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Genetics. Jul 1994; 137(3): 815–827.
PMCID: PMC1206041

Transposable Element Numbers in Cosmopolitan Inversions from a Natural Population of Drosophila Melanogaster


Population studies of the distribution of transposable elements (TEs) on the chromosomes of Drosophila melanogaster have suggested that their copy number increase due to transposition is balanced by some form of natural selection. Theory suggests that, as a consequence of deleterious ectopic meiotic exchange between TEs, selection can favor genomes with lower TE copy numbers. This predicts that TEs should be less deleterious, and hence more abundant, in chromosomal regions in which recombination is reduced. To test this, we surveyed the abundance and locations of 10 families of TEs in recombination-suppressing chromosomal inversions from a natural population. The sample of 49 chromosomes included multiple independent isolates of seven different inversions and a corresponding set of standard chromosomes. For all 10 TE families pooled, copy numbers were significantly higher overall within low frequency inversions than within corresponding regions of standard chromosomes. TEs occupied chromosomal sites at significantly higher frequencies within the In(3R)M0 and In(3R)K inversions than within the corresponding regions of standard 3R chromosomes. These results are consistent with the predictions of the ectopic exchange model.

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Selected References

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  • Aguade M. Restriction map variation at the adh locus of Drosophila melanogaster in inverted and noninverted chromosomes. Genetics. 1988 May;119(1):135–140. [PMC free article] [PubMed]
  • Ashley T, Moses MJ, Solari AJ. Fine structure and behaviour of a pericentric inversion in the sand rat, Psammomys obesus. J Cell Sci. 1981 Aug;50:105–119. [PubMed]
  • Bojko M. Synaptic adjustment of inversion loops in Neurospora crassa. Genetics. 1990 Mar;124(3):593–598. [PMC free article] [PubMed]
  • Brookfield JF. The population biology of transposable elements. Philos Trans R Soc Lond B Biol Sci. 1986 Jan 29;312(1154):217–226. [PubMed]
  • Brookfield JF, Montgomery E, Langley CH. Apparent absence of transposable elements related to the P elements of D. melanogaster in other species of Drosophila. Nature. 310(5975):330–332. [PubMed]
  • Charlesworth B, Langley CH. The population genetics of Drosophila transposable elements. Annu Rev Genet. 1989;23:251–287. [PubMed]
  • Charlesworth B, Lapid A. A study of ten families of transposable elements on X chromosomes from a population of Drosophila melanogaster. Genet Res. 1989 Oct;54(2):113–125. [PubMed]
  • Charlesworth B, Lapid A, Canada D. The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genet Res. 1992 Oct;60(2):103–114. [PubMed]
  • Charlesworth B, Lapid A, Canada D. The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements. Genet Res. 1992 Oct;60(2):115–130. [PubMed]
  • Chovnick A. Gene conversion and transfer of genetic information within the inverted region of inversion heterozygotes. Genetics. 1973 Sep;75(1):123–131. [PMC free article] [PubMed]
  • Coyne JA, Meyers W, Crittenden AP, Sniegowski P. The fertility effects of pericentric inversions in Drosophila melanogaster. Genetics. 1993 Jun;134(2):487–496. [PMC free article] [PubMed]
  • Davis PS, Shen MW, Judd BH. Asymmetrical pairings of transposons in and proximal to the white locus of Drosophila account for four classes of regularly occurring exchange products. Proc Natl Acad Sci U S A. 1987 Jan;84(1):174–178. [PMC free article] [PubMed]
  • Doolittle WF, Sapienza C. Selfish genes, the phenotype paradigm and genome evolution. Nature. 1980 Apr 17;284(5757):601–603. [PubMed]
  • Feinberg AP, Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. [PubMed]
  • Felsenstein J, Yokoyama S. The evolutionary advantage of recombination. II. Individual selection for recombination. Genetics. 1976 Aug;83(4):845–859. [PMC free article] [PubMed]
  • Gabriel-Robez O, Ratomponirina C, Croquette M, Couturier J, Rumpler Y. Synaptonemal complexes in a subfertile man with a pericentric inversion in chromosome 21. Heterosynapsis without previous homosynapsis. Cytogenet Cell Genet. 1988;48(2):84–87. [PubMed]
  • Goldberg ML, Sheen JY, Gehring WJ, Green MM. Unequal crossing-over associated with asymmetrical synapsis between nomadic elements in the Drosophila melanogaster genome. Proc Natl Acad Sci U S A. 1983 Aug;80(16):5017–5021. [PMC free article] [PubMed]
  • Greenbaum IF, Reed MJ. Evidence for heterosynaptic pairing of the inverted segment in pericentric inversion heterozygotes of the deer mouse (Peromyscus maniculatus). Cytogenet Cell Genet. 1984;38(2):106–111. [PubMed]
  • Haigh J. The accumulation of deleterious genes in a population--Muller's Ratchet. Theor Popul Biol. 1978 Oct;14(2):251–267. [PubMed]
  • Hale DW. Heterosynapsis and suppression of chiasmata within heterozygous pericentric inversions of the Sitka deer mouse. Chromosoma. 1986;94(6):425–432. [PubMed]
  • Harada K, Yukuhiro K, Mukai T. Transposition rates of movable genetic elements in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1990 Apr;87(8):3248–3252. [PMC free article] [PubMed]
  • Holliday R. Gene conversion: a possible mechanism for eliminating selfish DNA. Basic Life Sci. 1982;20:259–264. [PubMed]
  • Kaplan NL, Hudson RR, Langley CH. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. [PMC free article] [PubMed]
  • Langley CH, Tobari YN, Kojima KI. Linkage disequilibrium in natural populations of Drosophila melanogaster. Genetics. 1974 Nov;78(3):921–936. [PMC free article] [PubMed]
  • Langley CH, Ito K, Voelker RA. Linkage disequilibrium in natural populations of Drosophila melanogaster Seasonal variation. Genetics. 1977 Jun;86(2 Pt 1):447–454. [PMC free article] [PubMed]
  • Langley CH, Montgomery E, Hudson R, Kaplan N, Charlesworth B. On the role of unequal exchange in the containment of transposable element copy number. Genet Res. 1988 Dec;52(3):223–235. [PubMed]
  • Lindsley DL, Sandler L. The genetic analysis of meiosis in female Drosophila melanogaster. Philos Trans R Soc Lond B Biol Sci. 1977 Mar 21;277(955):295–312. [PubMed]
  • Lyttle TW, Haymer DS. The role of the transposable element hobo in the origin of endemic inversions in wild populations of Drosophila melanogaster. Genetica. 1992;86(1-3):113–126. [PubMed]
  • Mackay TF, Lyman RF, Jackson MS. Effects of P element insertions on quantitative traits in Drosophila melanogaster. Genetics. 1992 Feb;130(2):315–332. [PMC free article] [PubMed]
  • Malpica JM, Vassallo JM, Frías A, Fuentes-Bol F. On recombination among In(2L)t, alpha-Gpdh and Adh in Drosophila melanogaster. Genetics. 1987 Jan;115(1):141–142. [PMC free article] [PubMed]
  • Martin J. Meiosis in inversion heterozygotes in Chironomidae. Can J Genet Cytol. 1967 Mar;9(1):255–268. [PubMed]
  • Smith JM, Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed]
  • McClintock B. The significance of responses of the genome to challenge. Science. 1984 Nov 16;226(4676):792–801. [PubMed]
  • McDonald JF. Evolution and consequences of transposable elements. Curr Opin Genet Dev. 1993 Dec;3(6):855–864. [PubMed]
  • Mettler LE, Voelker RA, Mukai T. Inversion Clines in Populations of DROSOPHILA MELANOGASTER. Genetics. 1977 Sep;87(1):169–176. [PMC free article] [PubMed]
  • Miklos GL, Yamamoto MT, Davies J, Pirrotta V. Microcloning reveals a high frequency of repetitive sequences characteristic of chromosome 4 and the beta-heterochromatin of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2051–2055. [PMC free article] [PubMed]
  • Montgomery E, Charlesworth B, Langley CH. A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet Res. 1987 Feb;49(1):31–41. [PubMed]
  • Montgomery EA, Huang SM, Langley CH, Judd BH. Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics. 1991 Dec;129(4):1085–1098. [PMC free article] [PubMed]
  • Mukai T, Voelker RA. The genetic structure of natural populations of Drosophila melanogaster XIII. Further studies on linkage disequilibrium. Genetics. 1977 May;86(1):175–185. [PMC free article] [PubMed]
  • Mukai T, Mettler LE, Chigusa SI. Linkage disequilibrium in a local population of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1971 May;68(5):1065–1069. [PMC free article] [PubMed]
  • Orgel LE, Crick FH. Selfish DNA: the ultimate parasite. Nature. 1980 Apr 17;284(5757):604–607. [PubMed]
  • Pamilo P, Nei M, Li WH. Accumulation of mutations in sexual and asexual populations. Genet Res. 1987 Apr;49(2):135–146. [PubMed]
  • Payne F. Crossover Modifiers in the Third Chromosome of DROSOPHILA MELANOGASTER. Genetics. 1924 Jul;9(4):327–342. [PMC free article] [PubMed]
  • Sheen F, Lim JK, Simmons MJ. Genetic instability in Drosophila melanogaster mediated by hobo transposable elements. Genetics. 1993 Feb;133(2):315–334. [PMC free article] [PubMed]
  • Sniegowski PD, Pringle A, Hughes KA. Effects of autosomal inversions on meiotic exchange in distal and proximal regions of the X chromosome in a natural population of Drosophila melanogaster. Genet Res. 1994 Feb;63(1):57–62. [PubMed]
  • Sturtevant AH, Beadle GW. The Relations of Inversions in the X Chromosome of Drosophila Melanogaster to Crossing over and Disjunction. Genetics. 1936 Sep;21(5):554–604. [PMC free article] [PubMed]
  • Voelker RA, Cockerham CC, Johnson FM, Schaffer HE, Mukai T, Mettler LE. Inversions fail to account for allozyme clines. Genetics. 1978 Mar;88(3):515–527. [PMC free article] [PubMed]
  • Wilke CM, Adams J. Fitness effects of Ty transposition in Saccharomyces cerevisiae. Genetics. 1992 May;131(1):31–42. [PMC free article] [PubMed]
  • Yamaguchi O, Ichinose M, Matsuda M, Mukai T. Linkage disequilibrium in isolated populations of Drosophila melanogaster. Genetics. 1980 Oct;96(2):507–522. [PMC free article] [PubMed]

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