Genes Affecting Productivity in Natural Populations of DROSOPHILA MELANOGASTER

Two hundred second chromosomes were extracted from a Japanese population in October of 1972, and the viabilities and productivities of homozygotes and heterozygotes from them were examined. Viability was measured by the Cy method and productivity by the number of progeny produced per female. The frequency of lethal-carrying chromosomes was 0.315. When the average heterozygote viability was standardized as 1.000, the average homozygote viability was 0.595 including the lethal lines, and 0.866 excluding them. The frequency of recessive sterile chromosomes among 131 non-lethal lines was 0.092 in females and 0.183 in males. There were two instances in which homozygosis for the second chromosome caused sterility in both sexes, which was close to the number expected (2.2) on a random basis of 0.092 x 0.183 x 131. When the average heterozygote productivity of 200 lines was standardized as 1.000, the average homozygote productivity was 0.532 including female steriles, and 0.584 excluding them. The ratio of detrimental load to lethal load was 0.383, while the ratio of partial sterility load to complete sterility load was 5.767. The average viability of lethal heterozygotes was slightly, but not significantly, lower than that of lethal-free heterozygotes, while the average productivity of lethal heterozygotes was significantly lower than that of lethal-free heterozygotes. There was a significant association of sterility in either sex with low viability of homozygotes. However, no statistically significant differences in viability and productivity were detected between sterile heterozygotes and non-sterile heterozygotes. The heterozygous effects of viability and productivity polygenes were examined by regressions of the heterozygotes on the sum of corresponding homozygotes. The regression coefficients were slightly positive for both viability and productivity if lethal and sterile chromosomes were excluded. The correlation between viability and productivity in homozygotes was significantly positive when sterile chromosomes were included, but the significance disappeared when the sterile chromosomes were excluded. In the heterozygotes there were no detectable correlations between them.     

Gene Polymorphism in Natural Populations of DROSOPHILA PERSIMILIS

Genetic variation at 43 loci has been studied in six different populations of Drosophila persimilis by electrophoresis of enzymes and proteins. In D. persimilis the mean proportion of polymorphic loci is 0.362, the mean proportion of heterozygous loci per individual is 0.100 and the average number of alleles per locus is 1.651. In all populations, the loci coding for the hydrolytic and other nonspecific enzymes are much more variable than the loci coding for the enzymes of the glycolytic pathway, Kreb's cycle, other specific enzymes and larval proteins. Most loci have similar allele frequency in all populations except the two loci, Amylase and Pt-12, which show a pattern of associations of different alleles with different third chromosome inversions.     

Concurrent Multiple Paternity in Natural and Laboratory Populations of DROSOPHILA MELANOGASTER

Electrophoretic analysis of two or three linked enzyme loci in progenies of homozygous females from cage and natural populations demonstrates frequent concurrent multiple paternity in both cases.     

Enzyme and Chromosome Polymorphisms in Japanese Natural Populations of DROSOPHILA MELANOGASTER

Collections of D. melanogaster from Japanese populations were analyzed for enzyme and chromosomal polymorphisms. Allelic frequencies at the Adh and alphaGpd loci were compared with polymorphic inversion (In(2L)B, In(2R)C) frequencies in the second chromosome. There was a significant positive correlation between the frequencies of AdhS and In(2L)B, caused by linkage. On the other hand, inversion-free cage populations maintained in the laboratory for a long time showed considerably larger variation in the frequencies of these enzyme alleles, which seem very likely to be a consequence of random drift. Two fitness components of these enzyme and chromosomal variants were measured in two different environmental conditions; neither of the two loci showed heterozygote superiority in viability or productivity, while the inversion heterozygotes showed a superior productivity compared to the corresponding homozygotes in the fluctuating environment. These findings are compatible with the hypothesis that polymorphic isozyme genes are maintained by random drift of neutral genes in natural populations, and that association with linked inversions is a historical accident.     

Linkage Disequilibrium in Natural Populations of DROSOPHILA MELANOGASTER. Seasonal Variation

Linkage disequilibrium among ten polymorphic allozyme loci and polymorphic inversions on chromosomes 2 and 3 in a natural population of Drosophila melanogaster was examined early and late in the annual season. Similar to previous studies, little linkage disequilibrium was observed among allozymes. The two significant cases that were observed in the first sample behaved in a contradictory way. One declined much more rapidly than expected due simply to recombination; the other declined slowly as expected. There was little change in allozyme or inversion frequencies during the season.     

A Survey of Isozyme Polymorphism in a DROSOPHILA MELANOGASTER Natural Population

A survey of biochemical polymorphism among glucose- and non-glucose-metabolizing enzymes was carried out on the June 1973 collection from the South Amherst, Mass. Drosophila melanogaster natural population. Polymorphic levels are among the highest recorded for this species; polymorphism among glucose-metabolizing enzymes did not differ significantly from that among non-glucose-metabolizing enzymes. Two loci, G6Pd on the X and Est-6 on the 3rd chromosome, displayed significant excesses of heterozygotes. Adh on the 2nd and Idh, Odh and Ao on the 3rd chromosome showed significant heterozygote deficiencies. Idh is ten map units to the left of Est-6, Odh twelve map units to the right and Ao is seven units beyond Odh. Temperatures in the two-week June period prior to collection were exceedingly variable. Daily high/low ranged between 76°/40° and 97°/65°F. These results support the findings of Frydenberg and Simonsen (1973) that in some populations glucose-metabolizing enzymes tend to be as polymorphic as non-glucose-metabolizing ones. They also add to the evidence obtained from other plant and animal populations that increased biochemical polymorphism is associated with more variable and/or colder climates. The increase may in part be due to increased polymorphism among glucose-metabolizing enzymes. Comparisons utilizing published data on other D. melanogaster populations and on D. robusta indicate a clinal increase in heterozygosity among glucose-metabolizing enzymes as one moves northward.     

Balancing Selection, Inversion Polymorphism and Adaptation in Ddt-Resistant Populations of DROSOPHILA MELANOGASTER

The modes of selection important in maintaining an inversion-allozyme polymorphism in two laboratory populations of Drosophila melanogaster were examined. The populations, 731R and J2, are highly resistant to DDT. The polymorphism involves the Standard and In(3R)P chromosomal arrangements in very strong linkage association with the AO ¹ and AO⁴ allozymes, respectively, of the aldehyde oxidase locus—The mean fertilities of the three karyotypes were not significantly different in 731R, but, in J2, In/In was significantly inferior to St/St and St/In. Egg-to-adult viability tests indicated very strong heterozygote advantage at all frequency combinations of the karyotypes in both populations when DDT was present. When DDT was excluded, the viabilities varied over the frequency combinations but were not inversely correlated with karyotype frequency, as predicted by balancing frequency-dependent selection. Discrete, multiple-generation experiments showed a rapid increase in heterozygote frequency to about 80% in both populations when DDT was present. Without DDT, 731R showed apparent directional selection favoring St, whereas J2 showed persistence of the polymorphism, although with extensive fluctuation.—Thus, the inversion-allozyme polymorphism is directly involved in the adaptation to a specific environmental component, DDT, and the selective advantage of the heterozygotes is the important balancing force. Balancing frequency-dependent selection was not observed, which suggests the hypothesis that this form of selection may not be involved in adaptation to novel environmental conditions.     

Factors Influencing the Effect of Segregation Distortion in Natural Populations of DROSOPHILA MELANOGASTER

The major components of the SD system have been examined in two natural populations of D. melanogaster to investigate how SD behaves and is maintained in nature and to estimate its impact and efficiency. A twofold approach was used: (1) direct measurements of segregation distortion in wild males and (2) measurement of sensitivity of wild SD (+) chromosomes to SD action. Characterization of newly isolated SD chromosomes and of a large number of SD( +) chromosomes from nature demonstrated that (1) SD can operate efficiently in the wild genome: 45% of SD/SD(+) males collected from nature had k values larger than 0.70. (2) Forty-three of 44 newly recovered SD chromosomes are of the SD-72 type, having a small pericentric inversion that maintains tight linkage among the Sd, E(SD) and Rsp loci in the SD complex. In 1956, most SD chromosomes in Madison lacked this inversion. (3) Only 12 of the 44 SD chromosomes carried a recessive lethal (compared with five of six in 1956), and many of the viable SD chromosomes were fertile as homozygotes, indicating that SD homozygotes need not have obvious reductions in fitness. (4) Among more than 500 wild chromosomes assayed for response to distortion by a strong SD, at least 40-50% were sensitive, about 33% were partially sensitive and 17% were insensitive. This frequency of sensitives is higher than in reports from some other populations. An estimated 12% of the wild chromosomes were classified as true Rsp(i) by their constellation of effects, including a special test of ability to cause self-distortion of a "suicide" chromosome, R(cn)-10. In a direct assay with R(cn)-10, an independent sample of 99 chromosomes from nature gave 30% putative Rsp(i). Thus, these populations contain in the range of 12-30% Rsp(i). (5) Chromosomes supersensitive to SD, previously described for certain laboratory stocks, were also found to coexist in nature with SD. (6) Profiles of wild chromosomes with a panel of three or four different SD testers suggest a series of allelic alternatives at the Rsp locus including supersensitive, sensitive, semisensitive and insensitive, and that loci other than Rsp may also be important in determining the effect of SD in nature.     

Inversion Clines in Populations of DROSOPHILA MELANOGASTER

Twenty different natural populations of Drosophila melanogaster were sampled to determine the frequencies of inversions. Based on their frequencies and geographical distributions, the inversions could be classified as follows: (1) Common cosmopolitan inversions that are present in many populations in frequencies exceeding five percent and that may exhibit frequency clines over large geographical regions; (2) Rare cosmopolitan inversions that occur throughout the species range but usually at frequencies below five percent and that may be absent in many populations; (3) Recurrent endemic inversions that are found in several adjacent populations in frequencies usually not exceeding one or two percent; and (4) Unique endemic inversions that are found only among the progeny of a single individual and that may represent one aspect of the syndrome termed "hybrid dysgenesis". Four common cosmopolitan inversions that exhibit highly significant clines in populations in the eastern United States are In(2L)t, In(2R)NS, In(3L)P and In(3R)P.     

Association of Chromosome and Enzyme Polymorphisms in Natural and Cage Populations of DROSOPHILA MELANOGASTER

The frequencies of a polymorphic inversion, In(2L)t, and of Adh and αGpdh alleles were analyzed in three natural populations of Drosophila melanogaster from Japan. Significant positive correlations between the frequencies of In(2L)t and Adh^S or αGpdh^F were detected due to tight linkage. An analysis of correlation with latitude showed that the negative cline of Adh^S frequency could be explained entirely by its linkage with In(2L)t; the frequency of Adh^S on the standard chromosome did not show a latitudinal cline. To the contrary, the cline of αGpdh^F frequency itself was positive, and its linkage with In(2L)t makes the positive cline unclear. These results suggest that the two allozymes themselves respond to latitudinal natural selection in different ways. When these populations were transferred to laboratory cages and maintained for a long time, they lost the chromosomal polymorphism but retained stable enzyme polymorphisms, although allele frequencies in the cage were not the same as in nature. The frequencies of Adh and αGpdh alleles were close to those in earlier cage populations of the same geographical origin.     

Excess Polymorphism at the Adh Locus in DROSOPHILA MELANOGASTER

The evolutionary history of a region of DNA encompassing the Adh locus is studied by comparing patterns of variation in Drosophila melanogaster and its sibling species, D. simulans. An unexpectedly high level of silent polymorphism in the Adh coding region relative to the 5' and 3' flanking regions in D. melanogaster is revealed by a populational survey of restriction polymorphism using a four-cutter filter hybridization technique as well as by direct sequence comparisons. In both of these studies, a region of the Adh gene encompassing the three coding exons exhibits a frequency of polymorphism equal to that of a 4-kb 5' flanking region. In contrast, an interspecific sequence comparison shows a two-fold higher level of divergence in the 5' flanking sequence compared to the structural locus. Analysis of the patterns of variation suggest an excess of polymorphism within the D. melanogaster Adh locus, rather than lack of polymorphism in the 5' flanking region. An approach is outlined for testing neutral theory predictions about patterns of variation within and between species. This approach indicates that the observed patterns of variation are incompatible with an infinite site neutral model.     

The Alcohol Dehydrogenase Polymorphism in Populations of DROSOPHILA MELANOGASTER. I. Selection in Different Environments

The allozyme polymorphism at the alcohol dehydrogenase locus in Drosophila melanogaster was studied in order to obtain experimental evidence about the maintenance of this polymorphism. Populations started with different initial allele frequencies from homozygous F and S lines showed a convergence of frequencies on regular food at 25 degrees, leading to values equal to those in the base populations. These results were interpreted as due to some kind of balancing selection. In populations kept at 29.8 degrees, a lower equilibrium F frequency was attained. Addition of ethanol and some other alcohols to the food gave a rapid increase in F frequency, and high humidity decreased the F frequency slightly. Combination or alternation of ethanol and high humidity had variable effects in the populations tested. For a further analysis of the allele-frequency changes, estimates were obtained for egg-to-adult survival under different conditions and for adult survival on ethanol-supplemented food. On ethanol food (both at regular and high humidity), egg-to-adult survival of SS homozygotes was considerably lower than that of the FF and FS genotypes. Under regular conditions of food, temperature and humidity, a tendency to heterozygote superiority was observed, while at high humidity a relative high survival of SS was noticed in some tests. Adult survival of SS was lower than that of FF, but FS was generally intermediate, though the degree of dominance differed between populations. The results are consistent with the hypothesis of the occurrence of selection at the Adh locus.     

Density-Dependent Fertility Selection in Experimental Populations of DROSOPHILA MELANOGASTER

The effects of larval density on components of fertility fitness were investigated with two mutant lines of Drosophila melanogaster. The differences in adult body weight, wing length, larval survivorship and development time verified that flies reared at high density were resource limited. Experimental results indicate that: (1) relative fecundities of both sexes show density-dependent effects, (2) there is a strong density effect on male and female mating success, and (3) in general, there is a reduction in fecundity differences between genotypes at high density. These results imply that it may be important to consider fertility in models of density-dependent natural selection.     

Suppressor Systems of Segregation Distorter (SD) Chromosomes in Natural Populations of DROSOPHILA MELANOGASTER

Several natural populations of D. melanogaster were investigated for the presence (or absence) of the Segregation Distorter ( SD) chromosomes and their suppressor systems. The SD chromosomes were found, at frequencies of a few percent, in two independent samples taken in different years from a Raleigh, North Carolina, population, whereas no SD chromosomes were found in samples collected from several populations in Texas. The populations in these localities were found to contain suppressor X chromosomes in high frequencies (75% or higher). They also contained relatively low frequencies of partial suppressor or insensitive second chromosomes of varying degrees, but completely insensitive second chromosomes were practically absent in all populations examined. The frequencies of suppressor X chromosomes, as well as those of the partially insensitive or suppressor second chromosomes, were the same among the populations investigated. This suggests the possibility that the development of a suppressor system of SD in a population could be independent of the presence of an SD chromosome. Segregation distortion appeared to be occurring in natural genetic backgrounds, but the degree of distortion varied among males of different genotypes. There were many instances in which the SD chromosomes showed transmission frequencies from their heterozygous male parents that were smaller than 0.6 and, in several cases, even smaller than 0.5. The presence of a recessive suppressor, or suppressors, of SD in natural populations was suggested.