Genic VERSUS Chromosomal Variation in Natural Populations of DROSOPHILA SUBOBSCURA

Gametic frequencies in one mainland and one island population of D. subobscura were obtained by means of extracting wild chromosomes and subsequently analyzing them for inversions and allozymes. The high degree of cytological heterogeneity which characterizes these populations is not reflected in the genetic data. Two cases of non-random association were observed among eighteen pair-wise comparisons involving gene alleles and inversions to which the locus is linked. In both cases exchange of alleles at the locus is completely suppressed by the inversions. Four cases of linkage disequilibrium were detected among eighteen pairs of loci; two of them could best be explained as transient associations generated by random drift. The results suggest that disequilibria among enzyme loci are not widespread in natural populations—Populations with a lower degree of chromosomal variation are genetically as variable as populations with a higher degree of chromosomal variation. This observation does not support the hypothesis that selection in marginal homokaryotypic populations is for specialized homozygous genotypes.     

Evidence for Linkage Disequilibrium Maintained by Selection in Two Natural Populations of DROSOPHILA SUBOBSCURA

One island and one mainland population of Drosophila subobscura were found polymorphic at the XDH (xanthine dehydrogenase) and the AO (aldehyde oxidase) loci. It was observed that one allele at the XDH locus, which has a low frequency in both populations, is nonrandomly associated with the alleles at the AO locus. Two lines of evidence support the thesis that this linkage disequilibrium is due to epistasis rather than random drift: (1) D or r, measures of the disequilibrium, have the same sign and magnitude in both populations. (2) The linkage disequilibrium is not due to inversions. Inversions segregating on the chromosome carrying XDH and AO have been separated into two classes, between which exchange of alleles at the two loci is suppressed. Linkage disequilibrium for XDH and AO was observed within each class. In the absence of any exchange of alleles, these disequilibria must have arisen and been maintained independently. The suggestion is made that the epistatic disequilibrium results from the close structural and physiological relationship which exists between the two enzymes.     

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.     

Microgeographic and Temporal Genetic Differentiation in Natural Populations of DROSOPHILA SUBOBSCURA

Evidence of microgeographic and temporal genetic differentiation in natural populations of Drosophila subobscura is presented. The alcohol dehydrogenease locus was used as a genetic marker. Behavioral differences among the sexes and genotypes may explain these observations, although the molecular basis remains obscure.     

The Genetic Structure of Natural Populations of DROSOPHILA MELANOGASTER. Xii. Linkage Disequilibrium in a Large Local Population

Seven hundred and three second chromosomes were extracted from a Raleigh, North Carolina population of Drosophila melanogaster in 1970. Additionally, four hundred and eighty-nine third chromosomes were extracted from a large cage population founded from the flies in the 1970 Raleigh collection. The alpha glycerol-3-phosphate dehydrogenase-1, malate dehydrogenase-1, alcohol dehydrogenase, and alpha amylase loci were studied from the second chromosomes, and the esterase-6, esterase-C, and octanol dehydrogenase loci were analyzed from the third chromosomes. Inversions, relative viability and fecundity were studied for both classes of chromosomes. The following significant findings were obtained: (1) All loci examined were polymorphic or had at least two alleles at appreciable frequencies. Analysis of the combined data from this experiment with that of Mukai, Mettler and Chigusa (1971) revealed that the frequencies of the genes in the second chromosomes collected in early August were approximately the same over three years. (2) Linkage disequilibria between and among isozyme genes inter se were not detected except in a few cases which can be considered due to non-random sampling. (3) Linkage disequilibria between isozyme genes and polymorphic inversions were detected when the recombination values between the breakage points of the inversions and the genes in question were small. In only a few cases, were second and third order linkage disequilibria including polymorphic inversions detected. (4) Evidence for either variation among genotypes within loci or cumulative effects of heterozygosity was found for viability and fecundity. As a result of these findings, it was tentatively concluded that although selection might be perceptibly operating on some polymorphic isozyme loci, most of the polymorphic isozyme genes are selectively neutral or near-neutral in the populations studied.     

A Study of Linkage Disequilibrium in British Populations of DROSOPHILA SUBOBSCURA

Data have been obtained concerning the genetic content of samples of O chromosomes from three British populations, and J chromosomes from one population, of Drosophila subobscura. Some improvements to the genetic map of the O and J chromosomes have been made. Allele frequencies at the loci studied do not show much geographical variation, except where associations with geographically varying gene arrangements distort the picture. Striking nonrandom associations between alleles at three enzyme loci and closely linked O chromosome gene arrangements are present. Some historical explanation for these associations cannot at present be ruled out, but it is clear that a very high degree of genetic differentiation must exist between different gene arrangements in this species. There is no convincing direct evidence for linkage disequilibrium between pairs of enzyme loci, although there is a significant association between close linkage and a high value of the linkage disequilibrium measure. This suggests that there may be disequilibria between closely linked enzyme loci that are too small to be individually detectable. These results are in broad agreement with those reported by workers on other Drosophila species. At present there appears to be no evidence to support the concept that selection is sufficiently strong at individual enzyme loci to produce a high degree of nonrandom associations. (Franklin and Lewontin 1970).     

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.     

The Genetics of DROSOPHILA SUBOBSCURA Populations. V. a Study of Linkage Disequilibrium in Natural Populations between Genes and Inversions of the E Chromosome

The genetics of Hk and Est-9 complex gene have been studied in Drosophila subobscura. While Hk alleles mendelize normally, Est-9 is a complex locus consisting of several very closely linked genes with active and silent alleles. Both genes are located on chromosome E; a detailed genetic map was constructed with the help of visible markers and inversions. Both Hk and Est-9 are included in or are very near to inversions of the E chromosome. While Hk does not show linkage disequilibrium either with Est-9 or inversions, Est-9 does show disequilibrium in two ways: both with inversions and between different Est-9 genes. All natural populations studied show the same kind of association between Est-9 gene combinations and inversions. It is argued that these results are better explained by selection than by neutrality.     

Gametic Frequency of Second Chromosomes of the T-007 Type in a Natural Population of DROSOPHILA MELANOGASTER in Texas

The T-007 second chromosome, which was isolated from a natural population of Drosophila melanogaster in south Texas in 1970, is known to show, when made heterozygous in males with a standard cn bw second chromosome, a transmission frequency (k) of 0.35—much lower than the theoretically expected 0.5. Natural populations of this species in Texas contain second chromosomes that, against the standard cn bw genetic background, are associated with distorted transmission frequencies comparable to that of the T-007 chromosome. In order to explain how such chromosomes can persist in natural populations in nontrivial frequencies, it has been postulated that, although such chromosomes show reduced k values when tested under the genetic background of a laboratory stock such as cn bw, they may show, on the average, k values larger than 0.5 under natural genetic backgrounds. If this were true, the frequency of chromosomes of the T-007 type (T chromosomes) should be higher in male than in female gametes under natural genetic backgrounds. The present study was conducted to examine this possibility. The results clearly showed that the frequency of such chromosomes was much higher among male than among female gametes, and that the transmission frequency of this type of chromosome was higher than 0.5 under natural genetic backgrounds. These results suggest that T chromosomes behave like Segregation Distorter (SD) chromosomes in natural populations of this species in Texas. A possible relationship between T-007 and SD chromosomes is suggested.     

The Genetic Structure of Natural Populations of DROSOPHILA MELANOGASTER. Xi. Genetic Variability in a Local Population

Six hundred and ninety-one second chromosomes were extracted from a Raleigh, North Carolina population, and the following experimental results were obtained: (1) Salivary gland chromosomes of all lines were observed and the number of inversion-carrying chromosomes was 130, among which 76 carried In(2R)NS, 36 carried In(2L)t, 4 carried In(2L)t and In(2R)NS, and 14 carried different kinds of rare inversions. (2) Viabilities of homozygotes and heterozygotes were examined. The frequency of lethal-carrying chromosomes was 275/691 (or 0.398):70/130 (or 0.538) in inversion-carrying chromosomes and 205/561 (or 0.365) in inversion-free chromosomes. The former is significantly higher than the latter. The average homozygote viability was 0.4342 including lethal lines and 0.7163 excluding those, the average heterozygote viability being 1.0000. The detrimental load to lethal load ratio (D:L ratio) was 0.334/0.501 = 0.67. The average viability of lethal heterozygotes was less than that of lethal-free heterozygotes, significantly in inversion-free individuals but not significantly so in inversion-carrying individuals. Inversion heterozygotes seem to have slightly better viability than the inversion-free heterozygotes on the average, but not significantly so. (3) The average degree of dominance of viability polygenes was estimated to be 0.293 +/- 0.071 for all heterozygotes whose component chromosomes had better viabilities than 0.6 of the average heterozygote viability, 0.177 +/- 0.077 for inversion-free heterozygotes and 0.489 +/- 0.082 for inversion heterozygotes. (4) Mutation rates of viability polygenes and lethal genes were estimated on the basis of genetic loads and average degrees of dominance of lethal genes and viability polygenes. Estimates were very close to those obtained by direct estimation. (5) Possible overdominance and epistasis were detected, but the magnitude must be very small. (6) The effective size of the population was estimated to be much greater than 10,000 by using the allelism rate of lethal-carrying chromosomes (0.0040) and their frequency.-On the basis of these findings and the comparison with the predicted result (Mukai and Maruyama 1971), the mechanisms of the maintenance of genetic variability in the population are discussed.     

Multivariate Analysis of Gametic Disequilibrium in the Yanomama

The gametic disequilibria between all possible pairs of loci were examined for a set of eight codominant loci in each of fifty Yanomama villages, using a multivariate correlation analysis which reduces the results to a single measure of departure from multiple-locus-gametic equilibrium. Thirty-two of the fifty villages departed significantly from multiple-locus gametic equilibrium. The largest contributions to the departure from multiple-locus equilibrium were due to the disequilibria between MN and Ss and between Rh(Cc) and Rh(Ee), indicating the effects of tight linkage. After removing the effects of these obvious sources of disequilibrium, sixteen of the fifty villages still remained significantly out of equilibrium. The disequilibrium between any particular pair of loci was highly erratic from village to village, and (with the exception of the MN-Ss and Cc-Ee disequilibria) averaged out very close to zero overall, suggesting a lack of systematic forces (epistatic selection). The departure from equilibrium in any one village is in excess of that expected from random sampling alone, and is attributed primarily to the fission-fusion mode of village formation operative in the Yanomama and the fact that a single village consists of a few extended lineages. Village allele frequencies are highly correlated across loci, and most of the non-independence is accounted for by large correlations in the average allelic frequencies of different loci for related villages. It is suggested that these correlations also are due to territorial expansion and population growth. For the tribe as a whole, all but the tightly linked markers of the MNSs and Rh complexes are approximately uncorrelated, and large departures from multiple-locus Hardy-Weinberg expectation are primarily due to substantial Wahlund variance within the tribe. There is no need to postulate a role for selection in these disequilibria.     

The Genetic Structure of Natural Populations of DROSOPHILA MELANOGASTER. Xvii. a Population Carrying Genetic Variability Explicable by the Classical Hypothesis

About 400 second chromosomes were extracted from the Aomori population, a northernmost population of D. melanogaster on Honshu in Japan, and the following experimental results were obtained. (1) The frequency of lethal chromosomes was 0.23. (2) The effective size of the population was estimated to be about 3000, from the allelism rate of lethal chromosomes and their frequency. (3) The detrimental and lethal loads for viability were 0.243 and 0.242, respectively, and the D/L ratio became 1.00. (4) The average degree of dominance for mildly deleterious genes was estimated to be 0.178 ± 0.056. (5) Additive (σ²_A) and dominance (σ²_D) variances of viability were estimated to be 0.00276 ± 0.00090 and 0.00011 ± 0.00014, respectively. (6) There was no significant difference in environmental variances between homozygotes and heterozygotes. Using these estimates, we discuss the maintenance mechanisms of genetic variability of viability in the population. The mutation-selection balance explained these experimental results.     

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.     

Chromosomal Analysis of Ddt-Resistance in a Long-Term Selected Population of DROSOPHILA MELANOGASTER

The genetic basis of DDT-resistance was studied in a population of Drosophila melanogaster. This population was unique in that it had been continually selected for DDT-resistance since 1952 and had achieved a very high level of resistance. The genetic basis of resistance was studied by means of a chromosomal analysis. Fifteen combinations of resistant and control chromosomes were tested using a time-based DDT test. The analysis of the data showed that resistance was multifactorial with each of the three major chromosomes involved. Dominant and recessive second and third chromosome effects were found to be much more important than those of the first chromosome, which had no detectable recessive effects. Second and third chromosome resistance genes showed incomplete dominance. The average dominance of the second chromosome was much less than that of the third chromosome. These large-scale differences between chromosomes' effects and average dominance may indicate that a small number of resistance genes are involved. Two significant interactions between chromosomes were found. Scaling difficulties make the interactions difficult to interpret without further data. It seems possible that positive interactions between resistance have been developed by the long-term directional selection in this population.     

The Genetical Response to Natural Selection by Varied Environments. IV. Gametic Disequilibrium in Spatially Varied Environments

Gametic disequilibria between allozyme loci were related to spatial variation of the environment in caged populations of Drosophila melanogaster . Two experiments, one with flies collected at "Chateau Tahbilk," South Australia, and the other with flies from "Groningen," The Netherlands, were sampled at generations 16 and 32. Spatial variation of the environment was stimulated using three food media. Eight polymorphic allozyme loci were used to estimate gametic disequilibria from digenic combinations of allotypes. All populations were duplicated within an environment and maintained at about 2500 adults. Standardized gametic disequilibria were compared by a weighted least squares analysis of the z-transformed statistical correlation of allele frequencies. Gametic disequilibria were strongly dependent upon food niche and food-niche interactions. The effects also varied with sampling time and were similar in duplicate populations. Gametic disequilibria were most often detected in the "Groningen"-derived populations and their strength was not strongly associated with recombination fraction. Many of the disequilibria concerned unlinked loci. The strength of selection was probably considerable and populations were evolving genetic architectures which reflected niche selection by the different foods without marked genetic isolation between foods; gene frequencies did not vary between niches within a population cage.     

Population Dynamics of the Segregation Distorter Polymorphism of DROSOPHILA MELANOGASTER

Two two-locus models of the population dynamics of the segregation distortion (SD) polymorphism of Drosophila melanogaster are described. One model is appropriate for understanding the population genetics of SD in nature, whereas the other is a special case appropriate for understanding an artificial population that has been extensively analysed. The models incorporate the general features of the Sd and Rsp loci which form the core of the SD system. It is shown that the SD polymorphism can be established only when there is sufficiently tight linkage between Sd and Rsp. An approximate treatment, valid for tight linkage, is given of all the equilibria of the system and their stabilities. It is shown that the observed composition of natural and artificial populations with respect to the Sd and Rsp loci is predicted well by the model, provided that restrictions are imposed on the fertilities of certain genotypes. Highly oscillatory paths towards equilibrium are usually to be expected on the basis of this model. The selection pressures on inversions introduced into this system are also investigated.