Skip to main content
×
Home
    • Aa
    • Aa

The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements

  • Brian Charlesworth (a1), Angela Lapid (a1) and Darlene Canada (a1)
Summary
Summary

Data were collected on the distribution of nine families of transposable elements among a sample of autosomes isolated from a natural population of Drosophila melanogaster, by means of in situ hybridization of biotinylated probes to polytene chromosomes. There is no general tendency for elements to accumulate at the tips of chromosomes. Elements tend to be present in excess of random expectation in the euchromatin proximal to the centromeres of the major autosomes, and on chromosome four. There is considerable heterogeneity between different families in the extent of this excess. The overall abundance of element families is inversely related to the extent to which they accumulate proximally. The level of proximal accumulation for the major autosomes is similar to that on the fourth chromosome, but less than that for the X chromosome. There is an overall deficiency of elements in the mid-section of the X compared with the mid-sections of the major autosomes, with considerable heterogeneity between families. The magnitude of this deficiency is positively related to the extent to which elements accumulate proximally. No such deficiency is seen if the proximal regions of the X and autosomes are compared. There is a small and non-significant excess of elements in third chromosomes carrying inversions. There is some between-year heterogeneity in element abundance. The implications of these findings are discussed, and it is concluded that they generally support the hypothesis that transposable element abundance is regulated primarily by the deleterious fitness consequences of meiotic ectopic exchange between elements. If this is the case, such exchange must be very infrequent in the proximal euchromatin, and the elements detected in population surveys of this kind must be inserted into sites where they have negligible mutational effects on fitness.

Copyright
Corresponding author
*Corresponding author.
References
Hide All
Ashburner M. (1989). Drosophila. A Laboratory Handbook. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.
Begun D. J. & Aquadro C. F. (1992). Levels of naturally occurring DNA polymorphism correlate with recombination rate in D.melanogaster. Nature 356, 519520.
Bingham P. M. & Zachar Z. (1989). Retroposons and the FB transposon from Drosophila melanogaster. In Mobile DNA (ed. Berg D. E. and Howe M. M.), pp. 485502. Washington D.C.: American Society of Microbiology.
Bolshakov V. N. Zharkikh A. A. & Zhimulev I. F. (1985). Intercalary heterochromatin in Drosophila. II. Heterochromatic features in relation to local DNA content along the polytene chromosomes of Drosophila melanogaster. Chromosoma 92, 200208.
Charlesworth B. (1991). Transposable elements in natural populations with a mixture of insertion sites. Genetical Research 57, 127134.
Charlesworth B. & Charlesworth D. (1983). The population dynamics of transposable elements. Genetical Research 42, 127.
Charlesworth B. & Charlesworth D. (1985). Genetic variation in recombination in Drosophila. I. Responses to selection and preliminary genetic analysis. Heredity 54, 7184.
Charlesworth B. & Langley C. H. (1986). The evolution of self-regulated transposition of transposable elements. Genetics 112, 359383.
Charlesworth B. & Langley C. H. (1989). The population genetics of Drosophila transposable elements. Annual Review of Genetics 23, 251287.
Charlesworth B. & Lapid A. (1989). A study often families of transposable elements on X chromosomes from a population of Drosophila melanogaster. Genetical Research 54, 113125.
Charlesworth B. Lapid A. & Canada D. (1992). The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genetical Research 60, 103114.
Charlesworth B. Coyne J. A. & Barton N. H. (1987). The relative rates of evolution of sex chromosomes and autosomes. American Naturalist 130, 113146.
Coyne J. A. & Milstead B. (1987). Long-distance migration of Drosophila melanogaster. 3. Dispersal of alleles from a Maryland orchard. American Naturalist 130, 7082.
Crow J. F. & Simmons M. J. (1983). The mutation load in Drosophila. In The Genetics and Biology of Drosophila, vol. 3c (ed. Carson H. L. Ashburner M. and Thomson J. N.), pp. 135. London: Academic Press.
Eanes W. F. Wesley C. & Charlesworth B. (1992). Accumulation of P elements in minority inversions in natural populations of Drosophila melanogaster. Genetical Research 59, 19.
Gowen J. W. & Gay E. H. (1983). Gene number, size and kind in Drosophila. Genetics 18, 131.
Hartl D. L. Ajioka J. W. Cai H. Lohe A. R. Lozovskaya E. R. Smoller D. A. & Duncan I. W. (1992). Towards a Drosophila genome map. Trends in Genetics 8, 7075.
Hochman B. (1976). The fourth chromosome of Drosophila melanogaster. In The Genetics and Biology of Drosophila, vol. 1b (ed. Ashburner M. and Novitski E.), pp. 903928. London: Academic Press.
Kaplan N. L. Hudson R. R. & Langley C. H. (1989). The ‘hitchhiking effect’ revisited. Genetics 123, 887889.
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 49, 3141.
Lefevre G. (1976). A photographic representation of the polytene chromosomes of Drosophila melanogaster salivary glands. In The Genetics and Biology of Drosophila, vol. 1a (ed. Ashburner M. and Novitski E.), pp. 3136. London: Academic Press.
Lindsley D. L. & Grell E. H. (1968). Genetic Variations of Drosophila melanogaster. Washington: Carnegie Institution.
Lindsley D. L. & Zimm G. (1992). The Genome of Drosophila melanogaster. San Diego: Academic Press.
Maynard Smith J. & Haigh J. (1974). The hitch-hiking effect of a favourable gene. Genetical Research 23, 2335.
Miklos G. L. G. & Cotsell J. N. (1990). Chromosome structure at interfaces between major chromosomal types: β-heterochromatin and β-heterochromatin. Bioessays 12, 17.
Montgomery E. A. & Langley C. H. (1983). Transposable elements in IMendelian populations. II. Distribution of three copy a-like elements in a natural population. Genetics 104, 473483.
Montgomery E. A. Charlesworth B. & Langley C. H. (1987). A test for the role of natural selection in the stabilization element copy number in a population of Drosophila melanogaster. Genetical Research 49, 3141.
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.
Mosteller F. & Tukey J. W. (1977). Data Analysis and Regression. Reading, Mass.: Addison-Wesley.
Simmons M. J. & Crow J. F. (1977). Mutations affecting fitness in Drosophila. Annual Review of Genetics 11, 4978.
Shrimpton A. E. Montgomery E. A. & Langley C. H. (1986). Om mutations in Drosophila ananassae are linked to insertions of a transposable element. Genetics 114, 125135.
Stephan W. Wiehe T. H. E. & Lenz M. W. (1992). The effect of strongly selected substitutions on neutral polymorphism: analytical results based on diffusion theory. Theoretical Population Biology 41, 237254.
Tanda S. Shrimpton A. E. Ling-Ling C. Itayama H. Matsubayashi H. Saigo K. Tobari Y. N. & Langley C. H. (1988). Retrovirus-like features and site specific insertions of a transposable element, torn, in Drosophila ananassae. Molecular and General Genetics 214, 405411.
Wallace B. (1968). Mutation rates for autosomal lethals in Drosophila melanogaster. Genetics 60, 389393.
Yamamoto M.-T. Mitchelson A. Tudor M. O'Hare K. Davies J. A. & Miklos G. L. G. (1990). Molecular and cytogenetic analysis of the heterochromatin-euchromatin junction region of the Drosophila melanogaster X chromosome. Genetics 125, 821832.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Genetics Research
  • ISSN: 0016-6723
  • EISSN: 1469-5073
  • URL: /core/journals/genetics-research
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 2 *
Loading metrics...

Abstract views

Total abstract views: 60 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 21st October 2017. This data will be updated every 24 hours.