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.DOI: http://dx.doi.org/10.7554/eLife.08688.001

The neurogenetics of group behavior inDrosophila melanogaster

“…Although it is very difficult to directly interrogate the intentionality of fly behavior, a suitable proxy might be found in testing whether walking trajectories are enriched in social encounters when compared with random null models or shuffled trajectories (Schneider et al, 2012b). Additionally, one can use robots or artificial flies (Agrawal et al, 2014;Zabala et al, 2012) to further identify and manipulate key sensory features -hydrocarbon profiles, shapes, colors and odors -that draw flies to one another, making group behaviors possible (Bartelt et al, 1985;Lin et al, 2015).…”

“…This aggregation can be modulated by the distribution of environmental resources, genetic determinants that determine the degree of resource exploitation versus exploration/ foraging (Sokolowski, 2010), and social mechanisms. For example, adult males lay pheromones that attract females to food sources (Lin et al, 2015), and larvae deposit aggregation pheromones (Mast et al, 2014) that may be used to facilitate food digestion (Durisko et al, 2014) and create opportunities for cannibalistic interactions (Vijendravarma et al, 2013).…”

The Adipokinetic Hormone Receptor Modulates Sexual Behavior, Pheromone Perception and Pheromone Production in a Sex-Specific and Starvation-Dependent Manner in Drosophila melanogaster

“…This effect was sex-specific: no effect was found in males, neither for cVA nor for 7-T. It would be interesting to test whether the AKH signaling regulates the production of other pheromonal compounds such as 9-tricosene, 7-pentacosene, 7,11-non-acosadiene or CH503 (Antony et al, 1985;Ferveur and Sureau, 1996;Yew et al, 2009;Lin et al, 2015). We expected that less 7,11-HD (aphrodisiac), but more 7-T (anti-aphrodisiac) would reduce the attractiveness of females lacking AKHR.…”

Targeted manipulation of neuronal activity in behaving adult flies

“…Furthermore, flies are more likely to show aggressive behavior when female or a food source is present, and the amount of food within the chamber can influence the probability and nature of aggressive behavior (Hoffmann 1987;Chen et al 2002;Lim et al 2014). Flies can also leave pheromones or other chemicals behind in chambers, which can affect the social behaviors of new inhabitants (Suh et al 2004;Wang and Anderson 2010;Lin et al 2015). Thus, cleaning chambers between experiments will reduce residual pheromones that could influence behavioral outcomes in future experiments (Zawistowski and Richmond 1987).…”

“…Systems have also been developed that direct laser pulses to specific body parts of a moving fly . Other systems restrict light to particular regions of a chamber allowing flies to "choose" whether the neurons are activated (or not) by moving into (or out of) the illuminated region, or coupling neural activation with particular localized features of a larger chamber, such as odors (Suh et al 2007;Lin et al 2013a;Aso et al 2014b;Klapoetke et al 2014;Lin et al 2015).…”