Gene Differences between the Sex Ratio and Standard Gene Arrangements of the X Chromosome in DROSOPHILA PERSIMILIS

The sibling species Drosophila pseudoobscura and D. persimilis each carry two gene arrangements in the right arm of the X chromosome; Standard (ST) and Sex Ratio (SR). The SR sequence of D. persimilis and the ST sequence of D. pseudoobscura have the same banding pattern. These cytologically identical arrangements carry different alleles at the esterase-5 (Est-5) and phosphoglucomutase-1 ( Pgm-1) loci. All the alleles on the SR arrangement of D. persimilis are also present on the ST arrangement of that species, and the same allele was most common in all cases. However, the allele frequencies at the Pgm-1 locus are significantly different between the two arrangements. Within the ST arrangement of D. persimilis, the alleles at the Est-5 and Pgm-1 loci are in linkage equilibrium.     

Direct Evidence of Genic Differentiation between Sex Ratio and Standard Gene Arrangements of X Chromosome in DROSOPHILA PSEUDOOBSCURA

Evidence of strong association of alleles at the Esterase-5 and adult Acid phosphatase-6 loci with the Sex Ratio and the Standard X chromosome arrangements in D. pseudoobscura is presented. There is no differentiation at these two loci, either in the Sex Ratio or the Standard arrangement from two widely separated geographic populations. At the Esterase-5 locus, alleles characteristic of one arrangement are found in low frequencies in the other arrangement. It is concluded, from these and other observations that the differentiation between the Sex Ratio and the Standard arrangement, at these two loci, is a result of natural selection favoring different coadapted gene blocks in these arrangements. The average heterozygosity at these two loci in different karyotypes is in the following order: ST/SR > ST/ST >> SR/SR which agrees very well with the fitness estimates of these karyotypes.     

Gene Differences between Third-Chromosome Inversions of DROSOPHILA PSEUDOOBSCURA

Associations of alleles of the acid phosphatase-3 locus with the different third-chromosome inversions from different populations of D. pseudoobscura are described. We observe only the allele AP-3 ^1.0 in the Standard and Arrow-head inversions and the allele AP-3^.98 in the Santa Cruz, Treeline, Cuernavaca and the Pikes Peak arrangements. The Chiricahua gene arrangement is polymorphic.     

Genic Heterogeneity at Two Alcohol Dehydrogenase Loci in DROSOPHILA PSEUDOOBSCURA and DROSOPHILA PERSIMILIS

A sequential electrophoretic survey of the second chromosome loci, alcohol dehydrogenase-6 (Adh-6) and octanol dehydrogenase ( Odh), was performed on 147 isochromosomal lines of Drosophila pseudoobscura and 60 lines of its sibling species, D. persimilis. Gels run with a variety of acrylamide concentrations and buffer pH's revealed the presence of 18 alleles of Adh-6 in the two species, where only eight had been previously detected by conventional electrophoretic methods. Only two alleles were added with our techniques to the previous total of nine in both species at the largely monomorphic Odh locus. Both enzymes show a predominance of one allele, with the other variants being fairly rare. There was no evidence of increased genetic divergence between the two species, but we found a striking increase in differentiation of Adh-6 alleles between the main body of D. pseudoobscura populations and the conspecific isolate from Bogotá, Colombia. These results are compared with our previous surveys of xanthine dehydrogenase in these species and discussed in reference to theories of genic polymorphism.     

Dosage Compensation of Genes on the Left and Right Arms of the X Chromosome of DROSOPHILA PSEUDOOBSCURA and DROSOPHILA WILLISTONI

We have investigated the occurrence of dosage compensation in D. willistoni and D. pseudoobscura, two species whose X chromosome is metacentric with one arm homologous to the X and the other homologous to the left arm of chromosome 3 of D. melanogaster. Crude extracts were assayed for isocitrate dehydrogenase (XR), glucose-6-phosphate dehydrogenase (XL?), 6-phosphogluconate dehydrogenase (XL?), and α-glycerophosphate dehydrogenase (chromosome 2) in D. willistoni, and for esterase-5 (XR), glucose-6-phosphate dehydrogenase (XL?), 6-phosphogluconate dehydrogenase (XL?) and amylase (chromosome 3) in D. pseudoobscura. Our results indicate that a mechanism for dosage compensation is operative in both arms of the X chromosome of these two species.     

Linkage Disequilibrium in Natural Populations of DROSOPHILA MELANOGASTER

Two large, stable populations (Texas and Japan) of Drosophila melanogaster were surveyed at 21 allozyme loci on the second and third chromosomes and for chromosomal gene arrangements on those two chromosomes. Over 220 independent gametes were sampled from each population. The types and frequencies of the surveyed genetic variation are similar to those observed previously and suggest only slight differentiation among geographically distant populations. Linkage disequilibrium among linked allozymes loci is only slightly, if at all, detectable with these sample sizes. Linkage disequilibrium between linked inversions and allozymes loci is common especially when located in the same arm. These disequilibria appear to be in the same direction for most comparisons in the two population samples. This result is interpreted as evidence of similar selective environments (ecological and genetic) in the two populations. It is also noted that the direction of these linkage disequilibria appears to be oriented with respect to the gene frequencies at the component loci.     

Distinctions among Allelic Variants Associated with Chromosome 3 Inversions in DROSOPHILA PSEUDOOBSCURA and DROSOPHILA PERSIMILIS

Efforts were made to discriminate new genetic variants among electrophoretic alleles that are associated with chromosome 3 inversions of Drosophila pseudoobscura and D. persimilis. Apparent genetic similarities for electrophoretic alleles between these two species and among the common inversions they carry were reexamined by altering gel concentration and buffer pH. At the amylase locus, the 1.09 electrophoretic allele could be further separated into two allelic classes that differentiated the WT and KL arrangements. Similarly, the 0.84 electrophoretic allele was divided into two allelic classes, one characteristic of the Santa Cruz phylad arrangements, TL and SC, and the other found in strains of the Standard phylad arrangements and CH. Uncommon amylase alleles proved to be different alleles in the two species. No new allelic variants, however, could be found among strains with the amylase 1.00 allele, the commonest allele in the Standard phylad of both species. No major new allelic variation was detected for acid phosphatase-3 and larval protein-10 that revealed any further differentiation among species or inversions. Variation at all three loci in strains of the Bogota population remained genetically similar to variation in strains of mainland D. pseudoobscura.     

Components of Selection in X Chromosome Lines of DROSOPHILA MELANOGASTER: Sex Ratio Modification by Meiotic Drive and Viability Selection

Selection coefficients and segregation parameters have been estimated in 18 randomly chosen lines carrying wild X chromosomes on the cn bw genetic background. Each line was studied in replicated crosses of four types, with approximately 100 replications per line per cross. Crosses in which male X chromosomes differed exhibited significant sex ratio heterogeneity. Maximum likelihood estimation of segregation parameters revealed two lines in which the proportion of X-bearing gametes produced by males was significantly different from Mendelian expectations. These observations suggest that segregation distortion is a common feature of naturally occurring genetic variation. Non-Mendelian segregation has important evolutionary implications.     

A Study of Linkage Disequilibrium in Populations of DROSOPHILA MELANOGASTER

This paper presents the results of a study of linkage disequilibrium between five polymorphic enzyme genes located on chromosome 3 of D. melanogaster. Three sets of chromosomes were examined: two represented samples from successive years of the same natural population, and one came from a large laboratory population. Out of the thirty possible tests for linkage disequilibrium between pairs of loci, two were significant at the 5% level and two at the 1% level. This result cannot reasonably be ascribed to chance alone. The pairs of loci that had a significant correlation in one sample had higher than average correlations in the other samples (though not necessarily in the same direction); this effect was highly significant statistically. There was no tendency for the high correlations to be associated with tightness of linkage between the loci concerned. All five loci were involved in at least one significant effect. It was concluded that these results are difficult to explain on the neutral allele theory of protein polymorphism, but are consistent with the concept of selective control of allele frequencies.     

Evidence for Extensive Genetic Differentiation between the Sex-Ratio and the Standard Arrangement of DROSOPHILA PSEUDOOBSCURA and D. PERSIMILIS and Identification of Hybrid Sterility Factors

This study deals with sex-ratio genes tightly linked within the Sex-Ratio inversion. By taking advantage of the fact that the Sex-Ratio chromosome of Drosophila persimilis [SR(B)] is homosequential to the Standard chromosome of D. pseudoobscura [ST(A)], we carried out two reciprocal introgression experiments. Individual segments of SR(B) or ST(A) were introgressed into the genome of D. pseudoobscura or D. persimilis, respectively. Males possessing a hybrid SR(B)-ST(A) X chromosome and a genetic background derived from either of the two species were tested for fertility and sex-ratio expression.—It was found that, in terms of the meiotic drive genes, the Sex-Ratio chromosome differs extensively from the Standard chromosome. Because recombinations of these genes result in a complete loss of sex-ratio expression, this finding lends strong support to the hypothesis of gene coadaptation. Coadaptation, in this context, is the advantage of being transmitted preferentially. In light of this finding, the evolution of the sex-ratio system in these two sibling species is discussed.—Introgression experiments also yielded information about hybrid sterility. With reciprocal introgression, sterility interactions were found to be "asymmetric." The asymmetry is fully expected from the viewpoint of evolution of postmating reproductive isolation.     

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).     

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.     

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.     

Allozymic Variation and Linkage Disequilibrium in Some Laboratory Populations of DROSOPHILA MELANOGASTER

Nine laboratory populations of D. melanogaster were surveyed by starch gel electrophoresis for variation at 17 enzyme loci. A single-fly extract could be assayed for all 17 enzymes, so that the data consist of 17-locus genotypes.--Pairwise linkage disequilibria were estimated from the multilocus genotypic frequencies, using both Burrows' and Hill's methods. Large amounts of linkage disequilibrium were found, in contrast to the results reported for natural populations.-Knowledge of the approximate sizes of these populations was used to compare the observed heterozygosities and linkage disequilibria with predictions of the neutral allele hypothesis. The relatively large amount of linkage disequilibrium is consistent with the small sizes of the populations. However, the levels of heterozygosity in at least some populations suggest that some mechanism has been operating to retard the rate of decay by random drift. Several examples of significant deviation from Hardy-Weinberg frequencies and the large amount of linkage disequilibrum present in these populations indicate that a likely mechanism is selective effects associated with neutral alleles because of linkage disequilibrium with selected loci (e.g., "associative overdominance"). The results are therefore consistent with both neutralist, and selectionist hypotheses, but suggest the importance of considering linkage disequilibrium between neutral and selected loci when attempting to explain the dynamics of enzyme polymorphisms.     

Gene Flow and the Geographical Distribution of a Molecular Polymorphism in DROSOPHILA PSEUDOOBSCURA

This paper discusses the relation between the geographical distribution of an enzyme polymorphism and population structure in Drosophila pseudoobscura. California populations of this species living in very different montane and lowland habitats separated by several kilometers are similar to each other in the frequency of an esterase allele. Previous estimates suggest that gene flow is too limited to account for this homogeneity of genetic structure, so that it must reflect some balancing force of natural selection. We show, however, that dispersal over unfavorable habitats is much greater than earlier supposed. Isolated populations of D. pseudoobscura separated by 15 km from other populations are subject to large amounts of immigration. This is shown by changes in the seasonal abundance of this species and in the annual pattern of lethal alleles in such populations. The genetic structure of an experimentally perturbed isolated population in an oasis returned to normal within a single year, suggesting that such populations are ephemeral and that the oasis is subject to annual recolonization by distant migrants. Direct assessment of marked flies shows that they can move at least 10 km in 24 hours over a desert. Such extensive gene flow may help explain the distribution of the esterase allele, and is relevant to the high level of molecular polymorphism and its general lack of geographic differentiation throughout the range of D. pseudoobscura.