Sex-biased gene expression in an hemimetabolous insect: pattern during development, extent, functions involved, rate of sequence evolution, and comparison with an holometabolous insect
Dynamics of sex-biased gene expression over development in the stick insect Timema californicum
Recommendation: posted 25 October 2021, validated 08 November 2021
An individual’s sexual phenotype is determined during development. Understanding which pathways are activated or repressed during the developmental stages leading to a sexually mature individual, for example by studying gene expression and how its level is biased between sexes, allows us to understand the functional aspects of dimorphic phenotypes between the sexes.
Several studies have quantified the differences in transcription between the sexes in mature individuals, showing the extent of this sex-bias and which functions are affected. There is, however, less data available on what occurs during the different phases of development leading to this phenotype, especially in species with specific developmental strategies, such as hemimetabolous insects. While many well-studied insects such as the honey bee, drosophila, and butterflies, exhibit an holometabolous development ("holo" meaning "complete" in reference to their drastic metamorphosis from the juvenile to the adult stage), hemimetabolous insects have juvenile stages that look similar to the adult stage (the hemi prefix meaning "half", referring to the more tissue-specific changes during development), as seen in crickets, cockroaches, and stick insects. Learning more about what happens during development in terms of the identity of genes that are sex-biased (are they the same genes at different developmental stages? What are their function? Do they exhibit specific sequence evolution rates? Is one sex over-represented in the sex-biased genes?) and their quantity over developmental time (gradual or abrupt increase in number, if any?) would allow us to better understand the evolution of sexual dimorphism at the gene expression level and how it relates to dimorphism at the organismic level.
Djordjevic et al (2021) studied the transcriptome during development in an hemimetabolous stick insect, to improve our knowledge of this type of development, where the organismic phenotype is already mostly present in the early life stages. To do this, they quantified whole-genome gene expression levels in whole insects, using RNA-seq at three different developmental stages. One of the interesting results presented by Djordjevic and colleagues is that the increase in the number of genes that were sex-biased in expression is gradual over the three stages of development studied and it is mostly the same genes that stay sex-biased over time, reflecting the gradual change in phenotypes between hatchlings, juveniles and adults. Furthermore, male-biased genes had faster sequence divergence rates than unbiased genes and that female-biased genes.
This new information of sex-bias in gene expression in an hemimetabolous insect allowed the authors to do a comparison of sex-biased genes with what has been found in a well-studied holometabolous insect, Drosophila. The gene expression patterns showed that four times more genes were sex-biased in expression in that species than in stick insects. Furthermore, the increase in the number of sex-biased genes during development was quite abrupt and clearly distinct in the adult stage, a pattern that was not seen in stick insects. As pointed out by the authors, this pattern of a "burst" of sex-biased genes at maturity is more common than the gradual increase seen in stick insects.
With this study, we now know more about the evolution of sex-biased gene expression in an hemimetabolous insect and how it relates to their phenotypic dimorphism. Clearly, the next step will be to sample more hemimetabolous species at different life stages, to see how this pattern is widespread or not in this mode of development in insects.
Djordjevic J, Dumas Z, Robinson-Rechavi M, Schwander T, Parker DJ (2021) Dynamics of sex-biased gene expression during development in the stick insect Timema californicum. bioRxiv, 2021.01.23.427895, ver. 6 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.01.23.427895
Nadia Aubin-Horth (2021) Sex-biased gene expression in an hemimetabolous insect: pattern during development, extent, functions involved, rate of sequence evolution, and comparison with an holometabolous insect. Peer Community in Evolutionary Biology, 100135. https://doi.org/10.24072/pci.evolbiol.100135
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
The authors declare that they have received no specific funding for this study
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2021.01.23.427895
Version of the preprint: 4
Author's Reply, 11 Oct 2021
Decision by Nadia Aubin-Horth, posted 29 Jun 2021
Thank you for submitting your preprint " Dynamics of sex-biased gene expression over development in the stick insect Timema californicum" to PCI Evol Biol. Your manuscript has been read by two reviewers, whose comments are enclosed. As you will see, the reviews are largely positive, and, based on these reviews as well as my own evaluation, I would recommend your manuscript to be eventually included in PCI Evol Biol. However, before reaching a final decision, I would ask you to revise your manuscript according to the recommendations by the reviewers. Please address the main issues underscored by the reviewers, including the following:
- Addressing the issue of comparing only one species of each developmental type and interpreting it in the context of evolution in a more explicit manner.
- Discussing more explicitly how a whole animal transcriptome approach may affect the data
- Respond to the reviewer’s comment about the rationale for not using a fold change cut-off in addition to a statistical significance threshold in the case of studying development while using whole-animal transcriptomes.
- Presenting the statistics supporting some of the claims and modifying some figures to insure that your message is clearly understood by the readers.
I also encourage you to revise your manuscript according to the more minor suggestions from the reviewers, which will certainly improve it.