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

  • Robin N. Beech (a1) and Andrew J. Leigh Brown (a1)

We 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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Aquadro C. H., Deese S. F., Bland M. M., Langley C. H. & Laurie-Ahlberg C. C. (1986). Molecular population genetics of the alcohol dehydrogenase gene region of Drosophila melanogaster. Genetics 114, 11651190.
Beech R. N. (1987). Insertion-deletion variation in the DNA of three natural populations of Drosophila melanogaster. Unpublished Ph.D. Thesis, University of Edinburgh.
Bender W., Akam M., Karch F., Beachy P. A., Peifer M., Spierer P., Lewis E. B. & Hogness D. S. (1983). Molecular genetics of the bithorax complex in Drosophila melanogaster. Science 221, 2329.
Bossy B., Hall L. M. C. & Spierer P. (1984). Genetic activity along 315 kb of the Drosophila chromosome. EMBO Journal 3, 25372541.
Brookfield J. F. Y. (1982). Interspersed, repetitive DNA sequences are unlikely to be parasitic. Journal of Theoretical Biology 94, 281299.
Brown A. H. D. (1975). Sample sizes required to detect linkage disequilibrium between two or three loci. Theoretical Population Biology 8, 184201.
Cabrera C. V., Martinez-Arias A., & Bate M. (1987). The expression of three members of the achaete-scute gene complex correlates with neuroblast segregation in Drosophila. Cell 50, 425433.
Campuzano S., Carramolino L., Cabrera C. V., Ruiz-Gomez M., Villares R., Boronat A. & Modellel J. (1985). Molecular genetics of the achaete-scute gene complex of Drosophila melanogaster. Cell 40, 327338.
Campuzano S., Balcells L., Villares R., Carramolino L., Garcia-Alonso L. & Modellel J. (1986). Excess function hairy-wing mutants caused by gypsy and copia insertions within structural genes of the achaete-scute locus of Drosophila. Cell 44, 303312.
Carramolino L., Ruiz-Gomez M., Guerrero M. C., Campuzano S. & Modellel J. (1982). DNA map of mutations at the scute locus of Drosophila melanogaster. EMBO Journal I, 11851191.
Charlesworth B. (1985). The population genetics of transposable elements. In Population Genetics and Molecular Evolution (ed. Ohta T. and Aoki K.), pp. 213232. New York: Springer Verlag.
Charlesworth B. & Charlesworth D. (1983). The population dynamics of transposable elements. Genetical Research 42, 127.
Chia W., Howes G., Martin M., Meng Y., Moses K. & Tsubota S. (1986). Molecular analysis of the yellow locus of Drosophila melanogaster. EMBO Journal 5, 35973605.
Cooper D. W., Johnston P. G., Vandeberg J. L., Maynes G. M. & Chew G. K. (1979). A comparison of genetic variability at X-linked and autosomal loci in kangaroos, man and Drosophila. Genetical Research 33, 243252.
Dubinin N. P., Sokolov N. N. & Tiniakov G. G. (1937). Crossing over between the genes yellow, achaete and scute. Drosophila Information Service 8, 76.
Economou-Pachnis A., Lohse M. A., Furano A. V. & Tsichlis P. N. (1985). Insertion of long interspersed repeated elements in the Igh (immunoglobulin heavy chain) and Mlvi-2 (molony leukaemia virus integration 2) loci of rats. Proceedings of the National Academy of Sciences, USA. 82, 28572861.
Errede B., Cardillo T. S., Sherman F., Dubois E., Deschamps J. & Waine J. M. (1980). Mating signals control expression of mutations resulting from insertion of a transposable repetitive element adjacent to diverse yeast genes. Cell 22, 427436.
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.
Feinberg A. P. & Vogelstein B. (1984). A technique for radiolabelling DNA restriction endonuclease fragments to a high specific activity. Analytical Biochemistry 132, 613.
Fitzpatrick B. J. & Sved J. A. (1986). High levels of fitness modifiers induced by hybrid dysgenesis in Drosophila melanogaster. Genetical Research 48, 8994.
Frischauf A.-M., Lehrach H., Poustka A. & Murray N. (1983). Lambda replacement vectors carrying poly linker sequences. Journal of Molecular Biology 170, 827842.
Garcia-Bellido A. (1979). Genetic analysis of the achaete-scute system of Drosophila melanogaster. Genetics 91, 491520.
Garcia-Bellido A. (1981). From the gene to the pattern: chaeta differentiation. In Cellular Controls in Differentiation (ed. Lloyd C. W. and Rees D. E.), pp. 281304. New York: Academic Press.
Gellert M. (1981). DNA topoisomerases. Annual Review of Biochemistry 50, 879910.
Golding G. B., Aquadro C. F. & Langley C. H. (1986). Sequence evolution within populations under multiple types of mutation. Proceedings of the National Academy of Sciences, USA 83, 427431.
Haldane J. B. S. (1927). A mathematical theory of natural and artificial selection. Part V. Selection and mutation. Proceedings of the Cambridge Philosophical Society 23, 836844.
Hill W. G. (1974). Estimation of linkage disequilibrium in finite populations. Heredity 33, 229239.
Hobbs H. H., Lehrman M. A., Yamamoto T. & Russell D. W. (1985). Polymorphism and evolution of alu sequences in the human low density lipoprotein receptor gene. Proceedings of the National Academy of Sciences, USA 82, 76517655.
Hudson R. R. (1982). Estimating genetic variability with restriction endonucleases. Genetics 100, 711719.
Jimenez F. & Campos-Ortega J. A. (1979). A region of the Drosophila genome necessary for CNS development Nature 282, 310312.
Johnson D. A., Gautsch J. W., Sportsman R. J. & Elder J. H. (1984). Improved technique utilizing non fat dry milk for analysis of proteins and nucleic acids transferred to nitrocellulose. Genetical Analysis Techniques 1, 38.
Kaplan N. & Brookfield J. F. Y. (1983). Transposable elements in Mendelian populations. III. Statistical results. Genetics 104, 485495.
Kreitman M. (1983). Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304, 412417.
Kleckner N. (1981). Transposable elements in prokaryotes. Annual Review of Genetics 15, 341404.
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.
Langley C. H., Brookfield J. F. Y. & Kaplan N. (1983). Transposable elements in Mendelian populations. I. A theory. Genetics 104, 457471.
Langley C. H., Montgomery E. & Quattlebaum W. E. (1982). Restriction map variation in the adh region of Drosophila. Proceedings of the National Academy of Sciences, USA 79, 56315635.
Langley C. H., Voelker R. A., Brown A. J. Leigh, Ohnishi S., Dickson B. & Montgomery E. (1981). Null allele frequencies at allozyme loci in natural populations of Drosophila melanogaster. Genetics 99, 151156.
Brown A. J. Leigh (1983). Variation at the 87A heat shock locus in Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 80, 53505354.
Brown A. J. Leigh & Moss J. E. (1987). Transposition of the I element and copia in a natural population of Drosophila melanogaster. Genetical Research 49, 121128.
Levis R., O'Hare K. & Rubin G. M. (1984). Effects of transposable element insertions on RNA encoded by the white gene of Drosophila. Cell 38, 471481.
Lewontin R. C. (1964). The interaction of selection and linkage. I. General considerations; heterotic models. Genetics 49, 4967.
Mackay T. F. C. (1986). Transposable element induced fitness mutations in Drosophila melanogaster. Genetical Research 48, 7787.
Maniatis T., Fritsch E. F. & Sambrook J. (1983). Molecular Cloning: A Laboratory Manual. Cold Spring Harbour Laboratory. New York: Cold Spring Harbour.
Montgomery E. A., Charlesworth B. & Langley C. H. (1987). A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genetical Research 49, 3141.
Morton N. E. (1971). Population genetics and disease control. Social Biology 18, 243251.
Muller H. J. (1955). On the relation between chromosome changes and gene mutations. Brookhaven Symposia 8, 126147.
Nei M. & Tajima F. (1983). Maximum likelihood estimation of the number of nucleotide substitutions from restriction site data. Genetics 105, 207217.
Parkhurst S. M. & Corces V. G. (1986). Interactions among the gypsy transposable element and the yellow and suppressor of Hairy-wing loci in Drosophila melanogaster. Molecular and Cellular Biology 6, 4753.
Pirrotta V. & Brockl C. (1984). Transcription of the Drosophila white locus and some of its mutants. EMBO Journal 3, 563568.
Rigby P. J., Breckmann M., Rhodes C. & Berg P. (1977). Labelling deoxyribonucleic acid in vitro by nick translation with DNA polymerase I. Journal of Molecular Biology 113, 237251.
Rowe T. C., Wang J. C. & Liu L. F. (1986). In vivo localization of DNA topoisomerase II cleavage sites in Drosophila melanogaster. Molecular Biology and Evolution 5, 3040.
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.
Simmons M. J. & Crow J. F. (1977). Mutations affecting fitness in Drosophila populations. Annual Review of Genetics 11, 4978.
Southern E. M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. Journal of Molecular Biology 98, 503517.
Udvardy A., Schedl P., Saunder M. & Hsieh T.-S. (1985). Novel partitioning of DNA cleavage sites for Drosophila topoisomerase II. Cell 40, 933941.
Villares R. & Cabrera C. V. (1987). The achaete-scute gene complex of Drosophila melanogaster: conserved domains in a subset of genes required for neurogenesis and their homology to myc. Cell 50, 415424.
Vieira J. & Messing J. (1982). The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with universal primers. Gene 19, 259268.
Voelker R. A., Langley C. H., Brown A. J. Leigh, Ohnishi S., Dickson B., Montgomery E. & Smith S. C. (1980). Enzyme null alleles in a natural population of Drosophila melanogaster: frequencies in a North Carolina population. Proceedings of the National Academy of Sciences, USA 77, 10911095.
Wahl G. M., Stern M. & Stark G. R. (1979). Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl paper and rapid hybridization using dextran sulphate. Proceedings of the National Academy of Sciences, USA 76, 36833687.
White K. (1980). Defective neural development in Drosophila melanogaster embryos deficient for the tip of the X chromosome. Developmental Biology 80, 332344.
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