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Spontaneous and Ethyl Methanesulfonate-Induced Mutations Controlling Viability in Drosophila Melanogaster

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Spontaneous and Ethyl Methanesulfonate-Induced Mutations Controlling Viability in Drosophila Melanogaster SPONTANEOUS AND ETHYL METHANESULFONATE-INDUCED MUTATIONS CONTROLLING VIABILITY IN DROSOPHILA MELANOGASTER. I. RECESSIVE LETHAL MUTATIONS OHM1 OHNISHI Laboratory of Genetics, Faculty of Agriculture, Kyoto University, Kyoto 606, Japan Manuscript received December 18, 1976 Revised copy received July 15,1977 ABSTRACT The efficiency of the adult feeding method for EMS treatment in Dro- sophila melanogaster was studied by measuring the frequency of induced recessive lethals on the second chromosome. The treatment was most effective when mature spermatozoa or spermatids were treated and was much less effec- tive on earlier stages. The number of mutations induced was proportional to the concentration except at the highest doses. The recessive lethal rate was estimated to be about 0.012 per second chromosome per IO-4~.In addition, about 0.004-0.005 recessive lethals per 10-4 M were found in a later genera- tion in chromosomes that had not shown the lethal effect in the previous gen- eration. When the experiments are done in a consistent manner and gametes treated as mature sperm or spermatids are sampled, the results are highly reproducible. However, modifications of the procedure, such as starvation before EMS treatment, can considerably alter the effectiveness of the mutagen. A central problem in population genetics is the relative importance of various factors determining genetic variability in natural populations. Interest in recurrent mutation as a major source of variation has been stimulated by the work of MUKAIand his associates (MUKAI1964; MUKAIet al. 1972), who re- ported a very high spontaneous rate for viability-affecting polygenic mutations in Drosophila melanogaster. From the standpoint of human welfare, the im- portance of mutations is enhanced by the possibility that a number of chemi- cals in our environment may be mutagenic. Ethyl methanesulfonate (EMS) is known to produce base-pair substitutions and chromosome changes. It also induces polygenic mutations affecting viability (MUKAI1970). Mutation and chromosome breaking effects have been reported by ALDERSON(1965) ,EPLER (1966), LIMand SNYDER(1968), JENKINS(1967) , LEE, SEGAand BISHOP(1970), BRINK(1970), YOST,IVES and HALL(1967), ABRAHAMSON,KIRIAZIS and SOBOL(1969), and BISHOPand LEE (1969). For a review of molecular mechanisms, see DRAKE(1969,1970). Supported in part by grants from the Public Health Service to the University of Wisconsin (GM-08217 and GM-22038). Genetics 87 : 519-527 November, 1977. 520 0. OHNISHI Most of the experiments have been done at high concentrations, around 1 0-2 M. The present series of experiments was undertaken to study the nature of mutations produced by feeding with relatively low concentrations of EMS. The main purpose was to study the rate of occurrence and the effects on viability of polygenic mutations. These results are reported in parts I1 and I11 of this series (OHNISHI1977a,b). This paper reports experiments on the induction of lethal mutations as a function of concentration. They establish the linearity of the mu- tation rate with concentration at low doses and offer guidance as to the range of concentrations to be used in the further experiments. MATERIALS AND METHODS The wild stock of Drosophila melanogaslei- used in these and all the following experiments was an inbred line established from a natural population in Madison, Wisconsin. The strain was sib-mated for more than three years. A male from this stock was mated with the labora- tory strain In(2) SMI, a12 Cy sp2 / In(2) Pm, dp b Pm dsss7;. From the progeny, a Cy/+ and a Pm/+ male were each backcrossed to the inbred wild-type strain. Again Cy/+ and Pm./+ progeny males were backcrossed to the inbred +/+ strain. This backcrossing procedure was repeated for 20 generations, after which a Cy/+ female and a Pm/+ male were mated to establish a Cy/Pm strain. This strain, except for the second chromosomes, has a genetic background derived from the wild-iype strain. The wild-type strain will he abbreviated +/+, and the marker strain that has background genotype isogenic with the wild-type strain will be designated Cy/Pm. The EMS treatment followed essentially the methods of LEWISand BACHER(1968). The EMS was in a 1% solution of sucrose. A piece of tissue paper soaked with 2.4 ml of this solu- tion was placed in a cylindrical shell vial, 23 x 93". Males 0 to 24 hours old were left in this vial for 24 hours at room temperature (ca 25"), then mated immediately in vials with standard culture medium. Seven concentrations of EMS were used, ranging from 1 x 10-4 to 2.5 x 10-2 M. At each concentratim 160 Pm/+ males were treated, 20 per vial. Each EMS-treated male was immediately mated with two Cy/Pm females. If the brood pattern was to he studied, the male was transferred to new Cy/Pm females on the 4th, 7th, and 10th day after treatment. The mating system for detecting recessive lethal mutations on the second chromosome is the standard method and is shown in Figure 1 as Lethal Test 1. To avoid the possibility of sampling large clusters of lethal mutations from a few males, only two Pm/+ males were sampled from the progeny of an individual treated male. The final mating between Cy/+ males and females (one or two pairs) was made in a vial with heavily yeasted food and kept at 25". The offspring were observed on the 12th or 13th day. The cultures in which no wild- type flies appeared by the 13th day were kept for three more days to make a final decision of lethality. If less than one percent of the progeny were +/+, the treated chromosome was clas- sified as lethal. In some experiments recessive lethals not manifested until a later generation (so-called mosaic mutations) were also studied (AUERBACHand KILBEY1971). The scheme to detect these is also shown in Figure 1 as Lethal Test 2. These tests involved one further generation of back- crossing before the chromosome was made homozygous. A chromosome that was not classified as lethal in Test 1, but was lethal in Test 2, was designated as a mosaic lethal. This method for detecting mosaic mutations does not answer the question of whether a given normal chromo- some carries a mosaic mutation, hut it gives an unbiased estimate of the frequency 3f lethals among the progeny of nonlethal F, chromosomes. The reason for treating Pm/+ rather than +/+ males was to obtain results comparable to those of Part I1 and TI1 of these experiments, where the type 3f male was treated in suc- EMS-INDUCED MUTATIONS IN DROSOPHILA 521 dEMS treatment -cy x --(id)Pm' Pm I + -cy x p" (16) Pm I + cy c'y +!T Lethal Test 1 cycy +i+ Lethal Test 2 FIGURE1.-Mating scheme to detect complete and mosaic recessive lethal mutations on chromosome 11. cessive generations (OIINISHI 3 977a,b), However, in order to compare mutation frequencies induced in the two genotypes, some experiments were also carried out with treated +/-I- males. EXPERIMENTAL RESULTS Although there is a report by ALDERSON(1965) that feeding adult flies with EMS causes some death, there was 100 percent survival in all the experiments reported here. However, there was sonie sterility, particularly in the higher con- centrations. About 10 percent of the males were sterile after treatment with 2.5 X M, and 5% and 3% with 1 X and 5 X M respectively. The percentage of sterility is roughly proportional to EMS concentration. The observed frequencies of chromosomes containing one or more recessive lethals induced by EMS are shown in Table 1. Those from the Pm/+ first brood data are converted to the number of lethal mutations per chromosome, assuming a Poisson distribution, in Table 2. Figure 2 shows the data in graphical form. It is apparent that the increase is very nearly linear, except €or a slight down- ward curvature at high doses. It might be expected that some of the effects of high concentrations might be to produce multiple-hit rearrangements, leading to an upward curvature. The failure to find this might be due to a compensatory effect stemming from a small fraction of flies that €ailed to feed on the EMS. PELECANOSand ALDERSON(1964) reported that at very high doses about 15 percent of the flies yielded no mutations, presumably because they failed to ingest any EMS. Table 2 shows a further analysis of the data. If 15 percent of the flies fail to feed during the treatment, as suggested by the results of PELECANOSand ALDER- SON (1964), we can correct the data accordingly. Assuming that this is true in my experiments, the expected number of mutants among those flies that feed 522 0. OHNISHI TABLE 1 Frequency of recessive lethal chromosomes induced by EMS Pm/+ 0 368 2 0.54 I XIO-4 209 3 1.44 5 x 10-4 206 IO 4.85 1 X 10-3 259 35 13.51 222 38 17.12 2% 25 12.20 182 11 6.04 2.5 X lk3 276 83 30.07 269 98 36.43 215 63 29.30 236 27 11.44 5 X IO-3 280 118 42.12 211 106 50.24 190 88 46.32 211 28 13.27 1 X IC2 156 94 60.26 +/+ 2.5 X le2 192 155 80.73 2.5 x 10-3 156 53 33.97 5 X lW 140 66 47.14 (a) Number of chromosomes tested. (b) Number of lethal chromosomes. (c) % of lethal chromosomes. on the EMS is given in the last two columns. As can be seen, with this correction the estimated number of EMS-induced mutations is almost exactly linear, and the number induced per M is nearly constant for all concentrations tested.
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