Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-26T14:56:10.711Z Has data issue: false hasContentIssue false

Background selection and patterns of genetic diversity in Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Brian Charlesworth
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1101 E. 57th Street, Chicago, IL 60637-1573, USA
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.

Theoretical models of the effects of selection against deleterious mutations on variation at linked neutral sites (background selection) are used to predict the relations between chromosomal location and genetic variability at the DNA level, in Drosophila melanogaster. The sensitivity of the predictions to variation in the mutation, selection and recombination parameters on which they are based is examined. It is shown that many features of the observed relations between chromosomal location and level of genetic diversity in D. melanogaster can be explained by background selection, especially if the weak selective forces acting on transposable elements are taken into account. In particular, the gradient in diversity in the distal portion of the X chromosome, and the lack of diversity on chromosome 4 and at the bases of the major chromosomes, can be fully accounted for. There are, however, discrepancies between predicted and observed values for some loci in D. melanogaster, which may reflect the effects of forces other than background selection.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

References

Aguadé, M. (1988). Restriction map variation of the Adh locus of Drosophila melanogaster in inverted and noninverted chromosomes. Genetics 119, 135140.Google Scholar
Aguadé, M., Miyashita, N., & Langley, C. H., (1989a). Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics 122, 607615.CrossRefGoogle ScholarPubMed
Aguadé, M., Miyashita, N., & Langley, C. H. (1989 b). Restriction-map variation at the zeste-tko region in natural populations of Drosophila melanogaster. Molecular Biology and Evolution 6, 123130.Google ScholarPubMed
Aguadé, M., Miyashita, N., & Langley, C. H., (1992). Polymorphism and divergence in the Mst26A male accessory gland gene region in Drosophila melanogaster. Genetics 132, 755770.Google Scholar
Aguadé, M. & Langley, C. H., (1994). Polymorphism and divergence in regions of low recombination in Drosophila. In Non-neutral Evolution: Theories and Molecular Data (ed. B., Golding), pp. 6776. London: Chapman and Hall.Google Scholar
Aguadé, M., Meyers, W., Long, A. D., & Langley, C. H., (1994). Reduced DNA sequence polymorphism in the su(s) and s(wa) regions of Drosophila melanogaster as revealed by SSCP and stratified DNA sequencing. Proceedings of the National Academy of Sciences of the USA 91, 46584662.Google Scholar
Aquadro, C. F., 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.Google Scholar
Aquadro, C. F., Jennings, R. M. J., Bland, M. M., Laurie, C. C., & Langley, C. H., (1992). Patterns of naturally occurring restriction map variation and linkage disequilibrium in the Ddc region of Drosophila melanogaster. Genetics 132, 443452.CrossRefGoogle ScholarPubMed
Aquadro, C. F., Begun, D. J., & Kindahl, E. C., (1994). Selection, recombination, and DNA polymorphism in Drosophila. In Non-neutral Evolution: Theories and Molecular Data (ed. B., Golding), pp. 4656. London: Chapman and Hall.CrossRefGoogle Scholar
Ashburner, M., (1989). Drosophila. A Laboratory Handbook. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.Google Scholar
Barton, N. H., (1995). Linkage and the limits to natural selection. Genetics 140, 821884.CrossRefGoogle ScholarPubMed
Begun, D. J., & Aquadro, C. F., (1991). Molecular population genetics of the distal portion of the X chromosome in Drosophila. evidence for genetic hitchhiking of the yellow-achaete region. Genetics 129, 11471158.CrossRefGoogle ScholarPubMed
Begun, D. J., & Aquadro, C. F., (1992). Levels of natural occurring DNA polymorphism correlate with recombination rate in Drosophila melanogaster. Nature 356, 519520.CrossRefGoogle Scholar
Begun, D. J., & Aquadro, C. F., (1993). African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature 365, 548550.Google Scholar
Berry, A. J., Ajioka, J. W., & Kreitman, M., (1991). Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics 129, 11111117.Google Scholar
Bièmont, C., (1992). Population genetics of transposable DNA elements: a Drosophila point of view. Genetica 86, 6784.CrossRefGoogle ScholarPubMed
Braverman, J. M., Hudson, R. R., Kaplan, N. L., Langley, C. H., & Stephan, W., (1995). The hitchhiking effect on the site frequency spectrum of DNA polymorphism. Genetics 140, 783796.Google Scholar
Brooks, L. D., (1988). The evolution of recombination rates. In The Evolution of Sex (ed. Michod, R. E. & Levin, B. R.), pp. 87105. Sunderland, MA: Sinauer.Google Scholar
Caballero, A., (1995). On the effective size of populations with separate sexes, with particular reference to sexlinked genes. Genetics 139, 10071011.Google Scholar
Charlesworth, B., (1991). Transposable elements in natural populations, with a mixture of selected and neutral insertion sites. Genetical Research 57, 127134.CrossRefGoogle ScholarPubMed
Charlesworth, B., (1994). The effect of background selection against deleterious alleles on weakly selected, linked variants. Genetical Research 63, 213228.Google Scholar
Charlesworth, B., & Langley, C. H., (1991). Population genetics of transposable elements in Drosophila. In Evolution at the Molecular Level (ed. Selander, R. K., Clark, A. G. & Whittam, T. S.), pp. 150–76. Sunderland, MA: Sinauer.Google Scholar
Charlesworth, B., & Lapid, A., (1989). A study of ten transposable elements on X chromosomes from a population of Drosophila melanogaster. Genetical Research 54, 113125.CrossRefGoogle ScholarPubMed
Charlesworth, B., Lapid, A., & Canada, D., (1992a). The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genetical Research 60, 103114.Google Scholar
Charlesworth, B., Lapid, A., & Canada, D., (1992b). The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements. Genetical Research 60, 115130.CrossRefGoogle Scholar
Charlesworth, B., Morgan, M. T., & Charlesworth, D., (1993). The effect of deleterious mutations on neutral molecular variation. Genetics 134, 12891303.CrossRefGoogle ScholarPubMed
Charlesworth, D., Charlesworth, B., & Morgan, M. T., (1995). The pattern of neutral molecular variation under the background selection model. Genetics 141, 1619–632.CrossRefGoogle ScholarPubMed
Chovnick, A., (1973). Gene conversion and transfer of genetic information within the inverted region of inversion heterozygotes. Genetics 74, 123131.Google Scholar
Cobbs, G., (1978). Renewal approach to the theory of genetic linkage: case of no chromatid interference. Genetics 89, 563581.CrossRefGoogle Scholar
Crow, J. F., & Simmons, M. J., (1983). The mutation load in Drosophila. In The Genetics and Biology of Drosophila. Vol. 3c (ed. Ashburner, M., Carson, H. L. & Thomson, J. N.), pp. 135. London: Academic Press.Google Scholar
Denell, R. E., & Keppy, D. O., (1979). The nature of genetic recombination near the third chromosome centromere of Drosophila melanogaster. Genetics 93, 117130.CrossRefGoogle ScholarPubMed
Dubinin, N. P., Sokolov, N. N., & Tiniakov, G. G., (1937). Crossing over between the genes ‘yellow’ and ‘scute’. Drosophila Information Service 8, 76.Google Scholar
Gillespie, J. H., (1994). Alternatives to the neutral theory. In Non-neutral Evolution: Theories and Molecular Data (ed. Golding, B.), pp. 17. London: Chapman and Hall.Google Scholar
Green, M. M., (1975). Conversion as a possible mechanism of high coincidence values in the centromeric region of Drosophila. Molecular and General Genetics 44, 12431256.Google Scholar
Grell, R. F., (1962). A new model for secondary non-disjunction: the role of distributive pairing. Genetics 47, 17371754.Google Scholar
Haldane, J. B. S., (1919). The combination of linkage values and the calculation of distance between loci of linked factors. Journal of Genetics 8, 299309.Google Scholar
Haldane, J. B. S., (1927). A mathematical theory of natural and artificial selection. V. Selection and mutation. Proceedings of the Cambridge Philosophical Society 23, 838844.Google Scholar
Heino, T. I., Saura, A. O., & Sorsa, V., (1994). Maps of the salivary gland chromosomes of Drosophila melanogaster Drosophila Information Service 73, 621738.Google Scholar
Houle, D., Hughes, K. A., Hoffmaster, D. K., Ihara, J. T., Assimacopoulos, S., & Charlesworth, B., (1994). The effect of spontaneous mutation on quantitative traits. I. Variances and covariances of life history traits. Genetics 138, 773785.Google Scholar
Hudson, R. R., (1994). How can the low levels of DNA sequence variation in regions of the Drosophila genome with low recombination rates be explained? Proceedings of the National Academy of Sciences of the USA 91, 68156818.CrossRefGoogle ScholarPubMed
Hudson, R. R., & Kaplan, N. L., (1994). Gene trees with background selection. In Non-neutral Evolution: Theories and Molecular Data (ed. Golding, B.), pp. 140–53. London: Chapman and Hall.CrossRefGoogle Scholar
Hudson, R. R., & Kaplan, N. L., (1995). Deleterious background selection with recombination. Genetics 141, 16051617.Google Scholar
Hudson, R. R., Kreitman, M., & Aguadé, M., (1987). A test of molecular evolution based on nucleotide data. Genetics 116, 153159.CrossRefGoogle ScholarPubMed
Hughes, K. A., (1995). The inbreeding decline and average dominance of genes affecting male life-history characters in Drosophila melanogaster. Genetical Research 65, 4145.Google Scholar
Ives, P. T., (1947). Report of P. T. Ives. Drosophila Information Service 21, 6869.Google Scholar
Ives, P. T., (1967). Relocation of the or locus closer to pd. Drosophila Information Service 42, 76.Google Scholar
Kaplan, N. L., Hudson, R. R., & Langley, C. H., (1989). The ‘hitch-hiking’ effect revisited. Genetics 123, 887899.CrossRefGoogle Scholar
Karess, R. E., & Glover, D. M., (1989). Rough deal: a gene required for proper mitotic segregation in Drosophila. Journal of Cell Biology 109, 29512961.Google Scholar
Keightley, P. D., (1994). The distribution of mutation effects on viability in Drosophila melanogaster. Genetics 138,1–8.Google Scholar
Kosambi, D. D., (1944). The estimation of map distance from recombination values. Annals of Eugenics 12, 172175.CrossRefGoogle Scholar
Kreitman, M., (1991). Detecting selection at the level of DNA. In Evolution at the Molecular Level (ed. Selander, R. K., Clark, A. G. & Whittam, T. S.), pp. 202221. Sunderland, MA: Sinauer.Google Scholar
Kreitman, M., & Wayne, M. L., (1994). Organization of genetic variation at the molecular level: lessons from Drosophila. In Molecular Ecology and Evolution: Approaches and Applications (ed. Schierwater, B., Streit, B., Wagner, G. P. & DeSalle, R.), pp. 157184. Basel: Birkhäuser.Google Scholar
Krimbas, C. B., & Powell, J. R., (1992). Introduction. In Inversion Polymorphism in Drosophila.(ed. Krimbas, C. B. & Powell, J. R.), pp. 152. Boca Raton, FL: CRC Press.Google Scholar
Langley, C. H., Montgomery, E. A., Hudson, R. R., Kaplan, N. L., & Charlesworth, B., (1988). On the role of unequal exchange in the containment of transposable element copy number. Genetical Research 52, 223235.Google Scholar
Langley, C. H., MacDonald, J., Miyashita, N., & Aguadé, M. (1993). Lack of correlation between interspecific divergence and intraspecific polymorphism at the suppressor of forked region in Drosophila melanogaster and Drosophila simulans. Proceedings of the National Academy of Sciences of the USA 90, 18001803.Google Scholar
Lefevre, G., (1971). Salivary chromosome bands and the frequency of crossing over in Drosophila melanogaster. Genetics 67, 497513.Google Scholar
Lefevre, G., (1976). A photographic representation of the polytene chromosomes of Drosophila melanogaster salivary glands. In The Genetics and Biology of Drosophila (ed. Ashburner, M. & Novitski, E.), pp. 3136. Orlando, FL: Academic Press.Google Scholar
Lemeunier, F., & Aulard, S., (1992). Inversion polymorphism in Drosophila melanogaster. In Drosophila Inversion Polymorphism (ed. Krimbas, C. B. & Powell, J. R.), pp. 339406. Boca Raton, FL: CRC Press.Google Scholar
Lewis, E. B., (1945). The relation of repeats to position effects in Drosophila melanogaster. Genetics 30, 137166.Google Scholar
Lindsley, D. L., & Sandler, L., (1977). The genetic analysis of meiosis in female Drosophila. Philosophical Transactions of the Royal Society of London, Series B 277, 295312.Google ScholarPubMed
Lindsley, D. L., & Zimm, G. G., (1992). The Genome of Drosophila melanogaster. San Diego, CA: Academic Press.Google Scholar
Lucchesi, J. C., (1976). Inter-chromosomal effects. In The Genetics and Biology of Drosophila, Vol. 1 a (ed. Ashburner, M. & Novitski, E.), pp. 315330. New York: Academic Press.Google Scholar
Martin-Campos, J. M., Comeron, J. M., Miyashita, N., & Aguadé, M. (1992). Intraspecific and interspecific variation at the y-ac-sc region of Drosophila simulans and Drosophila melanogaster. Genetics 130, 805816.CrossRefGoogle ScholarPubMed
Smith, J. Maynard, & Haigh, J., (1974). The hitch-hiking effect of a favourable gene. Geneticul Research 23, 2335.Google Scholar
Miklos, G. L. G., & Cotsell, J. N., (1990). Chromosome structure at interfaces between major chromatin types: alpha- and 6era-heterochromatin. BioEssays 12, 16.Google Scholar
Miyashita, N. T., (1990). Molecular and phenotypic variation of the Zw locus region in Drosophila melanogaster. Genetics 125, 407419.Google Scholar
Miyashita, N. T., & Langley, C. H., (1988). Molecular and phenotypic evolution of the white locus in Drosophila melanogaster. Genetics 120, 199212.Google Scholar
Miyashita, N. T., & Langley, C. H., (1994). Restriction map polymorphism in the forked and vermilion regions of Drosophila melanogaster. Japanese Journal of Genetics 69, 297305.Google Scholar
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.Google Scholar
Montgomery, E. A., Huang, S.-M., Langley, C. H., & Judd, B. H., (1991). Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics 129, 10851098.Google Scholar
Moriyama, E. N., & Powell, J. R., (1996). Intraspecific nuclear DNA variation in Drosophila. Molecular Biology and Evolution 13, 261277.Google Scholar
Mukai, T, Chigusa, S. I., Mettler, L. E., & Crow, J. F., (1972). Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. Genetics 72, 335355.CrossRefGoogle ScholarPubMed
Nagylaki, T., (1995). The inbreeding effective population number in dioecious populations. Genetics 139, 473485.Google Scholar
Nordborg, M., Charlesworth, B., & Charlesworth, D., (1996). The effect of recombination on background selection. Genetical Research 67, 159174.Google Scholar
Nuzhdin, S. V., & Mackay, T. F. C., (1995). The genomic rate of transposable element movement in Drosophila melanogaster. Molecular Biology and Evolution 12, 180181.Google Scholar
Ohnishi, O., (1977). Spontaneous and ethyl methanesulfonate- induced mutations controlling viability in Drosophila melanogaster. II. Homozygous effects of polygenic mutations. Genetics 87, 529545.Google Scholar
Ohnishi, S., & Voelker, R. A., (1979). Comparative studies of allozyme loci in Drosophila.simulans and D. melanogaster. II. Gene arrangement on the third chromosome. Japanese Journal of Genetics 54, 203209.Google Scholar
Owen, A. R. G., (1951). An extension of Kosambi's formula. Nature 168, 208209.Google Scholar
Padilla, H. M., & Nash, W. G., (1977). A further characterization of the cinnamon gene in Drosophila melanogaster. Molecular and General Genetics 155, 171177.CrossRefGoogle Scholar
Payne, F., (1924). Crossover modifiers in the third chromosome of Drosophila melanogaster. Genetics 9, 327342.CrossRefGoogle ScholarPubMed
Redfield, H., (1955). Recombination increase due to heterologous inversions and the relation to cytological length. Proceedings of the National Academy of Sciences of the USA 41, 10841091.Google Scholar
Roberts, D. B., Brock, H. W., Rudden, N. C., & Evans-Roberts, S., (1985). A genetic and cytogenetic analysis of the region surrounding the LSP-1-β gene in Drosophila melanogaster. Genetics 109, 145156.Google Scholar
Roberts, D. R., & Evans-Roberts, S., (1979). The genetic and cytogenetic localization of the three structural genes coding for the major protein of Drosophila larval serum. Genetics 93, 663679.Google Scholar
Roberts, P. A., (1962). Interchromosomal effects and the relation between crossing-over and non-disjunction. Genetics 47, 16911710.Google Scholar
Roberts, P. A., (1976). The genetics of chromosome aberration. In The Genetics and Biology of Drosophila, vol. 1 a (ed. Ashburner, M. & Novitski, E.), pp. 68184. New York: Academic Press.Google Scholar
Sato, T., (1984). A new homeotic mutation affecting antennae and legs. Drosophila Information Service 60, 180182.Google Scholar
Schalet, A., (1972). Crossing over in the major heterochromatic region of the X chromosome in normal and inverted sequences. Drosophila Information Service 48, 111113.Google Scholar
Schalet, A., & Lefevre, G., (1976). The proximal region of the X chromosome. In The Genetics and Biology of Drosophila, vol. 1 b (ed. Ashburner, M. & Novitski, E.), pp. 847902. London: Academic Press.Google Scholar
Schüpbach, T., & Wieschaus, E., (1989). Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129, 11191136.Google Scholar
Simonsen, K. L., Churchill, G. A., & Aquadro, C. F., (1995). Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141, 413429.Google Scholar
Sinclair, D. A., (1975). Crossing over between closely linked markers spanning the centromere of chromosome 3 in Drosophila melanogaster. Genetical Research 26, 173186.Google Scholar
Sniegowski, P. D., Pringle, A., & Hughes, K. A., (1994). Effect of autosomal inversions on meiotic exchange in distal and proximal regions of the X chromosome in a natural population of Drosophila melanogaster. Genetical Research 63, 5762.Google Scholar
Stephan, W., (1995). An improved method for estimating the rate of fixation of favorable mutations based on DNA polymorphism data. Molecular Biology and Evolution 12, 959962.Google Scholar
Sturtevant, A. H., (1931). Known and probably inverted sections of the autosomes of Drosophila melanogaster. Carnegie Institution of Washington Publications 421, 127.Google Scholar
Sturtevant, A. H., (1949). Sequence of loci near the centromere of chromosome 2. Drosophila Information Service 23, 98.Google Scholar
Sturtevant, A. H., (1956). A highly specific complementary lethal system in Drosophila melanogaster. Genetics 41, 118123.Google Scholar
Takano, T. S., Kusakabe, S., & Mukai, T., (1991). The genetic structure of natural populations of Drosophila melanogaster. XXII. Comparative studies of DNA polymorphism in northern and southern populations. Genetics 129, 753761.Google Scholar
Wesley, C. S., & Eanes, W. F., (1994). Isolation and analysis of the breakpoint sequences of chromosome inversion In (JL)Payne in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA 91, 31323136.Google Scholar
Wiehe, T. H. E., & Stephan, W., (1993). Analysis of a genetic hitchhiking model and its application to DNA polymorphism data. Molecular Biology and Evolution 10, 842854.Google Scholar