1. Evolutionary Biology
  2. Genetics and Genomics
Download icon

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
Research Article
  • Cited 7
  • Views 1,978
  • Annotations
Cite this article as: eLife 2021;10:e63194 doi: 10.7554/eLife.63194

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.

Metrics

  • 1,978
    Page views
  • 249
    Downloads
  • 7
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Evolutionary Biology
    2. Genetics and Genomics
    Osvaldo Villa et al.
    Short Report Updated

    The influence of genetic variation on the aging process, including the incidence and severity of age-related diseases, is complex. Here, we define the evolutionarily conserved mitochondrial enzyme ALH-6/ALDH4A1 as a predictive biomarker for age-related changes in muscle health by combining Caenorhabditis elegans genetics and a gene-wide association scanning (GeneWAS) from older human participants of the US Health and Retirement Study (HRS). In a screen for mutations that activate oxidative stress responses, specifically in the muscle of C. elegans, we identified 96 independent genetic mutants harboring loss-of-function alleles of alh-6, exclusively. Each of these genetic mutations mapped to the ALH-6 polypeptide and led to the age-dependent loss of muscle health. Intriguingly, genetic variants in ALDH4A1 show associations with age-related muscle-related function in humans. Taken together, our work uncovers mitochondrial alh-6/ALDH4A1 as a critical component to impact normal muscle aging across species and a predictive biomarker for muscle health over the lifespan.

    1. Evolutionary Biology
    Linda H Lidborg et al.
    Research Article Updated

    Humans are sexually dimorphic: men and women differ in body build and composition, craniofacial structure, and voice pitch, likely mediated in part by developmental testosterone. Sexual selection hypotheses posit that, ancestrally, more ‘masculine’ men may have acquired more mates and/or sired more viable offspring. Thus far, however, evidence for either association is unclear. Here, we meta-analyze the relationships between six masculine traits and mating/reproductive outcomes (96 studies, 474 effects, N = 177,044). Voice pitch, height, and testosterone all predicted mating; however, strength/muscularity was the strongest and only consistent predictor of both mating and reproduction. Facial masculinity and digit ratios did not significantly predict either. There was no clear evidence for any effects of masculinity on offspring viability. Our findings support arguments that strength/muscularity may be sexually selected in humans, but cast doubt regarding selection for other forms of masculinity and highlight the need to increase tests of evolutionary hypotheses outside of industrialized populations.