Fitting It All Together: How Courtship- and Mating-Responsive Genes Affect Drosophila melanogaster Male Behavior

Abstract

Behavior is a complex process resulting from the integration of genetic and environmental information. Thus, the genetically tractable Drosophila melanogaster was utilized to better understand the interplay between these factors since Drosophila males and females exhibit sex-specific courtship behaviors that are innate yet modifiable. These sex-specific behaviors, as well as sexually dimorphic development, are regulated, in part, by the somatic sex-determination hierarchy. Since reproductive behaviors rely on the rapid integration of multiple sensory cues, it is likely that the perception and integration of such cues and mating-induced physiological changes are mediated in part by changes in gene expression. Therefore, it was hypothesized that assaying gene expression changes in response to courtship or mating in Drosophila males would uncover new targets of the sex-determination hierarchy and other behaviorally important loci. We took a novel approach to find these behaviorally-responsive loci by utilizing microarray technology to assess courtship- or mating-induced gene expression changes in Drosophila male whole bodies or heads. Mutations in candidate loci were tested for effects on reproductive behaviors and present the first data showing that egghead (egh) and female-specific independent of transformer (fit) affect male reproductive behavior. egh is up regulated in male heads 20 min after courting and is required post-developmentally in a subset of neurons for robust male courtship behavior. fit, a fat body-expressed sex-determination hierarchy target gene, is up regulated in male whole bodies after 5 min of courtship. fit is also up regulated in male heads after 20 min of courtship or 2 hrs after mating. Mutations in fit result in male-male courtship; more specifically, fit mutants direct courtship towards males and also elicit courtship from wild-type males. By analyzing fit's role in courtship behavior, we also shed light on the role the fat body plays in modulating behavior. These studies provide the first pieces of evidence that gene expression changes occur in Drosophila males performing reproductive behaviors. This novel approach identified behaviorally important loci that are expressed in the nervous system and the fat body, indicating that both tissues modulate behavior. Also identified were sex-determination hierarchy target genes and it is likely that further analysis of the remaining candidates will reveal more members of this genetic cascade.