In most animals, males and females show different (dimorphic) patterns of behaviour. But we know relatively little about how the neural circuits that underlie sexually dimorphic behaviours are organized. Jai Yu and colleagues at the Research Institute of Molecular Pathology in Austria, in collaboration with Greg Jefferis at the MRC Laboratory of Molecular Biology in Cambridge, UK, recently attempted to untangle sex-specific neural circuitry in fruit flies. In a recent paper published in Current Biology, they attempted to map out connectivity among the neurons that control how male flies court female flies.
In the presence of females, male fly brains integrate sensory cues and produce complex motor output in the form of stereotyped leg, abdomen and wing movements (including an audible courtship ‘song’ generated by the wings). The behaviours are innate, and a male version (splice variant) of the gene fruitless controls the entire behavioural sequence. Females expressing the male version of the gene behave like males; males without the male version behave like females. The gene is expressed in ∼1500 neurons throughout the fly brain. How does this constellation of neurons control a complex sequence of sex-specific behaviours? Yu and colleagues reasoned that the essential first step was to simply examine how fruitless expressing neurons connect to one another in male and female brains. To begin with, they developed a genetic technique that allowed them to systematically visualize the anatomy of small numbers of fruitless expressing neurons throughout the brain. After generating hundreds of genetic lines with different groups of fruitless neurons labelled, they then charted where individual groups of neurons were in relation to each other and common structural landmarks. Examination of the overlap among cellular processes from different groups allowed the team to make predictions about how fruitless expressing cells are connected to one another in males and females.
First the group showed that multiple fruitless expressing sensory pathways converge on one part of the fly brain (lateral protocerebral complex), suggesting that this area is the core site for integration of sensory cues during courtship. Next they identified pathways for motor output from the lateral protocerebral complex. Surprisingly, when they compared dimorphisms between males and females, they only found 11 anatomical dimorphisms in the circuit. Interestingly, they also uncovered a general rule: neurons that are present in both sexes but have dimorphic arborizations tend to be in primary sensory pathways or motor pattern generating circuits, whereas sex-specific neurons are usually in areas postulated to be involved in higher order information processing (e.g. lateral protocerebral complex). These results suggest that anatomical dimorphisms are actually not that common in the circuit, and are concentrated primarily in areas of the brain that are involved in making decisions.
Overall, Yu and co-workers have done something in flies that is very difficult to do in most animals. They have constructed a comprehensive potential wiring diagram for a large circuit controlling complex sex-specific behaviours. That said, it is important to remember that this work only predicts where connections could be – it does not actually prove the presence of any synapses. But this is what makes this paper great; it generates a large number of testable hypotheses and opens up new opportunities to study how neural circuits give rise to sexually dimorphic behaviour.
