Sensitive windows for phenotypic plasticity within and across generations; where empirical results do not meet the theory but open a world of possibilities
Sensitive windows for within- and trans-generational plasticity of anti-predator defences
Recommendation: posted 02 August 2023, validated 04 August 2023
It is easy to define phenotypic plasticity as a mechanism by which traits change in response to a modification of the environment. Many complex mechanisms are nevertheless involved with plastic responses, their strength, and stability (e.g., reliability of cues, type of exposure, genetic expression, epigenetics). It is rather intuitive to think that environmental cues perceived at different stages of development will logically drive different phenotypic responses (Fawcett and Frankenhuis 2015). However, it has proven challenging to try and explain, or model how and why different effects are caused by similar cues experienced at different developmental or life stages (Walasek et al. 2022). The impact of these ‘sensitive windows’ on the stability of plastic responses within or across generations remains unclear. In their paper entitled “Sensitive windows for within- and trans-generational plasticity of anti-predator defences”, Tariel-Adam (2023) address this question.
In this paper, Tariel et al. acknowledge the current state of the art, i.e., that some traits influenced by the environment at early life stages become fixed later in life (Snell-Rood et al. 2015) and that sensitive windows are therefore more likely to be observed during early stages of development. Constructive exchanges with the reviewers illustrated that Tariel et al. presented a clear picture of the knowledge on sensitive windows from a conceptual and a mechanistic perspective, thereby providing their study with a strong and elegant rationale. Tariel et al. outlined that little is known about the significance of this scenario when it comes to transgenerational plasticity. Theory predicts that exposure late in the life of parents should be more likely to drive transgenerational plasticity because the cue perceived by parents is more likely to be reliable if time between parental exposure and offspring expression is short (McNamara et al. 2016). I would argue that although sensible, this scenario is likely oversimplifying the complexity of evolutionary, ecological, and inheritance mechanisms at play (Danchin et al. 2018). Tariel-Adam et al. (2023) point out in their paper how the absence of experimental results limits our understanding of the evolutionary and adaptive significance of transgenerational plasticity and decided to address this broad question.
Tariel-Adam et al. (2023) used the context of predator-prey interactions, which is a powerful framework to evaluate the temporality of predator cues and prey responses within and across generations (Sentis et al. 2018). They conducted a very elegant experiment whereby two generations of freshwater snails Physa acuta were exposed to crayfish predator cues at different developmental windows. They triggered the within-generation phenotypic plastic response of inducible defences (e.g., shell thickness) and identified sensitive windows as to evaluate their role in within-generation phenotypic plasticity versus transgenerational plasticity. They used different linear models, which lead to constructive exchanges with reviewers, and between reviewers, well trained on these approaches, in particular on effect sizes, that improved the paper by pushing the discussion all the way towards a consensus.
Tariel-Adam et al. (2023) results showed that the phenotypic plastic response of different traits was associated with different sensitive windows. Although early-life development was confirmed to be a sensitive window, it was far from being the only developmental stage driving within-generation plastic responses of defence traits. This finding contributes to change our views on plasticity because where theoretical models predict early- and late-life sensitive windows, empirical results gathered here present a more continuous opportunity for sensitive windows over the lifetime of freshwater snails. This is likely because multifactorial mechanisms drive the reliability and adaptive significance of predator cues. To me, this paper most original contribution lies probably in the empirical investigation of sensitive windows underlying transgenerational plasticity. Their finding implies mechanistic ties between sensitive windows driving within-generation and transgenerational plasticity for some traits, but they also shed light on the possible independence of these processes. Although one may be disheartened by these findings illustrating the ability of nature to combine complex mechanisms in order to produce somewhat unpredictable scenarios, one can only find that this unlimited range of phenotypic plasticity scenarios is a wonder to investigate because much remains to be understood. As mentioned in the conclusion of the paper, the opportunity for sensitive windows to drive such a range of plastic responses may also be an opportunity for organisms to adapt to a wide range of environmental demands.
Danchin E, A Pocheville, O Rey, B Pujol, and S Blanchet (2019). Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis. Biological Reviews, 94: 259-282. https://doi.org/10.1111/brv.12453
Fawcett TW, and WE Frankenhuis (2015). Adaptive Explanations for Sensitive Windows in Development. Frontiers in Zoology 12, S3. https://doi.org/10.1186/1742-9994-12-S1-S3
McNamara JM, SRX Dall, P Hammerstein, and O Leimar (2016). Detection vs. Selection: Integration of Genetic, Epigenetic and Environmental Cues in Fluctuating Environments. Ecology Letters 19, 1267–1276. https://doi.org/10.1111/ele.12663
Sentis A, R Bertram, N Dardenne, et al. (2018). Evolution without standing genetic variation: change in transgenerational plastic response under persistent predation pressure. Heredity 121, 266–281. https://doi.org/10.1038/s41437-018-0108-8
Snell-Rood EC, EM Swanson, and RL Young (2015). Life History as a Constraint on Plasticity: Developmental Timing Is Correlated with Phenotypic Variation in Birds. Heredity 115, 379–388. https://doi.org/10.1038/hdy.2015.47
Tariel-Adam J, E Luquet, and S Plénet (2023). Sensitive windows for within- and trans-generational plasticity of anti-predator defences. OSF preprints, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.31219/osf.io/mr8hu
Walasek N, WE Frankenhuis, and K Panchanathan (2022). An Evolutionary Model of Sensitive Periods When the Reliability of Cues Varies across Ontogeny. Behavioral Ecology 33, 101–114. https://doi.org/10.1093/beheco/arab113
Benoit Pujol (2023) Sensitive windows for phenotypic plasticity within and across generations; where empirical results do not meet the theory but open a world of possibilities. Peer Community in Evolutionary Biology, 100639. 10.24072/pci.evolbiol.100639
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.
This work was performed within the framework of the EUR H2O’Lyon (ANR-17-EURE-0018) of Université de Lyon (UdL), within the program ‘Investissements d’Avenir’ operated by the French National Research Agency (ANR). This work was also funded by the CNRS and by the TEATIME grant (ANR-21-CE02-0005) from the ANR
Evaluation round #2
DOI or URL of the preprint: https://doi.org/10.31219/osf.io/mr8hu
Version of the preprint: 2
Author's Reply, 31 Jul 2023
Decision by Benoit Pujol, posted 18 Jul 2023, validated 18 Jul 2023
Dear authors, as you will see in their comments, the three reviewers have been very positive about the revised version of your paper. I share their conclusion that your paper deserves to be recommended. Beforehand however, because it is important to allow for constructive exchanges between authors and reviewers, I'd appreciate if you would address their somehow conflicting comments highlighted in the review of Timthée Bonnet, whom I would tend to agree with, and consider the points 2.3 and 2.5 raised by David Murray-Stoker. If your response is clear enough for me to consider without contacting the reviewers, I will not contact them at the next round and will recommend the revised version of your preprint. I expect these very minor points to be addressed easily, and may start preparing the recommendation in advance to speed up the process.
Congratulations on a very interresting paper
Reviewed by David Murray-Stoker, 15 Jul 2023
Reviewed by Willem Frankenhuis, 08 Jun 2023
Reviewed by Timothée Bonnet, 21 Jun 2023
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.31219/osf.io/mr8hu
Version of the preprint: 1
Author's Reply, 29 May 2023
Decision by Benoit Pujol, posted 09 Feb 2023, validated 09 Feb 2023
Dear Dr. Tariel-Adam and collaborators,
Thank you for submitting your preprint to PCI Evolutionary Biology for recommendation. I have read your preprint entitled “Sensitive windows for within- and trans-generational plasticity of anti-predator defences” and I have read the comments of the three reviewers who have complementary expertise on your research topic.
The three reviewers and I agree about the quality of your research and the value of this preprint. The paper is clearly written, straight to the point, and Figures participate actively to make experimental approaches easy to understand. The reviewers and I found that your research targets a valuable question on phenotypic plasticity and its adaptive significance when considering that it may be restricted to specific developmental windows that are themselves, as you state in the abstract: “highly sensitive and responsive to environmental changes". You will see in their reviews that although the three reviewers appreciated your work, they raised some concerns that I would like you to address. I have an additional request, which is to adda a paragraph at thei end of discussion on the contribution of your findings to the theory. In the introduction, you present the state of art with strong bibliographic support and outline the hypotheses that are tested in this paper. As a result, we understand what is at stake in terms of contribution of your work. In the discussion, you discuss the proximal conclusion that can be drawn from your results but do not discuss the implication of your findings to the actual theory. Such discussion would add substantially to the scope of this work.
Looking forward to reading the next version of this promising paper.