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Why do women lose their ability to bear children long before they grow old? Daughters-in-law may be to blame, discovers Alison Motluk

IT FLIES in the face of natural selection, yet in humans it seems fixed and universal: at around age 50, not far past the midpoint of life, normal healthy women lose their capacity to bear children. Following a decade of gentle winding down, the whole reproductive system screeches to a halt. It is as though, after a few years of wearing bifocals, all women suddenly went blind.

Menopause is a mystery. It leaves women with 20, 30, perhaps even 50 years of life – squandered time in evolutionary terms, because no further genes can be passed on. Yet the selection pressure for menopause must have been strong: there are no known pockets of women around the world who do not go through it. All the evidence suggests menopause has been around a long time, and that the age at which it hits has changed little. Increased longevity seems not to have budged our closing hours. Nor, apparently, has lifestyle; it hits hunter-gatherers at pretty much the same age as hip New Yorkers.

In an attempt to explain this phenomenon, anthropologists suggest that menopause lets women see their last child through to maturity, or that it enables them to provide for their grandchildren. Both ideas make evolutionary sense, since they allow mothers to pass on more of their genes to subsequent generations. But when the numbers are crunched, they just dont seem enough to explain why women would forgo turning out a few more babies of their own. The sums dont add up – the benefits arent sufficient to stop breeding, says Michael Cant from the University of Exeter at Penryn, UK. Theres a missing piece of the puzzle. As a zoologist, whose main work has been in banded mongooses and paper wasps, he had an idea about what that missing piece might be. Put bluntly, he suspects that daughters-in-law could be to blame.

Change, not decay

Humans are odd. Elsewhere in the animal kingdom, reproductive senescence tends to set in alongside other bodily deterioration: Females just churn out fewer young in the same way that, for instance, the heart pumps blood a little less efficiently, the ears hear a little less sharply and the skin becomes less elastic. Growing old is like that for humans too – with the singular exception of female fertility. Whereas average life expectancy for women in the developed world is about 80 and among hunter-gatherers about 65 or 70, the mean last birth, in populations that do not use contraceptives, is just 38. By age 51, half of women have ceased ovulating, menstruating and producing the high levels of oestrogen associated with fertility; by age 60, more than 99 per cent have made the transition.

Two main hypotheses have been put forward to explain human menopause. The mother hypothesis suggests that at a certain point, a mother will do better in the genetic stakes by avoiding the risks associated with childbirth and additional child-rearing and instead concentrate on raising the kids she already has. This idea recognises the fact that human mothering is particularly demanding. We are able to produce babies at shorter intervals than other primates, and ours are born extremely needy: it takes them more than a decade to become independent. There is no doubt that motherless children are less likely to survive and that childbirth is risky. However, a woman who dies in childbirth compromises the survival chances of at most two or three dependent children, whereas early reproductive senescence guarantees that every woman forgoes the opportunity to produce at least two or three more babies. Even if menopause made sense in the light of the mother hypothesis, it need not happen so early: most women, both now and historically, not only live well past the maturity of their last born, they also see their grandchildren mature.

Is menopause the ghost of competition between successive generations?

Which leads to the second theory, the grandmother hypothesis . This suggests that a healthy grandmother, who is not burdened with dependent offspring, helps ensure the survival of her genes by contributing to the care of her extended genetic brood, her grandchildren. There is evidence that grandmothers really do make a difference to the survival chances of their grandchildren (Nature, vol 428, p 178) , but is this enough to compensate for the children they did not bear themselves? A woman passes on 50 per cent of her genes to her own child and only 25 per cent to a grandchild, so she would have to make a very substantial contribution indeed. Kim Hill at Arizona State University in Mesa and Magdalena Hurtado at the University of New Mexico in Albuquerque, calculated the genetic benefits of grandmothering as compared to continued reproduction for older women in the Ache tribe of Paraguay and concluded that they simply werent big enough to explain why women cease to reproduce so young (Human Nature, vol 2, p 315).

Even when the mother and grandmother benefits are added together, they are too small to justify such an early end of fertility, says Thomas Kirkwood, a gerontologist at the University of Newcastle, UK (BioEssays, vol 23, p 282). Thats where Cants idea comes in (Proceedings of the National Academy of Sciences, vol 105, p 5332).

Intrigued by this whole menopause debate, Cant and his colleague Rufus Johnstone at the University of Cambridge, UK, noted a striking oversight. Researchers were looking at the benefits and costs to the postmenopausal females, says Cant, but no one seemed to consider the costs to other women of the group. His work as a zoologist had made him mindful of the fact that in societies where females cooperate over child-rearing – where food is shared and non-mothers step in to assist in the care of young – you have to consider the costs and benefits to all the females, because all of them will be competing for the same scarce resources. Reproductive competition has been overlooked in human studies, says Cant. It might give us insight into why women stop breeding when they do.

The first clue that they could be onto something came when Cant and Johnstone mapped out the overlap in reproductive years between human generations. It was such a striking pattern, says Cant. Although human mothers may survive for the majority of their daughters lifespan, they will continue to reproduce for at most a small fraction of their daughters reproductive span. This sets humans apart from most primates (see diagram, right) but reproductive separation is found in other mammals. In mearcats and naked mole rats, for instance, mothers and daughters do not reproduce at the same time either. But here its the younger females that forgo reproducing in deference to the older ones. What is most unusual about humans, says Cant, is that its the other way round.

He and Johnstone were convinced that this lack of reproductive overlap in humans evolved to minimise reproductive conflict between the generations. So they began to study patterns of human dispersal, which determines the relationships between competing females within a social unit.

In most mammals, young males leave and join another group while young females stay with their mother. As they reach sexual maturity, females are highly related to the group, so have an incentive, in evolutionary terms, to help their mothers and aunts raise their siblings and cousins, rather than producing babies of their own. But humans seem to have evolved a different pattern.

According to Cant and Johnstone, several lines of evidence, including mitochondrial DNA and Y chromosome analysis, as well as studies of modern hunter-gatherers, suggest that in our ancestors it was overwhelmingly the females who moved. So older women were competing for resources with young women who had come from elsewhere. Cant points out that when a young woman leaves her family group and joins another, she is unrelated to anyone in her new home and is thus insensitive to the costs she might inflict on the older females by having children. As females age, however, they are increasingly related to the group, and have less to lose and more to gain by helping with the care and provisioning of the younger generation.

Did menopause evolve because older women found it less costly in evolutionary terms to forgo reproduction than their daughters-in-law did? A system in which females become more related to their group as they age has this predicted outcome, says Cant. He calls menopause the ghost of reproductive competitions past”.

Menopause on–off switch

Wendy Saltzman, at the University of California, Riverside, is intrigued by the idea. In marmosets, the species she studies, subordinate females do not ovulate or copulate, in what she believes is a response to the threat of infanticide from more dominant individuals. However, there is a key difference between this and menopause: the marmosets condition is self-imposed and females can switch things back on when it is in their interest to do so, whereas menopause leaves women with no choice. Why this inflexible reproductive shut­off instead of a plastic system? she wonders.

Saltzman also questions how competitive human females actually are. I would need to be convinced that there really was intensive competition, she says. This doubt is shared by Sarah Blaffer Hrdy, an anthropologist at the University of California at Davis. Not only is there no evidence of reproductive suppression, she says, There is reason to think women in small groups would benefit from the presence of a co-breeding female.

There are also questions surrounding the issue of female dispersal. For one thing, this happens in two other primate species, yet they lack menopause. Our closest relatives, chimps and bonobos, both show the same migration pattern as ancestral humans, but instead of experiencing menopause, female fertility seems merely to decline slowly with age. However, Cant points out that unlike humans, they are not cooperative breeders so the same competition dynamics do not apply.

A second objection is harder to dismiss. Kristen Hawkes, at the University of Utah in Salt Lake City, disputes whether human migration patterns are really female-biased as Cant describes them. He misrepresents the human data he cites. She says that studies of modern hunter-gatherers show that many young females only leave their natal home after they have had a couple of babies, a detail that doesnt fit well with the model proposed by Cant and Johnstone. Hrdy also takes issue with this. Hunter-gatherers are famously flexible in their residence patterns, she notes.

If all that werent bad enough, there is also the anomaly of killer whales – possibly the only other animal with clear-cut menopause followed by many more years of life. Killer whale society does not have female dispersal: both females and males stay with the natal group, and simply breed with members of other pods as they cross paths. Nevertheless, says Cant, in this case too, females become more related to their group as they age, giving older females greater incentives to forgo reproduction than younger females.

Cant and Johnstone are staunch in the face of their critics. Female dispersal leads to asymmetry which leads to reproductive competition. But maybe thats not the only, or even the main, driving force, says Cant, and if the female dispersal idea fails,the reproductive competition theory could still be right. ~


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