The polarity of Drosophila wing hairs displays remarkable fidelity. Each of the approximately 30,000 wing epithelial cells constructs an actin-rich prehair that protrudes from its distal vertex and points distally. The distal location and orientation of the hairs is virtually error free, thus forming a nearly perfect parallel array. This process is controlled by the planar cell polarity signalling pathway. Here we show that interaction between two tiers of the planar cell polarity signalling mechanism results in the observed high fidelity. The first tier, mediated by the cadherin Fat, dictates global orientation by transducing a directional signal to individual cells. The second tier, orchestrated by the 7-pass transmembrane receptor Frizzled, aligns each cell's polarity with that of its neighbours through the action of an intercellular feedback loop, enabling polarity to propagate from cell to cell. We show that all cells need not respond correctly to the presumably subtle signal transmitted by Fat. Subsequent action of the Frizzled feedback loop is sufficient to align all the cells cooperatively. This economical system is therefore highly robust, and produces virtually error-free arrays.

The ability to select a better option from multiple acceptable ones is important for animals to optimize their resources. The mechanisms that underlie such decision-making processes are not well understood. We found that selection of egg-laying site in Drosophila melanogaster is a suitable system to probe the neural circuit that governs simple decision-making processes. First, Drosophila females pursue active probing of the environment before depositing each egg, apparently to evaluate site quality for every egg. Second, Drosophila females can either accept or reject a sucrose-containing medium, depending on the context. Last, communication of the "acceptability" of the sucrose-containing medium as an egg-laying option to the reproductive system depends on the function of a group of insulin-like peptide 7 (ILP7)-producing neurons. These findings suggest that selection of egg-laying site involves a simple decision-making process and provide an entry point toward a systematic dissection of this process.

SUMMARY Mating induces changes in the receptivity and egg-laying behavior in Drosophila females, primarily due to a peptide pheromone called sex peptide which is transferred with the sperm into the female reproductive tract during copulation. Whereas sex peptide is generally believed to modulate fruitless-GAL4-expressing neurons in the central nervous system to produce behavioral changes, we found that six to eight sensory neurons on the reproductive tract labeled by both ppk-GAL4 and fruitless-GAL4 can sense sex peptide to control the induction of postmating behaviors. In these sensory neurons, sex peptide appears to act through Pertussis toxin-sensitive G proteins and suppression of protein kinase A activity to reduce synaptic output. Our results uncover a neuronal mechanism by which sex peptide exerts its control over reproductive behaviors in Drosophila females.