The Drosophila melanogaster pheromone Z4-11Al is encoded together with habitat olfactory cues and mediates species-specific communication

Abstract

AbstractMate recognition in animals evolves during niche adaptation and involves habitat and social olfactory signals. Drosophila melanogaster is attracted to fermenting fruit for feeding and egg-laying. We show that, in addition, female flies release a pheromone (Z)-4-undecenal (Z4-11Al), that elicits flight attraction in both sexes. The biosynthetic precursor of Z4-11Al is the cuticular hydrocarbon (Z,Z)-7,11-heptacosadiene (7,11-HD), which is known to afford reproductive isolation between the sibling species D. melanogaster and D. simulans. A pair of alternatively spliced receptors, Or69aB and Or69aA, is tuned to Z4-11Al and to food olfactory cues, respectively. These receptors are co-expressed in the same olfactory sensory neurons, and feed into a neural circuit mediating species-specific, long-range communication: the close relative D. simulans, which shares food resources and co-occurs with D. melanogaster, does not respond. That Or69aA and Or69aB have adopted dual olfactory traits highlights the interplay of habitat and social signals in mate finding. These olfactory receptor genes afford a collaboration between natural and sexual selection, which has the potential to drive phylogenetic divergence.Significance StatementVolatile insect sex pheromones carry a message over a distance, they are perceived by dedicated olfactory receptors, and elicit a sequence of innate behaviours. Pheromones mediate specific mate recognition, but are embedded in and perceived together with environmental olfactory cues. We have identified the first long-range, species-specific pheromone in Drosophila melanogaster. A pair of spliced olfactory receptors, feeding into the same neural circuit, has developed a dual affinity to this pheromone and kairomones, encoding adult and larval food. Blends of this pheromone and kairomone specifically attract D. melanogaster, but not the close relative D. simulans. This becomes an excellent paradigm to study the interaction of social signals and habitat olfactory cues in premating reproductive isolation and phylogenetic divergence.