Colloquium paper: how grandmother effects plus individual variation in frailty shape fertility and mortality: guidance from human-chimpanzee comparisons

Abstract

In the first paper to present formal theory explaining that senescence is a consequence of natural selection, W. D. Hamilton concluded that human postmenopausal longevity results from the contributions of ancestral grandmothers to the reproduction of their relatives. A grandmother hypothesis, subsequently elaborated with additional lines of evidence, helps explain both exceptional longevity and additional features of life history that distinguish humans from the other great apes. However, some of the variation observed in aging rates seems inconsistent with the tradeoffs between current and future reproduction identified by theory. In humans and chimpanzees, our nearest living relatives, individuals who bear offspring at faster rates do not cease bearing sooner. They continue to be fertile longer instead. Furthermore, within both species, groups with lower overall mortality rates have faster rates of increase in death risk with advancing age. These apparent contradictions to the expected life history tradeoffs likely result from heterogeneity in frailty among individuals. Whereas robust and frail alike must allocate investments between current and future reproduction, the more robust can afford more of both. This heterogeneity, combined with evolutionary tradeoffs and the key role of ancestral grandmothers they identify, helps explain aspects of human aging that increasingly concern us all.

Fig. 1.

Female age structures modeled from life tables. Each bar shows the percentage of the population in the 5-year age class indicated in the vertical axis. Yellow bars, juvenile years; green bars, childbearing years; purple bars, post-fertile years. Humans are on the right, represented by Hadza hunter-gatherers with Blurton Jones’s data (6). In this population, life expectancy at birth is 33 years. With growth rate 1.3%/year, 32% of the women (those over 15) are past the age of 45. Growing populations are younger because more are born than die. If this population was stationary, the percentage of adult women past the age of 45 would be 39% (8). The left side of the figure represents the synthetic wild chimpanzee population constructed by Hill and colleagues (63) using data from five wild study sites. Average age at first birth is 13 in wild chimpanzees so the 10- to 14-year age class is included in the childbearing years. Fertility ends by ~45 in both species. Less than 3% of the adult chimpanzees (counted as those over 10 years) are past the age of 45. The chimpanzee model assumes a stationary population.

Fig. 2.

The slope of the log of the hazard of death from age 30–80 by the log of the intercept at age 30 (IMR) taken from the values of A and G in Gompertz models calculated from life tables for a convenience sample of eleven human (yellow circles) and two synthetic chimpanzee populations (black circles). See table 1 of ref. for the values plotted here. The sample includes five hunter-gatherer populations, the US and Japan to represent lower mortality levels falling in the upper left corner (the lowest IMRs and the steepest slopes), and two other cases to represent high mortality populations depending on agriculture. Here, two pygmy populations from Migliano (65) are added, the Aeta and the Batak. The chimpanzees are the synthetic wild population from Hill et al. (54) and the synthetic captive population from Dyke et al. (64). All life tables are female except for the !Kung and Agta, for which sexes were not distinguished in the original sources. Parameters were calculated on 5-year age classes, conditional on survival to the beginning of the age class preceding age 30. For the 11 human populations (yellow circles), the correlation between these estimates is −0.955.

Fig. 3.

Two model subpopulations, one frail (open green circles) and the other robust (filled blue squares), exposed to two conditions of age-independent mortality. Initial mortality rates are low (similar to the US and Japan) for the lower set of lines and high (similar to Hadza hunter-gatherers) for the upper set of lines. Both subpopulations face Gompertz age-specific risk. Initial mortality rates for the two subpopulations differ by 0.35/year in both conditions with slopes of 0.03/year and 0.085/year, respectively. The simulations plot the age-specific mortality rate for the population pooled from these two subpopulations (grey diamonds). The trendlines in red (described by the equations and correlation coefficients) measure how well the population mortality curves fit Gompertz models. The slope of the trendline is the demographic aging rate. For the population in the high mortality condition, that slope is about half as steep as in the low mortality condition. Relative size of the subpopulations at the initial adult age makes a difference. Here it is assumed to be the same at both high and low background mortalities because background risk is assumed to affect the frail proportion in two opposing ways. When age-independent mortality is high, so is the risk of early life tradeoffs that leave survivors more frail (see the discussion of early origins in the text). However, higher mortality also strengthens mortality selection across juvenile years, leaving a smaller fraction of the frail juveniles alive at maturity. On the other hand, when background mortality is low, fewer have faced early survival tradeoffs that increase frailty, making the frailer subpopulation smaller initially. Yet, weaker mortality selection across the juvenile years leaves more of the frail subpopulation surviving to adulthood.

Fig. 4.

Age-specific fertility rates (ASFR) for humans and chimpanzees. Humans (red circles) are represented by the average of three hunter-gatherer populations: !Kung Bushmen of Botswana (4), Ache of Paraguay (4), and Hadza of Tanzania (6). Estimates for chimpanzees in the wild (blue squares) come from the conservative fertility schedule synthesized from six study sites by Emery Thompson et al. (22). The bumps reflect small sample size (627 risk years in the initial chimpanzee adult age class declining to 8 risk years in the 45- to 49-year interval (ref. , supplementary table 2). The percentages along the horizontal axis indicate the proportion of those reaching adulthood that survive to the age class. The top row of percentages are estimates for chimpanzees from the number of risk years in each age class (ref. , supplementary table 2). They are just slightly lower than the model in Fig. 1 from the life table (54). The bottom row is human estimates from the female life table for Hadza hunter-gatherers (6).

Fig. 5.

Number of births (green circles) and age at death (diamonds) in cohorts of UPDB women by their birth year across the 19th century (ref. 150, redrawn from ref. 96). Only women who survived past the age of 50 are included.