In my earlier post I discussed the “Grandmother Hypothesis” as an explanation for human reproductive senescence, or menopause. A problem arises in understanding why women forgo one-third (and sometimes as much as one-half) of their reproductive lives, a condition unique in the natural world. Could this just be a neutral mutation, an artifact of longer human lives, or might it be a product of natural selection? If the latter, what selection pressure(s) could result in this unique human adaptation? The grandmother hypothesis posits that women who stopped ovulating in their golden years were freed from the costs of reproduction and were better able to invest in their existing children and grandchildren (thus helping to ensure that more individuals with their menopause inducing genes thrived and had children themselves).
University of Toronto Biochemist Larry Moran at Sandwalk takes issue with my support for this hypothesis, as discussed by Razib at Gene Expressions. Moran refers to the hypothesis as an “adaptationist just so story” and insists that the study cited offers no evidence that menopause has adaptive value:
Given that there were many families that received no help from grandmothers, whether they had the menopause allele or not, and given that there were many families who received help even if the grandmothers did not have the menopause allele, the question is “what is the adaptive value of menopause under those circumstances.”
Moran asks an excellent question and it touches directly on the problem of testing hypotheses of human evolution. How do you test for the preferential selection of allele frequencies if a trait is already fixed in a population? Unlike in mice or fruit flies it’s impossible, for both ethical and practical reasons, to engineer human knockouts that don’t develop the menopausal phenotype in order to conduct a controlled experiment. However, the grandmother hypothesis was given strong support by a 2004 study in Nature by Mirkka Lahdenperä, Virpi Lummaa, Samuli Helle, Marc Tremblay and Andrew F. Russell. As they state the problem:
Previous research on humans provides some evidence that post-reproductive mothers can benefit the reproductive output of their offspring. However, it has not yet been possible to test whether prolonged post-reproductive longevity in humans is associated with greater grandchild production, and hence greater fitness, because data covering the complete reproductive histories of several generations of individuals are scarce.
Using multigenerational data sets from the eighteenth and nineteenth centuries (prior to modern medicine) they conclude that the fitness benefits are substantial:
Grandchild survival to adulthood is enhanced by 12% when grandmothers are under 60 at their birth, but by only 3% when grandmothers are over this age. Grandmothers have no effect on the survival probability of their grandchildren between birth and two years of age (GLMM: 21 = 0.08, P = 0.78), but have significant positive effects when offspring are between two and five (GLMM: 21 = 7.09, P = 0.008), and between five and 15 (GLMM: 21 = 4.18, P = 0.041).
(For those who don’t understand what these numbers signify, the important number is P. Any P-value at or below 0.05 means the probability meets the strict threshold required of modern science.)
So, in other words, post-menopausal women had a huge impact on the survival of their grandkids. This left Moran impressed, but perplexed:
12% is, indeed, a very large effect but what does it have to do with evolution?
What Lahdenperä et al. have done is demonstrate that post-menopausal women actually do show significant fitness benefits. As I’m sure Moran knows, fitness benefits are the precondition for evolution. But the story doesn’t end there.
Following up on Lahdenperä’s work, Daryl P. Shanley and colleagues writing in the Proceedings of the Royal Academy: Biological Sciences utilized a remarkably complete and instructive data set from the Keneba and Manduar regions of Gambia. They were able to locate birth and death records that date from 1950 to 1975 and include 5,500 people. Furthermore, since the records predate the existence of a medical clinic they offer a window into the world of hunter-gatherers without the benefits of modern health care. What the data reveal once again is that children were significantly more likely to survive to adulthood if they had a grandmother’s assistance.
Their results show children were more than 10 times less likely to survive if their mother died before they reached two years old. However, children between one and two were twice as likely to survive if their maternal grandmother was still alive. This was the only other relative that mattered (sorry dads – I’m a new father myself so I feel your pain).
Shanley et al. then took their conclusions to the next level by modeling the fitness benefits that would occur if women experienced menopause later or earlier than age 50 (as women do now worldwide). According to their data the Gambian population had a growth rate of r=0.013 (derived from Table 1 above). The authors then calculated how r would vary if they imposed menopause at different ages between 45 and 65.
Estimated relationship between the intrinsic rate of natural increase, r, and age at menopause for four cases: (i) no effect of mother or grandmother on child survival; (ii) death of mother assumed to result in 13.4-fold increase in mortality of children aged 0-1 years and 11.7-fold increase in mortality of children aged 1-2 years and death of grandmother assumed to result in 2.0-fold increase in mortality of grandchildren aged 1-2 years; (iii) as (ii) where the 11.7-fold increase in mortality of children aged 1-2 years following the death of the mother is assumed to decrease linearly between ages 2 and 15 years; (iv) as in (ii) where the the 2.0-fold increase in mortality of grandchildren aged 1-2 years following the death of the grandmother is assumed to decrease linearly between ages 2 and 15 years.
Their conclusions are that the women experience the greatest fitness benefits by undergoing menopause right around age 50. Too early and they forego further reproductive opportunities. Too late and they actually have reduced fitness by continuing to have children and not assisting their daughters and grandchildren. Menopause, it seems, was a fitness enhancing solution. These two studies have gotten around the problem of setting up a controlled test using human subjects and developed an empirical means to test the fitness benefits of reproductive senescence.
Moran’s concern that the grandmother hypothesis is a “just so story” is an important one. Too often, researchers construct an argument that sounds good but that can’t be tested empirically. While there’s certainly room to critique these studies based on the reliability of the data used or the model Shanley et al. develop, the fact is that the grandmother hypothesis is on solid empirical ground. I would encourage Moran to take a close look at the numbers himself to see if they meet his standards.
However, Moran has a further question about the evolution of menopause:
Since you are a supporter of this adaptationist explanation can you describe for me the kind of society where you think this allele became fixed in the population? Was it a hunter-gather society of small bands or a large agricultural society of small towns? Or something else?
Unfortunately there’s no evidence to offer Moran an informed answer, but there may be a way to find out. A 2004 study in The Lancet found that premature menopause is associated with mutations in mitochondrial DNA. Since mtDNA is passed from mother to daughter it is not recombined the way nuclear DNA is during sexual reproduction. This makes it an excellent genetic clock (I’m sure everyone has heard of “Mitochondrial Eve”). It’s possible that a similar global analysis of mtDNA could be performed in order to date this potential marker of menopause. Once an approximate date is established paleoanthropological data can be used to estimate group size and foraging patterns at the time menopause may have been undergoing selection. It’s a place to start.
In conclusion, the grandmother hypothesis is far more than a mere “just so story.” Hypotheses that avail themselves to testing and the potential for disproof are the markers of good science. It’s often as easy to throw out the accusation of a just so story as it is to make one. Fortunately, by engaging with the evidence used to support a given hypothesis, scientific progress can be made.
Shanley, D., Sear, R., Mace, R., & Kirkwood, T. (2007). Testing evolutionary theories of menopause Proceedings of the Royal Society B: Biological Sciences, 274 (1628), 2943-2949 DOI: 10.1098/rspb.2007.1028