Skip to main content
SpringerLink
Log in

Transposable elements and genome evolution: the case of Drosophila simulans

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Drosophila simulans presents a large variation in copy number among various transposable elements (TEs) and among natural populations for a given element. Some elements such as HMS beagle, blood, flea, tirant, coral, prygun jockey, F, nomade and mariner are absent in most populations, except in one or two which have copies on their chromosome arms. This suggests that some TEs are being awakened in D. simulans and are in the process of invading the species while it is colonizing the world. The elements 412 and roo/B104 present a wide insertion polymorphism among D. simulans populations, but only the 412 copy number follows a temperature cline. One population (Canberra from Australia) has a very high copy number for the 412 element and for many other TEs as well, indicating that some populations may have lost control of some of their TEs. While the 412 transposition rate is similar in all populations, its transcription level throughout developmental stages varies with populations, depending on copy number. Populations with 412 copy number higher than 10–12 exhibit co-suppression, while the expression in populations with lower numbers depends on the insertion location. All these results suggest genomic invasions by 412 and other TEs during the worldwide spread of the D. simulans species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anxolabéhère, D., M.G. Kidwell & G. Periquet, 1988. Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. Mol. Biol. Evol. 5: 252–269.

    PubMed  Google Scholar 

  • Arnault, C. & I. Dufournel, 1994. Genome and stresses: reactions against aggressions, behavior of transposable elements. Genetica 93: 149–160.

    Article  PubMed  CAS  Google Scholar 

  • Arnault, C., C. Lœvenbruck & C. Biémont, 1997. Transposable element mobilization is not induced by heat shocks in Drosophila melanogaster. Naturwissenschaften 84: 410–414.

    Article  PubMed  CAS  Google Scholar 

  • Bhadra, U., M. Pal-Bhadra & J.A. Birchler, 1997. A trans-acting modifier causing extensive overexpression of genes in Drosophila melanogaster. Mol. Gen. Genet. 254: 621–634.

    Article  PubMed  CAS  Google Scholar 

  • Biémont, C., 1992. Population genetics of transposable DNA elements. A Drosophila point of view. Genetica 86: 67–84.

    Article  PubMed  Google Scholar 

  • Biémont, C., 1994. Dynamic equilibrium between insertion and excision of P elements in highly inbred lines from an M' strain of Drosophila melanogaster. J. Mol. Evol. 39: 466–472.

    Article  PubMed  Google Scholar 

  • Biémont, C., C. Vieira, C. Hoogland, G. Cizeron, C. Lœvenbruck, C. Arnault & J.P. Carante, 1997. Maintenance of transposable element copy number in natural populations of Drosophila melanogaster and D. simulans. Genetica 100: 161–166.

    Article  PubMed  Google Scholar 

  • Bonnivard, E., C. Bazin, B. Denis & D. Higuet, 1999. A scenario for the hobo transposable element invasion, deduced from the structure of natural populations of Drosophila melanogaster using tandm TPE repeats. Genet. Res. Camb. 75: 13–23.

    Google Scholar 

  • Bonnivard, E. & D. Higuet, 1998. Stability of European natural populations of Drosophila melanogaster with regard to the P-M system: a buffer zone made up of Q populations. J. Evol. Biol. 12: 633–647.

    Article  Google Scholar 

  • Bonnivard, E., D. Higuet & C. Bazin, 1997. Characterization of natural populations of Drosophila melanogaster with regard to the hobo system: a new hypothesis on the invasion. Genet. Res. Camb. 69: 197–208

    CAS  Google Scholar 

  • Brookfield, J.F.Y., 1991. Models of repression of transposition in P-M hybrid dysgenesis by P cytotype and by zygotically encoded repressor proteins. Genetics 128: 471–486.

    PubMed  CAS  Google Scholar 

  • Brookfield, J.F.Y., 1996. Models of the spread of non-autonomous selfish transposable elements when transposition and fitness are coupled. Genet. Res. 67: 199–209.

    Google Scholar 

  • Brookfield, J.F.Y. & R.M. Badge, 1997. Population genetics models of transposable elements. Genetica 100: 281–294.

    Article  PubMed  CAS  Google Scholar 

  • Bucheton, A., R. Paro, H.M. Sang, A. Pélisson & D.J. Finnegan, 1984. The molecular basis of IR hybrid dysgenesis in D. melanogaster: identification, cloning and properties of the I factor. Cell 38: 153–163.

    Article  PubMed  CAS  Google Scholar 

  • Bucheton, A., C. Vaury, M.C. Chaboissier, P. Abad, A. Pélisson & M. Simonelig, 1992. I elements and the Drosophila genome. Genetica 86: 175–190.

    Article  PubMed  CAS  Google Scholar 

  • Busseau, I., M.C. Chaboissier, A. Pélisson & A. Bucheton, 1994. I factors in Drosophila melanogaster: transposition under control. Genetica 93: 101–116.

    Article  PubMed  CAS  Google Scholar 

  • Cavarec, L. & T. Heidmann, 1993. The Drosophila copia retrotransposon contains binding sites for transcriptional regulation by homeoproteins. Nucleic Acids Res. 21: 5041–5049.

    PubMed  CAS  Google Scholar 

  • Chakrani, F., P. Capy & J.R. David, 1993. Developmental temperature and somatic excision rate of mariner transposable element in three natural populations of Drosophila simulans. Genet. Sel. Evol. 25: 121–132.

    CAS  Google Scholar 

  • Cizeron, G. & C. Biémont, 1999. Polymorphism in structure of the retrotransposable element 412 in Drosophila simulans and D. melanogaster populations. Gene 232: 183–190.

    Article  PubMed  CAS  Google Scholar 

  • Costa, R., A.A. Peixoto, G. Barbujani & C.P. Kyriacou, 1992. A latitudinal cline in a Drosophila clock gene. Proc. R. Soc. Lond. 250: 43–49.

    CAS  Google Scholar 

  • Coyne, J.A., 1989. Mutation rates in hybrids between sibling species of Drosophila. Heredity 63: 155–162.

    PubMed  Google Scholar 

  • Crozatier, M., C. Vaury, I. Busseau, A. Pélisson & A. Bucheton, 1988. Structure and genomic organization of I elements involved in I-R hybrid dysgenesis in Drosophila melanogaster. Nucleic Acids Res. 16: 9199–9213.

    PubMed  CAS  Google Scholar 

  • Csink, A.K. & J.F. Mcdonald, 1990. Copia expression is variable among natural populations of Drosophila. Genetics 126: 375–385.

    PubMed  CAS  Google Scholar 

  • Daniels, S.B., S.H. Clark, M.G. Kidwell & A. Chovnick, 1987. Genetic transformation of Drosophila melanogaster with an autonomous P element: phenotypic and molecular analyses of long-established transformed lines. Genetics 115: 711–723.

    PubMed  CAS  Google Scholar 

  • Daniels, S.B., K.R. Peterson, L.D. Strausbaugh, M.G. Kidwell & A. Chovnick, 1990. Evidence for horizontal transmission of the P transposable element between drosophila species. Genetics 124: 339–355.

    PubMed  CAS  Google Scholar 

  • David, J.R. & L. Tsacas, 1981. Cosmopolitan, subcosmopolitan and widespread species: different strategies within the Drosophilid family (Diptera) C.R. Soc. Biogéo. 57: 11–26.

    Google Scholar 

  • Dawid, I.B., E.O. Long, P.P. DiNocera & M.L. Pardue, 1981. Ribosomal insertion-like elements in Drosophila melanogaster are interspersed with mobile sequences. Cell 25: 399–408.

    Article  PubMed  CAS  Google Scholar 

  • Dimitri, P., 1997. Constitutive heterochromatin and transposable elements in Drosophila melanogaster. Genetica 100: 85–93.

    Article  PubMed  CAS  Google Scholar 

  • Duke, J.S. & H.A. Mooney, 1999. Does global change increase the success of biological invaders? Trends Genet. 14: 135–139.

    Google Scholar 

  • Duvernell, D.D. & B.J. Turner, 1999. Variation and divergence of Death Valley pupfish populations at retrotransposon-defined loci. Mol. Biol. Evol. 16: 363–371.

    CAS  Google Scholar 

  • Eichenbaum, Z. & Z. Livneh, 1998. UV light induces IS 10 transposition in Escherichia coli. Genetics 149: 1173–1181.

    PubMed  CAS  Google Scholar 

  • Evgen'ev, M.B., G.N. Yenikolopov, N.I. Peunova & Y.V. Ilyin, 1982. Transposition of mobile genetic elements in interspecific hybrids of Drosophila. Chromosoma 85: 375–386.

    Article  PubMed  Google Scholar 

  • Flavell, A.J., S.W. Ruby, J.J. Toole, B.E. Roberts & G.M. Rubin, 1980. Translation and developmental regulation of RNA encoded by the eukaryotic transposable element copia. Proc. Natl. Acad. Sci. USA 77: 7107–7111.

    Article  PubMed  CAS  Google Scholar 

  • Garza, D., M. Medhora, A. Koga & D.L. Hartl, 1991. Introduction of the transposable element mariner into the germline of Drosophila melanogaster. Genetics 128: 303–310.

    PubMed  CAS  Google Scholar 

  • Giraud, T. & P. Capy, 1996. Somatic activity of the mariner transposable element in natural populations of Drosophila simulans. Proc. R. Soc. Lond. 263: 1481–1486.

    CAS  Google Scholar 

  • Good, A.G., G.A. Meister, H.W. Brock, T.A. Grigliatti & D.A. Hickey, 1989. Rapid spread of transposable P elements in experimental populations of Drosophila melanogaster. Genetics 122: 387–396.

    CAS  PubMed  Google Scholar 

  • Hale, L.R. & R.S. Singh, 1991. Contrasting patterns of genetic structure and evolutionary history as revealed by mitochondrial DNA and nuclear gene-enzyme variation between Drosophila melanogaster and Drosophila simulans. J. Genet. 70: 79–90.

    Article  Google Scholar 

  • Hamblin, M.T. & M. Veuille, 1999. Population structure among african and derived populations of Drosophila simulans: evidence for ancient subdivision and recent admixture. Genetics 153: 305–317.

    PubMed  CAS  Google Scholar 

  • Heslop-Harrison, J.S., A. Brandes, S. Taketa, T. Schmidt, A.V. Vershinin, E.G. Alkhimova, A. Kamm, R.L. Doudrick, T. Schwarzacher, A. Katsiotis, S. Kubis, A. Kumar, S.R. Pearce, A.J. Flavell & G.E. Harrison, 1997. The chromosomal distribution of Tyl-copia group retrotransposable elements in higher plants and their implications for genome evolution. Genetica 100: 197–204.

    Article  PubMed  CAS  Google Scholar 

  • Hirochika, H., K. Sugimoto, Y. Otsuki, H. Tsugawa & M. Kanda, 1996. Retrotransposons of rice involved in mutations induced by tissue culture. Proc. Natl. Acad. Sci. USA 93: 7783–7788.

    Article  PubMed  CAS  Google Scholar 

  • Irvin, S.D., K.A. Wetterstrand, C.M. Hutter & C.F. Aquadro, 1998. Genetic variation and differentiation at microsatellite loci in Drosophila simulans: evidence for founder effects in new world populations. Genetics 150: 777–790.

    PubMed  CAS  Google Scholar 

  • Jensen, S., M-P. Gassama & T. Heidmann, 1999. Taming of transposable elements by homology-dependent gene silencing. Nature Genetics 21: 209–212.

    Article  PubMed  CAS  Google Scholar 

  • Ke, N. & D.F. Voytas, 1999. cDNA of the yeast retrotransposon Ty5 preferentially recombines with substrates in silent chromatin. Mol. Cell. Biol. 19: 484–494.

    PubMed  CAS  Google Scholar 

  • Kidwell, M.G. & D.R. Lisch, 1997. Transposable elements as sources of variation in animals and plants. Proc. Natl. Acad. Sci. USA 94: 7704–7711.

    Article  PubMed  CAS  Google Scholar 

  • Kimura, K. & M.G. Kidwell, 1994. Differences in P element population dynamics between the sibling species Drosophila melanogaster and D. simulans. Genet. Res. 63: 27–38.

    PubMed  CAS  Google Scholar 

  • Labate, J.A., C.H. Biermann & W.F. Eanes, 1999. Nucleotide variation at the runt locus in Drosophila melanogaster and Drosophila simulans. Mol. Biol. Evol. 16: 724–731.

    PubMed  CAS  Google Scholar 

  • Labrador, M., M. Farré, F. Utzet & A. Fontdevilla, 1999. Interspecific hybridization increases transposition rates of Osvado. Mol. Biol. Evol. 16: 931–937.

    PubMed  CAS  Google Scholar 

  • Labrador, M., M.C. Seleme & A. Fontdevila, 1998. The evolutionary history of Drosophila buzzatii. XXXIV. The distribution of the retrotransposon Osvaldo in original and colonizing populations. Mol. Biol. Evol. 15: 1532–1547.

    PubMed  CAS  Google Scholar 

  • Lachaise, D., M. Cariou, J.R. David, F. Lemeunier, L. Tsacas & M. Ashburner, 1988. Historical biogeography of the Drosophila melanogaster species subgroup. Evol. Biol. 22: 159–227.

    Google Scholar 

  • Löwer, R., J. Löwer & R. Kurth, 1996. The viruses in all of us: Characteristics and biological significance of human endogenous retrovirus sequences. Proc. Natl. Acad. Sci. USA 93: 5177–5184.

    Article  PubMed  Google Scholar 

  • Maca, J. & G. Bächli, 1994. On the distribution of Chymomyza amoena (Loew), a species recently introduced into Europe. Bull. Soc. ent. Suisse 67: 183–188.

    Google Scholar 

  • Martin, G., D. Wiernasz & P. Schedl, 1983. Evolution of Drosophila repetitive-dispersed DNA. J. Mol. Evol. 19: 203–213.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, J.F., 1995. Transposable elements: possible catalists of organismic evolution. Trends Ecol. Evol. 10: 123–126.

    Article  Google Scholar 

  • McDonald, J.F., 1998. Transposable elements, gene silencing and macroevolution. Trends Ecol. Evol. 13: 95–98.

    Google Scholar 

  • Mhiri, C., J.B. Morel, S. Vernettes, J.M. Casacuberta, E. Lucas & M.A. Grandbastien, 1997. The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. Plant Mol. Biol. 33: 257–266.

    Article  PubMed  CAS  Google Scholar 

  • Montchamp-Moreau, C., 1990. Hybrid dysgenesis in P-transformed lines of Drosophila simulans. Evolution 44: 194–203.

    Article  Google Scholar 

  • Oakeshott, J.G., J.B. Gibson, P.R. Anderson, W.R. Knibb, D.G. Anderson & G.K. Chambers, 1992. Alcohol dehydrogenase and glycerol-3-phosphate dehydrogenase clines in Drosophila melanogaster on different continents. Evolution 36: 86–96.

    Article  Google Scholar 

  • O'Neill, R.J.W., M.J. O'Neill & J.A.M. Graves, 1998. Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393: 68–72.

    Article  PubMed  Google Scholar 

  • Orr, M.R. & T.B. Smith, 1998. Ecology and speciation. Trends Ecol. Evol. 13: 502–506.

    Article  Google Scholar 

  • Pagel, M. & R.A. Johnstone, 1992. Variation across species in the size of the nuclear genome supports the junk-DNA explanation for the C-value paradox. Proc. R. Soc. Lond. 249: 119–124

    CAS  Google Scholar 

  • Parkhurst, S.M. & V.G. Corces, 1987. Developmental expression of Drosophila melanogaster retrovirus-like transposable elements. EMBO J. 6: 419–424.

    PubMed  CAS  Google Scholar 

  • Pignatelli, P.M. & T.F.C. Mackay, 1989. Hybrid dysgenesis-induced response to selection in Drosophila melanogaster. Genet. Res. Camb. 54: 183–195.

    CAS  Google Scholar 

  • Robertson, H.M. & D.J. Lampe, 1995. Distribution of transposable elements in arthropods. Annu. Rev. Entomol. 40: 333–357.

    Article  PubMed  CAS  Google Scholar 

  • Rubin, G.M. & A.C. Spradling, 1982. Genetic transformation of Drosophila with transposable element vectors. Science 218: 348–353.

    PubMed  CAS  Google Scholar 

  • Russell, A.L. & R.C. Woodruff, 1999. The genetics and evolution of the mariner transposable element in Drosophila simulans: worldwide distribution and experimental population dynamics. Genetica 105: 149–164.

    Article  PubMed  CAS  Google Scholar 

  • Scherer, G., J. Telford, C. Baldari & V. Pirrotta, 1981. Isolation of cloned genes differentially expressed at early and late stages of Drosophila embryonic development. Dev. Biol. 86: 438–447.

    Article  PubMed  CAS  Google Scholar 

  • Sherwood, S.W. & J. Patton, 1982. Genome evolution in Pocket Gophers (genus Thomomys). II. Variation in cellular DNA content. Chromosoma 85: 163–179.

    Article  PubMed  CAS  Google Scholar 

  • Sun, X., J. Wahlstrom & G. Karpen, 1997. Molecular structure of a functional Drosophila centromere. Cell 91: 1007–1019.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, Jr., J.N. & R.C. Woodruff, 1980. Increased mutation in crosses between geographically separated strains of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 77: 1059–1062.

    Article  PubMed  Google Scholar 

  • Tsitrone, A., S. Charles & C. Biémont, 1999. Dynamics of transposable elements under the selection model. Genet. Res. 74: 159–164.

    Article  Google Scholar 

  • Uozu, S., H. Ikehashi, N. Ohmido, H. Ohtsubo, E. Ohtsubo & K. Fukui, 1997. Repetitive sequences: cause for variation in genome size and chromosome morphology in the genus Oryza. Plant Mol. Biol. 35: 791–799.

    Article  PubMed  CAS  Google Scholar 

  • Vaury, C., A. Bucheton & A. Pélisson, 1989. The β-heterochromatic sequences flanking the I elements are themselves defective transposable elements. Chromosoma 98: 215–224.

    Article  PubMed  CAS  Google Scholar 

  • Vaury, C., M.C. Chaboissier, M.E. Drake, O. Lajoinie, B. Dastugue & A. Pélisson, 1994. The doc transposable element in D. melanogaster and D. simulans: genomic distribution and transcription. Genetica 93: 117–124.

    Article  PubMed  CAS  Google Scholar 

  • Vieira, C., P. Aubry, D. Lepetit & C. Biémont, 1998. A temperature cline in copy number for 412 but not roo/B104 retrotransposons in populations of Drosophila simulans. Proc. R. Soc. Lond. 265: 1–5.

    Article  Google Scholar 

  • Vieira, C. & C. Biémont, 1996a. Geographical variation in insertion site number of retrotransposon 412 in Drosophila simulans. J. Mol. Evol. 42: 443–451.

    Article  PubMed  CAS  Google Scholar 

  • Vieira, C. & C. Biémont, 1996b. Selection against transposable elements in D. simulans and D. melanogaster. Genet. Res. 68: 9–15.

    Article  PubMed  CAS  Google Scholar 

  • Vieira, C. & C. Biémont, 1997. Transposition rate of the 412 retrotransposable element is independent of copy number in natural populations of Drosophila simulans. Mol. Biol. Evol. 14: 185–188.

    PubMed  CAS  Google Scholar 

  • Vieira, C., D. Lepetit, S. Dumont & C. Biémont, 1999. Wake up of transposable elements following Drosophila simulans worldwide colonization. Mol. Biol. Evol. 16: 1251–1255.

    PubMed  CAS  Google Scholar 

  • Walbot, V., 1998. UV-B damage amplified by transposons in maize. Nature 397: 398–399.

    Article  CAS  Google Scholar 

  • Withers, P. & R. Allemand, 1998. Chymomyza amoena (Loew), drosophile nouvelle pour la France (Diptera Drosophilidae). Bull. mens. Soc. linn. Lyon 67: 159–160.

    Google Scholar 

  • Woodruff, R.C., J.N. Thompson & R.F. Lyman, 1979. Intraspecific hybridization and the release of mutator activity. Nature 278: 277–279.

    Article  PubMed  CAS  Google Scholar 

  • Yoder, J.A., C. Walsh & T.H. Bestor, 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13: 335–340.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Biométrie et Biologie Evolutive, UMR C.N.R.S. 5558, Université Lyon1, 69622, Villeurbanne, France (Phone: (

    Christian Biémont, Cristina Vieira, Nathalie Borie & David Lepetit

Authors
  1. Christian Biémont
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristina Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nathalie Borie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David Lepetit
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Biémont, C., Vieira, C., Borie, N. et al. Transposable elements and genome evolution: the case of Drosophila simulans. Genetica 107, 113–120 (1999). https://doi.org/10.1023/A:1003937603230

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1003937603230

Search

Navigation