Male fruit flies have several tricks for finding a mate, from detecting pheromones in the dark to relying on visual cues in light.
Now, new research reveals that these little suitors are taking advantage of a flexible network of modular brain circuits to quickly adapt to different mating cues. The study, published in Natureis the first to describe how various species of fruit flies connect new sensory stimuli, such as pheromones, into a set of basic brain circuits without needing to develop new neural pathways from scratch.
The findings offer a broader framework for understanding how brain wiring can change to influence the evolution of behavior. “The diversity of behaviors across the animal kingdom is enormous, but the underlying mechanisms of how evolution shapes nervous systems have been very difficult to unravel,” says Vanessa Ruta, head of the Laboratory of Neurophysiology and Behavior. “Here we discovered what we believe is a key neural mechanism that gives brain circuits the flexibility to rewire across species.”
Plug and play
One of the great mysteries of behavioral evolution is how, as species diversify, brain circuits keep pace with the rapid changes in social cues that allow individuals to find their ideal mates. Courtship behaviors, for example, evolve rapidly, making it difficult to imagine the fly brain completely reinventing itself every time a new pheromone enters the Drosophila repertoire.
But until now it was not possible to identify where in the nervous system evolution acts to alter behavior, so the key characteristics that make such circuits so adaptable remained a mystery. Ruta’s group turned to fruit flies, where closely related species share similar brains but rely on very different signals for mating rituals. D. simulansFor example, it relies primarily on visual cues to find a partner, while D. yakuba developed a new ability to use pheromones to find a mate even in complete darkness. These and other variations presented an opportunity to study how similar brains detect and perceive different social cues.
“We started looking for parts of the brain that might be primed for flexibility,” says Rory Coleman, first author of the study and a postdoctoral fellow in the Ruta lab. “We were looking for features that could make the circuit intrinsically adaptive, possible evolutionary hotspots that drive behavioral diversification.”
After comparing pheromone-sensing circuits across multiple species (using behavioral assays, genetic tools, neuroimaging, and CRISPR genome editing), they ultimately selected sensory neurons in the male forelimbs and P1 neurons in the upper brain as key to modulating courtship between species. . The team found that the basic neural components of male mating behaviors, such as P1 neurons, are present in all species, but different sensory signals can be flexibly connected to this node. This allows fly species to develop different mating strategies without having to rewire their entire brain.
For example, the researchers found that P1 neurons activated in response to completely different types of pheromones in D. melanogaster and D. yakuba. However, the role of P1 neurons in courtship initiation was still conserved in both species. “An important discovery of our work is that there are discrete nodes within the brain of each of these species that can flexibly integrate new sensory modalities,” says Ruta. “This flexibility allows conserved nodes like P1 neurons to still initiate courtship in different species but respond to different signals from their females.”
A social brain
This research falls under the umbrella of Rockefeller’s Price Family Center for the Social Brain, an initiative that focuses on understanding the neural, cellular and molecular foundations of social behavior. In addition to shedding light on flexibility in the face of novel sensory stimuli, the present work also illustrates an experimental approach to studying how social behaviors evolve across species. “Our results demonstrate that Drosophila is a powerful system for studying the evolution of behavior,” says Ruta.
By examining how variations in neural circuits shape behaviors such as mating, the lab hopes to advance our understanding of the complex interplay between brain function and social behaviors, providing a framework for understanding how social circuits are built to produce adaptive behaviors in the human brain. And while the brain structures of flies and humans differ substantially, some of the underlying principles of how neural circuits evolve and adapt are likely to be conserved across species.
“We hope that comparative evolutionary studies like this will reveal the basic rules that shape how neural circuits have been built across the animal kingdom, including humans,” Coleman says. “Many neurological disorders are thought to arise from incorrect wiring of circuits,” Ruta adds. “By examining neural circuits through the lens of evolution, we hope to shed light on what neural motifs can change and how they can be altered, not through the ravages of disease, but as a consequence of evolutionary selection.”