A single mutation alters production and discrimination of Drosophila sex pheromones

Abstract

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 desatl 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 desatl flies. Moreover, mutant males were unable to discriminate the sex pheromones of con-trol flies. Expression of desatl 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 differ-ent products of the same gene, reflecting the pleiotropic activity of desatl .

Figure 1

The transposable element is inserted in the desat1 gene. The triangle indicates the position of the PGal4 transposable element, at chromosomal site 87B_10-11. We used Southern blotting to check that only one transposon was inserted in the genome of the desat1^1573-1 strain. The gene altered by the PGal4 (PGawB) transposon was mapped after cloning and sequencing of the two DNA fragments flanking the insertion point (…CGGCT GTTTT and GTTGA CATGC…). Comparison with the BDGP database <www.fruitfly.org> revealed that they share a complete identity with two contiguous sequences of the desat1 gene. The 3′ extremity of the transposon was mapped at −1691 bp of the transcription start (ATG). The black boxes represent the coding region (with the translation STOP) and the grey boxes alternative 5′UTR for the desat1 gene. The desat2 gene is located at less than 4 kb from the 5′UTR of desat1.

Figure 2

Gas chromatograms of individual male and female flies of control Canton-S and mutant desat1^1573-1 strains. Each peak corresponds to a single CH and sexually dimorphic CHs are cis 7-tricosene (7-T) in control males; cis, cis 7,11-heptacosadiene (7,11-HD) and cis, cis 7,11-nonacosadiene (7,11-ND) in control females. In mutant flies, n-tricosane (23LIN), n-pentacosane (25LIN) and n-heptacosane (27LIN) are the principal CHs.

Figure 3

Simultaneous discrimination of two object flies by subject control males. Tests were either carried out in red light (shaded), or in white light (plain). Each pair of mirrored bars represents the mean (±s.e.m.) courtship index that a 5-day-old subject male directed toward the two headless objects (CI₁, CI₂) simultaneously presented, during a 5 min observation period. The genotypes of subject males are shown above the histograms, the genotypes of object flies beneath each bar. Subjects are (a) Canton-S (Cs), and Cs with the white¹¹¹⁸ mutation (w¹¹¹⁸), (b) various desat1^1573-1 alleles (1573-1, -D′1, -N2, -E1, and-J2,; see table 1). Objects are desat1^1573-1 mutant (desat) and control (Cs) females and males. The t-value and the probability (with the Student’s t-test) for discrimination between the two objects is shown below each bar; d.f.=68–84 for each test except for subject w¹¹¹⁸ paired with Cs (d.f.=40), and for subject 1573-1 males in white light (d.f.=48). The values for CI₁/CI₂ are as follows: for aA (43.3/9.4), aB (46/7.3), aC (25.2/17.9), aD (33.6/20.6), aE (33.3/21.3), aF (12/6.5), aG (35.2/11.8), aH (22.8/22), bA (21.9/17.5), bB (41.4/6.2), bC (41.8/17.6), bD (41/20.9), bE (29.8/16.1), bF (34/22.2).

Figure 4

Gal4 expression driven by the desat1^1573-1 strain. (a) Ventral view of a 7-day-old female abdomen. Expression was found in the ventral and lateral oenocytes (oe). The fat body showed a diffuse signal that declined during adulthood (not shown). (b) Right lateral view of a proboscis of a 1-day-old male. Gal4 expression was strong in the labial palp (lp; arrowhead), but weak in the maxillary palp (mp). (c) Posterior view of an antenna in a 7-day-old female. Expression was mostly found in the third segment (AIII; arrowhead), but not or weakly in the second segment (AII) or in the arista (ar). The reporter UAS-CD8GFP transgene was used to visualize the activity of desat1^1573-1 either by direct detection of the GFP (a,c) or by immunohistochemistry (b). Scale bar, 100μm.