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

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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

(2021) High rates of evolution preceded shifts to sex-biased expression in Leucadendron, the most sexually dimorphic angiosperms
Dryad Digital Repository, doi:10.5061/dryad.jsxksn0b4.

https://doi.org/10.5061/dryad.jsxksn0b4
(2021) High rates of evolution preceded shifts to sex-biased gene expression in Leucadendron, the most sexually dimorphic angiosperms
PRJEB45774.

https://www.ebi.ac.uk/ena/browser/view/PRJEB45774

Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0001-8523-6888
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.
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.

Copyright

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.