells, called AIP neurons, control these threat displays. When AIP neurons are optogenetically activated by researchers in experiments, the study showed, flies will exhibit a threat display even when no other fly is present. If the neurons are silenced, a fly is still physically able to attack another fly it comes into contact with, but it no longer performs the preamble to the fight—the threat display.
Curiously, the fly's brain contains very few AIP neurons—only five to seven are present in each of the insect's two brain hemispheres. How does this tiny group of brain cells coordinate and orchestrate the complex actions of the fly's wings and legs to repurpose them in a choreography of four distinct threat behaviors?
Over the past five years, neuroscientists studying Drosophila have developed an intricate map showing the connections between every cell within the male fruit fly brain. With this map—called a connectome—Cao identified four major neurons that are "downstream" from the AIP. This means that the neurons receive signals that originate in the AIP but do not send signals back to it.
Cao discovered that two of the neurons emanating from the AIP are neurons described as "descending." These descending neurons each have a long fiber that extends from the fly's central brain down to the motor nerve cord, the fly's equivalent of the human spinal cord. Signals originating in the central brain travel down these neurons to control movements of the fly's body. When each of the descending neurons is activated on its own, only weak movements occur in the fly's wings. But activating both simultaneously, Cao found, produces the exact wing movements of the threat display—the V shape and the rapid forward pump.
The other two neurons located downstream from the AIP are "interneurons," which project out and connect to many other downstream descending neurons. When one of these interneurons is activated, Cao found that a fly will walk around continuously. Activating the other causes the fly to stand still. And when the two interneurons are simultaneously activated, Cao discovered, a fly displays the stuttering, charging movements characteristic of a threat display.
Importantly, the descending neurons that control wing movements for threat displays are different cells from the descending neurons that control them in flight: They evolved specifically for that purpose and do not seem to do anything else. However, the neurons involved in turning and charging are part of a larger group of descending neurons used for routine locomotion like walking. The two interneurons activated by the AIP for the charging movements only selectively activate neurons of this larger group and send patterns of signals to produce the short bursts of movement specific to threat displays.
"It's a neurobiological mechanism for what evolutionary biologists call exaptation: Taking parts or processes of an organism that evolved for one function and adapting them to perform a different function—on the fly, so to speak," Anderson says.
In future work, Cao plans to investigate how external sensory cues such as the sight of another fly or the smell of its pheromones shift the animal into a mode where it will exhibit a threat display. Further research could investigate other fruit fly species—there are thousands—to examine their threat displays, if present, and whether they have similar neural circuits.
The paper is titled "Neural coordination of wing and leg movements during a terrestrial threat display." Cao and Anderson are the study's authors. The work was funded by the National Institutes of Health and a Josephine de Karman Trust fellowship, awarded by the Pasadena Community Foundation.
A close up of Drosophila Melanogaster, the common lab fruit fly.
Credit: Caltech
A male fruit fly (top) intimidates another fly with lunging movements and sharp flaps of its wings.
Credit: S. Cao
A male fruit fly demonstrating a threatening wing pump at 20x slow-motion.
Credit: S. Cao
In this video, a fly has its AIP neurons modified to be light-activated with a tool called optogenetics. When the lights are turned on, the fly exhibits a "threat display," even without the presence of another fly.
Credit: Duistermars et. al., 2018
