Skip to main content
SpringerLink
Log in

P elements and the determinants of hybrid dysgenesis have different dynamics of propagation in Drosophila melanogaster populations

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Intraspecific hybrid dysgenesis (HD) appears after some strains of D. melanogaster are crossed. The predominant idea is that the movement of transposable P elements causes HD. It is believed that P elements appeared in the D. melanogaster genome in the middle of the last century by horizontal transfer, simultaneously with the appearance of HD determinants. A subsequent simultaneous expansion of HD determinants and P elements occurred. We analyzed the current distribution of HD determinants in natural populations of D. melanogaster and found no evidence of their further spread. However, full-sized P elements were identified in the genomes of all analyzed natural D. melanogaster strains independent of their cytotypes. Thus, the expansion of P elements does not correlate with the expansion of HD determinants. We found that the ovaries of dysgenic females did not contain germ cells despite the equal number of primordial germ cells in early stages in dysgenic and non-dysgenic embryos. We propose that HD does not result from DNA damage caused by P element transposition, but it would be the disruption in the regulation of dysgenic ovarian formation that causes the dysgenic phenotypes.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anxolabéhère D, Kidwell MG, Periquet G (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(3):252–269

    PubMed  Google Scholar 

  • Aravin A, Tuschl T (2005) Identification and characterization of small RNAs involved in RNA silencing. FEBS Lett 579(26):5830–5840

    Article  CAS  PubMed  Google Scholar 

  • Basquin D, Spierer A, Begeot F, Koryakov DE, Todeschini AL, Ronsseray S, Vieira C, Spierer P, Delattre M (2014) The Drosophila Su(var) 3–7 gene is required for oogenesis and female fertility, genetically interacts with piwi and aubergine, but impacts only weakly transposon silencing. PLoS One 9(5):e96802

    Article  PubMed Central  PubMed  Google Scholar 

  • Biémont C, Monti-Dedieu L, Lemeunier F (2004) Detection of transposable elements in Drosophila salivary gland polytene chromosomes by in situ hybridization. Methods Mol Biol 260:21–28

    PubMed  Google Scholar 

  • Bingham PM, Kidwell MG, Rubin GM (1982) The molecular basis of P–M hybrid dysgenesis: the role of the P element, a P-strain-specific transposon family. Cell 29(3):995–1004

    Article  CAS  PubMed  Google Scholar 

  • Black DM, Jackson MS, Kidwell MG, Dover GA (1987) KP elements repress P-induced hybrid dysgenesis in Drosophila melanogaster. EMBO J 6(13):4125–4135

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brennecke J, Malone CD, Aravin AA, Sachidanandam R, Stark A, Hannon GJ (2008) An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 322(5906):1387–1392

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clancy DJ, Hime GR, Shirras AD (2011) Cytoplasmic male sterility in Drosophila melanogaster associated with a mitochondrial CYTB variant. Heredity 107(4):374–376 (Edinb)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Corbett-Detig RB, Zhou J, Clark AG, Hartl DL, Ayroles JF (2013) Genetic incompatibilities are widespread within species. Nature 504(7478):135–137

    Article  CAS  PubMed  Google Scholar 

  • Daniels SB, Peterson KR, Strausbaugh LD, Kidwell MG, Chovnick A (1990) Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124(2):339–355

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dorogova NV, Akhmametyeva EM, Kopyl SA, Gubanova NV, Yudina OS, Omelyanchuk LV, Chang LS (2008) The role of Drosophila Merlin in spermatogenesis. BMC Cell Biol 9:1

    Article  PubMed Central  PubMed  Google Scholar 

  • Eggleston WB, Johnson-Schlitz DM, Engels WR (1988) P–M hybrid dysgenesis does not mobilize other transposable element families in D. melanogaster. Nature 331(6154):368–370

    Article  CAS  PubMed  Google Scholar 

  • Engels W, Preston C (1980) Components of hybrid dysgenesis in a wild population of Drosophila melanogaster. Genetics 95(1):111–128

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fukui T, Inoue Y, Yamaguchi M, Itoh M (2008) Genomic P elements content of a wild M’ strain of Drosophila melanogaster: KP elements do not always function as type II repressor elements. Genes Genet Syst 83(1):67–75

    Article  CAS  PubMed  Google Scholar 

  • Ilinsky Y (2013) Coevolution of Drosophila melanogaster mtDNA and Wolbachia genotypes. PLoS One 8(1):e54373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Itoh M, Woodruff RC, Leone MA, Boussy IA (1999) Genomic P elements and P–M characteristics of eastern Australian populations of Drosophila melanogaster. Genetica 106(3):231–245

    Article  CAS  PubMed  Google Scholar 

  • Itoh M, Sasai N, Inoue Y, Watada M (2001) P elements and P–M characteristics in natural populations of Drosophila melanogaster in the southernmost islands of Japan and in Taiwan. Heredity 86(Pt 2):206–212 (Edinb)

    Article  CAS  PubMed  Google Scholar 

  • Itoh M, Takeuchi N, Yamaguchi M, Yamamoto MT, Boussy IA (2007) Prevalence of full-size P and KP elements in North American populations of Drosophila melanogaster. Genetica 131(1):21–28

    Article  CAS  PubMed  Google Scholar 

  • Kelleher ES, Edelman NB, Barbash DA (2012) Drosophila interspecific hybrids phenocopy piRNA-pathway mutants. PLoS Biol 10(11):e1001428. doi:10.1371/journal.pbio.1001428

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Khurana JS, Wang J, Xu J, Koppetsch BS, Thomson TC, Nowosielska A, Li C, Zamore PD, Weng Z, Theurkauf WE (2011) Adaptation to P element transposon invasion in Drosophila melanogaster. Cell 147(7):1551–1563

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kidwell MG (1983) Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proc Natl Acad Sci USA 80(6):1655–1659

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kidwell MG, Novy JB (1979) Hybrid dysgenesis in Drosophila melanogaster: sterility resulting from gonadal dysgenesis in the P–M system. Genetics 92(4):1127–1140

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kidwell MG, Kidwell JF, Sved JA (1977) Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility and male recombination. Genetics 86(4):813–833

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kovalenko LV, Zakharenko LP, Voloshina MA, Karamysheva TV, Rubtsov NB, Zakharov IK (2006) Behavior of hobo and P transposons in yellow2-717 unstable line of Drosophila melanogaster and its derivatives after crossing with a laboratory strain. Genetika 42(6):748–756 (Russian)

    CAS  PubMed  Google Scholar 

  • Lewis AP, Brookfield JFY (1987) Movement of Drosophila melanogaster transposable elements other than P elements in a P–M hybrid dysgenic cross. Mol Gen Genet 208:506–510 (art%3A10.1007%2FBF00328147)

    Article  CAS  Google Scholar 

  • Moschetti R, Dimitri P, Caizzi R, Junakovic N (2010) Genomic instability of I elements of Drosophila melanogaster in absence of dysgenic crosses. PLoS One 5(10):pii: e13142

    Article  Google Scholar 

  • Norris ES, Woodruff RC (1992) Visible mutations induced by P–M hybrid dysgenesis in Drosophila melanogaster result predominantly from P element insertions. Mutat Res 269(1):63–72

    Article  CAS  PubMed  Google Scholar 

  • Ogura K, Woodruff RC, Itoh M, Boussy IA (2007) Long-term patterns of genomic P element content and P–M characteristics of Drosophila melanogaster in eastern Australia. Genes Genet Syst 82(6):479–487

    Article  CAS  PubMed  Google Scholar 

  • Onder BS, Kasap OE (2014) P element activity and molecular structure in Drosophila melanogaster populations from Firtina Valley, Turkey. J Insect Sci 14:16

    Article  PubMed  Google Scholar 

  • Patel NH (1994) Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. Methods Cell Biol 44:445–487

    Article  CAS  PubMed  Google Scholar 

  • Pertceva JA, Dorogova NV, Bolobolova EU, Nerusheva OO, Fedorova SA, Omelyanchuk LV (2010) The role of Drosophila hyperplastic discs gene in spermatogenesis. Cell Biol Int 34(10):991–996

    Article  CAS  PubMed  Google Scholar 

  • Riegler M, Sidhu M, Miller WJ, O’Neill SL (2005) Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol 15(15):1428–1433

    Article  CAS  PubMed  Google Scholar 

  • Rozhkov NV, Schostak NG, Zelentsova ES, Yushenova IA, Zatsepina OG, Evgen’ev MB (2013) Evolution and dynamics of small RNA response to a retroelement invasion in Drosophila. Mol Biol Evol 30(2):397–408

    Article  CAS  PubMed  Google Scholar 

  • Rubin GM, Kidwell MG, Bingham PM (1982) The molecular basis of P–M hybrid dysgenesis: the nature of induced mutations. Cell 29(3):987–994

    Article  CAS  PubMed  Google Scholar 

  • Sokolova MI, Zelentsova ES, Rozhkov NV, Evgen’ev MB (2010) Morphologic and molecular manifestations of hybrid dysgenesis in ontogenesis of Drosophila virilis. Ontogenez 41(6):451–454

    CAS  PubMed  Google Scholar 

  • Song J, Liu Jixia, Schnakenberg Sandra L, Ha Hongseok, Xing Jinchuan, Chen Kevin C (2014) Variation in piRNA and transposable element content in strains of Drosophila melanogaster. Genome Biol Evol 6(10):2786–2798

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Verspoor RL, Haddrill PR (2011) Genetic diversity, population structure and Wolbachia infection status in a worldwide sample of Drosophila melanogaster and D. simulans populations. PLoS One 6(10):e26318

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zakharenko LP, Kovalenko LV, Mai S, Zakharov IK (2007) Persistent locus-specific instability of yellow 2-717 and Notch (Uc-1) in Drosophila melanogaster coincides with hobo multiplication. Tsitologiia 49(11):977–981 (Russian)

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are thankful to P. Haddrill and D. Houle for sending flies from strains with completely sequenced genomes, M. Sonnenfeld for proofreading and referees for valuable comments. This work was funded by the Russian Foundation for Basic Research #14-04-00929 and Base project #YI.53.1.2.

Author information

Authors and Affiliations

  1. Institute of Cytology and Genetics SB RAS, Prospekt Lavrentyeva, 10, Novosibirsk, Russian Federation, 630090

    Olesia M. Ignatenko, Lyudmila P. Zakharenko, Natalia V. Dorogova & Svetlana A. Fedorova

  2. Novosibirsk State University, Pirogova Str., 2, Novosibirsk, Russian Federation, 630090

    Olesia M. Ignatenko, Lyudmila P. Zakharenko & Svetlana A. Fedorova

Authors
  1. Olesia M. Ignatenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lyudmila P. Zakharenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalia V. Dorogova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Svetlana A. Fedorova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lyudmila P. Zakharenko.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10709_2015_9872_MOESM1_ESM.tif

Fig. S1 Hybridization of P element probes to the polytene chromosomes of larval salivary glands of Canton S-4 strains. Arrows show hybridization sites of the P elements at 40x16 magnification. Scale bar is 10 mkm. (TIFF 163 kb)

10709_2015_9872_MOESM2_ESM.jpg

Fig. S2 PCR of genomic DNA two strains labeled Canton S (CS1: Canton S-1 and CS2: Canton S-2). M-marker; C1 – negative control (H2O); C2 – positive control (PCR of cloned P element). (JPEG 16 kb)

10709_2015_9872_MOESM3_ESM.tif

Fig. S3 Hybridization of P element probes to the polytene chromosomes of larval salivary glands of Canton S-3 strains as negative control. (TIFF 3164 kb)

10709_2015_9872_MOESM4_ESM.tif

Fig. S4 Hybridization of P element probes to the polytene chromosomes of larval salivary glands of GH strains as positive control. (TIFF 1776 kb)

10709_2015_9872_MOESM5_ESM.jpg

Fig. S5 Hybridization of P element probe to the polytene chromosomes of larval salivary glands of y; cn bw sp. Arrows show hybridization sites of the P elements at 40x16 magnification. (JPEG 46 kb)

10709_2015_9872_MOESM6_ESM.doc

Table S1 The range of cytotype depending on the percentage of defective ovaries in different cross-directions. (DOC 32 kb)

10709_2015_9872_MOESM7_ESM.doc

Table S2 The number of strains of each cytotype found in natural populations of D. melanogaster on different continents (Itoh et al. 1999; Itoh et al. 2001; Itoh et al. 2007; Ogura et al. 2007; Onder and Kasap 2012; Table 1). (DOC 52 kb)

10709_2015_9872_MOESM8_ESM.doc

Table S3 Current localization of blood hybridization sites in genomes of laboratory strains of D. melanogaster. (DOC 98 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ignatenko, O.M., Zakharenko, L.P., Dorogova, N.V. et al. P elements and the determinants of hybrid dysgenesis have different dynamics of propagation in Drosophila melanogaster populations. Genetica 143, 751–759 (2015). https://doi.org/10.1007/s10709-015-9872-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-015-9872-z

Keywords

Search

Navigation