Skip to main content
SpringerLink
Log in

The Association Between Breeding System and Transposable Element Dynamics in Daphnia Pulex

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Transposable elements (TEs) are major sources of genetic variation, and mating systems are believed to play a significant role in their dynamics. For example, insertion number is expected to be higher in sexual than in asexual organisms due to the inability of TEs to colonize new genomes in the absence of sex. The goal of this study was to determine the impact of the loss of sexual reproduction on TE load. Daphnia pulex has two reproductive modes, obligate and cyclical parthenogenesis, which differ with respect to the production of diapausing eggs. Cyclical parthenogens produce them meiotically, while obligate parthenogens produce them clonally. Pokey is a TTAA-specific DNA transposon, and is a stable component of Daphnia genomes. We used a PCR-based approach, TE-Display, to estimate the number of Pokey insertions in 22 cyclic and 22 obligate isolates of D. pulex. As expected, the copy number of Pokey insertions is significantly higher in cyclic than in obligate isolates. However, the distribution of elements among isolates within each breeding system is similar, which is congruent with the recent establishment of obligate lineages from a cyclic ancestor. We also assayed 46 isolates from eight cyclic populations and found that very few Pokey insertions were observed in more than one isolate, suggesting that Pokey has been active recently. Sequencing of PCR products from the TE-Display analysis shows that Pokey inserts into both coding and noncoding regions of the genome. However, there is no obvious similarity among sequences downstream of the TTAA Pokey insertion site.

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

  • Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein data base search program. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Arkhipova I, Meselson M (2000) Transposable elements in sexual and ancient asexual taxa. Proc Natl Acad Sci USA 97:14473–14477

    Article  PubMed  CAS  Google Scholar 

  • Arkhipova I, Meselson M (2004) Deleterious transposable elements and the extinction of asexuals. Bioessays 27:76–85

    Article  Google Scholar 

  • Arkhipova I, Meselson M (2005) Diverse DNA transposons in rotifers of the class Bdelloidea. Proc Natl Acad Sci USA 102:11781–11786

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (1980) How selfish is DNA? Nature 285:617–618

    Article  PubMed  CAS  Google Scholar 

  • Crease T (1986) Mitochondrial DNA variation in Daphnia pulex Leydig producing by obligate and cyclic parthenogenesis. Ph.D. dissertation, Washington University, St. Louis, MO

  • Crease T, Lynch M (1991) Ribosomal DNA variation in Daphnia pulex. Mol Biol Evol 8:620–640

    CAS  Google Scholar 

  • Crease T, Stanton D, Hebert P (1989) Polyphyletic origin of asexuality in Daphnia pulex. II. Mitochondrial DNA variation. Evolution 43:1016–1026

    Article  Google Scholar 

  • Doyle J, Doyle J (1987) A rapid DNA isolation procedure for small quantities of fresh leaf. Phytochem Bull 19:11–15

    Google Scholar 

  • Eickbush T, Eickbush D (2007) Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:477–485

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Finnegan D (1990) Transposable elements and DNA transposition in eukaryotes. Curr Opin Cell Biol 2:471–477

    Article  PubMed  CAS  Google Scholar 

  • Gladyshev E, Meselson M, Arkhipova I (2007) A deep-branching clade of retrovirus-like retrotransposons in Bdelloid rotifers. Gene 390:136–145

    Article  PubMed  CAS  Google Scholar 

  • Hebert P (1995) The Daphnia of North America. CD-ROM. University of Guelph, Guelph, ON

    Google Scholar 

  • Hebert P, Beaton M, Schwartz S, Stanton D (1989) Polyphyletic origins of asexuality in Daphnia pulex: I. Breeding system variation and levels of clonal diversity. Evolution 43:1004–1015

    Article  Google Scholar 

  • Hebert P, Finston T (2001) Macrogeographic patterns of breeding system diversity in the Daphnia pulex group from the United States and Mexico. Heredity 87:153–161

    Article  PubMed  CAS  Google Scholar 

  • Hebert P, Ward R, Weider L (1988) Clonal diversity patterns and breeding system variation in Daphnia pulex: an asexual–sexual complex. Evolution 42:147–159

    Article  Google Scholar 

  • Hebert P, Schwartz S, Ward R, Finston T (1993) Macrogeographic patterns of breeding system diversity in the Daphnia pulex group. I. Breeding systems of Canadian populations. Heredity 70:148–161

    Article  Google Scholar 

  • Hickey D (1982) Selfish DNA: a sexually transmitted nuclear parasite. Genetics 101:519–531

    PubMed  CAS  Google Scholar 

  • Innes D, Schwartz S, Hebert P (1986) Genotypic diversity and variation in mode of reproduction among populations in the Daphnia pulex group. Heredity 57:345–355

    Article  Google Scholar 

  • Kidwell M, Lisch D (2001) Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 55:1–24

    PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–164

    Article  PubMed  CAS  Google Scholar 

  • McTaggart S, Dudycha J, Omilian A, Crease T (2007) Rates of recombination in the ribosomal DNA of apomictically propagated Daphnia obtusa lines. Genetics 175:311–320

    Article  PubMed  CAS  Google Scholar 

  • Nuzhdin S, Petrov D (2003) Transposable elements in clonal lineages: lLethal hangover from sex. Biol J Linn Soc 79:33–41

    Article  Google Scholar 

  • Omilian A, Taylor D (2001) Rate acceleration and long-branch attraction in a conserved gene of cryptic daphniid (Crustacea) species. Mol Biol Evol 18:2201–2212

    PubMed  CAS  Google Scholar 

  • Omilian A, Cristescu M, Dudycha J, Lynch M (2006) Ameiotic recombination in asexual lineages of Daphnia. Proc Natl Acad Sci USA 103:18638–18643

    Article  PubMed  CAS  Google Scholar 

  • Paland S, Colbourne J, Lynch M (2005) Evolutionary history of contagious asexuality in Daphnia pulex. Evolution 59:800–813

    PubMed  CAS  Google Scholar 

  • Penton E, Crease T (2004) Evolution of the transposable element Pokey in the ribosomal DNA of the species in the subgenus Daphnia (Crustacea: Cladocera). Mol Biol Evol 21:1727–1739

    Article  PubMed  CAS  Google Scholar 

  • Penton E, Sullender B, Crease T (2002) Pokey, a new DNA transposon in Daphnia (Cladocera: Crustacea). J Mol Evol 55:664–673

    Article  PubMed  CAS  Google Scholar 

  • Sullender B (1993) Preliminary characterization and population genetic survey of the Daphnia rDNA transposable element, Pokey. Ph.D. dissertation, University of Oregon, Eugene, Eugene, OR

  • Sullender B, Crease T (2001) The behavior of a Daphnia pulex transposable element in cyclically and obligately parthenogenetic populations. J Mol Evol 53:63–69

    PubMed  CAS  Google Scholar 

  • Wright S, Schoen D (1999) Transposon dynamics and the breeding system. Genetics 107:139–148

    Article  CAS  Google Scholar 

  • Wright S, Le QH, Schoen D, Bureau T (2001) Population dynamics of an Ac-like transposable element in self- and cross-pollinating Arabidopsis. Genetics 158:1279–1288

    PubMed  CAS  Google Scholar 

  • Zeyl C, Bell G, Green D (1996) Sex and the spread of retrotransposon Ty3 in experimental populations of Saccharomyces cerevisiae. Genetics 143:1567–1577

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Financial support for the work was provided by a research grant from the Natural Sciences and Engineering Research Council of Canada to T.J.C. We thank M. Lynch and D. Innes for generously providing some of the D. pulex isolates used in this study and A. Holliss and E. Holmes for analysis of TED fragments and sequencing of plasmid clones on the ABI3730. Comments provided by two anonymous reviewers improved an earlier version of the paper.

Author information

Authors and Affiliations

  1. Department of Integrative Biology, University of Guelph, Guelph, ON, Canada, N1G 2W1

    Pegah Valizadeh & Teresa J. Crease

Authors
  1. Pegah Valizadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Teresa J. Crease
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Teresa J. Crease.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Valizadeh, P., Crease, T.J. The Association Between Breeding System and Transposable Element Dynamics in Daphnia Pulex . J Mol Evol 66, 643–654 (2008). https://doi.org/10.1007/s00239-008-9118-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-008-9118-0

Keywords

Search

Navigation