Food odors trigger Drosophila males to deposit a pheromone that guides aggregation and female oviposition decisions

Abstract

Animals use olfactory cues for navigating complex environments. Food odors in particular provide crucial information regarding potential foraging sites. Many behaviors occur at food sites, yet how food odors regulate such behaviors at these sites is unclear. Using Drosophila melanogaster as an animal model, we found that males deposit the pheromone 9-tricosene upon stimulation with the food-odor apple cider vinegar. This pheromone acts as a potent aggregation pheromone and as an oviposition guidance cue for females. We use genetic, molecular, electrophysiological, and behavioral approaches to show that 9-tricosene activates antennal basiconic Or7a receptors, a receptor activated by many alcohols and aldehydes such as the green leaf volatile E2-hexenal. We demonstrate that loss of Or7a positive neurons or the Or7a receptor abolishes aggregation behavior and oviposition site-selection towards 9-tricosene and E2-hexenal. 9-Tricosene thus functions via Or7a to link food-odor perception with aggregation and egg-laying decisions.Animals rely on their sense of smell to navigate their environments; for example, the smell of food attracts animals to particular locations. These food-rich sites are also popular places for meeting, mating, and rearing offspring. Scent molecules emitted by animals can also attract others to a particular location or affect their behaviour. These molecules are known as pheromones.Little is understood about how cues from food and pheromones interact to influence animal behavior. Studies of the Drosophila species of fruit fly have been conducted to tease out these interactions. Fruit flies are attracted to the smell of food—particularly overripe or rotting fruit—and often congregate at a food source to mate and lay their eggs. But whether it is the food itself or other cues that trigger these behaviors is not clear.Now, Lin et al. reveal that male fruit flies emit a pheromone in response to the smell of food. This pheromone attracts females to the food to mate and encourages the females to lay their eggs at the food-rich site. This allows the male fly to have some say as to where his offspring will be laid and also increases the chances that his offspring will survive.Using genetic and other experiments, Lin et al. found that the pheromone is detected by a receptor on the antennae of the female flies. This stimulates a specific type of brain cell that causes the female to lay her eggs at the site where the pheromone has been deposited. A chemical released by rotting fruit also stimulates these receptors and encourages the females to congregate and lay eggs.The body of a male fly is coated by many different pheromones, yet he deposits only a select few upon smelling a food odor. How this occurs remains to be determined, but suggests that different pheromones might be localized to different body parts. By rubbing just those parts onto their surroundings, the male might be able to deposit a specific pheromone. How food odors specifically trigger this response, or if other flying insects also deposit pheromones in response to food odors, remains to be determined.