Grandmother hypothesis

The grandmother hypothesis is a theory to explain the existence of menopause, rare in mammal species, in human life history and how a long post-fertile period (up to one third of a woman's lifespan)^[1] could confer an evolutionary advantage.

Holding longevity constant, a female that undergoes menopause should have a lower total fertility rate, making menopause intriguing from an evolutionary perspective.

Background

In female placentals, the number of ovarian oocytes is fixed during embryonic development; possibly as an adaptation to reduce the accumulation of mutations.^[2] At birth there are, typically, one million ova; when menopause begins, only 400 eggs would have actually matured.^[3] The intriguing question is why somatic cells decline at a slower rate and why humans invest more in somatic longevity than other primates.^[4]

More important than the question of why longevity has been extended, however, is why selection has not adjusted female life-history to match. The most frequently cited adaptive causes for the menopause are variations on the ‘mother’, or ‘grandmother’ hypothesis. These theories advocate that the high costs attributed to female reproduction could prevail over the benefits of continuous propagation. It is true that with advancing age and decreasing fertility, there is also a corresponding increase of miscarriages and birth defects, such as Down’s syndrome.^[5] Age is less significant in the increased foetal abnormalities than is the number of the ova left in the ovarian follicular reserves.^[6]

A possible explanation is the rate of oocyte depletion. With ova numbers fixed before birth^[7] , it is logical to think extension of fertility would require increased oocyte stocks, which may be a limiting factor, or a slower rate of follicular attrition. In humans, the rate of follicular atresia increases at older ages (around 38-40), for reasons that are not known. In other mammal chimpanzees and Japanese macaques there is no similar acceleration in the rate of follicular atresia, so this pattern remains an evolutionary puzzle.^{[8] [9]} A model of "biphasic" or abruptly accelerating follicle loss has been contested on statistical grounds^{[10] [11] [12]} Oocyte stocks and the rate of follicular attrition vary between mammal species ^[13] , but it remains puzzling why humans start out with so many oocytes and show a late-life acceleration in the rate of oocyte atresia. See also non-adaptive hypotheses for menopause

The grandmother effect

G.C. Williams was the first to posit^[14] that menopause might be an adaptation. Williams suggested that at some point during evolution, it became advantageous for females to stop "dividing [their] declining faculties between the care of extant offspring and the production of new ones" (p. 408). Since a female's dependent offspring would die as soon as she did, he argued, older mothers should stop producing new babies and focus on the offspring they already had. In so doing, they would avoid the risk of dying during childbirth and thereby eliminate a potential threat to the continued survival of current offspring.

In addition, postmenopausal women can contribute knowledge and skills to other group members to enhance group fitness.^[15] If the other group member receiving investment were kin, then this would increase the fitness of a post-menopausal woman.^{[16] [17]}

This kin selection emerged with climate-driven changes, around 1.8 –1.7 million years ago, in female foraging and food sharing practices. These adjustments increased juvenile dependency, forcing mothers to opt for a low-ranked, common food source (tubers) that required adult skill to harvest and process. Such demands constrained female birth intervals and consequently their fertility; thus providing an opportunity for selection to favour the grandmother hypothesis.^[18]

Evidence for

If the grandmother effect were true, post-menopausal women should continue to work after the cessation of fertility and use the proceeds to preferentially provision their kin. Studies of Hadza women have provided such evidence,^[19] but they have not shown that this behaviour actually increased the grandmother’s fitness by producing more grandchildren. Furthermore, some commentators felt that the role of Hadza men, who contribute 96% of the mean daily intake of protein, was ignored;^[20] though the authors have addressed this criticism in numerous publications. ^{[19] [21] [22] [23]} Other studies also demonstrated reservations about behavioural similarities between the Hadza and our ancestors.^[24]

One quantitative model, however, showed limited increases in fitness.^[25] One of the reasons given for low benefits is the inflexibility of the age at which menopause occurs. It could be that fertility behaviour is adjusted depending on long-term expected fitness.^[26] Such choice, however, is not available to an already infertile female – she cannot ‘choose’ to redirect investment.

The grandmother effect and longevity

It is said that the grandmother hypothesis “is a central determinant of our longevity.”^[27] Analyses of historical data have found that the length of a female’s post-reproductive lifespan was reflected in the reproductive success of her offspring and the survival of her grandchildren.^{[28] [29]}

Maternal vs paternal grandmothers

Similar studies found comparative effects but only in the maternal grandmother – paternal grandmothers had a detrimental effect on infant mortality,^[30][31] as well as differing assistance strategies for maternal and paternal grandmothers. Maternal grandmothers concentrate on offspring survival, whereas paternal grandmothers increase birth rates.^[32] These finding are actually consistent with the grandmother hypothesis because of paternity uncertainty. Equally, a grandmother could be both a maternal and paternal grandmother and thus in division of resources, a daughter’s offspring should be favored. Other studies have focused on the genetic relationship between grandmothers and grandchildren. Such studies have found that the effects of maternal / paternal grandmothers on grandsons / granddaughters may vary based on degree of genetic relatedness, with paternal grandmothers having positive effects on granddaughters but detrimental effects on grandsons,^[33] and paternity uncertainty may be less important than chromosome inheritance.^[34]

Evidence against

Such historical studies are, however, unable to quantify grandmotherly assistance; they are merely correlations between infant mortality and the existence of a grandparent. One study that calculated grandmaternal assistance to both offspring and grandchildren did not find appreciable effects to warrant termination of fertility as early as 50.^[25]

Another problem concerning the grandmother hypothesis is that it requires a history of female philopatry. Though some studies suggest that hunter-gatherer societies are patriarchal,^[35] mounting evidence shows that residence is fluid among hunter-gatherers ^{[36] [37]} and that married women in at least one patrilineal society visit their kin during times when kin-based support can be especially beneficial to a woman's reproductive success.^[38]

Others dispute the hypothesis, arguing that the grandmother herself will use up resources that could be used for new young.

In addition, all variations on the mother, or grandmother effect, fail to explain longevity with continued spermatogenesis in males. It also fails to explain the detrimental effects of losing ovarian follicular activity, such as osteoporosis, osteoarthritis, Alzheimer's disease and coronary artery disease.^[39]

Alternatively, the debilitating symptoms that usually accompany menopause in Western cultures could be seen as a natural cull of non-reproductive members of a species. Hot flashes, loss of short term memory, decreased ability to concentrate and difficulty in the learning of new tasks would, in the wild, leave the sufferer at greater risk from predators and topographical dangers such as falls from a height. This natural cull would leave more food, usually in relatively short supply, for the reproductive members of a species whose youth could mean that they are less experienced at finding it. However, cross-cultural studies of menopause have found that menopausal symptoms are quite variable among different populations, and that some populations of females do not recognize, and may not even experience, these "symptoms".^[40] This high level of variability in menopausal symptoms across populations brings into question the plausibility of menopause as a sort of "culling agent" to eliminate non-reproductive females from competition with younger, fertile members of the species.

See also

• The How and the Why – a play based on the controversy surrounding the Grandmother hypothesis and the evolution of human reproduction

References