TheDrosophila melanogasterpheromone Z4-11Al is encoded together with habitat olfactory cues and mediates species-specific communication

Abstract

20Mate recognition in animals evolves during niche adaptation and involves habitat and 21 social olfactory signals. Drosophila melanogaster is attracted to fermenting fruit for 22 feeding and egg-laying. We show that, in addition, female flies release a pheromone (Z)-23 , that elicits flight attraction in both sexes. The biosynthetic 24 precursor of Z4-11Al is the cuticular hydrocarbon (Z,Z)-7,11-heptacosadiene (7, 25 which is known to afford reproductive isolation between D. melanogaster and D. 26 simulans. A pair of alternatively spliced receptors, Or69aB and Or69aA, is tuned to Z4-27 11Al and to food olfactory cues, respectively. These receptors are co-expressed in the 28 same olfactory sensory neurons, and feed into a neural circuit mediating species-specific, 29 long-range communication: the close relative D. simulans does not respond. That Or69aA 30 and Or69aB have adopted dual olfactory traits highlights the interplay of habitat and 31 social signals in mate finding. These olfactory receptor genes afford a collaboration 32 between natural and sexual selection, which has the potential to drive phylogenetic 33 divergence. 34 Keywords 35 pheromone, kairomone, olfaction, reproductive isolation 36 Introduction 37 Volatile insect pheromones transmit species-specific messages over a distance. Premating 38 communication with pheromones facilitates and accelerates mate-finding, and reduces 39 predation risk and energy expenditure, which is particularly adapative in short-lived 40 insects (1,2). 41Sexual communication subserves mate-finding and reproduction. The sensory drive 42 hypothesis predicts that mate recognition in animals evolves during niche adaptation and 43 that premating sexual communication involves olfactory specialization to both social 44 signals and habitat cues (3). Pheromones are released into an atmosphere that is filled 45 with environmental, habitat-related olfactory cues, some of which signal mating sites and 46 food sources. The response to pheromones and habitat odourants (kairomones) is under 47Drosophila species, they cannot account for species-specific communication (18)(19)(20). 62Interspecific matings of D. melanogaster with sibling species are inhibited by the female-63 produced cuticular hydrocarbon (Z,Z)-7,11-heptacosadiene (7,11-HD), which is not 64 volatile and perceived through gustatory receptors only at close range (21-23). This 65 raises the question whether Drosophila uses, in addition, volatile pheromone signals that 66 mediate specific mate recognition at a distance. 67We have identified the first long-range, species-specific pheromone in D. melanogaster. A 68 pair of spliced olfactory receptors, feeding into the same neural circuit, has developed a 69 dual affinity to this pheromone and to environmental semiochemicals, encoding adult and 70 larval food. A blend of this pheromone and a food odourant specifically attracts D. 71 melanogaster, but not the close relative D. simulans. This becomes an excellent paradigm 72 to study the interaction of social signals and hab...