Putting the Men in Menopause

Can mating behavior explain the evolution of menopause in humans?

By | September 1, 2013

© CLAIRE ARTMAN/CORBISMenopause puzzles evolutionary biologists. After all, avoiding mortality and ensuring reproduction are the two most fundamental tenets of Darwinian natural selection. Theoretically, species should evolve so that individuals live only as long as they reproduce. So why did humans evolve a long adulthood with females becoming nonreproductive about halfway through?

Menopause, quantified as the proportion of expected time in adulthood during which an individual is nonreproductive, is remarkable in humans relative to most other species in the animal kingdom. Among the many hypotheses that have been proposed to explain the origin of menopause, two have garnered substantial attention. According to the most popular explanation, known as the grandmother hypothesis, older females increase their genetic contribution to future generations by assisting in rearing their grandchildren rather than continuing to bear and rear children of their own. This scenario requires that older females become grandmothers twice for each forgone additional opportunity to become mothers themselves, as grandmothers typically share half as many genes with their grandchildren as with their own children. The other leading explanation, called the life-span artifact hypothesis, implies that menopause is the by-product of an increase in life expectancy. This scenario assumes that over the history of our species, only males have extended fertility coupled with increased longevity, possibly to father more children. Research into these hypotheses has yielded equivocal results.

Dissatisfied with either explanation on its own, my colleagues Richard Morton and Rama Singh and I recently published a novel hypothesis, formulated on the basis of a thought experiment involving the effects of a change in mating behavior (PLOS Comp Bio, 9:e1003092, 2013). Imagine a population in which individuals lived long lives, throughout which they were able to reproduce. In this scenario, any gender-specific mutations that diminished fertility late in life would be selected against. If a mating behavior change were introduced, however, such that females reproduced only at a young age, natural selection would become relaxed in older females. Consequently, effects from the female-specific mutations that diminished fertility late in life would become effectively neutral, and such mutations would accumulate over time. Eventually, female fertility would decline with age; in other words, menopause would evolve.

Because older males would continue to reproduce late in life, natural selection would continue to operate negatively on corresponding male-specific mutations that diminished fertility late in life, as well as on any non-gender-specific mutations that diminished survival late in life; neither, therefore, would become effectively neutral nor accumulate in males.

Theoretically, species should evolve so that individuals live only as long as they reproduce. So why did humans evolve a long adulthood with females becoming nonreproductive about halfway through?

To formalize this new hypothesis, we developed a computational model and assessed, through computer simulation, the idea that menopause originated as a consequence of a change in mating behavior. Data that mimic real-world survivorship and fertility were generated by evolving virtual populations. From a behavioral perspective, the mating-behavior change that was introduced in the computer simulations could be viewed as a male preference for young females or as young females outcompeting older females for access to males. Ultimately, the model showed that, when only young females mate, menopause arises. Intriguingly, the reverse scenario also holds true: if only young males mate, then male menopause will arise—an observation that could be  tested by investigating whether menopausal male fruit flies could be evolved in a laboratory setting.

This “change in mating behavior” explanation is a nonadaptive hypothesis for the origin of menopause: it requires neither inclusive fitness benefits through which older, nonreproducing women assist younger women in their reproductive efforts (i.e., the grandmother hypothesis), nor an assumption that fertility always diminished at a typical, prescribed age in older women and remained so despite increased survival through extended reproduction by males (i.e., the life-span artifact hypothesis), possibly accompanied by increased male fitness. A change in mating behavior allows alleles that diminish fertility to accumulate in an effectively neutral manner. Similar genetic mechanisms are theorized as the ultimate causes for other conditions, including senescence.

Of course, the hypotheses for why menopause evolved are not mutually exclusive, but the neutral, change-in-mating-behavior hypothesis, itself, provides a sufficient, mechanistic explanation for how menopause could arise. Why older women historically stopped reproducing and the precise temporal relationship between the origin of grandmothers and extended life spans in human populations are puzzles that remain unsolved, but that will now invite much speculation.

From a practical perspective, real-world counterparts for deleterious mutations that arise during the computer simulation, if such mutations do exist, might have effects on traits other than fertility. So, if corresponding candidate mutant alleles responsible for the onset of menopause were suspected to reside in human genomes, then the novel hypothesis may be received as a challenge to researchers to identify and study those genes, ultimately promoting research in human health.

Jon Stone (aka Doc Roc) is an associate professor at McMaster University in Hamilton, Ontario, where he holds a SHARCNET Chair in Computational Biology and is associate director of the Origins Institute.

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Avatar of: Mrs. Dempsey

Mrs. Dempsey

Posts: 1

September 26, 2013

I'm obviously missing something because the "uniqueness" of menopause to humans doesn't seem so unique to me.  Don't many species become less fertile as they age?  For example, I know breeders of horses and dogs that have animals that will no longer either get pregnant or stay pregnant due to advanced age, and that is considered normal.  I have chickens that are too old to lay, and that is normal.  How is menopause in humans so different?

Avatar of: Neurona

Neurona

Posts: 35

September 26, 2013

Isn't it true that a female mammal is born with all the ova she'll ever have? Couldn't evolution of a longer lifespan mean that this finite supply of gametes accumulates the effects of ongoing environmental insults (e.g. oxidative damage to mitochondria) that might negatively impact the viability of the aging ova?   

Avatar of: Hugh-F-61

Hugh-F-61

Posts: 41

September 26, 2013

A problem with this is why selection would not stop a maladaptive cessation of mating by older females. There would be no selective advantage for males because any successful pregnancy would increase the fitness of both parents. Unless men have changed a lot, I don’t think older women would have been unable to find any mates. This model simply says that something that isn’t happening isn’t conserved by selection, and presupposes its conclusion, a circular argument. There  may have been very little selection for prolonged female fertility. Each child would compete with slightly older siblings. Humans have a very long childhood and females might actually rear more and fitter offspring by exclusively supporting children born just pre menopause into adolescence than to produce more but die before they could become independent. Also, later offspring are heavily discounted in an expanding population. A female who starts reproducing at 13 will have grandchildren when she is about 26-30 years and great grandchildren when she is 50. If the population doubles each generation she will have 4 children, 16 grandchildren, and her own last child will be competing with 64 great grandchildren, so the combined transfer of her genes in the 64 great grandchildren will be 16 times the contribution by one more late child of her own. When populations grow, the first offspring has a very large value compared to the last one. The menopause might just have evolved because there was so little selection to go on reproducing once there were adult grandchildren to do it for you. Especially if elderly females could still do a little to help rear all those offspring.

Avatar of: JT Avery

JT Avery

Posts: 1

September 28, 2013

IMHO, I would argue the theory is inaccurately based on "modern" life expectancies and behaviors, but please explain what I might be missing:

1) If the estimates of life expectancy of our species under the selection of prehistoric pressures is the most accurate in the evolutionary sense -- that is, those who survive childhood reach the age of 50-55 -- menopause at 50-55 seems about right, and "..become nonrreproductive halfway through.", does not seem accurate at all.

2) There is mention of younger females out-competing older ones, but no mention as to how these older males are managing to out-compete the younger males for those younger females.

3) Why isn't the difficulty of older females bringing a pregnancy to full term considered a significant selective pressure -- that is, to truncate reproduction and select for individual or group survival instead?

Avatar of: winymure

winymure

Posts: 1

September 28, 2013

Well I have something to add to this theory. I do believe a change in mating behavior "could" have occured somewhere during our evolution as a species. But I don't think younger females out competed the older females, and I don't think males solely preferred younger females. It may be a combination of several factors. 1. As you age you are more like to die or have complications in giving birth, our bodies break down etc, so older females may have passed the duty of child bearing to the younger healthier females. Which makes sense because an older female may die or have complications as she aged. 2. Other factors such as younger female competing and males preferring younger females could have occured. But i think older females simply opted out combined with rating a mates health resulted in the evolutionary outcome of menopause. Thoughts......

Avatar of: KendraYoung

KendraYoung

Posts: 1

October 22, 2013

The headline “Putting the men in menopause” is very suiting for this article, as it foreshadows the scientific content of the article as well as the study being discussed. The motivation and purpose of the study is clearly outlined, as well as alternative hypotheses such as the grandmother hypothesis, and the life-span artifact hypothesis. I agree with the opinion presented in this  online story. It indicates to the reader that evolutionary conclusions from this study are based on mating research of multiple generations throughout history, and not based on recent mating selections in today’s society. Stone indicates that the study suggests menopause arose due to a change in mating behavior historically, leading to genetic drift, non-gender specific mutations, and the outcome of females undergoing menopause. One way to determine genetic drift is “to recognize genotype and allele frequencies…could have easily been different from what they turned out to be.” By the author suggesting evolution could have worked in an alternative way, such that females mating preference for younger males could lead to males undergoing menopause, indicates to the reader that the act of evolution being exhibited through menopause is not adaptive through natural selection but a random result of genetic drift. 

 

Alternative hypothesis’ however should not be ruled out; such as the idea that grandmothers share about half the genes with their grandchildren as they would their own offspring, requires them to become grandmothers twice to compensate for the inability to reproduce one offspring. This makes evolutionary sense when regarding the fact that as one ages, a mother may be incapable of raising her offspring as they require for success.  The discussion of this, as well as the life-span artifact hypothesis; the idea that menopause is the resultant of extended longevity in females, leaves the reader with an unbiased opinion to compare and contrast theories using the scientific method. To deem one theory "right" over the other would be unscientific and evolutionarily incorrect as all are plausible. When analyzing the life span artifact hypothesis for example- because of increased ability for humans to live an extended life in the most recent years, could menopause have always occured and we were just unable to detect it? ...as most died before the age of 50. An unanswered question. 

Regardless of the theory, throughout the article, the “blame” of menopause on men is truly shown as not goal-oriented, but a mere outcome of small accumulations leading to population changes resulting in evolution throughout time, and correctly reflecting the scientific study done. 

October 24, 2013

The original study and this story written by Dr. Jon Stone are interesting as they provide a different explanation to evolution of menopause. Dr. Stone provides support for the change in mating behavior hypothesis; however, Dr. Stone is too quick to discredit the grandmother hypothesis.  Grandmother hypothesis states the menopause evolved because it was evolutionarily advantageous to nurture grandchildren. This increases the inclusive fitness of the grandmother. Not only that but older women are at a higher risk of stillbirth or a miscarriage. Therefore, menopause may have evolved to prevent older women from reproduces as it is evolutionarily disadvantageous.

Although this story emphasizes one theory to help explain why menopause originated, there are many other hypotheses, such as grandmother hypothesis, artifact hypothesis and mother hypothesis, which could also be the reasons to why menopause evolved.  

Avatar of: N.K

N.K

Posts: 1

October 24, 2013

After reading numerous articles addressing the same study, I must admit that this author most accurately reflects the key findings of the research paper his team at McMaster University produced. Under the premise that males have shifted in preference toward young females, where female-specific mutations deleterious to fertility exist in the population, it is certainly reasonable to posit that this preferential selection may have driven the onset of menopause in females over time. 

Evidently, this study offers a refreshing hypothesis and nonadaptive approach to understanding the origin of menopause in older women. Personally, I think it seems trivial for natural selection to select for the evolution of female infertility at later life, just for the sake of women helping their grandchildren survive for a longer period. With this in mind, however, I also believe that the other theories are not mutually exclusive, as stated above, for surely no one influence in itself could determine the course of the evolution of a physiological concept so complex as menopause in women. I believe the other theories, namely the grandmother theory and the life-span artifact hypothesis, are certainly just as plausible. Perhaps men evolved a preference to younger women as a response, since they'd be more likely to produce viable offspring with these 'more fertile' women. (etc).

Nonetheless for any of those who are critical of the stochastic computer simulations used to compile the data, the article presents the idea for further exploration of the hypothesis via testing whether male fruit flies can evolve the male equivalent of menopause in a lab setting. If the theory holds true, we may just have one less missing piece of the puzzle.

Avatar of: blindboy

blindboy

Posts: 1

December 17, 2013

My hypothesis, in support of the research, is that sex selection was influenced by the higher death rate of males. Males even now have a higher death rate at every age. Although I am not aware of any data to support it, it seems a reasonable guess that this differential death rate was greater in earlier human populations in which the males were hunters.

In the resulting gender imbalance it would have been adaptive for males to choose younger, healthier partners leaving older women with few reproductive opportunities.

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