CHAPTER 6 (CORRECTED FROM THE PUBLISHED VERSION)
Human Age Structures, Paleodemography,
and the Grandmother Hypothesis
Kristen Hawkes and Nicholas Blurton Jones
Evolutionary life-history theory and demography provide strong reasons to
suppose that long human life spans are not a recent novelty. Here we focus
on one robust model of mammalian life history evolution, and a grandmother
hypothesis about our own lineage that is based upon it. This hypothesis
takes long adult life spans to be an ancient human trait. Claims that
few adults survived to old age until the last century are a serious challenge to
it. Such claims are generally based on the inference that when life
expectancy is less than forty, most adults die before they grow old. We use
demographic evidence to show that inference is wrong. Findings in paleodemography
also show that ancient skeletal assemblages do not reflect the
age structure of past populations. By contrasting human and chimpanzee
age structures, we further underline that point. The comparison with chimpanzees
also serves to highlight the likely importance of ancestral grandmothers
in human evolution.
Life History Evolution
Initial work in life-history evolution recognized that the strength of selection
on genes with age-specific expression must depend on mortality
schedules since juvenile and adult mortality rates have quite different effects
on the lifetime reproductive success of the individuals carrying those
genes (Fisher 1930; Williams 1957; Hamilton 1966; Gadgil and Bossert
1970; Charnov and Schaffer 1973). Scaling regularities, of interest in their
own right, offer especially important clues for students of mammalian lifehistory
evolution as rates of adult mortality, maturation, and fecundity scale
with adult body size (Harvey and Clutton-Brock 1985). Consequently, the
rate and timing variables correlate with each other, and mammal life histories
fall along a fast-slow continuum even when body size is statistically
controlled (Harvey, Read, and Promislow 1989).
Eric Charnov (1991, 1993) built a model that reproduces this variation
from a few basic trade-offs underlying mammalian life histories. In this most
successful theory to explain the empirical patterns (see discussion in Harvey
and Purvis 1999; Purvis et al. 2003), stationary populations are assumed
THE GRANDMOTHER HYPOTHESIS 119
and adult mortality rates determine other life-history variables. When adult
mortality rates decline (adult life spans lengthen), the risk of waiting to reproduce
goes down, so selection favors longer duration of growth to reach
larger adult size. Average adult life span thus determines the optimal age at
maturity, which in turn sets the adult size.
Charnov's simple model has the particularly important property that it
identifies the (approximately) invariant relationships among species' average
life-history traits (Charnov 1993). Values of the traits themselves change
across the fast-slow continuum--some mammals mature in months, others
take two decades. But the relationship between the age at maturity and average
adult life span does not change. The model shows that this results
from trade-offs between the costs and benefits of delaying maturity in the
face of adult mortality risk.
Charnov (1993) displayed the approximately invariant relationship between
these features in primates by plotting average age at maturity and average
adult life span across fifteen subfamilies, drawing data from Harvey
and Clutton-Brock (1985). Our subfamily fell just as predicted by the mammalian
invariant. While unnoted at the time, this showed that our late age at
maturity is the expected consequence for a primate with our long adult life
spans. Yet for humans, unlike other primates, a substantial component of
adulthood is postmenopausal (Pavelka and Fedigan 1991). In wild nonhuman
primates, very few of the adult females are past the age of terminal
fertility (Hawkes, O'Connell, and Blurton Jones 2003). Not so in humans.
Even though fertility declines at similar ages in humans and chimpanzees
(Gage 1998; Nishida et al. 2003; Hawkes 2003), we usually live much
longer. From the perspective of the life-history model, those longer life
spans are the reason for our late maturity. And, as previously expected on
other grounds (Williams 1957), the whole adult life span must be
reproductive. Moreover, the evolution of that longer (and substantially
postmenopausal) life span becomes the key to explaining other aspects of
our life histories (Hawkes et al. 1998).
A Grandmother Hypothesis
The modern Hadza (Blurton Jones et al. 1992) provide clues toward a likely
explanation for the evolution of our longevity. Hunting and gathering in the
arid tropics of the East African Rift, these modern people display a connection
between the foraging patterns of children and their mothers and
grandmothers that suggests a scenario for our ancestral past that includes a
reproductive role for senior females and a consequent shift in rates of aging
(Hawkes 2003). Young Hadza children are energetic foragers (Blurton
Jones 1993; Blurton Jones, Hawkes, and O'Connell 1989). Mothers take
120 KRISTEN HAWKES AND NICHOLAS BLURTON JONES
advantage of this, choosing to focus on foods the children can handle efficiently
when those resources are in season (Hawkes, O'Connell, and Blurton
Jones 1995). But the year-round staple in this habitat is deeply buried
tubers, which young children are not strong enough to collect effectively.
Senior Hadza women, long-experienced gatherers, spend even more time
acquiring these foods than do women of childbearing age (Hawkes, O’Connell,
and Blurton Jones 1989). With acquisition rates similar to those of
younger adults (Hawkes, O'Connell, and Blurton Jones 1989; Blurton Jones
and Marlowe 2002), their overall harvest of these resources is greater, making
a substantial contribution to the nutritional needs that youngsters cannot
fulfill for themselves. Weaned Hadza children usually depend on the
foraging effort of their mothers. But when their mothers have a newborn,
the weaned juveniles' nutritional welfare depends on the effort of their
grandmothers instead (Hawkes, O'Connell, and Blurton Jones 1997).
The economic productivity of these older women and the feeding dependence
of weaned children combined with current paleoanthropology
suggest the following evolutionary scenario (O'Connell, Hawkes, and
Blurton Jones 1999, 2002; Hawkes, O'Connell, and Blurton Jones 2003).
Australopithecines are assumed to be ancestral to genus Homo (Klein 1999;
Wood and Collard 1999). On grounds of body size, brain size, and maturation
rates, australopithecines are often characterized as "bipedal apes,"
estimated to have life histories similar to those of modern chimpanzees
(Smith and Tompkins 1995). At weaning, juveniles probably fed themselves.
But the increasing aridity and seasonality of late Pliocene east and southern
Africa would have constricted the forests and likely reduced the availability
of fruits that young juveniles could handle (deMenocal 1995). The
same ecological changes would favor plants that cope well with dry seasons
by, for example, holding nutrients in underground storage organs. Such
resources can give high return rates to those with the strength to extract and
process them. Young juveniles cannot do it. To rely on these resources and
succeed in these changing environments, mothers would have to provision
offspring who are still too small to extract and process the tubers for
themselves.
Increased food-sharing would allow mothers and the youngsters accompanying
them to remain in habitats they otherwise could not and to colonize
new, previously unexploited habitats. But the feeding dependence of
those juveniles would delay a mother's next child. Maternal provisioning
would create a novel opportunity for older females whose declining fertility
made them less likely to have a newborn of their own: feeding their justweaned
grandchildren would allow childbearing-aged daughters to have
shorter interbirth intervals without reductions in offspring survivorship.
THE GRANDMOTHER HYPOTHESIS 121
Assuming these populations initially had aging rates and adult age structures
like modem chimpanzees, the ecological change would alter the fitness
benefits for slight variation in rates of senescence. The more vigorous
elders would raise the fertility of their daughters and nieces more, resulting
in more grandchildren endowed with their qualities and lengthening adult
life spans (see Hawkes 2003 for further discussion of trade-offs and the evolution
of rates of senescence).
The longer average adult life spans would in turn adjust the trade-offs
captured in Charnov’s mammal model, favoring delayed maturity and
growth to larger maternal size. This hypothesis makes distinctive features
of human life histories a consequence of the productivity of ancestral
grandmothers (Alvarez 2000; Hawkes et al. 1998). The later maturation,
increased body size, and rapid spread into previously unoccupied habitats
by the first widely successful members of genus Homo are consistent with
this scenario (O'Connell, Hawkes, and Blurton Jones 1999, 2002; Hawkes,
O'Connell, and Blurton Jones 2003; Hawkes 2003).
This grandmother hypothesis claims central importance for the distinctive
adult age structure of human populations. The evolutionary scenario
proposes that ancestral populations with substantial fractions of elders
actually antedate our species. According to it, our life histories evolved
and have been maintained by low adult mortalities, implying that old age
structures usually characterize human populations. But do they? Serious
contrary assertions abound (Washburn 1981; Weiss 1981; Trinkaus 1995;
Olshansky, Carnes, and Grahn 1998; Kennedy 2003; Crews and Gerber
2003). High levels of mortality in the past are widely assumed to have
sharply limited numbers of surviving elders.
That assumption is fueled by confusion about the information contained
in the widely used demographic statistic, life expectancy at birth (eo). Since
life expectancy has been steadily increasing in industrialized countries
(Oeppen and Vaupel 2002) with ever increasing fractions of seniors, it is
easy to mistakenly infer that lower life expectancy in the past means few
survived to old age. However, within the range of variation of human age
structures, the fraction of elders--very sensitive to variation in fertility level--
is remarkably insensitive to variation in life expectancy at birth. We use
Ansley Coale and Paul Demeny's (1966) Regional Model Life Tables and
Stable Populations to illustrate this point.
The Coale and Demeny Model Life Tables
Coale and Demeny used the same stable population theory used in evolutionary
life-history theory to model the age distributions implied by 326 observed
human life tables. Populations converge on a stable (unchanging)
THE GRANDMOTHER HYPOTHESIS 123
1956). Coale and Demeny used their table 13 to draw attention to "the
small effect of mortality and the large effect of fertility on the mean age of
the population" (1983, 31). Panels A, B, and C show that at the same
fertility level (GRR), the age structures are similar across varying mortality
levels. Consider panel A: when fertility is held constant (each cluster of
three bars), the mean age of the population varies less than four years over
three-fold differences in life expectancy. Conversely, at the same mortality
level, mean age decreases by about ten years at each doubling of fertility
(compare all the white bars, all the hatched bars, all the black bars).
Panel B shows that the fraction of the population under fifteen years old
varies less across different mortality levels with the same fertility (each cluster
of three bars), than with differing fertility at the same mortality (compare
all the white bars, all the hatched bars, all the black bars). The fraction
of adults over forty-five is shown in panel C, similar across mortality levels
with the same fertility but decreasing with increases in fertility. Note that,
perhaps contrary to initial intuition, at a given fertility (the three bar clusters),
populations with higher mortality levels have older mean ages, fewer
children, and more women past childbearing age.
Panel D of figure 6.1 shows the population growth rate that results from
particular combinations of fertility and mortality. A GRR of 1 (very low fertility)
makes populations decline at all mortality levels, but the decline is
steeper when overall mortality is high. Conversely, a GRR of 4 (high fertility,
an average of four daughters per woman who lived to forty-five) results
in a growing population at all mortality levels with growth higher when mortality
is lower. Specific population growth rates imply particular combinations
of these variables. Where growth rates are highest, the fraction of juveniles
is highest and of adults over forty-five is lowest.
This variation in human populations occurs within limits: the fraction of
women past their childbearing years drops below 20 percent only when
fertility is (unsustainably) high. Population growth reduces the fraction of
elders because each succeeding cohort is larger than the last. Noting the
ecological unsustainability of continuing growth, Coale (1959) made this
point about age structure with special force by pointing out that the fraction
of elders would always decrease with increasing population growth even if
no one ever died.
Following Coale and Demeny's table 13, we used the West series. Drawn
from the largest amount of data and the most cosmopolitan group of countries,
this category is least tied to European regions. The North, East, and
South families show the same patterns. While the shapes differ enough to
distinguish for population planning, they are nearly identical on the dimensions
highlighted here. The proportion of living seniors found in all
models indicates a tendency for women to remain healthy past the end of
124 KRISTEN HAWKES AND NICHOLAS BLURTON JONES
fertility. This is explicitly recognized in another demographic convention, the
"dependency ratio," the number of females assumed to be too young or too
old to be productive, relative to the number in the "productive" ages. Those
under fifteen and over sixty (sometimes over sixty-five) are considered
dependent. Those between the ages of fifteen and fifty-nine (or fifteen and
sixty-four) are classified as producers. Each of the Coale and Demeny stable
age models specifies a dependency ratio. Just as the use of the birth-woman
ratio recognizes that there is limited variation in the shape of human agespecific
schedules, this dependency ratio recognizes that women continue to
be productive adults well into their grandmothering years.
The Coale and Demeny models illustrate general features of human agespecific
mortality and fertility and the effects of changing mortality and
fertility levels on age structure. But the sample of life tables they used to
construct their models included only those based on good national vital sta-
THE GRANDMOTHER HYPOTHESIS 125
tistics. So they came largely from European populations. They explicitly
recognized an "unresolvable" problem: “[T]here is no strong reason for
supposing that the age patterns of mortality exhibited in these four
families covers anything like the full range of variability in age patterns in
populations under different circumstances. . . . The question of what is the
pattern of mortality in a population of an underdeveloped area is
essentially unresolvable, because there exists no way to determine the
exact age of an illiterate person who does not know it himself" (1983, 25).
That pessimistic view assumes that mortality schedules can only be
constructed from data on large populations collected by demographers'
standard census methods, ruling out the appraisal of mortality experience
in small nonliterate populations, the setting for most of human history and
all of prehistory. "Unresolvable" with demographers' census methods, this
is the central inquiry of anthropological demographers.
126 KRISTEN HAWKES AND NICHOLAS BLURTON JONES
Anthropological Demography
Seeking to broaden the range of reference models for ethnographers and
paleodemographers, Kenneth Weiss (1973) constructed an alternative set of
stable models meant to represent the populations often studied by anthropologists.
He used data from fifty populations to build his model life
tables. Fourteen data sets came from ethnographic censuses. Thirty-six of
them were derived from archaeological assemblages.
Weiss concluded his analysis with the question "why are there no old
folks?" (1973, 78). But inspection of Weiss's own data and analysis does not
show the finding this question implies. Most of his source cases (Weiss 1973,
appendix A) and most of his model populations do contain old people. His
archaeological cases average more than one-fifth of adults past their midforties.
In the ethnographic censuses, almost one-third of the adults are past
their mid-forties. The difference between the archaeological and ethnographic
samples is statistically significant, but neither of the averages
justifies Weiss's surmise. Old folks are not absent. Weiss concluded that no
"evolutionary/adaptive reason for the post-reproductive survival of human
beings” is needed because “survival to old age is rare among ‘primitive’
peoples” (Weiss 1981, 41). But the data he assembled himself do not bear out
that claim. We will return to the difference between ethnographic and
archaeological cases below.
Ethnographic demography has been especially influential in highlighting
the "old" age structure of human populations even when overall mortality
levels are relatively high. Nancy Howell (1979) faced exactly the problem
noted by Coale and Demeny when she applied demographic tools to !Kung
hunter-gatherers in the Dobe area of western Botswana. Her subjects did not
know their ages, so she had to develop methods for estimating them. Through
interviews she ranked individuals by age and then used historically known
events to anchor points in this array with Gregorian years. To smooth the
final age estimates of adults, she chose a stable model from the Coale and
Demeny series, West 5. Checks for internal consistency, especially the age
differences between mothers and children, showed that she could not be far
off in her age assignments.
A central question of Howell's study was whether the age pattern of mortality
experience for the !Kung conformed to the Coale and Demeny models.
The models, after all, have been constructed by summarizing the experience of
well-studied populations of agricultural and industrialized societies, people who
live under different conditions than those of hunter-gatherers. . . . If
the !Kung experience fits the model life tables, we can tentatively conclude
that the general of the model life tables express general features of human
THE GRANDMOTHER HYPOTHESIS 127
biological processes that are sensitive to environmental fluctuations in level but
not in age patterns of mortality (Howell 1979, 79-80).
Several estimation procedures and a series of simulations led her to conclude
that, indeed, the observed characteristics of this population did not
differ from the age patterns of the models. Elsewhere she explicitly characterized
the "uniformitarian assumption" that her analyses supported this way:
"the human animal has not basically changed in its direct biological response
to the environment in processes of ovulation, spermatogenesis, length
of pregnancy, degree of helplessness of the young and rates of maturation
and senility over time" (Howell 1976, 25).
The population of hunter-gatherers she analyzed did not suffer agespecific
mortality rates that leave no elders. The West 5 model she chose as
best representing the !Kung population has life expectancy at birth of thirty
years. Yet with this high level of mortality, a third of the women (those over
fifteen) are over the age of forty-five. This age structure is displayed in figure
6.2, panel A. Howell also constructed another schedule, based on observed
!Kung deaths between 1964 and 1973 (both sexes combined). That
mortality schedule gives a life expectancy at birth of fifty, and an age structure
with 46 percent of the adults past the age of forty-five.
Other anthropological demographers worried that the use of Coale and
Demeny's models to estimate ages might obscure differences between the
mortality schedules in small populations and those in the (European) regional
models. Timothy Gage argued that "the uniformitarian view is overly
simplistic and clearly incorrect at some level of specificity"(1998, 198-99).
He noted that in the European cases used by Coale and Demeny, high mortality
"is associated with high-density urban areas in the early 1800s. . . .
[M]ortality in low-density populations may not follow this pattern" (1998,
205). As noted above, life tables built from archaeological data have different
age structures. The age structures are younger, containing significantly
fewer elders. If the Coale and Demeny mortality shapes are restricted to
high-density populations, as Gage suggests, the small fraction of living elders
estimated from skeletal series might accurately represent human mortality
experience in other socioecological contexts. Howell's !Kung demography
stands against this, but it is one case, and a case in which the Coale and
Demeny models were used in the age estimations.
Three other demographic projects, undertaken with less reliance on the
Coale and Demeny series, add to the burden of evidence in favor of Howell's
depiction of old age structures in small-scale, low-density, non-European
populations. Renee Pennington and Henry Harpending (1993) studied the
demography of the Ngamiland Herero, the Bantu pastoralists who moved
into the Dobe area occupied by the !Kung mostly after 1950.
128 KRISTEN HAWKES AND NICHOLAS BLURTON JONES
THE GRANDMOTHER HYPOTHESIS 129
130 KRISTEN HAWKES AND NICHOLAS BLURTON JONES
While Pennington and Harpending disagreed with aspects of Howell's
analysis of the Dobe !Kung population, they noted strong similarity between
their Herero survival curve and the survival curve Howell had constructed
from observed !Kung deaths. Howell had speculated that these observed
deaths underestimated actual, long run !Kung mortality, but Pennington and
Harpending concluded that, on the contrary, "her estimates of !Kung
survivorship are quite reasonable" (1993,221). In their Herero life table for
the period before 1966, life expectancy is about 50, and 49.5 percent of the
women (those over fifteen) are over forty-five.
Kim Hill and Magdalena Hurtado's (1996) Ache demography describes a
hunter-gatherer population with a very different history than the !Kung,
occupying a very different habitat. The !Kung (and Herero) live in arid
southern Africa; the foraging Ache are Native Americans who live just outside
the Amazon Basin in the forests of eastern Paraguay. Hill and Hurtado
constructed a population register for the Ache back to the early 1900s. Their
survival schedule for forest-living Ache females--without any reliance on the
Coale and Demeny models--gives a life expectancy at birth of thirty-seven,
and an adult age distribution in which 39 percent of the women (those fifteen
years and older) are past their fertility (that is, forty-five and older). This
second hunter-gatherer age structure is shown in figure 6.2, panel B.
Additional evidence of old age structure in low-density populations comes
from a third hunter-gatherer demography (Blurton Jones et al. 1992; Blurton
Jones, Hawkes, and O’Connell 2002), the Hadza discussed above in
summarizing the grandmother hypothesis. Like the !Kung, Hadza foragers
inhabit the arid African tropics, but they live in northern Tanzania just south
of the equator in the East African Rift. From census data collected by James
Woodburn in 1966-67, the population was initially analyzed by Tim Dyson
(1977), who selected the Coale and Demeny model North 6 to represent it.
Blurton Jones and Lars Smith conducted another census in 1985. Using the
two censuses and an initial set of age estimates, Blurton Jones corroborated
Dyson's analysis (Blurton Jones et al. 1992). Subsequent censuses and
reproductive interviews allowed Blurton Jones to further correct the
population age ranking, tie births and deaths to datable events, and construct
a mortality schedule independent of the Coale and Demeny models (Blurton
Jones, Hawkes, and O’Connell 2002). This schedule represents a stable age
distribution in which 40.7 percent of the adults (those fifteen and over) are
forty-five or older, shown in figure 6.2, panel C.
The Archaeological Assemblages
Skeletal remains are often said to tell a different story. Weiss (1973) recognized
that mortuary assemblages might not reflect the mortality experience
132 KRISTEN HAWKES AND NICHOLAS BLURTON JONES
Libben skeletons was not subject to the usual archaeological biases. Their life
table showed the "typical low infant mortality and high adult mortality of
many skeletal series and thus contrasts inversely with most extant
'anthropological populations'. . . This general discrepancy between skeletal
and ethnographic censuses is usually attributed to underenumeration of infants
and errors of age estimation among adults from skeletal series" (Lovejoy
et al. 1977, 291). But they claimed instead that the age profile was a reflection
of the actual age structure of a population unexposed to the battery of
novel pathogens with European arrivals in America.
Howell (1982) elaborated the implications of such a possibility by drawing
out the social and economic consequences of the life table proposed for
Libben. She compared the age structure for this life table to a Coale and
Demeny model with the same level of mortality. The comparison under-lined
both how little life expectancy says about adult age structure and also how
the family relationships and economic interdependencies known for human
populations would be absent in the Libben reconstruction.
The female age structure of the West 1 model from Coale and Demeny
that has the same life expectancy, (eo)= 20, as the Libben model is shown in
figure 6.2, panel D. It is not so different from the three hunter-gatherer
populations, panels A, B, and C. The very different age structure of the
Libben life table is shown in panel E. Only about half the Libben population
is adult (over fifteen) and only 2.9 percent of those are past their childbearing
years, that is, there are almost no grandmothers. In contrast, 65
percent of the West 1 population, panel D, is adult (over fifteen), and 27.4
percent of them are past their childbearing years. Howell (1982) pointed out
that the dependency ratio of the Libben population implies improbably heavy
loads on relatively few young adults. In West 1, there are many adults, and
those in their grandmothering years could help younger adults with the
children.
Human vs. Chimpanzee Age
Structures and Grandmothers Again
Because chimpanzees are our closest living relatives, many (but not all, cf.
Gage 1998; Crews and Gerber 2003) look to similarities and differences between
humans and chimps to specify questions about the evolution of human
life histories. Our genetic similarities and the paleoanthropological
reasons to see chimpanzees as models for australopithecine life histories
make these comparisons particularly important (Hawkes 2003).
Figure 6.2, panel F shows the age structure implied by a life table for wild
THE GRANDMOTHER HYPOTHESIS 133
chimpanzees (Hill et al. 2001). The chimpanzee population is just slightly
younger than the Libben model and has a higher mortality level, but the
adult age structures are very similar. With their shorter adult life spans,
chimpanzees mature earlier than humans. Classifying all those over ten as
adults (from the age-specific fertility schedule of Nishida et al. 2003) is parallel
to classifying all over fifteen as adults in human populations. That
makes 58.5 percent of the chimpanzee population adult (compared to 50.7
percent for Libben). Females past childbearing age are all but absent in both
models: less than 3 percent of the adults are past forty-five.
Consistent with aging rates implied by this demographic picture of
chimpanzees, observers describe chimpanzees as frail with age by their midthirties
(Goodall 1986; Nishida et al. 2003). In humans, strength measures of
foraging women show no marked decline through the forties, fifties, and
well into the sixties (Blurton Jones and Marlowe 2002; Walker and Hill
2002). Chimpanzees have an age structure similar to the one suggested for
Libben. Humans do not. As noted initially, life-history variation across the
mammals is correlated with variation in adult age structures. Life-history
differences between chimpanzees and humans add to Howell's reasons to
surmise that the Libben cemetery assemblage does not represent the mortality
experience of the human population that left the remains.
The difference in adult age structure between chimpanzees and humans is
associated with a difference in subsistence dependence of juveniles. When
chimpanzee infants are weaned, they become nutritionally independent and
forage for themselves. By contrast, although human children can be surprisingly
eager and successful foragers at very young ages (Blurton Jones,
Hawkes, and O’Connell 1989; D. W. Bird and R B. Bird 2002; R. B. Bird
and D. W. Bird 2002), they continue to depend on others to supply
substantial fractions of food after their mothers are investing in a subsequent
baby. The subsistence dependence of human juveniles increases with
reliance on foods that are difficult for youngsters to exploit efficiently
enough to completely feed themselves (for example, Hawkes, O'Connell,
and Blurton Jones 1995). In the case of the Hadza, the foraging effort of
postmenopausal women affects the nutritional welfare of their grandchildren
when the mothers of those children are nursing new babies (Hawkes,
O’Connell and Blurton Jones 1997). The grandmother hypothesis links our
age structure and our unusual pattern of bearing the next baby before the
previous one is independent. Ancestral human mothers could overlap
dependents because they had help.
Sarah Hrdy (1999, 2001) has characterized humans as cooperative
breeders. She notes that mothers' commitment to their infants may be conditional
on social support. Because we overlap dependent offspring, help
134 KRISTEN HAWKES AND NICHOLAS BLURTON JONES
can be crucial, and mothers may face large trade-offs between investment
in a newborn and other offspring. That need for support (our relatively
short interbirth intervals, Hawkes et al. 1998) would only evolve if help was
likely. Short-term variation in the availability of help would make it advantageous
for mothers to strategically adjust their commitment to a new baby.
Uncertain maternal commitment, combined with the importance of allomaternal
help, would also have favored features in infants and toddlers that
enhanced their likelihood of attracting investors (Hrdy 1999). By this lifehistory
argument, both the range of helpers and the maternal and infant
strategies to assess and to extract help depend on the human age structure. If
so, our special form of cooperative breeding is a legacy of the importance of
ancestral grandmothers.
Only recently have investigators begun to look at grandmothers' help
(Hill and Hurtado 1991, 1996; Rogers 1993; Shanley and Kirkwood 2001;
Sear, Mace, and McGregor 2000; Voland and Beise 2002; Leonetti et al. this
volume, Jamison et al. 2002; Hames and Draper in press; Lahdenpera et al.
2004). There are important difficulties. For example, senior women distributing
their help to maximize its marginal effect might supply most to those
kin most in need. Then comparisons between the welfare of juveniles with
grandmothers and those without would necessarily underestimate the magnitude
of grandmother effects (Blurton Jones, Hawkes, and O'Connell this
volume). Assessing the fitness benefits (and costs) that flow through characteristic
human age structures is challenging.
Conclusion
Adult age structure and other life-history characteristics are interrelated
across the mammals. The most successful evolutionary models currently
available to explain that systematic variation make adult life span the determinant
of other life-history variables. If theory that applies to primates in
general also applies to us, then our late maturity and slow aging imply that
old adult age structures have generally been characteristic of humans.
Counterarguments that life expectancies of forty or less imply few elders in
past populations are in error. Human populations that experience such high
mortality levels nevertheless include large fractions of women past childbearing
age.
Claims of discrepant evidence from paleodemography depend on unwarranted
inferences from mortuary assemblages about the mortality experience
of past populations. Other aspects of the fossil and archaeological
evidence are consistent with the hypothesis that old age structures are a feature
of our lineage that antedate Homo sapiens (O'Connell et al. 1999, 2002;
THE GRANDMOTHER HYPOTHESIS 135
Hawkes, O'Connell, and Blurton Jones 2003). An especially important clue
to our evolutionary history is the persistence of a chimpanzee-like agespecific
fertility decline to menopause accompanied by much slower aging in
other aspects of our physiology (Hawkes 2003).
Ronald Lee (2003) has developed an evolutionary model of aging in
which subsistence contributions to kin (transfer effects), not remaining fertility,
can favor lower age-specific mortality rates. We construe this as a formal
treatment of elements of the verbal grandmother hypothesis, showing
how slowed senescence would have been favored in our lineage under socioecological
circumstances that prompted the economic productivity of elders.
With increased reliance on foods difficult for young juveniles to
handle, elder females unencumbered by their own infants could use their
productivity to help provision grandchildren, consequently shifting the age
structure and the social organizational possibilities of genus Homo.
Summary
A grandmother hypothesis in combination with Charnov's model of mammalian
life-history evolution can explain the long potential life spans, short
interbirth intervals, late age at maturity, and midlife menopause that distinguish
humans from our closest living relatives. We summarize the model
and hypothesis that assume that low adult mortality is a general characteristic
of human populations. Then we examine the implications of large variation
in human life expectancies over time, something widely seen as evidence
against the hypothesis. Shorter expectations of life in the past are
misread to imply that few adults survived to old age. We use model life
tables and anthropological demography to show this error. Then we turn to
paleodemography. Life tables that depict past human age structures unlike
any known for living populations have already drawn skepticism from
demographers. Models that highlight patterns of life-history variation across
species supply additional reasons for doubt. We conclude that claims of
younger age structures in the human past are not well warranted. Current
evidence is consistent with the hypothesis of an ancient shift to characteristically
human age structures when ancestral grandmothers helped to provision
younger kin.
Acknowledgments
We thank the conference organizers for their patient work and Helen
Alvarez, Nancy Howell, Sarah Hrdy, Jim O'Connell, Shannen Robson and
Alan Rogers for advice on earlier drafts.
136 KRISTEN HAWKES AND NICHOLAS BLURTON JONES
References
Alvarez, H. P. 2000. "Grandmother hypothesis and primate life histories.” American
Journal of Physical Anthropology 133: 435-50.
Austad, S. N. 1997. "Postreproductive survival." In Between Zeus and the Salmon,
ed. K. W. Wachter and C. E. Finch. Washington, DC: National Academy Press, 161-
74.
Bird, D. W., and R B. Bird. "Children on the reef: Slow learning or strategic foraging."
Nature13: 269-97.
Bird, R B., and D. W. Bird. "Constraints of knowing or constraints of growing? Fishing
and collecting by the children of Mer." Nature 13: 239-67.
Blurton Jones, N. G. 1993. “The lives of hunter-gatherer children: Effects on parental
behavior and parental reproductive strategies." In Juvenile Primates, ed. M. E. Pereira
and L. A. Fairbanks. Oxford: Oxford University Press, 309-26.
Blurton Jones, N. G., K. Hawkes, and J. F. O'Connell. 1989. "Studying costs of children
in two foraging societies: Implications for schedules of reproduction." In
Comparative Socioecology of Mammals and Man, ed. V. Standen and R Foley. London:
Blackwell, 365-90.
-------. 1997. "Why do Hadza children forage?" In Uniting Psychology and Biology:
Integrative Perspectives on Human Development, ed. N. Segal, G. E. Weisfeld, and
C. C. Weisfeld. Washington, DC: American Psychological Association, 279-313.
-------. 2002. “The antiquity of post-reproductive life: Are there modern impacts on
hunter-gatherer post-reproductive life spans?" Journal of Human Biology 14: 184-
205.
Blurton Jones, N. G., and F. W. Marlowe. 2002. "Selection for delayed maturity: Does it
take 20 years to learn to hunt and gather?" Human Nature 13: 199-238.
Blurton Jones, N. G., L. C. Smith, J. F. O'Connell, K. Hawkes, and C. Kamazura.
1992. "Demography of the Hadza, an increasing and high density population of
savanna foragers." American Journal of Physical Anthropology 89:159-81.
Bocquet-Appel, J.-P. and C. Masset. 1982. "Farewell to paleodemography." Journal of
Human Evolution 11:321-33.
Charlesworth, B. 1994. Evolution in Age Populations, 2nd ed. Cambridge: Cambridge
University Press.
Charnov, E. L. 1991. "Evolution of life history variation in female mammals." Proceedings
of the National Academy of Sciences (USA) 88: 1134-37.
--------. 1993. Life History Invariants: Some Explorations of Symmetry in Evolutionary
Ecology. Oxford: Oxford University Press.
Charnov, E. L., and W. M. Schaffer. 1973. "Life history consequences of natural se-
THE GRANDMOTHER HYPOTHESIS 137
lection: Cole's result revisited.” American Naturalist 107:791-93.
Coale, A.J. 1956. “The effects of changes in mortality and fertility on age composition.”
Millbank Memorial Fund Quarterly 34:79-114.
--------. 1959. "Increases in expectation of life and population growth." International
Population Conference, International Union for the Scientific Study of Population,
Vienna, 1959, 36-41.
Coale, A. J., and P. Demeny. 1966. Regional Model Life Tables and Stable Populations,
2nd ed. Princeton: Princeton University Press.
Coale, A.J., and T. J. Trussell. 1974. "Model fertility schedules: Variations in the age
structure of childbearing in human populations." Population Index 40:185-258.
Cole, L. C. 1954. “The population consequences of life history phenomena." Quarterly
Review of Biology 29: 103-37.
Crews, D. E., and L. M. Gerber. 2003. "Reconstructing life history of hominids and
humans." Collegium Antropologicum 27: 7-22.
deMenocal, P. B. 1995. "Plio-Pleistocene African climate." Science 270:53-59.
Dyson, T. 1977. The Demography of the Hadza in Historical Perspective. Edinburgh,
Scotland: Centre for African Studies, University of Edinburgh.
Fisher, R. A. 1930. The Genetical Theory of Natural Selection. Oxford: Oxford University
Press.
Gadgil, M., and W. Bossert. 1970. "Life history consequences of natural selection."
American Naturalist 104: 1-24.
Gage, T. B. 1998. “The comparative demography of primates: With some comments on
the evolution of life histories." Annual Review of Anthropology 27: 197-221.
Goodall, J. 1986. The Chimpanzees of Gombe. Cambridge: Harvard University Press.
Hames, R., and P. Draper. In press. "Women's work, child care, and helpers at the nest in
a hunter-gatherer society." Human Nature 15:319-341.
Hamilton, W. D. 1966. "The molding of senescence by natural selection.” Journal of
Theoretical Biology 12:12-45.
Harvey, P. H., and T. H. Clutton-Brock. 1985. "Life history variation in primates."
Evolution 39: 559-81.
Harvey, P. H., and A. Purvis. 1999. "Understanding the ecological and evolutionary
reasons for life history variation: Mammals as a case study." In Advanced Eco-logical
Theory: Principles and Applications, ed. J. McGlade. Oxford: Blackwell Science,
232-48.
138 KRISTEN HAWKES AND NICHOLAS BLURTON JONES
Harvey, P. H., A. E. Read, and D. E. L. 1989. “Life history variation in placental
mammals: Unifying data with theory." Oxford Surveys in Evolutionary Biology 6:13-
31.
Hawkes, K. 2003. "Grandmothers and the evolution of human longevity.” American
Journal of Human Biology 15:380-400.
--------. 2004. "Human longevity: The grandmother effect." Nature 428: 128-29.
Hawkes, K., J. F. O'Connell, and N. G. Blurton Jones. 1989. "Hardworking Hadza
grandmothers." In Comparative Socioecology of Mammals and Man, ed. V. Standen
and R. Foley. London: Blackwell, 341-66.
--------. 1995. "Hadza children's foraging: Juvenile dependency, social arrangements, and
mobility amonghunter-gatherers." Current Anthropology 36: 688-700.
--------. 1997. "Hadza women's time allocation, offspring provisioning, and the
evolution of post-menopausal lifespans." Current Anthropology 38: 551-78.
--------. 2003. "Human life histories: Primate tradeoffs, grandmothering ecology, and the
fossil record." In Primate Life Histories and Socioecology, ed. P. Kappeler and M.
Pereira. Chicago: University of Chicago Press, 204-27.
Hawkes, K. ,J. F. O’Connell, N. G. Blurton Jones, E. L. Charnov, and H. Alvarez.
1998. "Grandmothering, menopause, and the evolution of human life histories."
Proceedings of the National Academy of Sciences (USA) 95:1336-39.
Hill, K. and A. M. Hurtado. 1991. "The evolution of premature reproductive senescence
and menopause in human females: An evaluation of the 'grandmother' hypothesis."
Human Nature 2: 313-50.
--------. 1996. Ache Life History: The Ecology and Demography of a Foraging People.
Hawthorne, NY: Aldine de Gruyter.
Hill, K., C. Boesch, J. A. Pusey, J. Williams, and R. Wrangham. 2001."Mor-tality rates
among wild chimpanzees." Journal of Human Evolution 39: 1-14.
Hoppa, R. D., and J. Vaupel, eds. 2003. Paleodemography: Age Distributions from
Skeletal Samples. Cambridge: Cambridge University Press.
Howell, N. 1976. "Toward a uniformitarian theory of human paleo-demography."
Journal of Human Evolution 5: 25-40.
--------. 1979. Demography of the Dobe !Kung. New York: Academic Press.
--------. 1982. "Village composition implied by a paleodemographic life table: The
Libben site." American Journal of Physical Anthropology 59: 263-69.
Hrdy, S. B. 1999. Nature: A History of Mothers, Infants, and Natural Selection.
New York: Pantheon.
THE GRANDMOTHER HYPOTHESIS 139
--------. 2001. "Mothers and others." Natural History 110: 50-64.
Jamison, C. S., L. L. Cornell, P. L. Jamison, and H. Nakazato. 2002. "Are grandmothers
equal? A review and a preliminary test of the 'grandmother hypothesis' in Tokugawa,
Japan." American Journal of Physical Anthropology 119: 67-76.
Kennedy, G. E. 2003. "Paleolithic grandmothers? Life history theory and early Homo."
Journal of the Royal Anthropological Institute (n.s.) 9:549-72.
Klein, R. G. 1999. The Human Career: Biological and Cultural Origins, 2nd ed.
Chicago: University of Chicago Press.
Konigsberg, L. W., and S. R Frankenberg. 1994. "Paleodemography ‘not quite dead.'"
Evolutionary Anthropology 3: 92-105.
Lahdenpera, M., V. Lummaa, S. Helle, M. Tremblay, and A. F. Russell. 2004. "Fit-ness
benefits of prolonged post-reproductive lifespan in women.” Nature 428: 178-81.
Lee, R. D. 2003. "Rethinking the evolutionary theory of aging: Transfers, not births,
shape senescence in social species." Proceedings of the National Academy of
Sciences (USA) 100: 9637-42.
Lovejoy, C. O., R. S. Meindl, T. R. Pryzbeck, T. S. Barton, K. G. Heiple, and D. Kotting.
1977. "Paleodemography of the Libben Site, Ottawa County, Ohio." Science
198:291-93.
Nishida, T., N. Corp, M. Hamai, M. T. Hasegawa, M. Hiraiwa-Hasegaawa, K. Hosaka,
K. D. Hunt, N. Itoh, K. Kawanaka, A. Matsumoto-Odal, J. C. Mitani, M. Nakamura, K.
Norikoshi, T. Sakamaki, L. Turner, S. Uehara, and K. Zamma.
2003. "Demography, female life history, and reproductive profiles among the chimpanzees
of Mahale.” American Journal of Primatology 59:99-121.
O’Connell, J. F., K. Hawkes, and N. G. Blurton Jones. 1999. "Grandmothering and the
evolution of Homo erectus." Journal Evolution 36: 2002.
--------. 2002. "Male strategies and Plio-Pleistocene archaeology.” Journal of Human
Evolution 43: 831-72.
Oeppen, J., and J. W. Vaupel. 2002. "Broken limits to life expectancy." Science 296:
1029-31.
Olshansky, S. J., B. A. Carnes, and D. Grahn. 1998. "Confronting the boundaries of
human longevity." American Scientist 86: 52-61.
Pavelka, M. S. M., and L. M. Fedigan. 1991. "Menopause: A comparative life history
perspective." Yearbook of Physical Anthropology 34: 13-38.
Pennington, R., and H. Harpending. 1993. The Structure of an African Pastoralist
Community: Demography, History, and Ecology of the Ngamiland Herero. Oxford:
Clarendon Press.
140 KRISTEN HAWKES AND NICHOLAS BLURTON JONES
Purvis, A., and P. H. Harvey. 1995. "Mammal life-history evolution: A comparative test
of Charnov's model." Journal of Zoology (London) 237: 259-83.
Purvis, A., A. J. Webster, P.-M. Agapow, K. E. Jones, and N. J. B. Isaac. 2003.
"Primate life histories and phylogeny." In Primate Life Histories and Socioecology,
ed. P. M. Kappeler and M. E. Pereira. Chicago: University of Chicago Press,
25-40.
Rogers, A. 1993. "Why menopause?" Evolutionary Ecology 7: 406-20.
Sear, R., R. Mace, and I. A. McGregor. 2000. "Maternal grandmothers improve the
nutritional status of children in rural Gambia." Proceedings Royal Society of London
B 267: 1641-47.
Shanley, D. P., and T. B. L. Kirkwood. 2001. "Evolution of the human menopause."
BioEssays 23: 282-87.
Smith, B. H., and R. L. Tompkins. 1995. "Toward a life history of the hominidae."
Annual Review of Anthropology 24:257-79.
Stearns, S. C. 1992. The Evolution of Life Histories. Oxford: Oxford University Press.
Trinkaus, E. 1995. "Neanderthal mortality patterns." Journal of Archaeological Science
22:121-42.
Voland, E., and J. Beise. "Opposite effects of maternal and paternal grand-mothers on
infant survival in historical Krummhorn.” Behavioral Ecology and Sociobiology 52:
435-43.
Walker, P. L., J. R. Johnson, and P. M. Lambert. 1988. "Age and sex bias in the
preservation of human skeletal remains." American Journal of Physical Anthropology
76:183-88.
Walker, R., and K. Hill. 2002. "Modeling growth and senescence in physical performance
among the Ache of eastern Paraguay." American Journal of Human Biology
15:196-208.
Washburn, S. L. 1981. "Longevity in primates." In Aging: Biology and Behavior, ed. J. L.
McGaugh and S. B. Kiesler. New York: Academic Press.
Weiss, K. M. 1973. "Demographic models for anthropology." Society for American Archaeology
Memoirs 27:1-86.
--------. 1981. “Evolutionary perspectives on human aging.” In Other Ways of Growing
Old, ed. P. T. Amoss and S. Harrell. Stanford: Stanford University Press.
Williams, G. C. 1957. “Pleiotropy, natural selection, and the evolution of senescence.”
Evolution 11:398-411.
Wood, B. A., and M. Collard. 1999. “The human genus.” Science 284-65-71.