1. Evolutionary Biology
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Asexual reproduction reduces transposable element load in experimental yeast populations

  1. Jens Bast  Is a corresponding author
  2. Kamil S Jaron
  3. Donovan Schuseil
  4. Denis Roze
  5. Tanja Schwander
  1. University of Lausanne, Switzerland
  2. Centre National de la Recherche Scientifique, France
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Cite this article as: eLife 2019;8:e48548 doi: 10.7554/eLife.48548

Abstract

Theory predicts that sexual reproduction can either facilitate or restrain transposable element (TE) accumulation by providing TEs with a means of spreading to all individuals in a population, versus facilitating TE load reduction via purifying selection. By quantifying genomic TE loads over time in experimental sexual and asexual Saccharomyces cerevisiae populations, we provide direct evidence that TE loads decrease rapidly under asexual reproduction.. We show, using simulations, that this reduction may occus via evolution of TE activity, most likely via increased excision rates. Thus, sex is a major driver of genomic TE loads and at the root of the success of TEs.

Data availability

Raw read data of the experiment is available at SRA (BioProject identifier PRJNA308843). All data processing and analyses scripts as well as the simulator together with explanations are available at https://github.com/KamilSJaron/reproductive_mode_TE_dynamics.

The following previously published data sets were used

Article and author information

Author details

  1. Jens Bast

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    For correspondence
    mail@jensbast.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0017-3860
  2. Kamil S Jaron

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1470-5450
  3. Donovan Schuseil

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Denis Roze

    Centre National de la Recherche Scientifique, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Tanja Schwander

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.

Funding

Deutsche Forschungsgemeinschaft (BA 5800/1-1)

  • Jens Bast

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (PP00P3_17062)

  • Tanja Schwander

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (PP00P3_139013)

  • Tanja Schwander

Deutsche Forschungsgemeinschaft (BA 5800/2-1)

  • Jens Bast

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

Reviewing Editor

  1. Graham Coop, University of California, Davis, United States

Publication history

  1. Received: May 17, 2019
  2. Accepted: September 4, 2019
  3. Accepted Manuscript published: September 5, 2019 (version 1)
  4. Version of Record published: October 8, 2019 (version 2)

Copyright

© 2019, Bast 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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Further reading

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    Recent theory has overturned the assumption that accelerating returns from individual specialisation are required to favour the evolution of division of labour. Yanni et al., 2020, showed that topologically constrained groups, where cells cooperate with only direct neighbours such as for filaments or branching growths, can evolve a reproductive division of labour even with diminishing returns from individual specialisation. We develop a conceptual framework and specific models to investigate the factors that can favour the initial evolution of reproductive division of labour. We find that selection for division of labour in topologically constrained groups: (1) is not a single mechanism to favour division of labour—depending upon details of the group structure, division of labour can be favoured for different reasons; (2) always involves an efficiency benefit at the level of group fitness; and (3) requires a mechanism of coordination to determine which individuals perform which tasks. Given that such coordination must evolve prior to or concurrently with division of labour, this could limit the extent to which topological constraints favoured the initial evolution of division of labour. We conclude by suggesting experimental designs that could determine why division of labour is favoured in the natural world.

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    Meiotic drivers are genetic elements that break Mendel’s law of segregation to be transmitted into more than half of the offspring produced by a heterozygote. The success of a driver relies on outcrossing (mating between individuals from distinct lineages) because drivers gain their advantage in heterozygotes. It is, therefore, curious that Schizosaccharomyces pombe, a species reported to rarely outcross, harbors many meiotic drivers. To address this paradox, we measured mating phenotypes in S. pombe natural isolates. We found that the propensity for cells from distinct clonal lineages to mate varies between natural isolates and can be affected both by cell density and by the available sexual partners. Additionally, we found that the observed levels of preferential mating between cells from the same clonal lineage can slow, but not prevent, the spread of a wtf meiotic driver in the absence of additional fitness costs linked to the driver. These analyses reveal parameters critical to understanding the evolution of S. pombe and help explain the success of meiotic drivers in this species.