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Genetic Analysis of Drosophila Virilis Sex Pheromone: Genetic Mapping of the Locus Producing Z-(Ll)-Pentacosene

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Genetic Analysis of Drosophila Virilis Sex Pheromone: Genetic Mapping of the Locus Producing Z-(Ll)-Pentacosene Genet. Res., Camb. (1996), 68, pp. 17-21 With 1 text-figure Copyright © 1996 Cambridge University Press 17 Genetic analysis of Drosophila virilis sex pheromone: genetic mapping of the locus producing Z-(ll)-pentacosene MOTOMICHI DOI*, MASATOSHI TOMARU, HIROSHI MATSUBAYASHI1, KIYO YAMANOI AND YUZURU OGUMA Institute of Biological Sciences, University of Tsukuba, 1-1-1, Tsukuba, Ibaraki 305, Japan (Received 27 June 1995 and in revised form 18 December 1995) Summary Z-(ll)-pentacosene, Drosophila virilis sex pheromone, is predominant among the female cuticular hydrocarbons and can elicit male courtship behaviours. To evaluate the genetic basis of its production, interspecific crosses between D. novamexicana and genetically marked D. virilis were made and hydrocarbon profiles of their backcross progeny were analysed. The production of Z- (ll)-pentacosene was autosomally controlled and was recessive. Of the six D. virilis chromosomes only the second and the third chromosomes showed significant contributions to sex pheromone production, and acted additively. Analysis of recombinant females indicated that the locus on the second chromosome mapped to the proximity of position 2-218. - and some work on the genetic basis of their control 1. Introduction has been done. Female cuticular hydrocarbons in Drosophila play an In D. simulans, intrastrain hydrocarbon poly- important role in stimulating males and can elicit male morphism is very marked, and two loci that are courtship behaviours, that is, some can act as a sex involved in controlling the hydrocarbon variations pheromone (Antony & Jallon, 1982; Jallon, 1984; have been identified. One is Ngbo, mapped to position Antony et al. 1985; Oguma et al. 1992; Nemoto et al. 65-3 on the second chromosome (Ferveur, 1991), the 1994). Sex pheromones, in most cases, can stimulate other is ke'te, mapped to position 18-5 on the X only conspecific males, acting as species-specific mate chromosome (Ferveur & Jallon, 1993). Scott & recognition signals. The signal differences between Richmond (1988) showed that in D. melanogaster close relatives could cause mate discrimination and males production of the predominant hydrocarbon contribute to sexual isolation (Lofstedt & Van Der was controlled by all three major chromosomes. Thus Pers, 1985; Cobb & Jallon, 1990). Sex pheromones there are at least three factors responsible for have now been identified in many insects, but the hydrocarbon production and variation in this male. evolutionary mechanisms involved in their diversity Coyne et al. (1994), however, showed that the and fixation processes among species are unclear hydrocarbon difference between the very close rela- (review by Roitberg & Isman, 1992). tives D. simulans and D. sechellia mapped to only the One reason for the lack of knowledge on how sex third chromosome. They concluded that isolating pheromones have diverged and been fixed is the lack mechanisms caused by hydrocarbon differences might of data on their genetic control. There have been have a fairly simple genetic basis. Therefore, although relatively few reports on genetic analysis of phero- many genes might contribute to pheromone pro- monal signals because of the difficulty of genetic work duction, a small number of genes may determine the in many taxa. However, in Drosophila, genetic species-specificity. techniques can be used, and many marker mutants (Z)-ll-pentacosene (11-P; 25 carbons with a single and cross experiments are available. Sex pheromones double-bond in position 11) is the major sex phero- have already been identified in four species - D. mone component in D. virilis females (Oguma et al. melanogaster, D. simulans (Jallon, 1984), D. pallidosa 1992). It comprises over one-third of the total, being (Nemoto et al. 1994) and D. virilis (Oguma et al. 1992) the predominant female cuticular hydrocarbon, and can elicit courtship behaviours in D. virilis males. D. * Corresponding author. 1 Current address: Department of Applied Biology, Kyoto Institute virilis is a widely distributed cosmopolitan species and of Technology, Matsugasaki, Kyoto 606, Japan. belongs to the virilis species group (consisting of 11 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.58, on 01 Oct 2021 at 17:29:33, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S001667230003384X M. Doi and others 18 species; Throckmorton, 1982). This group has been except the second could not be controlled, their well investigated as regards many aspects of evol- chromosome constitutions were mixed with utionary history, phylogeny, population dynamics novamexicana/virilis and virilis/virilis. and ecology using cytogenetic, population and bio- chemical approaches (Alexander, 1976). Many studies (iii) Hydrocarbon analysis have evaluated the phyiogenetic relationships among the group (reviewed by Spicer, 1992). Their cuticular In both experiments all females used for hydrocarbon hydrocarbons, especially in D. virilis, have also been analysis were 9-13 days old. Cuticular hydrocarbons investigated (Jackson & Bartelt, 1986; Bartelt et al. were removed from an individual female by washing 1986). This group is very suitable for examining the for 5 min in 50 /tl hexane in a microtube and agitation evolution of sex pheromones. We examined the genetic for 1 min. The fly was removed immediately after control of 11-P production in D. virilis by chromo- washing and the solvent fully evaporated from the somal and recombinant analyses using D. virilis and microtube. These microtubes were stored at —40 °C D. novamexicana. until GC analysis. Before GC analysis, 20 fi\ hexane containing 50 ppm docosane (C22), an internal stan- dard, was added to each microtube. After agitation 2. Materials and methods for 1 min, 1 /il of the solution was injected into a GC380 gas chromatograph (GL Science) equipped (i) Drosophila stocks with a FFAP column (0-25 mm ID x 25 m, D.F. = Two D. virilis strains (National Drosophila Species 0-25 fim, Quadrex), with a Flame Ionization Detector Resources Center nos. 15010-1051.83,15010-1051.54) for peak detection. Temperature was programmed and the D. novamexicana wild-type strain (National from 160 °C to 250 °C at 2-5 °C/min. We compared Drosophila Species Resources Center no. 15010- the peak area of 11-P with that of the internal 1031.4) were used in the crosses. Strain 1051.83, used standard C22 and measured the 11-P/C22 ratio. in the chromosomal analysis, had all its autosomes Differences in the 11-P/C22 ratio between genotypes except for the sixth chromosome (which is a tiny dot were tested with an analysis of variance (ANOVA) chromosome only about one map unit long) marked followed by the Tukey multiple comparison and t- with recessive markers. The genetic markers and their tests (Zar, 1984). map positions are as follows: broken (b, 2-188.0), gapped (gp, 3-118.5), cardinal (cd, 4-32.2), peach (pe, 3. Results 5-203.0) (Alexander, 1976; Gubenko & Evgen'ev, 1984). The other strain (1051.54), used in genetic (i) Chromosomal contributions to 11-P production mapping on the second chromosome, has four Chromosomal contributions to 11-P production were markers: Confluent (C, 2-45.0), broken, brick (bk, examined by measuring the 11-P/C22 ratios (Table 2-248.0), detached (dt, 2-255.0) (Alexander, 1976; 1). The mean ratio±S.E. in D. virilis b;gp;cd;pe Gubenko & Evgen'ev, 1984). females was 0-92 + 0044, indicating that one D. virilis All flies were kept on standard cornmeal and yeast female contains about 5-0/<g 11-P. This value was medium under a 14L (0700-2100 hours): 10D cycle at consistent with that of D. virilis wild strain (TK) 25 + 1 °C. reported by Oguma et al. (1992). The mean 11-P/C22 ratio+ S.E. of D. novamexicana females was 002 + 0001, less than one-tenth that of D. virilis. F, (ii) Crosses hybrid females also showed a low 11-P/C22 ratio All crosses were performed as mass mating with 40 (009±0-009), suggesting that the production of 11-P flies of each sex in a vial. To examine the chromosomal was recessive. Preliminary analysis in Ft males contribution to 11 -P production, first D. novamexicana indicated that the factor controlling 11-P production females were crossed to D. virilis b;gp;cd;pe males, was autosomal, because both Fx males from the and then Fx males were backcrossed to b;gp;cd;pe reciprocal crosses had a small amount of 11-P (data females. The backcross progeny were collected at 24 h not shown). intervals and female flies carrying only one homo- Table 1 also shows the mean 11-P/C22 ratio for zygous D. virilis chromosome, whose phenotypes were each genotype. An ANOVA was performed between [b], [gp], [cd], [pe] and [ + ], were selected. For all five genotypes of backcross progeny (Ft 145 = 204-15, genotypes, five females were maintained in each food P < 0-001), and the Tukey multiple comparison test vial until GC analysis. revealed that the second and the third chromosome For the mapping on the second chromosome, D. have significant effects on 11-P production. No novamexicana females were crossed to D. virilis significant effect was found for the fourth or the fifth C b bk dt males. Fl females were then backcrossed to chromosome. The 95 % confidence limits for the mean C b bk dt males and their progeny, classified into eight ratio in b;gp;cd;pe females were 0-837-1-009, and genotypes (see Table 2), were separately maintained those for the sum of the mean ratio in b females and until hydrocarbon analysis. Since all chromosomes in gp females were 0-813-0-959. This indicates that the Downloaded from https://www.cambridge.org/core. 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