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Evidence for interspecific transfer of the transposable element mariner betweenDrosophila andZaprionus

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Summary

The transposable element mariner occurs widely in themelanogaster species group ofDrosophila. However, in drosophilids outside of themelanogaster species group, sequences showing strong DNA hybridization with mariner are found only in the genusZaprionus. the mariner sequence obtained fromZaprionus tuberculatus is 97% identical with that fromDrosophila mauritiana, a member of themelanogaster species subgroup, whereas a mariner sequence isolated fromDrosophila tsacasi is only 92% identical with that fromD. mauritiana. BecauseD. tsacasi is much more closely related toD. mauritiana than isZaprionus, the presence of mariner inZaprionus may result from horizontal transfer. In order to confirm lack of a close phylogenetic relationship between the genusZaprionus and themelanogaster species group, we compared the alcohol dehydrogenase (Adh) sequences among these species. The results show that the coding region of Adh is only 82% identical betweenZ. tuberculatus andD. mauritiana, as compared with 90% identical betweenD. tsacasi andD. mauritiana. Furthermore, the mariner gene phylogeny obtained by maximum likelihood and maximum parsimony analyses is discordant with the species phylogeny estimated by using the Adh genes. The only inconsistency in the mariner gene phylogeny is in the placement of theZaprionus mariner sequence, which clusters with mariner fromDrosophila teissieri andDrosophila yakuba in themelanogaster species subgroup. These results strongly suggest horizontal transfer.

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References

  • Abad PC, Vaury C, Pelisson A, Chaboissier M, Busseau I, Bucheton A (1989) A long interspersed repetitive element—theI factor ofDrosophila teissieri—is able to transpose in differentDrosophila species. Proc Natl Acad Sci USA 86:8887–8891

    PubMed  Google Scholar 

  • Ashburner M (1989)Drosophila: a laboratory handbook. Cold Spring Harbor laboratory Press, Cold Spring Harbor NY

    Google Scholar 

  • Beverley SM, Wilson AC (1984) Molecular evolution inDrosophila and the higher diptera II. Time scale for fly evolution. J Mol Evol 21:1–13

    PubMed  Google Scholar 

  • Black DM, Jackson MS, Kidwell MG, Dover GA (1987)KP elements repressP-induced hybrid dysgenesis inD. melanogaster. EMBO J 6:4125–4135

    PubMed  Google Scholar 

  • Blackman RK, Gelbart WM (1989) The transposable elementhobo ofDrosophila melanogaster. In: Berg DE, Howe M (eds) Mobile DNA. American Society for Microbiology, Washington DC, pp 523–529

    Google Scholar 

  • Bodmer M, Ashburner M (1984) Conservation and change in the DNA sequences coding for alcohol dehydrogenase in sibling species ofDrosophila. Nature 309:425–430

    PubMed  Google Scholar 

  • Bucheton A (1990)I transposable elements and I-R hybrid dysgenesis inDrosophila. Trends Genet 6:16–21

    PubMed  Google Scholar 

  • Capy P, Chakrani F, Lemeunier F, Hartl DL, David JR (1990) Active mariner transposable elements are widespread in natural populations ofDrosophila simulans. Proc R Soc Lond B 242:57–60

    Google Scholar 

  • Capy P, Maruyama K, David JR, Hartl DL (1991) Insertion sites of the transposable elementmariner are fixed in the genome ofDrosophila sechellia. J Mol Evol 33:450–456

    PubMed  Google Scholar 

  • Charlesworth B, Langley CH (1989) The population genetics ofDrosophila transposable elements. Annu Rev Genet 23:251–287

    PubMed  Google Scholar 

  • Cohn VH, Moore GP (1988) Organization and evolution of the alcohol dehydrogenase gene inDrosophila. Mol Biol Evol 5:154–166

    PubMed  Google Scholar 

  • Daniels SB, Strausbaugh LD, Armstrong RA (1985) Molecular analysis of P element behavior inDrosophila simulans. Mol Gen Genet 200:258–265

    PubMed  Google Scholar 

  • Daniels SB, Chovnick A, Kidwell MG (1989) Hybrid dysgenesis inDrosophila simulans lines transformed with autonomous P elements. Genetics 121:281–291

    PubMed  Google Scholar 

  • Daniels SB, Chovnick A, Boussy IA (1990a) Distribution ofhobo transposable elements in the genusDrosophila. Mol Biol Evol 7:589–606

    PubMed  Google Scholar 

  • Daniels SB, Peterson KR, Strausbaugh LD, Kidwell MG, Chovnick A (1990b) Evidence for horizontal transmission of theP transposable element betweenDrosophila species. Genetics 124:339–355

    PubMed  Google Scholar 

  • Engels WR (1989) P elements inDrosophila melanogaster. In: Berg DE, Howe M (eds) Mobile DNA. American Society for Microbiology, Washington DC, pp 437–484

    Google Scholar 

  • Federoff NV (1989) Maize transposable elements. In: Berg DE, Howe M (eds) Mobile DNA. American Society for Microbiology, Washington DC, pp 375–411

    Google Scholar 

  • Felsenstein J (1988a) PHYLIP: phylogeny inference package. Version 3.2. Department of Genetics SK-50, University of Washington, Seattle WA

    Google Scholar 

  • Felsenstein J (1988b) Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22:521–565

    PubMed  Google Scholar 

  • Finnegan DJ (1989) TheI factor and I-R hybrid dysgenesis inDrosophila melanogaster. In: Berg DE, Howe M (eds) Mobile DNA. American Society for Microbiology, Washington DC, pp 503–517

    Google Scholar 

  • Fischer JA, Maniatis T (1985) Structure and transcription of theDrosophila mulleri alcohol dehydrogenase genes. Nucleic Acids Res 13:6899–6917

    PubMed  Google Scholar 

  • Garza D, Medhora M, Koga A, Hartl DL (1991) Introduction of the transposable elementmariner into the germline ofDrosophila melanogaster. Genetics 128:303–310

    PubMed  Google Scholar 

  • Grimaldi DA (1990) A phylogenetic, revised classification of genera in the Drosophilidae (Diptera). Bull Am Mus Nat Hist 197:1–139

    Google Scholar 

  • Hagemann S, Miller WJ, Pinsker W (1990)P-related sequences inDrosophila bifasciata: a molecular clue to the understanding ofP-element evolution in the genusDrosophila. J Mol Evol 31:478–484

    PubMed  Google Scholar 

  • Harris LJ, Baillie DL, Rose AM (1988) Sequence identity between an inverted repeat family of transposable elements inDrosophila andCaenorhabditis. Nucleic Acids Res 16:5993–5998

    Google Scholar 

  • Helms C, Graham MY, Dutchik JE, Olson MV (1985) A new method for purifying lambda DNA from phage lysates. DNA 4:39–49

    PubMed  Google Scholar 

  • Henikoff S, Plasterk HA (1988) Related transposons inC. elegans andD. melanogaster. Nucleic Acids Res 16:6234

    PubMed  Google Scholar 

  • Jacobson JW, Medhora MM, Hartl DL (1986) Molecular structure of a somatically unstable transposable element inDrosophila. Proc Natl Acad Sci USA 83:8684–8688

    PubMed  Google Scholar 

  • Jeffs P, Ashburner M (1991) Processed pseudogenes inDrosophila. Proc R Soc London B 244:151–159

    Google Scholar 

  • Kaplan N, Darden T, Langley CH (1985) Evolution and extinction of transposable elements in Mendelian populations. Genetics 109:459–480

    PubMed  Google Scholar 

  • Kreitman M (1983) Nucleotide polymorphism at the alcohol dehydrogenase locus ofDrosophila melanogaster. Nature 304:412–417

    PubMed  Google Scholar 

  • Kuner JM, Nakanishi M, Ari Z, Drees B, Gustavson E, Theis J, Kauvar L, Kornberg T, O'farrell PH (1985) Molecular cloning ofengrailed, a gene involved in the development of pattern inDrosophila melanogaster. Cell 42:309–316

    PubMed  Google Scholar 

  • Lachaise D, Cariou M, David JR, Lemeunier F, Tsacas L, Ashburner M (1988) Historical biogeography of theDrosophila melanogaster species subgroup. Evol Biol 22:159–227

    Google Scholar 

  • Lemeunier F, David JR, Tsacas L, Ashburner M (1986) Themelanogaster species group. In: Ashburner M, Carson HL (eds) The genetics and biology ofDrosophila. Academic Press, New York, pp 147–256

    Google Scholar 

  • Lidholm D-A, Gudmundsson GH, Boman HG (1991) A highly repetitive,mariner-like element in the genome ofHyalophora cecropia. Jour Biol Chem 266:11518–11521

    Google Scholar 

  • Maruyama K, Hartl DL (1991) Evolution of the transposable elementmariner inDrosophila species. Genetics 128:319–329

    PubMed  Google Scholar 

  • Maruyama K, Schoor KD, Hartl DL (1991) Identification of nucleotide substitutions necessary for trans-activation ofmariner transposable elements inDrosophila: analysis of naturally occurring elements. Genetics 128:777–784

    PubMed  Google Scholar 

  • Medhora M, Maruyama K, Hartl DL (1991) Molecular and functional analysis of themariner mutator elementMos1 inDrosophila. Genetics 128:311–318

    PubMed  Google Scholar 

  • Miller DW, Miller LK (1982) A virus mutant with an insertion of a copia-like transposable element. Nature 299:562–564

    PubMed  Google Scholar 

  • Misra S, Rio C (1990) Cytotype control ofDrosophila P element transposition: the 66 kd protein is a repressor of transposase activity. Cell 40:269–284

    Google Scholar 

  • Mizrokhi LJ, Mazo AM (1990) Evidence for horizontal transmission of the mobile elementjockey between distantDrosophila species. Proc Natl Acad Sci USA 87:9216–9220

    PubMed  Google Scholar 

  • Nitasaka E, Mukai T, Yamazaki T (1987) Repressor ofP elements inDrosophila melanogaster: cytotype determination by a defectiveP element with only open reading frames 0 through 2. Proc Natl Acad Sci USA 84:7605–7608

    Google Scholar 

  • O'Brochta DA, Handler AM (1988) Mobility ofP elements in drosophilids and nondrosophilids. Proc Natl Acad Sci USA 85:6052–6056

    Google Scholar 

  • Rio DC (1990) Molecular mechanisms regulatingDrosophila P element transposition. Annu Rev Genet 24:543–578

    PubMed  Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-termination inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    PubMed  Google Scholar 

  • Scavarda NJ, Hartl DL (1984) Interspecific DNA transformation inDrosophila. Proc Natl Acad Sci USA 81:7515–7519

    PubMed  Google Scholar 

  • Scavarda NJ, Hartl DL (1987) Germline abnormalities inDrosophila simulans transfected with the transposableP element. J Genet 66:1–15

    Google Scholar 

  • Schaeffer SW, Aquadro CF (1987) Nucleotide sequence of theAdh gene region ofDrosophila pseudoobscura: evolutionary change and evidence for an ancient gene duplication. Genetics 117:61–73

    PubMed  Google Scholar 

  • Simmons MJ, Bucholz LM (1985) Transposase titration inDrosophila melanogaster: a model of cytotype in the P-M system of hybrid dysgenesis. Proc Natl Acad Sci USA 82:8119–8123

    PubMed  Google Scholar 

  • Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517

    PubMed  Google Scholar 

  • Swofford DL (1989) PAUP: phylogenetic analysis using parsimony, version 3.0. Illinois Natural History Survey, Champaign IL

    Google Scholar 

  • Templeton AR (1983a) Convergent evolution and nonparametric inferences from restriction data and DNA sequences. In: Weir BS (eds) Statistical analysis of DNA sequence data Marcel Dekker, New York, pp 151–179

    Google Scholar 

  • Templeton AR (1983b) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221–244

    Google Scholar 

  • Throckmorton LH (1975) The phylogeny, ecology, and geography ofDrosophila. In: King RC (eds) Handbook of genetics. Plenum, New York, pp 421–469

    Google Scholar 

  • Tsacas L, Lachaise D, David JR (1981) Composition and biogeography of the afrotropical drosophilid fauna. In: Ashburner M, Carson HL, Thompson JN Jr (eds) The genetics and biology ofDrosophila. Academic Press, New York, pp 197–259

    Google Scholar 

  • Ullu E, Tschudi C (1984) Alu sequences are processed 7SL RNA genes. Nature 312:171–172

    PubMed  Google Scholar 

  • Xiong Y, Eickbush TH (1988) Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol Biol Evol 5:675–690

    PubMed  Google Scholar 

Download references

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Maruyama, K., Hartl, D.L. Evidence for interspecific transfer of the transposable element mariner betweenDrosophila andZaprionus . J Mol Evol 33, 514–524 (1991). https://doi.org/10.1007/BF02102804

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  • DOI: https://doi.org/10.1007/BF02102804

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