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An extraordinary feature of human reproduction is that women stop ovulating and menstruating when about 50 years old, a loss of fertility called menopause (from Greek roots for “month” and “stop”). This is way earlier than the maximum lifespan of about 125 years, so infertility is decades-long and may exceed the fertile phase. Given the unpleasant side-effects that can accompany menopause, it may aptly be called the second curse of womankind. Perhaps the only good thing about it is that it automatically banishes the first curse, menstruation. (See my August 6, 2014 post: The First Curse on Women: Menstruation.)
Functionless side-effect or evolved mechanism?
Is menopause a mere byproduct of other aspects of the life cycle or an adaptive response to natural selection? In their 1999 book Ever Since Adam and Eve, reproductive biologists Malcolm Potts and Roger Short pithily stated: “The immediate cause of the menopause is that the ovary runs out of its supply of eggs.” Karl Hansen and colleagues clearly confirmed this in a 2008 paper. Fertility actually starts to decrease long before menopause, peaking at 20-30 years before trending downward, declining particularly steeply after 35. The main underlying mechanism is depletion of starter follicles in the ovaries, from up to a million at birth. Menopause occurs at around age 50 when the number falls below a critical threshold of about 1,000. Ovary size in women also reflects changes in the follicle reserve. Thomas Kelsey and colleagues compiled almost 60,000 ovarian volumes for healthy women up to age 82. Their 2013 report showed that average volume rose steeply to peak at age 20 and thereafter progressively declined to about age 50. Less rapid decline continued into old age.
Relatively abrupt onset and fairly consistent timing indicate that menopause is not just a byproduct with fertility gradually declining due to ageing. In 1974 reproductive biologist Alan Treloar reported on ages of menarche (menstrual onset) and menopause for 324 women who had continuously recorded menstrual histories from student days to natural menopause. One striking finding was that age at menopause (averaging 50 years) was not correlated with age at menarche (averaging 14 years). This is not what we would expect if menopause simply resulted from follicle depletion. Subsequent studies have repeatedly shown that women with earlier menarche do not run out of eggs sooner, so other factors must be involved. It is also noteworthy that in western society over the past century, menstrual onset has become progressively earlier, whereas menopause has been starting later.
Age at menarche is not correlated with age at menopause, indicating separate mechanisms. (Adapted from Treloar 1974.)
Age at menarche is not correlated with age at menopause, indicating separate mechanisms. (Adapted from Treloar 1974.)
The Grandmother Hypothesis
A front-runner among proposed evolutionary explanations of menopause is the “grandmother hypothesis”, particularly championed by anthropologist Kristen Hawkes and colleagues. The basic premise is that ageing women make a greater contribution to the gene pool if they stop breeding themselves and instead promote survival of their grandchildren.
In a 2004 paper, Finnish biologist Mirkka Lahdenperä and colleagues reported strong indications that a prolonged post-reproductive lifespan in women really is associated with enhanced survival of grandchildren. They analysed multi-generational data sets for historical farming communities living during the 18th and 19th Centuries in Finland and Canada. Mean lifespan of post-menopausal women in both countries was around 70 years. For both populations, the length of a woman’s post-reproductive lifespan was significantly correlated with the number of grandchildren born. Further analysis of the Finnish data revealed that, in the presence of a living post-menopausal mother, both sons and daughters started breeding earlier, had more offspring and raised more to adulthood.
In 2007, longevity researcher Daryl Shanley and colleagues provided further strong support for the grandmother hypothesis and noted an additional factor: Post-menopausal individuals may offset maternal mortality risks (which rise with age) by protecting highly dependent younger children if a mother dies. Analysis of their remarkably complete data set of records gathered in 1950-1974 for over 5,500 individuals in four rural villages in The Gambia revealed that the increasing mortality risk of giving birth at older ages is not sufficient on its own to select for menopause. However, the combined effect of maternal and grandmaternal influences is.
Is menopause really unique to humans?
Human menopause is unquestionably extraordinary. But is it truly unique? Some authors use the term menopause for nonhuman primates, implying that any difference from humans is just a matter of degree. Among primates, females of other species, such as macaques and chimpanzees, can cease breeding for a few years as their lives draw to a close. Yet survival for decades after a relatively abrupt advent of menopause is unique to humans.
Although menopause of the extreme kind seen in women is virtually unique among mammals, as Craig Packer and colleagues showed in a seminal 1998 paper, some whales do show something similar. Biologists Katherine McAuliffe and Hal Whitehead briefly reported in 2005 that short-finned pilot whales and killer whales, and possibly sperm whales, have a lengthy post-reproductive phase comparable to menopause in humans. Reproduction ceases at about 40 years of age, but females “routinely live on for several more decades”. Whales reported to have menopause notably live in groups organized around matrilines.
Emma Foster and colleagues specifically examined menopause in killer whales in a 2012 paper based on extensive multigenerational census records for two populations. They showed that enhanced survival of male, but not female, offspring, was correlated with presence of post-reproductive mothers in the social group.
Is evolution necessarily involved?
The key question is this: Is depletion of the egg supply in a woman’s ovaries by age 50 an evolutionary adaptation? This brings to mind an astute, if irreverent, comment from a lecturer during a course on reproduction that I attended in my student days: “When God created woman, He did not expect her to live longer than thirty years.” This pungently makes the point that the age of fertility cessation in women may have been adapted to typical lifespans less than 50 years and that the long post-reproductive period seen today reflects a relatively recent increase in average lifespan.
In a series of studies reviewed in 2011, Rachel Caspari and colleagues explicitly proposed that grandparents were rare in ancient hominid populations, ranging from australopithecines to Neandertals, and that survival beyond an age of about 40 first became common among modern humans some 30,000 years ago. In order to circumvent widely acknowledged problems of estimating age of individuals, they used a simple ratio between old and young individuals based on dental criteria. Their results indicated that their “OY ratio”, and by inference adult survivorship, shifted dramatically upward very late in human evolution, in the Upper Paleolithic. It is difficult to imagine that a few tens of thousands of years would be sufficient for the evolution of menopause in association with grandmothering. Predictably, in a 2005 exchange, Hawkes and O’Connell challenged these results by questioning the validity of the OY ratio, while Caspari and Lee equally predictably roundly defended it. (OY Vey?) The issue remains undecided, but the bottom line is that we currently have no clear indication of when survival beyond an age of 50 became common during hominid evolution.
We must also remember that, while menopause in women and whales may correlate with enhanced survival of grandchildren, this was not necessarily a driving factor in its evolution. Correlation is not causation. (See my July 12, 2013 post: The Stork-and-Baby Trap.)
References
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Caspari, R. (2011) The evolution of grandparents. Sci. Am. 305(2):44-49.
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