Pheromones, chemical signals that convey social information, mediate many insect social behaviors, including navigation and aggregation. Several studies have suggested that behavior during the immature larval stages of Drosophila development is influenced by pheromones, but none of these compounds or the pheromone-receptor neurons that sense them have been identified. Here we report a larval pheromone-signaling pathway. We found that larvae produce two novel long-chain fatty acids that are attractive to other larvae. We identified a single larval chemosensory neuron that detects these molecules. Two members of the pickpocket family of DEG/ENaC channel subunits (ppk23 and ppk29) are required to respond to these pheromones. This pheromone system is evolving quickly, since the larval exudates of D. simulans, the sister species of D. melanogaster, are not attractive to other larvae. Our results define a new pheromone signaling system in Drosophila that shares characteristics with pheromone systems in a wide diversity of insects.
The release of chemical signals called pheromones is a common tactic used by animals in many social situations, such as to attract potential mates or to follow trails left by other members of their colony. Larvae of the fruit fly Drosophila melanogaster—a species commonly studied in the laboratory—gather together when sharing a food source and then cooperate in a way that may increase how efficiently they feed. It has been proposed that pheromones coordinate this behavior, but no larval pheromones had been identified.
Mast et al. noticed that Drosophila larvae crawling on a surface tended to occupy areas where other larvae had crawled before. This suggested that larvae had left attractive chemicals on the surface. Mast et al. identified two such substances by analyzing the chemicals left on the surface and then by testing the response of larvae to each compound.
Ultimately, Mast et al. found that a single sensory neuron in the larva is responsible for detecting these attractive chemical signals. Furthermore, two genes called pickpocket23 and pickpocket29 control this response. These genes were previously known for their roles in detecting sex pheromones, and they are members of a diverse family of calcium channel subunits that are involved in detecting multiple ‘sensory modalities’ such as touch and taste. When either pickpocket23 or pickpocket29 are inactivated, larvae ignore the social cues left by their neighbors.
Mast et al. also looked for an evolutionary role for these pheromones. Larvae of a closely related fly species called Drosophila simulans produce a subtly different blend of compounds to D. melanogaster, and this blend is not attractive to any of the species tested. While Drosophila simulans larvae were not attracted to the cues left by their own species, they were attracted to the pheromones produced by Drosophila melanogaster, indicating that they retain the sensory mechanisms to detect and respond to these pheromones. These results suggest that larvae experience a rapidly evolving, complex, pheromone-rich environment that may help them tailor their behavior to survive.