Enzyme null alleles in natural populations of Drosophila melanogaster: Frequencies in a North Carolina population

ABSTRACT We have sampled a London population of Drosophila melanogaster for null alleles at twenty-five allozyme loci. The same loci and biochemical techniques were used as in our previous survey of a North Carolina population (Voelker et al. 1980). This second survey is completely concordant with the first. No nulls were detected among the five X-linked loci. The mean frequency of nulls at the twenty autosomal loci was 0.0023. Although there is significant interlocus heterogeneity, the two populations appear to have the same frequencies at each locus. This suggests that null alleles at these allozyme loci are in mutation-selection balance, and we estimate the average heterozygous effect of an allozyme null to be 0.0015. Consideration of allozyme null-allele frequencies, the effects of allozyme null alleles on viability and fertility and the generally greater amount of genetic variability at allozyme loci determined by electrophoresis lead us to doubt the validity of generalizing from allozyme data to the whole genome.

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SUPPRESSOR SYSTEMS OF SEGREGATION DISTORTER (SD) CHROMOSOMES IN NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER

Genetics ◽

10.1093/genetics/106.2.279 ◽

1984 ◽

Vol 106 (2) ◽

pp. 279-292

Author(s):

Yuichiro Hiraizumi ◽

Anita M Thomas

Keyword(s):

North Carolina ◽

Drosophila Melanogaster ◽

Chromosome Segregation ◽

Natural Populations ◽

Low Frequencies ◽

X Chromosomes ◽

High Frequencies ◽

Heterozygous Male ◽

Segregation Distorter ◽

Carolina Population

ABSTRACT 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.

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Insertion-deletion variation at the yellow-achaete-scute region in two natural populations of Drosophila melanogaster

Genetics Research ◽

10.1017/s0016672300027804 ◽

1989 ◽

Vol 53 (1) ◽

pp. 7-15 ◽

Cited By ~ 8

Author(s):

Robin N. Beech ◽

Andrew J. Leigh Brown

Keyword(s):

North Carolina ◽

Drosophila Melanogaster ◽

Natural Populations ◽

The North ◽

Restriction Sites ◽

Dna Insertion ◽

Carolina Population ◽

Element Evolution ◽

High Level ◽

Transposable Genetic Elements

SummaryWe have surveyed the region of the X chromosome of Drosophila melanogaster which encodes the yellow, achaete and scute genes for restriction map variation. Two natural populations, one from North Carolina, U.S.A. and the other from southern Spain were screened for variation at about 70 restriction sites and for variation due to DNA insertion or deletion events in 120 kilobases of DNA. Mean heterozygosity per nucleotide was estimated to be 0·0024 and 15 large insertions were found in the 49 chromosomes screened. Extensive disequilibrium between polymorphic sites was found across much of the region in the North Carolina population. The frequency of large insertions, which usually correspond to transposable genetic elements, is significantly lower than has been observed in autosomal regions of the genome. This is predicted for X-linked loci by certain models of transposable element evolution, where copy number is restricted by virtue of the recessive deleterious effects of the insertions. Our results appear to support such models. The deficiency of insertions may in this case be enhanced by hitch-hiking effects arising from the high level of disequilibrium.

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Behavioral variation in Drosophila melanogaster: no evidence for common alleles of large- effect at the foraging gene in a population from North Carolina, USA

10.1101/004325 ◽

2014 ◽

Author(s):

Thomas Turner ◽

Christopher C Giauque ◽

Daniel R Schrider ◽

Andrew D Kern

Keyword(s):

North Carolina ◽

Drosophila Melanogaster ◽

Genetic Variation ◽

Foraging Behavior ◽

Additional Data ◽

Balancing Selection ◽

Natural Populations ◽

Specific Population ◽

Foraging Gene ◽

Population Genetic Variation

It has been postulated that natural populations of Drosophila melanogaster are comprised of two behavioral morphs termed "rover" and "sitter", and that this variation is caused mainly by large-effect alleles at a single locus. Contrary to common assertions, however, published support for the existence of common large effect alleles in nature is quite limited. To further investigate, we quantified the foraging behavior of 36 sequenced strains from a natural population, performed an association study, and described patterns of molecular evolution at the foraging locus. Though there was significant variation in foraging behavior among genotypes, this variation was continuously distributed and not significantly associated with genetic variation at the foraging gene. Patterns of molecular population genetic variation at this gene also provide no support for the hypothesis that for is a target of recent balancing selection. Though our data only apply to this specific population, we propose that additional data is required to support a hypothesis of common alleles of large effect on foraging behavior in nature.

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THE GENETIC STRUCTURE OF NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER XIII. FURTHER STUDIES ON LINKAGE DISEQUILIBRIUM

Genetics ◽

10.1093/genetics/86.1.175 ◽

1977 ◽

Vol 86 (1) ◽

pp. 175-185

Author(s):

Terumi Mukai ◽

Robert A Voelker

Keyword(s):

Drosophila Melanogaster ◽

Linkage Disequilibrium ◽

Natural Populations ◽

Linkage Disequilibria ◽

Two Factors ◽

Carolina Population ◽

Recombination Value ◽

Significant Linkage ◽

Octanol Dehydrogenase ◽

Double Crossovers

ABSTRACT The Raleigh, North Carolina, population of Drosophila melanogaster was examined for linkage disequilibrium in 1974, several years after previous analyses in 1968, 1969, and 1970. αglycerol-3-phosphate dehydrogenase-1 (αGpdh-1), malate dehydrogenase-1 (Mdh-1), alcohol dehydrogenase (Adh), and hexokinase-C (Hex-C, tentative name, F. M. Johnson, unpublished; position determined by the present authors to be 2-74.5) were assayed for 617 second chromosomes, and esterase-C (Est-C) and octanol dehydrogenase (Odh) were assayed for 526 third chromosomes. In addition, two polymorphic inversions in the second chromosomes [In(2L)t and In(2R)NS] were examined, and the following findings were obtained: (1) No linkage disequilibrium between isozyme genes was detected. Significant linkage disequilibria were found only between the polymorphic inversions and isozyme genes [In(2L)t vs. Adh, and In(2R)NS vs. Hex-C]. Significant disequilibrium was not detected between In(2L)t and αGpdh-1, which is included in the inversion, but a tendency toward disequilibrium was consistently found from 1968 to 1974. The frequency of two-strand double crossovers within inversion In(2L)t involving a single crossover on each side of αGpdh-1 was estimated to be 0.00022. Thus, the consistent but not significant linkage disequilibrium between the two factors can be explained by recombination after the inversion occurred. (2) Previously existing linkage disequilibrium between Adh and In(2R)NS (the distance is about 30 cM, but the effective recombination value is about 1.75%) was found to have disappeared. (3) No higher-order linkage disequilibrium was detected. (4) Linkage disequilibrium between Odh and Est-C (the distance of which was estimated to be 0.0058 ± 0.002) could not be detected (χ2 df=1 = 0.9).—From the above results, it was concluded that linkage disequilibria among isozyme genes are very rare in D. melanogaster, so that the Franklin-Lewontin model (Franklin and Lewontin 1970) is not applicable to these genes. The linkage disequilibria between some isozyme genes and polymorphic inversions may be explained by founder effect.

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The Relationship Between Dipeptidase Activity Variation and Larval Viability in Drosophila melanogaster

Genetics ◽

10.1093/genetics/117.3.503 ◽

1987 ◽

Vol 117 (3) ◽

pp. 503-512

Author(s):

Kazuo Hiraizumi ◽

Cathy C Laurie

Keyword(s):

Drosophila Melanogaster ◽

Null Allele ◽

Natural Populations ◽

Null Alleles ◽

Adult Survival ◽

Free Form ◽

Alternative Mechanism ◽

Fitness Components ◽

Restrictive Diet

ABSTRACT The enzyme dipeptidase-A (DIP-A) in Drosophila melanogaster is coded by a second chromosome locus that is polymorphic for three allozymes in natural populations. DIP-A appears to be the only enzyme in D. melanogaster capable of hydrolyzing the dipeptide glycyl-l-isoleucine, since flies homozygous for null alleles at this locus have no detectable glycyl- l-isoleucine-ase activity. DIP-A activity occurs in many tissues and throughout development, but is particularly high in the larval midgut, suggesting an important role in protein digestion. These observations suggested an experimental design for investigating the adaptive significance of genetic variation in DIP-A activity. Fitness components of DIP-A variants could be estimated and compared under two environmental conditions (defined diets under axenic conditions). In the restrictive environment, the essential amino acid l-isoleucine is provided only in the form of glycyl-l-isoleucine, whereas in the permissive environment, l-isoleucine is provided in free form. We predicted that DIP-A activity would be essential in the restrictive, but not in the permissive environment. The results reported here clearly contradict this prediction. Two stocks homozygous for DIP-A null alleles from different geographic locations are each viable on the restrictive diet. Furthermore, relative viability experiments in which null allele larvae compete with larvae having DIP-A activity provide no evidence for even a partial reduction in egg to adult survival on the restrictive diet. Apparently, the null allele larvae have some alternative mechanism for obtaining l-isoleucine from the dipeptide, even though no glycyl-l-isoleucine-ase activity can be detected in vitro. These results, along with the viability of null alleles for many other enzymes, support the idea that eukaryotes have an intricate network of alternative biochemical pathways through which the same necessary function may be achieved. Such "buffering capacity" makes it very difficult to analyze the effects of enzyme variants on fitness components.

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A comprehensive study of genic variation in natural populations of Drosophila melanogaster. V. Structural–functional constraints on protein molecules and enzymes and the levels and patterns of variation among genes

Genome ◽

10.1139/g92-019 ◽

1992 ◽

Vol 35 (1) ◽

pp. 109-119 ◽

Cited By ~ 1

Author(s):

Rama S. Singh

Keyword(s):

Molecular Structure ◽

Drosophila Melanogaster ◽

Balancing Selection ◽

Natural Populations ◽

Null Alleles ◽

Subunit Structure ◽

Functional Constraints ◽

Enzyme Variation ◽

Subunit Size ◽

Substrate Group

Ever since isozyme–allozyme polymorphisms were detected there has been an incessant effort to relate the amount of observed protein variation to various aspects of molecular structure and function. Structural–functional constraints can limit the amount of overall genie variation, and the observed variation can be due to neutral mutation and random genetic drift, mutation–selection balance, or balancing selection. The present analysis of structural–functional constraints on gene–enzyme variation in natural populations of Drosophila melanogaster shows that while both subunit size and substrate group show significant effects on number of alleles and mean heterozygosity, only substrate group affects population structure significantly. Subunit structure (monomer vs. multimer), IUB enzyme class (e.g., tranferase, lyase), and tolerance of null alleles showed no significant effect on level or pattern of variation. While partly interdependent these results suggest that efforts should be made to distinguish between constraints arising from molecular structure and physiological function.Key words: structural–functional constraints, subunit size, gene-enzyme variation, selection, neutrality.

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THE GENETIC STRUCTURE OF NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER. XI. GENETIC VARIABILITY IN A LOCAL POPULATION

Genetics ◽

10.1093/genetics/76.2.339 ◽

1974 ◽

Vol 76 (2) ◽

pp. 339-366

Author(s):

Terumi Mukai ◽

Osamu Yamaguchi

Keyword(s):

North Carolina ◽

Salivary Gland ◽

Genetic Variability ◽

Local Population ◽

Natural Populations ◽

Load Ratio ◽

Mutation Rates ◽

Degree Of Dominance ◽

Carolina Population ◽

Lethal Genes

ABSTRACT 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.

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THE GENETIC STRUCTURE OF NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER. XII. LINKAGE DISEQUILIBRIUM IN A LARGE LOCAL POPULATION

Genetics ◽

10.1093/genetics/77.4.771 ◽

1974 ◽

Vol 77 (4) ◽

pp. 771-793

Author(s):

Terumi Muki ◽

Takao K Watanabe ◽

Osamu Yamaguchi

Keyword(s):

Drosophila Melanogaster ◽

Local Population ◽

Natural Populations ◽

Large Cage ◽

Linkage Disequilibria ◽

Esterase 6 ◽

Relative Viability ◽

Carolina Population ◽

Isozyme Loci ◽

Glycerol 3 Phosphate Dehydrogenase

ABSTRACT 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 α glycerol-3-phosphate dehydrogenase-1, malate dehydrogenase-1, alcohol dehydrogenase, and α 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.

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Transcription analysis of alcohol dehydrogenase null alleles from natural populations of Drosophila melanogaster

Genome ◽

10.1139/g88-005 ◽

1988 ◽

Vol 30 (1) ◽

pp. 25-30 ◽

Cited By ~ 10

Author(s):

Allan L. Freeth ◽

John B. Gibson ◽

Ann V. Wilks

Keyword(s):

Drosophila Melanogaster ◽

Alcohol Dehydrogenase ◽

Northern Blot ◽

Natural Populations ◽

Molecular Properties ◽

Southern Analysis ◽

Null Alleles ◽

Normal Allele ◽

Transcription Analysis

Southern analysis of 19 Adh null activity alleles isolated from Tasmanian populations of Drosophila melanogaster have shown that there are no detectable insertions or deletions in an 11.8-kb region that contains the gene. Northern blot analyses of the null alleles have shown that they all produce a transcript about 100 bases longer than that produced by the normal allele and they accumulate a precursor of 1800 bases. The amount of the major transcript produced by the null alleles is about 10% of that produced by normal alleles. The molecular properties of the null alleles suggest that they share a common origin.Key words: alcoahol dehydrogenase, null alleles, mRNA, Drosophila melanogaster.

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