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Neural basis of Drosophila mating behaviours

Final Report Summary - FRU CIRCUIT (Neural basis of Drosophila mating behaviours)

This project aimed to define the anatomy and function of the neural circuits in the fly brain that generate the distinct mating behaviors of males and females. We anticipate that a detailed understanding of how these circuits generate complex sexually dimorphic behaviours will serve as a paradigm for a more general understanding of the operating principles of neural circuits in diverse species.

Our working hypothesis is that most of the relevant neurons express the fruitless (fru) gene. There are approximately 2000 such neurons in the fly (roughly 2% of the fly’s entire complement of neurons), and we have been able to subdivide these neurons genetically into 100 distinct cell types. The anatomical analysis of these neurons has defined a cellular resolution atlas of the “fru circuit”, allowing us to formulate hypotheses as to how this circuit detects and processes the relevant sensory inputs and generates the appropriate motor outputs. Many neurons in this circuit are sexually dimorphic, offering clues as to how the distinct behaviours of the two sexes might be generated.

The genetic analysis of the fru gene suggests that these neurons comprise most, if not all, of the neurons with sexually dimorphic functions in mating. Other neurons of course must also contribute, but are likely to have analogous functions in the two sexes. The genetic data further suggest that many, perhaps even most, of the fru neurons contribute in some way or other to a specific aspect of male or female mating. We developed genetic tools that allow us to activate or silence many of the distinct cell types, and thereby discern their roles, if any, in male or female mating. Thus far, we have succeeded in identifying key components of the circuitry that generates the male courtship song, and conditions his courtship behavior in response to experience. We have also identified neurons in the female central nervous system that change her mating behavior after an initial copulation.

In the course of this project, we developed genetic tools, instrumentation and software that will be broadly applicable to the investigation of other behaviors in Drosophila. These include large collections of enhancer lines that allow gene expression to be targeted to specific neurons, as well as novel modulators of neuronal activity. Our FlyMad system allows investigators to use such tools to rapidly modulate neuronal activity in a freely behaving fly. And finally, our MateBook system for automated fly tracking and courtship analysis is a powerful system for the quantitative analysis of a wide range of fly social behaviors. All of these tools are freely available to the research community.