Evolutionary dynamics of transposable elements in bdelloid rotifers

  1. Reuben W Nowell  Is a corresponding author
  2. Christopher G Wilson
  3. Pedro Almeida
  4. Philipp H Schiffer
  5. Diego Fontaneto
  6. Lutz Becks
  7. Fernando Rodriguez
  8. Irina R Arkhipova
  9. Timothy G Barraclough  Is a corresponding author
  1. University of Oxford, United Kingdom
  2. University College London, United Kingdom
  3. University of Cologne, Germany
  4. National Research Council of Italy, Italy
  5. University of Konstanz, Germany
  6. Marine Biological Laboratory, United States

Abstract

Transposable elements (TEs) are selfish genomic parasites whose ability to spread autonomously is facilitated by sexual reproduction in their hosts. If hosts become obligately asexual, TE frequencies and dynamics are predicted to change dramatically, but the long-term outcome is unclear. Here, we test current theory using whole-genome sequence data from eight species of bdelloid rotifers, a class of invertebrates in which males are thus far unknown. Contrary to expectations, we find a variety of active TEs in bdelloid genomes, at an overall frequency within the range seen in sexual species. We find no evidence that TEs are spread by cryptic recombination or restrained by unusual DNA repair mechanisms. Instead, we find that that TE content evolves relatively slowly in bdelloids and that gene families involved in RNAi-mediated TE suppression have undergone significant expansion, which might mitigate the deleterious effects of active TEs and compensate for the consequences of long-term asexuality.

Data availability

All raw sequencing data have been deposited in the relevant International Nucleotide Sequence Database Collaboration (INSDC) databases under the Study ID PRJEB39843. Genome assemblies and gene predictions have been deposited at DDBJ/ENA/GenBank with the same Study ID. Figure 2--source data 2 has been uploaded to Dryad Digital Repository (doi:10.5061/dryad.fbg79cnsr).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Reuben W Nowell

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    For correspondence
    reubennowell@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7546-6495
  2. Christopher G Wilson

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Pedro Almeida

    Division of Biosciences, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Philipp H Schiffer

    Institute of Zoology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6776-0934
  5. Diego Fontaneto

    Water Research Institute, National Research Council of Italy, Verbania Pallanza, Italy
    Competing interests
    The authors declare that no competing interests exist.
  6. Lutz Becks

    University of Konstanz, Konstanz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Fernando Rodriguez

    Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Irina R Arkhipova

    Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4805-1339
  9. Timothy G Barraclough

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    For correspondence
    tim.barraclough@zoo.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.

Funding

Natural Environment Research Council (NE/M01651X/1)

  • Timothy G Barraclough

Natural Environment Research Council (NE/S010866/2)

  • Christopher G Wilson
  • Timothy G Barraclough

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Antonis Rokas, Vanderbilt University, United States

Publication history

  1. Received: September 17, 2020
  2. Accepted: February 4, 2021
  3. Accepted Manuscript published: February 5, 2021 (version 1)
  4. Accepted Manuscript updated: February 11, 2021 (version 2)
  5. Version of Record published: March 8, 2021 (version 3)

Copyright

© 2021, Nowell et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Reuben W Nowell
  2. Christopher G Wilson
  3. Pedro Almeida
  4. Philipp H Schiffer
  5. Diego Fontaneto
  6. Lutz Becks
  7. Fernando Rodriguez
  8. Irina R Arkhipova
  9. Timothy G Barraclough
(2021)
Evolutionary dynamics of transposable elements in bdelloid rotifers
eLife 10:e63194.
https://doi.org/10.7554/eLife.63194
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