Molecular-Genetic Basis of Sex-Specific Behaviors

Understanding the neural and genetic basis of complex behaviors is a major outstanding question in neurobiology. The fruit fly, Drosophila melanogaster, displays innate, complex reproductive behaviors. These behaviors are regulated by transcription factors encoded by fruitless (fru) and doublesex (dsx). Both fru and dsx are sex-specifically spliced downstream of the sex determination hierarchy, resulting in production of male-specific isoforms of Fru and Dsx and a female-specific isoform of Dsx. These transcription factors direct sex differences in behavior by regulating expression of downstream genes. fru is a complex locus and only transcripts from the P1 promoter (fru P1) are sex-specifically spliced to generate male-specific isoforms (FruM). To gain insight into gene expression differences in fru P1-expressing neurons between males and females, we used Translating Ribosome Affinity Purification (TRAP). The results of this study and other studies led us to examine a family of proteins with known functions in synaptic connectivity encoded by defective proboscis extension response (dpr) and Dpr Interacting Protein (DIP) genes. We examined the co-expression of dprs/DIPs with fru P1 neurons. We found the majority of dprs/DIPs are co-expressed with fru P1-expressing neurons in both males and females, but with distinct patterns. When we activate and silence subsets of fru P1 neurons that overlap with dpr/DIP- expressing neurons, particular courtship phenotypes are observed, allowing us to assign functions to subpopulations of neurons. Overall, this work contributes to our understanding of how FruM is specifying and maintaining the neural circuitry for male courtship behavior, with a focus on the regulation and function of the dprs and DIPs. We also focus on the regulation of female reproductive behaviors, by examining interactions between the germline and female head tissues. We examined gene expression changes in head tissues of females with and without a germline, as virgins and at one- and three- day(s) post-mating, as well as in females that had been mated to males lacking a germline. A set of female post-mating behaviors was also characterized. Additionally, we performed a genome-wide association study which led to the identification of polymorphisms that contribute to natural variation of female re-mating behavior. Together, these studies provide insight into the molecular-genetic control of female reproduction.