The evolution of communication is a fundamental biological problem. The genetic control of the signal and its reception must be tightly coadapted, especially in inter-individual sexual communication. However, there is very little experimental evidence for tight genetic linkage connecting the emission of a signal and its reception. We found that a single genomic transposon inserted in the desat1 gene of Drosophila melanogaster simultaneously affected the emission and the perception of sex-specific signals. This mutation greatly decreased the production of unsaturated hydrocarbons on the cuticle of mature flies of both sexes. These substances represent the sex pheromones necessary for mate discrimination: control males could not discriminate the sex of mutant desat1 flies. Moreover, mutant males were unable to discriminate the sex pheromones of control flies. Expression of desat1 was found in the peripheral tissues that produce and detect sex pheromones. Excision of the transposon rescued both the production and discrimination phenotypes, but the two effects did not always coincide. This indicates that the emission and perception of pheromones are coded by different products of the same gene, reflecting the pleiotropic activity of desat1.

Sex pheromones are intraspecific chemical signals that are crucial for mate attraction and discrimination. In Drosophila melanogaster, the predominant hydrocarbons on the cuticle of mature female and male flies are radically different and tend to stimulate or inhibit male courtship, respectively. This sexual difference depends largely upon the number of double bonds (one in males and two in females) added by desaturase enzymes. A mutation was caused by a PGal4 transposon inserted in the desat1 gene that codes for the desaturase crucial for setting these double bonds. Homozygous mutant flies produced 70-90% fewer sex pheromones than control flies, and the pheromonal difference between the sexes was almost abolished. A total of 134 excision alleles were induced by pulling out all or a part of the transposon. The pheromonal profile was generally rescued in excision alleles with a completely or largely removed transposon whereas it remained mutant in alleles with a larger piece of the transposon. Five desat1 transcripts were detected during larval-to-adult development. Their levels were precisely quantified in 24-hr-old adults, a critical period for the production of sex pheromones. Three transcripts significantly varied between control females and males; however, the predominant transcript showed no difference. In mutant flies, the predominant transcript was highly decreased with the two sexually dimorphic transcripts.These two transcripts were also absent in the sibling species D. simulans, which shows no sexually dimorphic hydrocarbons. We also induced a larval-lethal allele that lacked all transcripts and failed to complement the defective hydrocarbon phenotype of mutant alleles.

Courtship conditioning is an associative learning paradigm in Drosophila melanogaster, wherein male courtship behavior is modified by experience with unreceptive, previously mated females. While the training experience with mated females involves multiple sensory and behavioral interactions, we hypothesized that female cuticular hydrocarbons function as a specific chemosensory conditioned stimulus in this learning paradigm. The effects of training with mated females were determined in courtship tests with either wild-type virgin females as courtship targets, or with target flies of different genotypes that express distinct cuticular hydrocarbon (CH) profiles. Results of tests with female targets that lacked the normal CH profile, and with male targets that expressed typically female CH profiles, indicated that components of this CH profile are both necessary and sufficient cues to elicit the effects of conditioning. Results with additional targets indicated that the female-specific 7,11-dienes, which induce naive males to court, are not essential components of the conditioned stimulus. Rather, the learned response was significantly correlated with the levels of 9-pentacosene (9-P), a compound found in both males and females of many Drosophila strains and species. Adding 9-P to target flies showed that it stimulates courting males to attempt to copulate, and confirmed its role as a component of the conditioned stimulus by demonstrating dose-dependent increases in the expression of the learned response. Thus, 9-P can contribute significantly to the conditioned suppression of male courtship toward targets that express this pheromone.