Menopause has not evolved as a general trait in mammals: A response to ‘Do mammals have menopause?’

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Reproductive senescence is widespread across mammals, but only a small number of species have physiological reproductive cessation and an extended post-reproductive lifespan. A recent commentary in Cell by Winkler & Goncalves (2023) suggests that menopause is actually a widespread trait of mammals, which would change our understanding of senescence and have implications for the study of menopause in humans. Here, we identify three main issues with the methodology of this commentary: the use of captive populations, the use of maximal lifespan, and misinterpretations of the data sources. We show that this methodology does not support the conclusions at the species-level, and conclude that, in line with the predictions of classic life-history theory, menopause is indeed a rare trait.

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  1. suggest that any physiological measures are betterindicators

    Suggestion: “...any physiological measure is a better indicator…” or “..suggest that physiological measures are better indicators…”

  2. c)

    Figure 1c: It would be interesting to see last birth vs. oopause in four ways: 1. last wild birth vs. captive oopause (as you show here), 2. last wild birth vs. wild oopause, 3. last captive birth vs. wild oopause, and 4. last captive birth vs. captive oopause. This could really emphasize the importance of data curation and how it could lead to misleading conclusions (Winkler & Goncalves).

  3. risk misinforming those unfamiliar with the evolutionary literature. We feel it is imperative thatthe state of the field in evolutionary biology is clarified, particularly for those working onmenopause from medical and cellular perspectives.

    This was incredibly engaging to read!!!!! I really appreciate you writing this rebuttal and keeping the translational/clinical audience in mind. And a HUGE thank you for making this available to anyone via bioRxiv so that the audience can think critically about the differing opinions and methodologies.

  4. end of reproduction calculated from demographic information

    I assume this refers to PrR where the numerator is determined based on the average time that an individual in the population no longer creates offspring, is that correct? If so, there would be the possibility that individuals may still have the ability to reproduce but aren’t creating offspring which would make physiological measures helpful to determine reproductive cessation despite social factors for all species, not just for the Asian elephant no?

  5. Whilst studying populations incaptivity may be of interest for investigating the physiological basis of reproductive cessationand the maximum theoretical lifespan of species, the evolutionary origin of traits can only bediscussed in the context of conditions where they have evolved by natural selection.

    I deeply appreciate this caveat and this is a powerful reminder to the non-evolutionary biology audience. I can see how it may be advantageous to study reproductive capabilities and cessation in unnatural contexts to better understand the mechanisms of reproductive aging but I agree with you in the sense that it wouldn’t be accurate to discuss the evolution of a trait in conditions that differ from how the trait evolved/emerged (captivity in this case).

    This question is a bit philosophical but I’m curious if you think the conditions of humans most closely resemble captive conditions? In certain societies, modern medicine and infrastructure removes the risk of death from predation, starvation, disease, etc. (longer lifespan) and the U.S. is experiencing a rise in infertility (arguably shorter reproductive lifespan). Would it be accurate to do comparative studies surrounding reproductive health at all given that human reproductive measurements may be more similar to those from captive populations?

  6. Summary: “Menopause has not evolved as a general trait in mammals: A response to ‘Do mammals have menopause?’” Chapman et al. offer a rebuttal to Winkler et al.’s assertion that menopause (or “oopause”) is widespread across mammals. (See below for a summary of “Do mammals have menopause?” by Winkler and Goncalves.) The authors address three main issues with the assertion and methodology:

    • dismissal of wild data and the use of captive populations — captive populations have artificially long lifespans and artificially early reproductive termination, thus, excluding wild data can lead to misleading conclusions
    • the use of maximal lifespan — the PrR measure is a better method to compare populations with different lifespans, as maximal lifespan can over- or under-estimate population lifespan
    • misinterpretations of the data sources — Chapman et. al found numerous instances where Winkler & Goncalves contradict the analysis in the sources they cite or used an oopause age that was younger than that of the cited source

    Chapman et al. also note that the term “oopause” is unnecessary, as the definition of menopause, from a cross-species comparative perspective, is “the irreversible loss of the physiological capacity to produce offspring due to intrinsic biological factors” which essentially encompasses the idea of “oopause.”

    Overall, the authors stress that to accurately conduct cross-species comparisons centered around menopause, we must focus on the species that experience prolonged life after reproduction in the wild using validated demographic measures such as post-reproductive representation (PrR).

    Summary: “Do mammals have menopause?” by Winkler & Goncalves In an attempt to devise a definition of reproductive senescence that is useful for comparative studies, Winkler and Goncalves argue in “Do mammals have menopause?” that “oopause, the permanent age-associated cessation of ovulation across all mammalian species,” is common among mammals. The authors assert that because a majority of mammalian species in captivity in zoos live significantly longer than their wild counterparts, demographic measurements in free-ranging/wild individuals are not reliable indicators of oopause. Thus, their analysis excluded demographic studies that only observed wild populations (primarily order Cetacea from “Analyses of ovarian activity reveal repeated evolution of post-reproductive lifespans in toothed whales'' by Ellis et al.) and concluded that most mammals experience oopause. Despite this conclusion, the authors do acknowledge that physiological data (e.g. follicles or corpora count, frequency/length of menstrual/estrous cycles, changing hormone concentration, microscopic analysis of cell types in vaginal smears, etc.) is lacking and needed for most mammalian orders to better understand oopause and potentially delay reproductive aging.