Content of review 1, reviewed on October 03, 2023
This is a very interesting study on a subject that is receiving increasing attention in the literature, and that could be pivotal to understand ageing processes and the nature of life history trade-offs. Namely, the authors set out to test the influence of female olfactory cues on male ageing in a mammal (Mus musculus), following recent groundbreaking research in nematodes and flies on sensory perception and ageing. I found the study to be timely, coherent, well designed, well analysed and generally well written, and I think it is a very welcome contribution to the field. My main concerns, which I list below, have to do with the functional framework provided in the introduction and in the discussion (including some of the interpretation of their results), but these should be easy to address and will hopefully contribute to make of this an outstanding paper.
1- In the introduction, I find that the depiction of the state-of-the-art of our understanding of life history trade-offs, and specifically those related to ageing, is incomplete and could be misleading for some readers. The authors are correct in stating that traditional theories have focussed on limitation in resource allocation (energy trade-offs), but then as challenges to this framework flag papers (e.g. Speakman & Garrat 2013) that actually don’t dispute this framework, but rather discuss about the role that different mechanism may play; the role of oxidative stress in the case of Speakman & Garrat. I would urge the authors to either not open this can of worms or, preferably, do so but then include a more comprehensive review of the current state of the art. This would necessarily have to include discussion on the role of energy vs. function trade-offs in the evolution of ageing (see Maklakov & Chapman ProB 2019) and correctly distinguish between challenges at different levels of the theory, at both proximate and ultimate levels, without conflating them. For example, what is common ground to all theories of ageing (Haldane’s selection shadow and resulting ideas), and the different resulting theories (mutation accumulation vs. antagonistic pleiotropy) and its flavours (i.e. antagonistic pleiotropy due to energy vs. function trade-offs -or a combination of the two-).
2- Understanding the role of sensory perception in ageing is, as alluded above and in the paper, critical to our understanding of ageing. However, as is stands the paper does not clarify at what level doing this may affect our understanding of ageing: will it affect what we know about what substantiates antagonistic pleiotropy and the importance of function vs energy trade-offs? To have a better understanding of the selective pressures at play? To understand the mechanistic bases of trade-offs? I appreciate the short introduction, but I think the authors should either by-pass the nuance concerning evolutionary theories of ageing (and simply focus on how their work will help understand the mechanisms of ageing) or flesh them out in a bit more detail and explain how their work (and work in sensory perception and ageing) fits in. Either way, I would appreciate a tighter introduction.
3- Talking specifically about the role of sensory perception in ageing, I also miss a proper functional framework for why sensory cues may be expected to modulate ageing. The authors have missed a key review paper by Nancy Linford (Linford et al. Ann Rev Cell Dev Biol. 2011) and relevant recent literature to this respect (e.g. Corbel et al. Am Nat 2022).
4- In relation to the above point, across the intro and discussion the manuscript seems to ignore that many of the costs of reproduction are not expected to be linked to fertilizations, but to competition over reproduction. Perhaps the main functional hypothesis to explain why reproductive cues may accelerate ageing, and why mating may reverse some of these costs, has to do precisely with female odours acting as a cue that allows males to prepare for competition in the sexual selection arena (again, see Linford et al. 2011 & Corbel et al. 2022).
5- Finally, the authors should discuss alternative explanations for some of the observed results. Namely, their experimental protocol also manipulates social context. For example, males that don’t sense female odours or are able to mate with them are also socially isolated, what does social isolation do to stress levels and ageing in a social animal such as the common mouse? Their design also manipulates density, with similar arising questions. Finally, how would the inclusion of male competitors change their results or may alter the interpretation of their results? Males perceiving cues from several females may be experiencing physiological changes that prepare them to compete over those females (as has been proposed for Drosophila), but such changes may only detected if males compete for territories/females, which is what would be expected in nature. Given the importance of sexual selection in this species, this is something the authors should address explicitly.
L 38. Is this really so? At what level? I would perhaps say “mechanistic understanding” here or reword this to clarify.
Source
© 2023 the Reviewer.
References
Michael, G., Heather, T., Christine, N., C., B. R. 2024. Exposure to female olfactory cues hastens reproductive ageing and increases mortality when mating in male mice. Proceedings of the Royal Society B: Biological Sciences.
