Genomic and Functional Studies of Drosophila Sex Hierarchy Regulated Gene Expression in Adult Head and Nervous System Tissues

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Abstract
The Drosophila sex determination hierarchy controls all aspects of somatic sexual differentiation, including sex-specific differences in adult morphology and behavior. To gain insight into the molecular-genetic specification of reproductive behaviors and physiology, we identified genes expressed in the adult head and central nervous system that are regulated downstream of sex-specific transcription factors encoded by doublesex (dsx) and fruitless (fru). We used a microarray approach and identified 54 genes regulated downstream of dsx. Furthermore, based on these expression studies we identified new modes of DSX-regulated gene expression. We also identified 90 and 26 genes regulated in the adult head and central nervous system tissues, respectively, downstream of the sex-specific transcription factors encoded by fru. In addition, we present molecular-genetic analyses of two genes identified in our studies, calphotin (cpn) and defective proboscis extension response (dpr), and begin to describe their functional roles in male behaviors. We show that dpr and dpr-expressing cells are required for the proper timing of male courtship behaviors. The fruit fly Drosophila is an excellent model system to use to understand the molecular-genetic basis of male courtship behavior, as the potential for this behavior is specified by a well-understood genetic regulatory hierarchy, called the sex determination hierarchy. The sex hierarchy consists of a pre-mRNA splicing cascade that culminates in the production of sex-specific transcription factors, encoded by doublesex (dsx) and fruitless (fru). dsx specifies all the anatomical differences between the sexes, and fru is required for all aspects of male courtship behavior. In this study, we measure gene expression differences between males and females, and between sex hierarchy mutants and wild-type animals, to identify genes that underlie the differences between males and females. We have performed these studies on adult head and nervous system tissues, as these tissues are important for establishing the potential for behaviors. We have identified several genes regulated downstream of dsx and fru and more extensively characterized two genes that are more highly expressed in males. One gene regulated downstream of dsx is expressed in the retina and is known to have a function in visual transduction. The other gene, regulated downstream of fru, plays a role in the timing of male courtship behavior.