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Mating behavior is an unlikely driver of women's reproductive aging.
September 1, 2013|
© JOHN SLATER/CULTURA/CORBISThe late statistician George E.P. Box, who famously wrote that “all models are wrong, but some are useful,” also wrote that “science is a means whereby learning is achieved, not by mere theoretical speculation on the one hand, nor by the undirected accumulation of practical facts on the other, but rather by a motivated iteration between theory and practice.”
Richard Morton, Jon Stone, and Rama Singh at McMaster University in Ontario, in their recent article in PLOS Computational Biology (9:e1003092, 2013), present a mathematical model exploring whether menopause could evolve as a result of male preferences for younger mates. Their model imagines that early in human evolutionary history, women remained fertile well into their 70s and even 80s, but men had a strong fixed preference for mating with younger women. The older women thus remained mateless, therefore gaining little fitness by retaining fertility, and as a result, accumulated mutations that reduced their ability to reproduce later in life. The central assumptions of this model, unfortunately, appear to be false. In Box’s framework, Morton and his colleagues have excelled at theoretical speculation, but seem to have skimped on the reference to practical facts.
Some facts: our female great-ape relatives experience loss of fertility near the end of their life spans, at just about the same chronological age human women do, implying that it is highly unlikely that our female ancestors reproduced at ages later than women do now. Sustained selection for later reproduction, were it to occur, would have had to overcome serious physiological and phylogenetic constraints. And far from being a starting point for human evolution, the preference of men for younger women is a peculiarly human trait, not something we got from our distant ancestors. We know this because most primate males preferentially mate with older, more experienced females. Given this, it seems evident that male preference for younger mates evolved as a result of the long human postfertile life span, and not the other way around. That is, if our ancient foremothers lost fertility as they aged, as women do now, males would be expected to evolve a preference for the younger mates who would be more likely to produce viable offspring.
Just as the evolutionary assumptions of the model ignore what we know about evolution, its social assumptions ignore what we can easily see in human societies throughout history: older women still have lovers. Older women may be underrepresented in advertising and discriminated against in the workplace, but very few of them are unable to gain access to sperm, and very many are in long-term sexual relationships with committed partners.
One cause of confusion, we believe, is revealed by Morton and colleagues’ choice of language. They don’t distinguish between reproductive senescence (the decline in fertility with age), menopause (the physiological cessation of cycling that occurs after fertility has already reached zero), and the postfertile stage in women’s evolved life history. Each of these three traits is “menopause” in their terminology, obscuring the fact that all three are related but very different traits with different evolutionary histories. The puzzle that Morton and colleagues attempt to address is not menopause, but rather the postfertile life span—in other words, why women’s reproductive senescence occurs so long before they die of old age.
This is actually the right evolutionary question, as it is the aspect that is unique to humans. In contrast to other primate species, and despite popular belief to the contrary, women live well beyond their reproductive years across environments and have done so even in the harshest of conditions. The presence of age-related decline in fertility and subsequent cessation of reproductive cycling, on the other hand, is not unique and doesn’t require a human-specific explanation. Despite focusing on the right question, however, Morton and colleagues offer a novel but unlikely theory for the female human’s postfertile life span.
Just as the evolutionary assumptions of the model ignore what we know about evolution, its social assumptions ignore what we can easily see in human societies throughout history: older women still have lovers.
We believe that neither menopause nor postfertile life span originated as a result of mating preferences, especially given other convincing explanations. The grandmother hypothesis and several variants suggest that because human children need extended care, reproductive efforts of older women are more profitably directed toward caring for existing young than producing new babies. However, mammalian reproductive biology also clearly plays a role. Almost all female mammals, if provided a safe environment, show earlier aging of the reproductive system than of the rest of the body. Humans didn’t need to evolve menopause or a postfertile life span from scratch, they just needed to delay nonreproductive aging a bit. Together, the numerous evolutionary forces and biological mechanisms already identified by biologists and anthropologists elegantly explain why all mammals undergo reproductive senescence and a menopause-like cessation of cycling, but only humans and a couple of whale species have postfertile life spans of any ecological importance.
Many of the false assumptions underlying the Morton team’s model are iterations of long-standing misconceptions. Evolutionary theory often ignores some very real biological constraints, assuming that age-specific fertility and mortality schedules can freely evolve; in reality, they are governed largely by trajectories, with what happens at one age affecting other ages. Similarly, treating menopause and a postfertile life stage as the same thing is common in the popular and scientific literature, and the unfortunate myth that older women don’t have sexual partners is also not new.
To be clear, we don’t suspect Morton and colleagues of being anti–older women or ignorant of biology; instead, we believe they have fallen for the great allure and inherent danger of computational biology.
Computational biology allows us to think in ways that would have been impractical not so many years ago. In tandem with molecular biology, it is transforming the way biology is done and the role of biologists in the modern world. While experimentalists must deal with the logistics and expense involved in gathering data, computational biologists can do their work with nothing but fast processors, big displays, elegant models, and beautiful figures. But the ability to bypass the cumbersome steps involved in going out to measure things cuts out some of the reality checks that come from contact with the organisms being described.
So the model presented by Morton et al. is wrong, as Box posited all models are, but is it nonetheless useful? Perhaps. Their false assumptions do not mean that mate preference has had zero effect on the length of human postfertile life span, and indeed, nothing prevents all these theories from operating in concert. A reworked model with more realistic assumptions could quickly show whether the idea is tenable. That possibility of going back and doing it again is another beauty of computational biology.
Daniel Levitis is an assistant professor in the Max-Planck Odense Center on the Biodemography of Aging at the University of Southern Denmark and a member of the board of the Evolutionary Demography Society. Alan Cohen is an assistant professor in the Department of Family Medicine at the University of Sherbrooke in Quebec, Canada. A version of their critique first appeared on the PLOS Computational Biology site as a comment on the Morton et al. paper.
September 26, 2013
Although none of us were there to see just exactly how long women kept their fertility, it seems to me to be a good assumption that it was retained through most of her lifetime in those ancient days of evolution toward humanity. I believe that in those early years of evolution where survival was paramount against a harsh and unforgiving environment, the maintenance of a long fertility was paramount.
In our current situation, however, with survival having an almost artificial meaning with the advent of the horror of modern warfare, and barring that moral sickness, human survival takes on a different significance. We are a highly complex social species, and survival by reproduction has been replaced somewhat by survival by living in a complex society. The role of mother is more one of wisdom in that arena and her wisdom aids in the survival of human beings in society. Even in senescence, when her mind is gone, her her mere presence serves as a reminder of that wisdom, an encouragement to living a moral life concerned for the other in society, just as she did for her children. Thus, those extra years post reproductivity serve to aid in survival in a social environment.
I guess it is proper to say that perhaps this is why it is taking longer and longer for the young to "fly the nest", because we are living in a more and more complex society, or perceived, at least, as more complex. Our education grows increasingly longer and we spend most of our ives accumulating information and turning it into knowledge, and we have less and less time available for turning knowledge into wisdom. Perhaps this is why we have a developed such a preocupation with living longer and longer. By the time we have been able to develop wisdom, the kids are gone, often far far away, and the transmission of wisdom becomes difficult. Thus, Mom's role, post fertility, becomes increasingly more and more important.
We do evolve to fit the needs we have created in addition to our environmental needs. Perhaps we need to develope a little wisdom and create a simpler society in which we can live in peace so that we can evolve into a wiser society in the short lives we have inherited from environmental evolution. Less tension, yes. Evolve slower, most certainly yes. Be happier, I truly think so.
September 26, 2013
As detailed above, Morton and Singh's model does not fit all the facts. This is not uncommon with models or even theories. There are so many facts now that it is very easy to overllok one or two. This ommission can be reduced by discussion with older and wiser minds, or just by asking people closer to the field. The trouble is, they are not always available. It is surprising how little many molecular biologists know about genetics or physiology or ecology, and vice versa.
October 24, 2013
As suggested by Levitis and Cohen, I do feel that the Morton et al. model could be revised and re-evaluated, and should not be entirely disregarded. The notion that sexual selection could have contributed to the origin of menopause does have widespread applicability, if properly argued. Perhaps it would be more effective to tie back in more classic evolutionary theory regarding sexual selection, in order to ensure model assumptions are more realistic.
October 24, 2013
I agree with the fact that it seems unreasonable to make the assumption that males have a sexual preference for females, yet at the same time when dealing with evolutionary patterns I feel like it may also be a reasonable one. In older generations, living conditions were poor and older individuals would die due to lack of treatment for disease or from these irrational life styles. As a result, men would chose younger women to ensure that they would reproduce viable offspring. Due to the type of life style, older women would die while giving birth, or they wouldn't be able to survive long enough to take care of the child till they could go off on their own. Thus resulting in younger mates.
In the study, both young and old females were given mutations to stimulate infertility. As they got older, the genes would activate creating phenotypes that lower the reproductivity of the individual. Since younger individuals didn't express these phenotypes they were able to reproduce more and were selected for. Thus the mutation would spread until it reached the stable level causing menopause. In older generations, with males only choosing younger mates to ensure offspring, the assumption seems to fit the data.
I do agree that everyones opinion is valid, and I agree that there may be different explanations. But I don't think that Morton, stone,a dn singhs assumptions were completely invalid. Maybe with a few alterations the model may give a very accurate representation of how menopause came to be.
October 24, 2013
Even though the goal here may have been to individually dissect aspects of Morton et al.’s assumptions rather than to form a unified argument against them, perhaps it should have been. Some points seem to contradict each other, leaving me confused. For example, it’s noted that our primate relatives actually prefer older female mates and so male preference for younger mates is uniquely human, but it is then noted that older women actually have no problem mating. So, is there an imbalance in younger versus older females mating or not?
Further, just because the chimps experience menopause at age 50 doesn’t imply that the original humans also experienced it at age 50. Since chimps only live a max of ~60 years, then early humans probably experienced menopause close to the end of their lives as well.
If you follow the logic of Morton et al.’s paper and accept the initial assumptions for their model which are not as far-fetched as claimed here, the findings are convincing. I do agree that the study would be more convincing if skewed mating assumption were verified, though I could not find actual data regarding ages of male/female pairs in human history over a significant amount of time. Still, since the whole point of the study was to find a model that could explain the appearance of menopause independent from existing hypotheses out there, it does the job. At the very least, it brings forth the understated effect of mate choice in relation to the evolutionary origin of menopause.