Sex and the single gene

All animals are born with their species-specific body plan and morphology, as well as a set of innate behaviours (instincts) that manifest themselves as stereotyped responses to environmental stimuli. Over the past several decades, enormous progress has been made in elucidating the molecular genetic pathways that specify morphological development. By contrast, we still know very little of the genetic pathways that specify innate behaviours. Recently, our group has begun to study male courtship behaviour in Drosophila melanogaster as a model innate behaviour. We have shown that the fruitless gene acts as a developmental switch that is both necessary and sufficient to "hard-wire" male courtship behaviour into the fly`s nervous system. The goal of the work proposed here is to investigate how this single gene is able to specify such a complex innate behaviour. Specifically, we will ask: (1) Which of the several different transcription factors encoded by fruitless are relevant for courtship behaviour? (2) What are the target genes activated by these isoforms, and what do they each contribute to courtship behaviour? (3) What other genes are required in the fruitless-expressing neurons for courtship behaviour? Thus, we aim to extend our understanding of this innate behaviour from the role of a single gene to the actions of a complex genetic hierarchy. We are motivated by the expectation that more general principles of behavioural development will emerge in the process.

All animals are born with a set of innate behaviours that allow them to respond to their environment including potential predators, prey, and mates in ways that are likely to promote their survival and reproduction. These innate behaviours and encoded in the genome and passed on from one generation to the next in the form of genetic instructions for assembling the appropriate neural circuits. Our aim is to unravel the nature of these genetic instruction for a specific model behaviour: the courtship ritual of male fruit flies (Drosophila melanogaster). We have previously shown that the fruitless (fru) gene acts as a genetic switch to preprogramme the relevant neural circuits. The gene is expressed in distinct forms in males and females. Mutant males that lack fru do not court, whereas females that have been genetically engineered to produce the male forms behave like males and court other females. The male fru forms come in multiple variants, and the goal of this project was to determine which of these variants are critical for courtship behaviour, where they are expressed in the nervous system, how they influence the development of the courtship circuitry. We found that each of these variants contribute to some aspects of courtship behaviour, although one variant (called fru-C) has a particularly critical role. We mapped the expression of each variant to specific cells in the male nervous system, and found that a number of these neuronal cells have distinct morphologies in males and females. These cellular differences could mostly be attributed to the function of the fru-C variant. These findings reveal how the fru gene shapes sex-specific neural architecture at the cellular level, and suggests how specific cellular dimorphisms might contribute to the behavioural differences between males and females. The next important step in this research will be to explain how fru changes the morphology and function of these neurons, and how these differences in turn affect the fly`s innate mating behaviour.