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Genetic Control of Pheromones in Drosophila Simulans. I. Ngbo, a Locus on the Second Chromosome

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Genetic Control of Pheromones in Drosophila Simulans. I. Ngbo, a Locus on the Second Chromosome Copyright 0 1991 by the Genetics Society of America Genetic Control of Pheromones in Drosophila simulans. I. Ngbo, a Locus on the Second Chromosome Jean-Franqois Ferveur Laboratoire de Biologie et Ginitique Evolutives, Centre National de la Recherche Scientijique, 91 198 Gijhur-Yvette, France Manuscript received May 9, 1990 Accepted for publication February 4, 1991 ABSTRACT 7-Tricosene and 7-pentacosene are predominant hydrocarbons on the cuticle of both sexes in Drosophila simulans. The pheromonal role of 7-tricosene has been clearly established for conspecific males, while a synergistic effect for 7-pentacosene has been postulated. Interstrain variation for the production of both compounds is very marked, but similar for both sexes. The genetic basis of this polymorphism was investigated. A major role was found for the second chromosome,which controls the 7-tricosene:7-pentacoseneratio. The main locus involved in controlling this variation,Ngbo, was mapped to position 65.3 on the second chromosome. The production of 7-pentacosene is directly related to the Ngbo genotype, which is additively expressed with two known alleles, Seychelles and Cameroon. These alleles act codominantly and are, respectively, hypomorphic and hypermorphicwith regard to their effect on 7-pentacosene production.The production of 7-tricosene, which is partially inversely related to that of 7-pentacosene, is also affected by secondary interactionswith the second chromosome and with the autosomal background. YDROCARBONS on the cuticle of Drosophila simulans because these compoundsare present in both H simulans females act as pheromones capable of sexes in similar amounts. inducing conspecific male courtship (JALLON 1984). BENAMARand JALLON (1983) suggested that the The hydrocarbon systems of matureflies of bothsexes level of 7-T in D. simulans was controlled by the X are virtually identical and mainly consist of long-chain chromosome.FERVEUR, COBB and JALLON (1989) hydrocarbons with one double bond, in position 7. showed that one pair of autosomes played a major The predominant cuticular hydrocarbonsshow a geo- role in controlling the ratio of 7-T:7-P, and that the graphical polymorphism: 7-tricosene(7-T; 23 car- production of 7-T was also dependent on sex-linked bons), which has been shown to induce wing display factor(s). The genetic control of male-predominant in conspecific males (JALLON1984), is the major hy- compounds (7-T and 7-P) in D. melanogaster appears drocarbon in both sexes of most strains. Flies from to be highly complex, possibly involving all chromo- somes (SCOTTand RICHMOND1988). around theBenin Gulf in Africa have higher levels of In order to further our understanding of genetic 7-pentacosene (7-P; 25 carbons). This variation simul- controlof Drosophila pheromone production, we taneously affects both sexes (LUYTEN1982). have undertaken an exhaustive investigation testing has been studied in bioassays with 7-T D. simulans. each potential hereditary factor. In this studywe have The roleof 7-P, the predominant hydrocarbon in chosen to concentrate on the relative and absolute some African strains, is not yet known, although 7-P production of 7-T and 7-P in D. simulans. We chose alonecannot stimulate precopulatory behavior in this species because the absence of a qualitative hydro- males from the 7-T-rich D. simulans Seychelles strain carbonsexual dimorphism allows both sexes to be (J.-M. JALLON, unpublished results). On thebasis of a analyzed and, unlike D. melanogaster, the interstrain study of inter- and intraspecific courtships, COBBand hydrocarbon polymorphism is very marked, and may JALLON (1 990)proposed that 7-P may also play a role be controlled by only a few genes. in stimulating courtship in D. simulans males, perhaps through synergistic effects. MATERIALS AND METHODS It has been suggested that 7-T or 7-P, which are Drosophila stocks and crosses: Strains of Drosophila si- predominant hydrocarbons in Drosophila melanogaster mulans were kept at 25 & 0.5”,under a 12: 12 dark:light males, mayplay a strain-specific “anti-aphrodisiac” cycle, on standard cornmeal food. The Cameroon strain is role in this species, following their transfer onto the derived from a small number of fertilized females collected in Yaounde in 1975. As with other D. simulans strains from femalecuticle during mating (SCOTT and JACKSON the Benin Gulf area, both sexes of Cameroon flies produce 1988). Such an effect should not be expected in D. more 7-P than 7-T. The Seychelles strain is derived from Genetics 128: 293-301 (June, 1991) 294 J.-F. Ferveur severalinseminated females collected in the Seychelles logarithmically transformed (log,) in order to reduce intra- archipelago in 198 I. As with most D. simulans strains (all strain variations in 7-T and 7-P levels. The variation in 7- except those fromthe Benin Gulf), both sexesproduce more T:7-P levels wascompared with changes in absolute amounts 7-T than 7-P. of 7-T and 7-P in small samples of flies raised together. The inheritance of hydrocarbon phenotype variation was These results suggested that absolute amounts of the two studied by crosses between the two parental strains (Came- substances would not be a suitable parameter for studying roon and Seychelles), based on flies bred in the same con- genetic determination, assignificant intrastrain variation ditions and analyzed within a short period of time. Chro- could occur within a short space of time (see RESULTS). mosomal localization of genes involved hydrocarbonin phe- notype variationwas carried out using the following marked strains: (1) G strain, which carried the recessive markers RESULTS garnet (I,44.4), net (11,O.O) and cinnabar (II,57.5) (a gift of J. COYNE).(2) NBPSP or secondchromosome recessive Hereditarycontrol of hydrocarbon variation: multimarker strain, which carries net (11,O.O) black (I1,45.0) Flies were characterized by their hydrocarbon phe- pearly (II,74.0) spread (IIJ30.0) and plum (11,108.0) (a gift notype (S or non-S) based on two quantitative char- of J. COYNE).(3) W strain, which carries the Curly mutation acters: % and % 7-P (see Figure 1). Mean (IX,6.8) (a gift of T. WATANABE).For crosses, five pairs of 7-T 7-T 4-day-old flies were placed in vials withfood. Each cross was and 7-P percentages were alsocalculated foreach replicated at least nine timesfor each experiment. group of flies. Results of chromatographic analysis Extraction and analysis of cuticular hydrocarbons:For of males and females from all sixteenstrains ob- each experiment, flies from different strains or crosses were tained from the two parental strains, Seychelles and collected and bred simultaneously. Flies were sexed under Cameroon, their backcrosses and F2 are shown in light etherization shortly after eclosion and were kept in FI, groups offive on fresh food. Following the method of Table 1. ANTONYand JALLON(1982), 4-day-old flies were individ- When strains differedfor some of their autosomes ually washed in 50 PI hexane in a microtube and agitated they showed significant differences either for S/non- for 1 min. Washed flies were immediately removed from S characterization (SS us. strain 1 males, SS us. strain eachmicrotube. In certain samples, 20 pl of a hexane 5 females), or for their mean percentage7-T and 7-P solution containing 800 ng of hexacosane (26C) as an inter- nal standard were added to each tube. When the solvent levels within the non-S class (CC us. strain 2 females; was fully evaporated, each microtube, now containing a dry CC us. strain 6 males). These differences were com- extract, was sealed with a Teflon cap and stored at -20" posed of twoeffects. The hydrocarbonphenotype until analysis. classification differentiated flies homozygous for Sey- Immediately before analysis 20 pl hexane were added to chelles autosomes from other genotypes; variations in each microtube, and after gentle agitation 5 PI of the re- sultant solution were injected into a Girdel 300 gas chro- mean % 7-T and % 7-P within the non-S class must matograph equipped with a C.P. Si1 5 capillary column (1 = be caused by the varying autosomal genotypes present 25 m; $ = 0.23 mm) with nitrogen as the vector gas (P = in this class. 0.5 bar). During analysis the temperature increased from Otherhereditary components (X chromosomes 170 to 250 at a rate of Z"/min. Peak detection was carried " tested only between females, Y chromosome and cy- out using a Flame Ionization Detector coupled with an SP 4270 Spectraphysics integrator which yields retention times toplasmic factors) showed no significant effects. Com- and areas under each peak. Extractsof different phenotypes parisonof S/non-S distributions between males of were injected in varying order to randomize experimental strains 1 and 5 was significant (P < 0.001). This effect variability. was initially attributed to the Y chromosome but upon The majorhydrocarbon compounds of D. simulans further investigation was revealed to be a sampling Seychelleshave been chemically identified by PECHIN~ et al. (1985) and show characteristic constantretention times effect caused by delayed eclosion of certain hydrocar- (+-0.2%under constant conditions) overmany generations. bon phenotypes. For each fly spectrum, we calculated the total quantities Although the production of 7-T and 7-P varied in of hydrocarbon using the summed areas of 13 compounds different strains, their sum (% 7-T + % 7-P) for all which are always detected in this species. Eachhydrocarbon strains pooled remained remarkably constant both for was characterized by its percentage relative to the total hydrocarbon sum. By comparing this figure to that of the males (57.5 f 0.2; n = 719) and for females (62.3 f internal hexacosane standard, the absolute quantity in ng 0.2; n = 750). Within the sample as a whole, and for could also be calculated. all strains exceptS X S, there was a significant negative Hydrocarbonparameters: To localizegenetic factors correlation between the proportions of7-T and of 7- involved in the 7-monoene polymorphism,different hydro- P inindividual flies.
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