Joint inference of evolutionary transitions to self-fertilization and demographic history using whole-genome sequences

  1. Stefan Strütt
  2. Thibaut Sellinger
  3. Sylvain Glémin
  4. Aurélien Tellier  Is a corresponding author
  5. Stefan Laurent  Is a corresponding author
  1. Max Planck Institute for Plant Breeding Research, Germany
  2. Technical University of Munich, Germany
  3. Université Rennes 1, CNRS, France

Abstract

The evolution from outcrossing to selfing is a transition that occurred recurrently throughout the eukaryote tree of life, in plants, animals, fungi and algae. Despite some short-term advantages, selfing is supposed to be an evolutionary dead-end reproductive strategy on the long-term and its tippy distribution on phylogenies suggests that most selfing species are of recent origin. However, dating such transitions is challenging while it is central for this hypothesis. We build on previous theories to explicit the differential effect of past changes in selfing rate or in population size on the probability of recombination events along the genome. This allows us to develop two methods making use of full genome polymorphism data to 1) test if a transition from outcrossing to selfing occurred, and 2) infer its age. The sequentially Markov coalescent based (teSMC) and the Approximate Bayesian Computation (tsABC) methods use a common framework based on a transition matrix summarizing the distribution of times to the most recent common ancestor along the genome, allowing to estimate changes in the ratio of population recombination and mutation rates in time. We first demonstrate that our methods can disentangle between past change in selfing rate from past changes in demographic history. Second, we assess the accuracy of our methods and show that transitions to selfing as old as approximatively 2.5Ne generations can be identified from polymorphism data. Third, our estimates are robust to the presence of linked negative selection on coding sequences. Finally, as a proof of principle, we apply both methods to three populations from Arabidopsis thaliana, recovering a transition to selfing which occurred approximately 600,000 years ago. Our methods pave the way to study recent transitions to predominant self-fertilization in selfing organisms and to better account for variation in mating systems in demographic inferences.

Data availability

The current manuscript is a computational study, so no data have been generated for this manuscript. Modelling code is available at the following repositories.tsABC: https://github.com/sstruett/tsABCteSMC: https://github.com/TPPSellinger/eSMC2scripts used for the analyses in Strütt and Sellinger et al: https://github.com/laurentlab-mpipz/struett_and_sellinger_et_al

The following previously published data sets were used

Article and author information

Author details

  1. Stefan Strütt

    Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2785-2815
  2. Thibaut Sellinger

    Department of Life Science Systems, Technical University of Munich, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Sylvain Glémin

    ECOBIO [Ecosystèmes, Biodiversité, Evolution), Université Rennes 1, CNRS, Rennes, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7260-4573
  4. Aurélien Tellier

    Department of Life Science Systems, Technical University of Munich, Munich, Germany
    For correspondence
    aurelien.tellier@tum.de
    Competing interests
    The authors declare that no competing interests exist.
  5. Stefan Laurent

    Max Planck Institute for Plant Breeding Research, Cologne, Germany
    For correspondence
    laurent@mpipz.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4016-5427

Funding

Max Planck Institute for Plant Breeding Research (open access funding)

  • Stefan Strütt
  • Stefan Laurent

No external funding was received for this work.

Copyright

© 2023, Strütt 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. Stefan Strütt
  2. Thibaut Sellinger
  3. Sylvain Glémin
  4. Aurélien Tellier
  5. Stefan Laurent
(2023)
Joint inference of evolutionary transitions to self-fertilization and demographic history using whole-genome sequences
eLife 12:e82384.
https://doi.org/10.7554/eLife.82384

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https://doi.org/10.7554/eLife.82384

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