Abstract

Animals searching for food and sexual partners often use odourant mixtures combining food-derived molecules and pheromones. For orientation, the vinegar fly Drosophila melanogaster uses three types of chemical cues: (i) the male volatile pheromone 11-cis-vaccenyl acetate (cVA), (ii) sex-specific cuticular hydrocarbons (CHs; and CH-derived compounds), and (iii) food-derived molecules resulting from microbiota activity. To evaluate the effects of these chemicals on odour-tracking behaviour, we tested Drosophila individuals in a wind tunnel. Upwind flight and food preference were measured in individual control males and females presented with a choice of two food sources labelled by fly lines producing varying amounts of CHs and/or cVA. The flies originated from different species or strains, or their microbiota was manipulated. We found that (i) fly-labelled food could attract—but never repel—flies; (ii) the landing frequency on fly-labelled food was positively correlated with an increased flight duration; (iii) male—but not female or non-sex-specific—CHs tended to increase the landing frequency on fly-labelled food; (iv) cVA increased female—but not male—preference for cVA-rich food; and (v) microbiota-derived compounds only affected male upwind flight latency. Therefore, sex pheromones interact with food volatile chemicals to induce sex-specific flight responses in Drosophila.

Highlights

  • When searching for food sources, prey, appropriate sexual partners, and the most suitable ecological niche, animals often use multiple sensory cues[1,2]

  • Landing preference was measured in a dual-choice test based on the frequency of individuals landing on each food source

  • Upwind flight and landing preference were assessed in single starved control Canton-S (CS) male and female flies presented with a dual choice between plain food (PF) and fly-labelled food (LF; Fig. 2)

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Summary

Introduction

When searching for food sources, prey, appropriate sexual partners, and the most suitable ecological niche, animals often use multiple sensory cues[1,2]. D. melanogaster flies mainly use two types of pheromones: 11-cis-vaccenyl acetate (cVA26,27), a male-specific volatile compound, and several sex-specific cuticular hydrocarbons (CHs), which are mostly—but not exclusively—detected by physical contact[28,29,30,31]. Some food-derived molecules (especially yeast and fermentation products) and pheromones are involved in Drosophila long- to close-distance attraction[21,42]. At a relatively close distance, fatty acid-derived compounds can influence aggregation and feeding[43,44] Some of these products deposited in frass depend on the activity of gut-associated bacteria[43]. An aldehyde compound (Z4-11Al) derived from the degradation of the main cuticular pheromone (7,11-heptacosadiene) produced by females of most strains can attract wild-type males of the two sibling species D. melanogaster and D. simulans at some distance and with some intraspecific variation[48]. An interand intraspecific variation for free flight odour tracking has been reported in several Drosophila species[49]

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