Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-06T03:53:43.809Z Has data issue: false hasContentIssue false

Linkage disequilibrium in the white locus region of Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Naohiko T. Miyashita*
Affiliation:
Laboratory of Genetics, Faculty of Agriculture, Kyoto University, Kyoto 606, Japan
Montserrat Aguadé
Affiliation:
Departament de Genética, Universitat de Barcelona, Barcelona 08071, Spain
Charles H. Langley
Affiliation:
Department of Genetics, University of California, Davis, California 95616, USA
*
* Corresponding author.
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Linkage disequilibrium between molecular polymorphisms in a 10 kb region in the white locus of Drosophila melanogaster, revealed with a battery of four-cutter restriction enzymes, was investigated in 266 lines sampled from seven natural populations around the world. A total of 73 (35 restriction site, 37 insertion/deletion and 1 inversion) polymorphisms were detected, of which 55 non-unique polymorphisms were analysed for linkage disequilibrium. Clustering of significant linkage disequilibrium was observed in the transcriptional unit of the white locus as in Miyashita & Langley (1988). It was shown that about two thirds of the 2-locus combinations showing significant linkage disequilibrium have similar degree and direction of association over different populations. Despite lower divergence in allelic frequencies of molecular polymorphisms among populations, an increase in the proportion of 2-locus pairs showing significant linkage disequilibrium is observed in the transcriptional unit. Large values of Ohta's D measure ratio (1982 a, b) cluster in the transcriptional unit, and correspond to significant linkage disequilibria. Although the exact molecular mechanism is not clear, these results suggest that epistatic selection is responsible for significant linkage disequilibrium in the transcriptional unit of this locus

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

References

Aguadé, M., Miyashita, N., & Langley, C. H., (1989). Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics 122, 607615.CrossRefGoogle ScholarPubMed
Aquadro, C. F., Deese, S. F., Bland, M. M., Langley, C. H., & Laurie-Ahlberg, C. C., (1986). Molecular population genetics of alcohol dehydrogenase gene region of Drosophila melanogaster. Genetics 114, 11651190.CrossRefGoogle ScholarPubMed
Begun, D. J., & Aquadro, C. H., (1992). Molecular population genetics of the distal portion of the X chromosome in Drosophila: evidence for genetic hitch-hiking of yellow-achaete region. Genetics 129, 11471158.CrossRefGoogle Scholar
Charlesworth, B., & Charlesworth, D., (1973). A study of linkage disequilibrium in populations of Drosophila melanogaster. Genetics 73, 351359.Google ScholarPubMed
Cockerham, C. C., (1969). Variance of gene frequencies. Evolution 23, 7284.CrossRefGoogle ScholarPubMed
Cockerham, C. C., (1973). Analysis of gene frequencies. Genetics 74, 679700.CrossRefGoogle ScholarPubMed
Dobzhansky, Th., (1970). Genetics of the Evolutionary Process. New York: Columbia University Press.Google Scholar
Eanes, W. F., Ajioka, J. W., Hey, J., & Wealey, C., (1989). Restriction-map variation associated with the G6PD polymorphism in natural populations of Drosophila melanogaster. Molecular Biology and Evolution 6, 384397.Google ScholarPubMed
Ewens, W. J., Spielman, R. S., & Harris, H., (1981). Estimation of genetic variation at the DNA level from restriction endonuclease data. Proceedings of the National Academy of Sciences, USA 78, 37483750.CrossRefGoogle ScholarPubMed
Green, M. M., (1959). Spatial and functional properties of pseudoalleles at the white locus in Drosophila melanogaster. Heredity 13, 302315.CrossRefGoogle Scholar
Hill, W. G., & Robertson, A., (1968). Linkage disequilibrium in finite populations. Theoretical and Applied Genetics (Der Zuchter) 38, 226231.CrossRefGoogle ScholarPubMed
Hudson, R. R., (1982). Estimating genetic variability with restriction endonucleases. Genetics 100, 711719.CrossRefGoogle ScholarPubMed
Judd, B. H., (1964). The structure of intralocus duplication and deficiency chromosomes produced by recombination in Drosophila melanogaster, with evidence for polarized pairing. Genetics 49, 253265.CrossRefGoogle ScholarPubMed
Kaplan, N. L., Hudson, R. R., & Langley, C. H., (1989). The ‘hitchhiking’ effect revisited. Genetics 123, 887899.CrossRefGoogle ScholarPubMed
Kimura, M., (1956). A model of a genetic system which leads to closer linkage by natural selection. Evolution 10, 278287.CrossRefGoogle Scholar
Kimura, M., (1983). The Neutral Theory of Molecular Evolution. London: Cambridge University Press.CrossRefGoogle Scholar
Kimura, M., & Ohta, T., (1971) Theoretical Aspects of Population Genetics. Princeton, New Jersey: Princeton University Press.Google ScholarPubMed
Kojima, K., Gillespie, J., & Tobari, Y. N., (1970). A profile of Drosophila melanogaster species' enzymes assayed by electrophoresis. I. Number of alleles, heterozygosities, and linkage disequilibrium in glucose-metabolizing systems and some other enzymes. Biochemical Genetics 4, 627637.CrossRefGoogle Scholar
Kreitman, M., (1983). Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304, 412–117.CrossRefGoogle ScholarPubMed
Kreitman, M., & Aguade, M., (1986). Genetic uniformity in two populations of Drosophila melanogaster revealed by filter hybridization of four-nucleotide-recognizing restriction enzyme digests. Proceedings of the National Academy of Sciences, USA 83, 35623566.CrossRefGoogle ScholarPubMed
Langley, C. H., & Aquadro, C. F., (1987). Restriction map variation in natural populations of Drosophila melanogaster: white locus region. Molecular Biology and Evolution 4, 651663.Google ScholarPubMed
Langley, C. H., Montgomery, E. A., & Quattlebaum, W. F., (1982). Restriction map variation in the Adh region of Drosophila. Proceedings of the National Academy of Sciences, USA 19, 56315635.CrossRefGoogle Scholar
Langley, C. H., Shrimpton, A. E., Yamazaki, T., Miyashita, N., Matsuo, Y., & Aquadro, C. F., (1988). Naturally occurring variation in the restriction map of the Amy region of Drosophila melanogaster. Genetics 119, 619629.CrossRefGoogle ScholarPubMed
Langley, C. H., Tobari, Y. N., & Kojima, K., (1974). Linkage disequilibrium in natural populations of Drosophila melanogaster. Genetics 78, 921936.CrossRefGoogle ScholarPubMed
Laurie, C. C., Bridgham, J. T., & Choudhary, M., (1991). Associations between DNA sequence variation and variation in expression of the Adh gene in natural populations of Drosophila melanogaster. Genetics 129, 489–199.CrossRefGoogle ScholarPubMed
Laurie-Ahlberg, C. C., & Stam, L. F., (1987). Use of P-element-mediated transformation to identify the molecular basis of naturally occurring variants affecting Adh expression in Drosophila melanogaster. Genetics 115, 129140.CrossRefGoogle ScholarPubMed
Lewontin, R. C., (1974). The Genetic Basis of Evolutionary Change. New York: Columbia University Press.Google Scholar
Lewontin, R. C., & Kojima, K., (1960). The evolutionary dynamics of complex polymorphisms. Evolution 14, 458472.Google Scholar
Smith, J. Maynard, & Haigh, J., (1974). The hitch-hiking effect of favorable gene. Genetical Research 23, 2335.CrossRefGoogle Scholar
Macpherson, J. N., Weir, B. S., & Brown, A. J. Leigh, (1990). Extensive linkage disequilibrium in achaete-scute complex of Drosophila melanogaster. Genetics 126, 121129.CrossRefGoogle ScholarPubMed
Martin-Campos, J. M., Comeron, J. M., Miyashita, N., & Aguadé, M., (1992). Intra- and interspecific variation at the y-ac-sc region of Drosophila simulans and melano-gaster. Genetics 130, 805816.CrossRefGoogle Scholar
Miyashita, N. T., (1990). Molecular and phenotypic variation of the Zw locus region in Drosophila melanogaster. Genetics 125, 407419.CrossRefGoogle ScholarPubMed
Miyashita, N., & Langley, C. H., (1988). Molecular and phenotypic variation of the white locus region in Drosophila melanogaster. Genetics 120, 199212.CrossRefGoogle ScholarPubMed
Mukai, T., Mettler, L. E., & Chigusa, S., (1971). Linkage disequilibrium in a local population of Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 68, 10651069.CrossRefGoogle Scholar
Mukai, T., Watanabe, T. K., & Yamaguchi, O., (1974). The genetic structure of natural populations of Drosophila melanogaster. XII. Linkage disequilibrium in a large local population. Genetics 77, 771793.CrossRefGoogle Scholar
Mukai, T., & Voelker, R. A., (1977). The genetic structure of natural populations of Drosophila melanogaster. XIII. Further studies on linkage disequilibrium. Genetics 86, 175185.CrossRefGoogle ScholarPubMed
Nei, M., (1973). Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences, USA 70, 33213323.CrossRefGoogle ScholarPubMed
Nei, M., & Li, W-H., (1979). Mathematical model for studying genetic variation in terms of restriction endo-nucleases. Proceedings of the National Academy of Sciences, USA 76, 52695273.CrossRefGoogle Scholar
Nei, M., & Tajima, F., (1981). DNA polymorphism detectable by restriction endonucleases. Genetics 97, 145163.CrossRefGoogle ScholarPubMed
Ohta, T., (1982 a). Linkage disequilibrium due to random genetic drift in finite subdivided populations. Proceedings of the National Academy of Sciences, USA 79, 19401944.CrossRefGoogle ScholarPubMed
Ohta, T., (1982 b). Linkage disequilibrium with the island nodel. Genetics 101, 139155.CrossRefGoogle Scholar
Ohta, T., & Kimura, M., (1969). Linkage disequilibrium due to random genetic drift. Genetical Research 13, 4755.CrossRefGoogle Scholar
Prakash, S., & Lewontin, R. C., (1968). A molecular approach to the study of genie heterozygosity. III. Direct evidence of coadaptation in gene arrangement of Drosophila. Proceedings of the National Academy of Sciences, USA 59, 398405.CrossRefGoogle Scholar
Prevosti, A., Garcia, M. P., Serra, L., Aguade, M., Ribo, G., & Sagarra, E., (1983). Association between allelic allozyme alleles and chromosomal arrangements in European populations and Chilean colonizers of Drosophila sub-obscura. Isozymes 10, 171191.Google Scholar
Riley, M. A., Hallas, M. E., & Lewontin, R. C., (1989). Distinguishing the forces controlling genetic variation at the Xdh locus in Drosophila pseudoobscura. Genetics 123, 359369.CrossRefGoogle ScholarPubMed
Schaeffer, S. W., Aquadro, C. F., & Langley, C. H., (1988). Restriction-map variation in the Notch region of Drosophila melanogaster. Molecular Biology and Evolution 5, 3040.Google ScholarPubMed
Steele, R. G. D., & Torrie, J. H., (1980). Principles and Procedures of Statistics. A Biometrical Approach. New York: McGraw-Hill.Google Scholar
Tajima, F., (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585595.CrossRefGoogle ScholarPubMed
Voelker, R. A., Cockerham, C. G., Johnson, F. M., Schaffer, H. E., Mukai, T., & Mettler, L. E., (1978). Inversions fail to account for allozyme clines. Genetics 88, 515527.CrossRefGoogle ScholarPubMed
Weir, B., (1990). Genetic Data Analysis. Sunderland, MA, USA: Sinauer Associates.Google Scholar
Wright, S., (1951). The genetical structure of populations. Annals of Eugenics 15, 323354.CrossRefGoogle ScholarPubMed
Yamaguchi, O., Ichinose, M., Matsuda, M., & Mukai, T., (1980). Linkage disequilibrium in isolated populations of Drosophila melanogaster. Genetics 96, 507522.CrossRefGoogle ScholarPubMed
Zouros, E., & Krimbas, C. B., (1973). Evidence of linkage disequilibrium maintained by selection in two natural populations of Drosophila subobscura. Genetics 73, 659674.CrossRefGoogle ScholarPubMed