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Grandmothers and the Evolution of Human Longevity: a Review of Findings and Future Directions

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Grandmothers and the Evolution of Human Longevity: a Review of Findings and Future Directions Evolutionary Anthropology 22:294–302 (2013) ARTICLE Grandmothers and the Evolution of Human Longevity: A Review of Findings and Future Directions KRISTEN HAWKES* AND JAMES E COXWORTH Women and female great apes both continue giving birth into their forties, but the biggest genetic contribution to not beyond. However humans live much longer than other apes do.1 Even in future generations. That makes selec- hunting and gathering societies, where the mortality rate is high, adult life spans tion stronger on traits expressed in average twice those of chimpanzees, which become decrepit during their fertile young adults and weaker on traits years and rarely survive them.2,3 Since women usually remain healthy through expressed at older ages. How fast the and beyond childbearing age, human communities include substantial propor- force of selection declines across tions of economically productive postmenopausal women.4–7 A grandmother adulthood depends on two things: hypothesis8–12 may explain why greater longevity evolved in our lineage while the chances of surviving to older female fertility still ends at ancestral ages. This hypothesis has implications for ages and what those survivors to the evolution of a wide array of human features. Here we review some history of older ages can do for their own the hypothesis, recent findings, and questions for ongoing research. inclusive fitness. Since natural selection spreads only traits that increase their own 13 THEORETICAL FOUNDATIONS and physiological systems. Natural reproduction, it should not favor a selection favors more investment in postreproductive period in the nor- Aging rates vary widely among liv- somatic maintenance only when it mal life span of any organism. What 14 ing things. Evolutionary explanations raises lifetime inclusive fitness. Two then, Williams asked, of meno- for varying senescence rates assume key theoretical contributions to the pause, which was then assumed to that organisms trade off investment evolutionary study of senescence spe- be a uniquely human trait? His in current reproduction against cifically mentioned humans, dwelling answer began with the important repair and maintenance of their cells on the midlife end of women’s fertil- point that the end of fertility is not ity as a crucial clue about our evolu- the end of reproduction. As long as tion. Their inferences represent two postmenopausal women contribute Kristen Hawkes’s hunter-gatherer eth- different ways of posing the evolu- to the welfare of their kin, they affect nography drew her attention to unex- tionary riddle of mismatch between the successful reproduction of their pected sex and age differences in genes. Williams hypothesized that foraging strategies. including the crucial rates of ovarian and somatic senes- productivity of grandmothers, which cence in women. menopause evolved when other prompted further comparisons of human changes in our lineage made late and chimpanzee life histories. births riskier and infants more James E. Coxworth’s central interest is Stopping Early dependent. Older mothers would be the application of evolutionary tools to 14 describe and explain male competitive George Williams elaborated on more likely to die in childbirth, leav- strategies, with particular emphasis on the consequences of the declining ing orphans unable to survive with- human evolution. This interest has led to force of natural selection across statistical and modeling contributions out them. He surmised that these and to projects investigating human life- adulthood. Even in populations of a circumstances would favor tenden- history evolution. hypothetical organism that did not cies to stop fertility early and for become increasingly frail with age, mothers to invest more in previously Key words: life history evolution; senescence; some individuals would die in acci- born offspring than in risky new cooperative child rearing; infant psychology; dents or from illness or predation, ones. male-male competition so sets of age-mates necessarily Subsequent work showed that 15 shrink with time. Adult cohorts are menopause is not uniquely human.16 largest at the beginning, the age of VC 2013 Wiley Periodicals, Inc. Menstrual cycling ends before death DOI: 10.1002/evan.21382 first reproduction. Thus, features in other primate females as well, if Published online in Wiley Online Library 7,17 (wileyonlinelibrary.com). expressed at early adult ages make they live long enough. In all ARTICLE A Review of Findings and Future Directions 295 mammals, including primates, a but, of the hunter-gatherer girls who selection must weaken as adult finite stock of oocytes develops survive to adulthood, about three- cohorts age, providing the founda- around or before birth and then is quarters live past the age of 45.29 At tion for Williams’14 arguments. Med- continuously depleted, mostly by cell any one time, a third or more of the awar also anticipated both death18; cycling stops when stocks adult females in human populations Hamilton’s 196431 explanation of the fall too low to support ovulation. Fol- are beyond the childbearing ages.7,27 importance of inclusive fitness and licle stock sizes and rates of atresia Hamilton’s 196630 suggestions about 19 vary across mammals, with some grandmother effects by saying, species still ovulating and giving Increased Longevity As a “Grandparents, though no longer fer- birth at older ages than humans do. Consequence of Grandmother tile, may yet promote (or impede) For example, elephants continue to Effects the welfare of their grandchildren, give birth into their sixties20 and 30 and so influence the mode of propa- Antarctic fin whales into their William Hamilton’s attention gation of their genes.”15 21 eighties. Yet there are clear simi- was drawn to grandmother effects Hamilton30 mathematically mod- larities in the oldest ages of parturi- when he used demographic data eled Williams’ verbal arguments tion among all living hominids and from a human population with mor- about the evolution of senescence. in rates of decline in follicle stocks tality even higher than that typical of Then, considering humans, he from birth to the late forties in hunter-gatherers to evaluate the fit 22 pointed out that the high rate of wom- humans and chimpanzees. These of his mathematical model of the en’s postfertile survival “inevitably commonalities among members of evolution of senescence. Evidence of suggests the special value of the old the hominid radiation are inconsis- woman ... during a long ancestral tent with the proposition that period.”31 Like Williams, Hamilton humans had an ancestor with older lacked information on the other great ages at last birth. It is likely that Hunter-gatherer life apes or human populations that were ancestral ovarian aging remained the expectancies are less not dependent on agriculture. Subse- same while increased longevity quent evidence from the Hadza, a evolved in our lineage.23 than half those of group of East African hunter- Williams14:407 also surmised that Western nations, but, of gatherers, highlighted a particular women’s notably long postfertile sur- value of old women: They acquire and vival was an “artifact of civilization.” the hunter-gatherer girls process foods that youngsters cannot In this, he was misled by the incorrect who survive to handle for themselves.32 inference that skeletal assemblages demonstrate the rarity of surviving adulthood, about elders in ancient human populations. three-quarters live past While debate continues,24–26 paleode- 29 A GRANDMOTHER HYPOTHESIS mographers have shown that the age the age of 45. At any Those Hadza observations, com- structure of past populations cannot one time, a third or more bined with Eric Charnov’s formal be retrieved by estimating ages of of the adult females in models of life-history evolution in specimens in skeletal assemblages. female mammals,33 prompted a Biases are imposed by comparative human grandmother hypothesis to explain collections; preservation varies with populations are beyond age at death; and standard measures the evolution of human life histories. widely misestimate adult ages. Even if childbearing ages. In Charnov’s models, adult mortality taphonomic and age estimation determines an optimal age at matu- biases could be controlled, skeletal rity. When mortality is high and assemblages are not random samples adult life spans are short, selection of the deaths that occurred in differ- favors early maturation because ent sexes at different ages.27 the substantial fraction of women those who wait are more likely to die The deep antiquity of human lon- who survived the childbearing years before reproducing. When mortality gevity is also obscured by wide- led him to point toward their role in is low, the cost of waiting goes spread assumptions that because the evolution of increased longevity. down; net advantage goes to delaying national life expectancies began to An earlier version of the idea that maturity to reach a larger adult size. exceed 50 years only in the twentieth selection could favor increased lon- Larger mothers can allocate more to 34 century,28 our postfertile life stage is gevity through grandmother effects offspring [see Hawkes for more an artifact of recent history. Life- was mentioned by Peter Medawar in discussion of the modeling assump- span averages are misleading guides a footnote to his 1951 lecture, “An tions]. Rates of growth are governed to adult survivorship because high Unsolved Problem in Biology,” pub- by trade-offs the models do not infant and juvenile mortalities have lished in 1952.15 In that paper Meda- address, but they vary among mam- strong effects on them.27 Hunter- war documented and began to solve malian orders. Primate growth rates gatherer life expectancies are less the puzzle of the evolution of senes- are notably slower than those of 35 than half those of Western nations, cence by showing why the force of most nonprimate mammals. 296 Hawkes and Coxworth ARTICLE Looking just at primates, Char- those elders subsidized their depend- dependencies point to pathways nov,33 Fig.
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