High rates of evolution preceded shifts to sex-biased gene expression in Leucadendron, the most sexually dimorphic angiosperms

  1. Mathias Scharmann  Is a corresponding author
  2. Anthony G Rebelo
  3. John R Pannell
  1. University of Lausanne, Switzerland
  2. South African National Biodiversity Institute, South Africa

Abstract

Differences between males and females are usually more subtle in dioecious plants than animals, but strong sexual dimorphism has evolved convergently in the South African Cape plant genus Leucadendron. Such sexual dimorphism in leaf size is expected largely to be due to differential gene expression between the sexes. We compared patterns of gene expression in leaves among ten Leucadendron species across the genus. Surprisingly, we found no positive association between sexual dimorphism in morphology and the number or the percentage of sex-biased genes. Sex bias in most sex-biased genes evolved recently and was species-specific. We compared rates of evolutionary change in expression for genes that were sex-biased in one species but unbiased in others and found that sex-biased genes evolved faster in expression than un-biased genes. This greater rate of expression evolution of sex-biased genes, also documented in animals, might suggest the possible role of sexual selection in the evolution of gene expression. However, our comparative analysis clearly indicates that the more rapid rate of expression evolution of sex-biased genes predated the origin of bias, and shifts towards bias were depleted in signatures of adaptation. Our results are thus more consistent with the view that sex bias is simply freer to evolve in genes less subject to constraints in expression level.

Data availability

Sequencing data have been deposited at the European Nucleotide Archive (ENA project PRJEB45774).

The following data sets were generated

Article and author information

Author details

  1. Mathias Scharmann

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    For correspondence
    mathias.scharmann@unil.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8523-6888
  2. Anthony G Rebelo

    Applied Biodiversity Research Division, South African National Biodiversity Institute, Cape Town, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  3. John R Pannell

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

Funding

Swiss National Science Foundation (310030_185196)

  • John R Pannell

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

Reviewing Editor

  1. Vincent Castric, Université de Lille, France

Publication history

  1. Preprint posted: January 13, 2021 (view preprint)
  2. Received: February 21, 2021
  3. Accepted: October 27, 2021
  4. Accepted Manuscript published: November 2, 2021 (version 1)
  5. Version of Record published: December 1, 2021 (version 2)

Copyright

© 2021, Scharmann 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. Mathias Scharmann
  2. Anthony G Rebelo
  3. John R Pannell
(2021)
High rates of evolution preceded shifts to sex-biased gene expression in Leucadendron, the most sexually dimorphic angiosperms
eLife 10:e67485.
https://doi.org/10.7554/eLife.67485

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