Functional coupling of acoustic and chemical signals in the courtship behaviour of the male Drosophila melanogaster.

During courtship, the male Drosophila melanogaster sends signals to the female through two major sensory channels: chemical and acoustic. These signals are involved in the stimulation of the female to accept copulation. In order to determine the respective importance in the courtship of these signals, their production was controlled using genetical and surgical techniques. Males deprived of the ability to emit both signals are unable to mate, demonstrating that other (e.g. visual or tactile) signals are not sufficient to stimulate the female. If either acoustic or chemical signals are lacking, the courtship success is strongly reduced, the lack of the former having significantly more drastic effects. However, the accelerated matings of males observed with males bearing wild-type hydrocarbons compared with defective ones, whichever the modality of acoustic performance (wing vibration or playback), strongly support the role of cuticular compounds to stimulate females. We can conclude that among the possible factors involved in communication during courtship, acoustic and chemical signals may act in a synergistic way and not separately in D. melanogaster.

Co-adaptation of pheromone production and behavioural responses in Drosophila melanogaster males.

In Drosophila melanogaster, male courtship behaviour is genetically controlled and is influenced by sex pheromones. 7-tricosene (7-T) induces a dose-dependent inhibition of male-male courtship, whereas 7,11-dienes stimulate male courtship of females. There is a geographical quantitative variation in the production of two predominant male hydrocarbons, 7-T and 7-pentacosene (7-P). We have previously found that 7-P, the main hydrocarbon from males of West African strains, stimulates males that mainly produce 7-T. Using both 'natural' and genetically engineered strains, we find that genetic factors coding for low levels of 7-P in males have co-evolved with factor(s) coding for male responses to high levels of 7-P. These two phenotypes are coded by factors on different chromosomes: the intraspecific polymorphism for the production of 7-T and 7-P is largely controlled by chromosome 2, whereas the variation in courtship towards 7-P-rich males is largely controlled by chromosome 3. The polymorphism of male courtship towards 7-P-rich males shows no correlation with the variation in male responses to female flies.

Genetic elimination of known pheromones reveals the fundamental chemical bases of mating and isolation in Drosophila.

Overexpression of the UAS-tra transgene in Drosophila melanogaster females led to the complete elimination of their cuticular pheromones. According to current models of Drosophila behavior, these flies should induce no courtship. In fact, they are still attractive to conspecific males. Three classes of stimuli are shown to induce courtship, with different effects on male behavior: (i) known pheromones produced by control females, (ii) stimuli produced by living control and transgenic flies, and (iii) as-yet-undetermined pheromones present on both control and transgenic flies. Only the latter class of pheromones are required for mating. They appear to represent a layer of ancestral attractive substances present in D. melanogaster and its sibling species; known cuticular pheromones modulate this attractivity positively or negatively. The absence of inhibitory pheromones leads to high levels of interspecific mating, suggesting an important role for these cuticular hydrocarbons in isolation between species.

Genetic feminization of pheromones and its behavioral consequences in Drosophila males.

Pheromones are intraspecific chemical signals important for mate attraction and discrimination. In the fruit fly Drosophila melanogaster, hydrocarbons on the cuticular surface of the animal are sexually dimorphic in both their occurrence and their effects: Female-specific molecules stimulate male sexual excitation, whereas the predominant male-specific molecule tends to inhibit male excitation. Complete feminization of the pheromone mixture produced by males was induced by targeted expression of the transformer gene in adult oenocytes (subcuticular abdominal cells) or by ubiquitous expression during early imaginal life. The resulting flies generally exhibited male heterosexual orientation but elicited homosexual courtship from other males.

Simultaneous influence on male courtship of stimulatory and inhibitory pheromones produced by live sex-mosaic Drosophila melanogaster.

Stable strains of Drosophila melanogaster flies producing mosaic sex-pheromones were created by manipulating the sex-determination gene transformer in different cellular patterns. Chromosomally male flies produced molecules that were partly or totally feminized, depending upon the strain. The influence on male courtship behaviour of live flies producing different mixtures of male and female pheromones was measured. The intensity of the male response was mainly a function of the stimulatory effect of 7, 11 nonacosadiene and 7, 11 heptacosadiene, two female pheromones, combined with the inhibiting effect of 7-tricosene, the male predominant molecule. These compounds were effective at very different doses. The influence of secondary molecules on male behaviours was also evaluated. The role of these substances is discussed with regard to their structure, sexual specificity, and evolutionary function.