Menopause: Adaptation or Epiphenomenon?
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Evolutionary Anthropology 43
ARTICLES
Menopause: Adaptation or Epiphenomenon?
JOCELYN SCOTT PECCEI
Menopause is a nonfacultative and irreversible cessation of fertility that occurs menopause because their hominid an-
in all female conspecifics well before the senescence of other somatic systems and cestors who ceased reproducing be-
the end of the average adult life span (Fig. 1).1–3 So defined, menopause occurs fore the end of their lives gained a
only in humans and one species of toothed whales.1– 4 According to evolutionary fitness advantage over their still-fertile
theories of senescence, there should be no selection for postreproductive individ- sisters in that they they could direct
uals.5 Thus, evolutionary biologists and anthropologists have long been interested their remaining reproductive effort
in why human females have menopause. Many have suggested that menopause is more profitably toward enhancing the
a hominine adaptation, the result of selection for a postreproductive life span that reproductive success of existing prog-
permitted increased maternal investment in existing offspring.3,6 –9 Others are eny.3,5–9,52–54 The fitness trade-off be-
persuaded that premature reproductive senescence is an epiphenomenon, either tween greater investment in offspring
the result of a physiological trade-off favoring efficient reproduction early in the already born versus producing more
fertile part of life or simply the by-product of increases in life span or life expect- offspring, amounting to a quality ver-
ancies.10 –17 Menopause poses two separate questions: why it originated and what sus quantity trade-off, very likely cul-
is maintaining it? minated during a time of rapid en-
cephalization in the hominine line,
which brought with it increases in in-
Evolutionary biologists consider all tinction between adaptations, fitness fant altriciality and the prolongation
complex design features of organisms trade-offs, and true phylogenetic con- of juvenile dependence.8,9,52–54 With
to be ultimately the result of natural straints is the level of explanation. prolonged helplessness and nutri-
selection. As such, menopause can al- Appeals to the role of constraints tional dependence of offspring, each
ways be considered an adaptation. At without explanation of why these con- successive offspring imposed a greater
the same time, it is also recognized straints themselves are not subject to cost on the mother,6 in terms of the
that an adaptation is always morpho- evolutionary change constitute proxi- depletion of her physical reserves and
logically, physiologically, and devel- mate explanations. Although it is use- the resources available for her to in-
opmentally constrained by an organ- ful for heuristic purposes to think in vest in existing offspring. With her
ism’s phylogenetic heritage.18 The terms of three distinct alternatives— own survival in question and the fu-
question of origin is whether meno- adaptation, trade-off, or constraint— ture of her existing offspring at stake,
pause is primarily an adaptation, in the explanations overlap and interact. producing late babies with low sur-
the sense that selection directly fa- For instance, a trade-off is part adap- vival probability was likely to lead to
vored a postreproductive life span in tation and part constraint. In addi- reproductive failure. In this scenario,
human females, or whether it is an tion, the question of menopause can- menopause results from selection for
epiphenomenon of selection for effi- not be isolated from the question of reproductive cessation and is about
cient early reproduction or physiolog- human longevity. In all three cases, stopping early.
ical constraints preventing prolonga- the bottom line is that selection favors There are two not necessarily mutu-
tion of fertility in the presence of early reproduction relative to life ally exclusive, adaptation hypotheses.
increases in human longevity. The dis- span. In this sense, reproductive se- The grandmother hypothesis is about
nescence is always premature. In this inclusive fitness; the benefit comes
paper I critically review the evidence from increasing the fertility of adult
for the adaptation, physiological daughters and nieces, and the sur-
Jocelyn Scott Peccei is a Research Asso- trade-off and by-product of increased vival of their offspring. The princi-
ciate at the Department of Anthropology, longevity explanations for the origin pal proponents of this hypothesis
University of California Los Angeles, Los
Angeles, CA 90095-1553, USA. E-mail:
of menopause. are Hawkes, Blurton Jones, and
jpeccei@ucla.edu O’Connell,7,22,55 but many other re-
THE ADAPTATION searchers have examined it.1,3,56 – 60
Key words: menopause, life-history evolution, fe- The mother hypothesis is about in-
EXPLANATION creasing the survival and fertility of
male reproductive strategies, grandmother hy-
potheses, follicular atresia In the strictly adaptationist view of one’s own offspring.5,6,8,9,61,62 The
menopause, maternal investment is grandmother hypothesis of Hawkes
Evolutionary Anthropology 10:43–57 (2001) the key factor. Human females have and colleagues7,22 and has recently44 Evolutionary Anthropology ARTICLES
creasing adult brain size was imposed
by maternal metabolic output during
gestation, there came a point when
changes in pelvic dimensions facilitat-
ing more efficient bipedal locomotion
put a stop to further rapid prenatal
brain growth.71 The resulting compro-
mise was that the further rapid brain
growth needed to attain greater adult
brain size had to continue postpar-
tum.52,71,72 With much organizational
development in addition to growth still
to take place postnatally, Homo infants
were born in a state of secondary altri-
ciality, requiring intensified investment
in infants and prolonged care of juve-
niles. Exactly when these life-history
changes occurred is still debated. Many
researchers believe major anatomical
and behavioral changes began with H.
erectus around 1.6 mya72,75–78 (but see
Ruff, Trinkhaus, and Holliday79). Re-
cent studies agree that maximum life
span has exceeded 50 years since early
H. erectus,74,80 which could indicate
that menopause is 1.8 mya. However,
Figure 1. Comparative senescence of physiological functions in human females (redrawn early H. erectus (H. ergaster) is not gen-
from Hill and Hurtado3). erally associated with delayed maturi-
ty.74,81,82 (but see Clegg and Aiello77).
evolved from an explanation for human evolution for intensification in The first appearance of delayed matu-
menopause into an explanation for the quantity-quality trade-off between rity is estimated at 1.5 mya.82 It seems
the exceptionally long postreproduc- prolonged fertility and increased ma- reasonable that changes in rates of de-
tive life span of human females.22,55 In ternal investment. Two reasons can be velopment kept pace with, but followed,
the old grandmother hypothesis, advanced for substantial increases in increases in both adult brain size and
menopause is an adaptation facilitat- maternal investment in the environ- secondary altriciality during human
ing grandmothering. In the new ment of evolutionary adaptedness: evolution.76 It also would be logical to
grandmother hypothesis, grandmoth- new ecological pressures due to assume that the transformation from
ering is the adaptation facilitating in- changes in climate and diet and sec- australopithecine to human-like life
creases in longevity; menopause is a ondary altriciality of hominid infants histories was completed by the time
by-product. Although the grand- due to cranial expansion and pelvic anatomically modern H. sapiens ap-
mother hypotheses have received constraints. peared on the scene. Thus, meno-
more attention than the mother hy- pause could have arisen any time be-
pothesis, I have argued that both ver- Ecological pressures tween 1.6 and 0.15 mya.
sions of the former are more problem- Cooling and drying trends during
atic than the mother hypothesis.62 the Plio-Pleistocene resulted in patch- Menopause Unique to Human
If menopause originated as an ad- iness and seasonality in vegetation, Females
aptation for postreproductive mater- necessitating dietary changes for sur- If a protracted period of postrepro-
nal investment, whether mothering or vival.21,63– 65 For the hominine line, ductive maternal investment is the
grandmothering, conditions had to this dietary shift is believed to have response to a unique set of socioeco-
exist that favored this adaptation. Box led to expansion of home ranges, ex- logical, anatomical, and physiologi-
2 lists the important predictions for ploitation of a variety of habitats, and cal pressures, and is also of critical
which the evidence supports meno- increasing foraging flexibility, includ- importance to the way we evolved
pause as an adaptation, followed by ing greater reliance on meat.20,64 –70 from our hominoid ancestors, we
the adaptation predictions that are These changes required increased in- would expect menopause to be unique
not supported. vestment in offspring. to humans or at least rare in other
Reasons for Increased species.
Secondary altriciality
Maternal Investment In addition, there were periods of en- Nonhuman primates
If menopause is an adaptation, we cephalization in the hominine line.71–73 Some decline in age-specific fertility
ought to find reasons in the course of Whereas initially the limitation on in- in later life is not uncommon amongARTICLES Evolutionary Anthropology 45
Box 1. Background on Menopause
We know that menopause has been around for at least number of follicles lost to ovulation is relatively small.38
3,000 years from a Biblical reference to Sarah in the book About 400 oocytes are ovulated over the menstruating
of Genesis (18:11),19 which says, “it ceased to be with lifespan.11
Sarah after the manner of women,” from which we can Oocytes remain inactive in their follicles in an arrested
infer not only that Sarah herself had stopped menstruating, phase of meiosis from the fifth month of gestation until they
but that the authors were quite familiar with the phenom- either succumb to atresia or become part of an ovulatory
enon. Although many researchers have speculated that cohort.39 Normally, only one oocyte in a cohort is singled
menopause is a very old trait,20 –22 we do not know whether out to complete meiosis; the rest provide hormonal sup-
menopause has been around since the hominoid-hominid port for the development of the primary follicle or oocyte,
split, Homo erectus, anatomically modern H. sapiens, or after which they too become atretic.39 As the follicle pool
simply since maximum life spans exceeded 50 years. The shrinks, it becomes more and more difficult to recruit a
life span predicted from body and brain size in early Homo large enough cohort of follicles to produce ovulation.39 In
suggests that a female postreproductive life span predates addition, as human females age, the “chosen” oocytes
H. sapiens.23 become increasingly susceptible to malfunction during
Although there is a strong central tendency in the age of completion of the meiotic process, producing chromo-
menopause in developed countries, with medians cluster- somally abnormal ova.39
ing around 50 years, there is considerable variation in the Physiological sources of variation in the age of meno-
age of menopause both within and between populations.16 pause include the original number of oocytes and the rates
In a sample of American women, the age of menopause of atresia.35 At present, histological investigation of ovaries
ranged from 40 to 59 years.24 Any age within this range is removed from females of all ages, including embryos, sug-
considered normal. Across populations, medians range gests that human females experience at least three differ-
from 43 years in Central Africa to 51.4 years among Cau- ent rates of atresia, from birth to puberty, from puberty to
casian Americans.16 With heritability estimates of 40% to about age 40, and from age 40 to menopause.37,40 The
60% heritability in the age of menopause,25–27 there is change in rate of atresia of greatest interest is the accel-
plenty of genetic variation to increase or decrease the eration that occurs around age 40, because it is believed to
mean age of menopause if such changes brought in- be functionally related to menopause.36,41 Without this ap-
creased fitness. Yet research suggests that there has been parent acceleration, which is thought to begin when some
no secular trend of any kind in the age of menopause over threshold number of oocytes remain (for example, 25,000),
the last 150 years.28 –31 More importantly, Greek and Ro- women would have enough oocytes to last 70 years.42 It is
man writings suggest that there probably has been little or unclear why the rate of atresia increases. However, it is
no secular movement for the last 2,500 years. Aristotle likely that individual variation in the age at which the ac-
(fourth century B.C.) and Pliny (first century A.D.) give 50 celeration occurs is a major determinant of variation in the
years as the maximum age of menopause.32 Texts from the age of menopause.38 Not surprisingly, given the high her-
Middle Ages give 50 years as the average age, with a range itability in the age at which menopause occurs, women
of 35 to 60 years.33,34 with a family history of clinically premature (⬍ 40 years)
Physiologically, menopause is the cessation of menses ovarian failure have earlier menopause.43– 45
due to the depletion of oocytes.35 Human females produce Several studies have examined the contribution of vari-
all the oocytes they will ever have by the fifth month of ous environmental and life-history factors to variation in the
gestation. Semelgametogenesis, the character of produc- age of menopause.24,29,46 –51 As with menarche, nutritional
ing all of one’s gametes at one time, is a trait common to status has been a prime environmental suspect. However,
female birds and mammals.11 In humans the maximum of the large-scale multivariate studies that have attempted to
approximately 7 million oocytes is reduced to 2 million by control for confounding variables such as socioeconomic
birth, 400,000 at puberty, and 1,000 at menopause.36 Oo- status, ethnicity, marital status and parity have failed to
cytes, which are surrounded by follicles in the ovaries, are show a nutritional effect.16 Other suspected risk factors are
lost mostly through a programmed process of cell death body weight, weight loss, alcohol consumption, and
induced by hormone withdrawal, known as atresia.37 Atre- stress. The only well-established environmental risk factor
sia is the sole cause of follicular death before puberty and is long-term cigarette smoking, which lowers the median
remains the predominant cause thereafter, because the age of menopause by approximately 1.5 years.29
nonhuman primates.83 Indeed, all pacity to reproduce until very old age. baleen whales are still reproductive in
iteroparous organisms can be ex- East African female elephants with a their nineties.88 The exception to this
pected to exhibit declining fertility as maximum life span of about 60 years general animal pattern are short-finned
a function of general senescence.84 still retain 50% of their reproductive pilot whales (Globicephala macroryn-
However, in contrast to human fe- capacity at age 55 years, an age which chus). In this species, females experi-
males, nonhuman primates and even only 5% of the population ever reach- ence menopause between the ages of 30
longer-lived species such as elephants, es.85– 87 Female tortoises remain fer- and 40 years and have a mean survival
whales, and tortoises retain their ca- tile far longer than 60 years,53 and of ⱖ 14 years after menopause.446 Evolutionary Anthropology ARTICLES
outlive their reproductive capacity.
Box 2. Adaptation Predictions This means that in many species there
is plenty of variation and raw material
Predictions Supported for selection to work on if a postrepro-
1. Reasons for reproductive senescence in the environment of evolution- ductive life span were to become ad-
ary adaptedness: altriciality of hominid infants and ecological pres- vantageous. It also implies that varia-
sures. tion in the length of reproductive life
2. Protracted postreproductive life span unique to human females. span is an ancestral condition, indi-
3. Fitness costs to prolonged fertility: reduced offspring survival. cating that selection for a postrepro-
ductive life span in hominid females
Predictions Not Supported would have been possible. Interest-
4. Fitness costs to prolonged fertility: premature maternal death and ingly, in Caro and coworkers’83 study,
sibling competition. chimpanzees had the highest percent-
5. Fitness benefits of reproductive cessation. age of females terminating reproduc-
6. Trade-off between fertility and longevity. tion before death, with 60%.
7. Nutritional contribution of females greater than males.
8. No negative health consequences of menopause.
Human males
Although human males usually ex-
hibit a decline in fertility, in most
In both field and captive studies, re- maturity lives to age 60, the average cases this is a function of advanced
searchers have reported menopause- reproductive-age chimpanzee female overall senescence, ill health, or socio-
like physiological phenomena in mon- does not live past 27 years. In other cultural and economic factors.1,93
keys and apes.2,83,89 –92 However, on words, half of all chimpanzee mothers This is not premature reproductive se-
close scrutiny of these reports, it is never outlive their reproductive ca- nescence. Most human males are
clear that the reproductive changes pacity; half of all reproductive-age physiologically capable of siring off-
observed in nonhuman primates rep- Ache women live at least 18 years after spring until very old age, and it is in
resent something different from hu- reproductive cessation. their interest to do so. For males and
man menopause, at least from a com- There is evidence that life spans ex- females, the estimated hazard rates of
parative life-history perspective.1,2 The ceeding reproductive capacity are part reproductive cessation due to biologi-
reproductive changes reported are idio- of our catarrhine legacy,23 and it is cal causes are very different. For
syncratic and generally far from spe- clear that, given the right environ- males the hazard rate of reproductive
cies-wide, while age at reproductive ment, female nonhuman primates will cessation due impotence rises very
cessation is extremely variable and pos-
treproductive life spans are relatively
short.1,2 In field studies, the majority
of the oldest individuals in all species
investigated show no signs of ovarian
failure.1 In studies of captive primate
species in breeding institutions, where
extrinsic sources of mortality are min-
imal, on average about 67% of old fe-
males continued to reproduce all their
lives, and in all species postreproduc-
tive life spans were still relatively
short compared to those of humans.83
Perhaps the best way to illustrate
how different the human female fer-
tility pattern is from that of other pri-
mates is to compare the maximum
age of reproduction and mean life ex-
pectancy at maturity of women and
our closest relatives, Pan troglodytes.
Hill and Hurtado’s87 comparative life-
history diagram for Ache women,
former foragers from Eastern Para-
guay, and common chimpanzees
shows that the maximum reproduc-
tive life span ends at age 42 years for
Ache women and age 34 for chimpan-
zee females (Fig. 2). But whereas the Figure 2. Comparative reproductive life histories of Ache women and female chimpanzees
average Ache woman who reaches (redrawn from Hill and Hurtado87).ARTICLES Evolutionary Anthropology 47
gradually after age 50 years, reaching over the age of 40 than it is for 20- the work performed by postreproduc-
only 0.3 at age 80. For females the year-olds, the risk of dying in child- tive women in extant foraging and
hazard rate of reproductive cessation birth at any age is small.16 Data from horticultural populations. Evidence of
due to menopause rises sharply from one traditional society—the Ache these benefits is mixed.
less than 0.1 to almost 1.0 between the when they still lived exclusively from In some traditional societies, in-
ages of 40 and 50.16 hunting and gathering—suggest that cluding the Hadza,7 the !Kung,101 the
for hunter-gatherer women the risk of Ye’kwana57,102 (horticulturalists in
Fitness Costs of Prolonged dying in childbirth is also small Venezuela), and the residents of the
(about 1 in 150.)87 Moreover, older Micronesian atoll, Ifaluk,56 evidence
Fertility women may not be at considerably supports the proposition that by pro-
If menopause is an adaptation, we greater risk.87 If there was an increase viding material goods and services
should find fitness costs of prolonged in age-specific risk, it would have been postreproductive women enable their
fertility in the form of reduced off- minimal, since the annual mortality daughters to raise more offspring,
spring survival and fertility. Here I rate for 20-year-old and 50-year-old thereby contributing to their own in-
will address three issues: reduced in- women was not much different (1% clusive fitness. Among the Hadza, the
fant survival with late pregnancies in and 2%, respectively).87 Thus, even time women allocate to food acquisi-
modern industrialized societies; the though among the Ache a mother’s tion continues to increase with age
fitness cost of premature maternal death led to the certain death of her beyond menopause.7,22 Older women
death in one foraging population; and children under the age of one year and spend significantly more time forag-
the fertility cost to offspring from sib- a five-fold increase in age-specific ing than do females in any other age
ling competition. Evidence supports mortality for her children over that category. Variation in children’s
only the first, although clearly more data age, reduced offspring survival due to weight is correlated with grandmoth-
from traditional societies are needed. premature maternal death was not a ers’ foraging time. Although the hy-
major source of infant mortality. Ac- pothesis has not been formally tested,
Elevated risk to baby cording to Hill and Hurtado,87 “the as- the implication is that relatively
associated with late pregnancies sumption that older women should higher weight in grandchildren trans-
cease reproduction because they may lates into a fitness advantage for the
If older mothers themselves are not
die soon and their children will not children and an inclusive fitness ad-
at high risk of dying in childbirth, late
survive maternal loss is notably incor- vantage for their hardworking grand-
pregnancy is still generally considered
rect” (p. 433). mothers. However, hardworking
to carry high risk for fetuses and neo-
grandmothers, like Hadza women
nates, at least in Western societies for
Fertility costs to offspring from aged 45 to 60, who bring in approxi-
which we have data.94 –99 The risks in-
sibling competition mately 1,000 more calories on a daily
clude increased probability of fetal
basis than the average person con-
loss, stillbirth, and birth defects. Con- Regarding fitness costs to high and, sumes, appear to be exceptional.60
trolling for frequency of intercourse, by inference, prolonged maternal fer- Ache and Hiwi women never produce
older women experience increasing tility in the form of reduced offspring surplus calories.60 In addition, even
difficulty in becoming and staying fertility, data from the Ache suggest Hadza grandmothers provide less
pregnant.16 Fetal wastage is the major that fertility costs from sibling compe- than 6% of the average daily protein
contributor to fertility decline up to tition may be gender-dependent and intake.60 Still, food sharing does not
age 45 years.16 The overall rate of fetal variable. For example, during the for- constitute the sole contribution of
loss for women over 40 is 0.5. Mater- est period, there was a negative asso- postmenopausal women to daughters’
nal age is also predictive of an increas- ciation between Ache daughters’ fer- reproductive success in traditional so-
ing incidence of most birth defects.96 tility and number of siblings—that is, cieties. Grandmothers are frequent
Indeed, 85% of the abortuses of between daughters’ fertility and moth- providers of child care and shelter and
women over age 40 have some detect- ers’.87 The association between help with food processing and fire-
able chromosomal abnormality, with daughters’ fertility and number of wood collecting. Older females also
Down syndrome representing the brothers was strongly negative. In acquire authority and are eligible for
most dramatic example of this contrast, there was a positive and special status.103 This newly acquired
trend.16 By age 43, the risk of carrying much greater correlation between authority involves the ability to influ-
a baby with Down syndrome baby is sons’ fertility and number of siblings. ence important decisions affecting
one in ten.100
younger kin, as well as the right to
Fitness cost of premature Fitness Benefits Associated extract labor from younger family
members. Accordingly, the work of
maternal death with Reproductive Cessation older women tends to be administra-
It used to be that the birth of each As a corollary to the fitness costs of tive, involving the delegation and as-
child jeopardized a mother’s previous prolonged reproduction, we expect to signment of subsistence tasks to
children because of her risk of dying find fitness benefits associated with younger women. Nonetheless, Hill
in childbirth, a risk that increased cessation of reproduction before and Hurtado’s3,87 mathematical anal-
with age.16 In affluent Western societ- death if menopause is an adaptation. ysis, which was designed to test the
ies of today, even though that risk is To discover these benefits, researchers hypothesis that reproductive cessa-
still seven times higher for women have traditionally relied on studies of tion offers fitness-enhancing opportu-48 Evolutionary Anthropology ARTICLES
nities, suggests that the fertility of controlling for access to resources.87 ever, it appears to be men, not post-
Ache sons and daughters and the sur- This trade-off may be undetectable in reproductive women, who provide the
vival of grandchildren were not signif- the Ache because the relevant data necessary nutritional supplement.60
icantly increased by the presence of come from a period of population Even the famous hardworking Hadza
postmenopausal mothers or grand- growth and abundance when life-his- grandmothers of Tanzania provide far
mothers. I appreciate the difficulties tory trade-offs may have been relaxed, fewer calories and protein through
of detecting such effects. To begin or because help from close kin with foraging than do Hadza male hunters
with, both the costs and the benefits few or no dependents permitted rela- of all ages. With new evidence of meat
are probably difficult to establish in tives to enjoy high fertility without consumption during the Plio-Pleisto-
extant populations because meno- negative consequences.87 cene65,70 and new evidence of males’
pause already exists. In addition, if nutritional contribution in extant for-
women differ in access to resources, aging societies, it is difficult to dismiss
Female Investment in
those with abundant resources may the importance of male investment in
continue bearing healthy fertile Offspring Greater than Male
human reproduction. In general,
daughters late in life, so that the phe- Investment women, young or old, do not appear
notypic relationship we observe be- If the postreproductive life span of to contribute more than males do to
tween mother’s and daughters’ fertil- human females is an adaptation per- the nutrition of weaned offspring.
ity is positive, even if in less optimal mitting increased maternal invest- Moreover, it is uncommon for post-
conditions late fertility is associated reproductive women to produce a
with reduced fitness. 104 nutritional surplus.60 Male hunter-
gatherers, in contrast, appear to sub-
Trade-Off Between Decreased If the postreproductive sidize the energetics of reproduction
Fertility and Increased throughout their adult lives.60 Thus,
life span of human the evidence does not support meno-
Longevity
females is an pause as an adaptation favoring post-
Here again, the evidence is mixed. reproductive maternal investment, at
According to life-history theory, in- adaptation permitting least as far as nutrition is concerned.
creased longevity should come at the increased maternal
cost of reduced fertility.105 Although
there are many reasons why studies investment, we might
working with variation among indi- expect female Negative Health
viduals might fail to show such a Consequences of Menopause
trade-off,18,104 when considered in investment in the
historical perspective there does ap- nutrition of their progeny Kenneth Hill108 has suggested that
pear to be a trade-off between fertility “the female reproductive period is
and human longevity.106 A recent
to be more important broadly protective of health” (p. 113)
study of an historical dataset contain- than male investment, at whereas, in affluent Western coun-
ing life-history records gathered from tries in particular, reproductive se-
the British aristocracy between the
least after menopause. nescence is associated with in-
eighth and nineteenth centuries, re- This does not appear to creases in cardiovascular disorders,
veals that for women who reached 60 osteoporosis, and cognitive impair-
be the case. ment.46,107–117 The notion of meno-
years, longevity was negatively corre-
lated with number of progeny and pause as an unhealthy state may not
positively correlated with age at first seem consistent with menopause as
childbirth.106 In addition, for women, an adaptation. However, all adapta-
ment, we might expect female invest- tions have costs and benefits, and
maternal and paternal heritability of
ment in the nutrition of their progeny the evidence regarding negative
longevity were about 40% and 20%,
respectively. According to Westen- to be more important than male in- health consequences of menopause
dorp and Kirkwood,106 these findings vestment, at least after menopause. is mixed. As Leidy11 emphasizes,
are “compatible with the hypothesis This does not appear to be the case. In chronic conditions commonly asso-
that human life history has a heritable hunter-gatherer societies for which ciated with estrogen withdrawal
component that involves a trade-off there are quantitative data, Kaplan need to be considered cross-cultur-
between fertility and longevity” (p. and colleagues60 show that juveniles ally and historically. Menopause
746). and reproductive-age women do not may not be the most important risk
In extant foraging societies, the ex- meet their own energy requirements. factor for heart disease or osteopo-
treme degree and duration of off- Comparison of maternal effort among rotic fractures.114 Indeed, consider-
spring dependence probably presents baboons and Ache foragers supports ing the incidence of osteoporosis in
a fitness challenge for women even the notion that, despite the heavier historical and cross-cultural per-
today. Yet a trade-off between mater- burden of multiple dependents, hu- spectives indicates that diet and ex-
nal fertility and subsequent survival man females work less hard during ercise levels are important variables
has not been identified. Data from the their reproductive years, whereas ba- determining the rate at which bone
Ache do not suggest a trade-off, even boon mothers work harder.107 How- is lost.118ARTICLES Evolutionary Anthropology 49
DISCUSSION surviving long enough to have a sec- ing and child care and, in the process,
ond child if she waited for the first to learn parenting skills. Still, even with
On balance, the evidence for selec-
become fully independent before giv- male provisioning and some econo-
tion for a postreproductive life span to
ing birth again. In the face of limited mies of scale associated with overlap-
increase maternal investment in exist-
adult life expectancies,123,124,125 the ping child care, early Homo females
ing offspring is inconclusive. I find lit-
fitness-enhancing strategy was to probably suffered chronic and in-
tle support for the notion that women,
shorten interbirth intervals and adapt creasing energy deficits during their
postreproductive or otherwise, are the reproductive years due to overlapping
major providers of the nutritional re- to overlapping child care.
Besides optimizing birth spacing, child care.126 –133
sources subsidizing human reproduc- In a previous analysis of the adap-
tion. However, the nutritional contri- overlapping child care also had some
tation hypotheses, I emphasize how
bution of males versus females is difficult it is to show that premature
probably the wrong comparison. reproductive senescence is the result
First, food sharing is not the only con- of selection for increased maternal in-
tribution open to postreproductive fe- . . . in all societies, vestment.62 However, if menopause is
males. Second, in sexually reproduc- an adaptation, I believe that mother-
ing species males and females have an historically and cross- ing, not grandmothering, is more
equal need for surviving offspring. culturally, women likely to be the reason. Although stud-
What differs within and between spe- ies on grandmother investment are
cies is how males and females allocate undergo menopause if
numerous, this approach is probably
resources to somatic effort and repro- they live long enough. If flawed, mainly because these women
ductive effort, and how reproductive
effort is divided between mating effort
premature reproductive already have undergone menopause.
They are not choosing between having
and parental effort.119 When males senescence is the result another baby and helping daughters;
contribute more than women do to of certain conditions in their only option is helping. To me the
the nutrition of their offspring, it is mother hypothesis is more compel-
because women must allocate their the environment of ling, given Hamilton’s134 rule, low life
energetic resources to other reproduc- evolutionary expectancies in the environment of
tion-related requirements. The diver- evolutionary adaptedness,80,123,124 the
sity of human mating systems reflects adaptedness, the likelihood of male philopatry,133,135,136
the fact that male and female repro- universality of as well as the expediency of overlap-
ductive strategies differ within our ping child care and the logical infer-
species as a result of varying socioen- menopause implies that ence that when fertility ceases a
vironmental conditions. Yet in all so- those conditions must woman is still likely to have a last-
cieties, historically and cross-cultur- born to care for.
ally, women undergo menopause if
still be present today.
they live long enough. If premature Menopause, or the THE EPIPHENOMENON
reproductive senescence is the result postreproductive life
of certain conditions in the environ- EXPLANATIONS
ment of evolutionary adaptedness, the span, must be the I come to the two explanations that
universality of menopause implies response to some cast menopause as an epiphenome-
that those conditions must still be non: the physiological trade-off favor-
present today. Menopause, or the unvarying constellation ing efficient early reproduction and
postreproductive life span, must be of pressures; my vote is the by-product of increased longevity
the response to some unvarying con- hypotheses. There is less to say about
stellation of pressures; my vote is for for prolonged offspring these, for until recently most evolu-
prolonged offspring dependence and dependence and tionary biologists and anthropologists
overlapping child care. have dismissed them as proximate ex-
Rapid encephalization required a
overlapping child care. planations that fail to justify the post-
change in female reproductive strat- reproductive life span in human fe-
egy. The challenge to females result- males. The underlying assumption of
ing from encephalization included the both these explanations is that evolu-
risk of the birth process itself,120 the potential advantages. First, a mother tion is constrained by phylogenetic
high metabolic costs of gestation and with multiple dependents can reduce history, developmental limitations,
lactation,16,52,121 offspring altriciality, her total lifetime reproductive cost be- and genetic correlations.18 In both
and increased and prolonged depen- cause certain tasks, such as protection cases, response to selection is limited
dence of juveniles.6,64,122 It was not against predators and conspecifics, by the “technology” of an organism,
feasible to solve the problem of pro- provision of shelter, and food prepa- which forces design trade-offs and
longed offspring dependence by in- ration, can benefit more than one de- negatively correlated, or antagonistic,
creasing interbirth intervals. The pe- pendent without the expenditure of responses. For example, a gardener
riod of dependence was too long: A much extra time and energy. Second, might wish to breed peapods contain-
mother faced a high probability of not older siblings can help with provision- ing more and larger peas, only to dis-50 Evolutionary Anthropology ARTICLES
cover that she cannot have both, ei- the adaptation and physiological tion are more difficult to establish.
ther because oversized pods are too trade-off hypotheses is that in the lat- There are also two predictions that
heavy to ripen on the vine (design ter menopause per se is not what you are specific to the physiological trade-
trade-off) or because the size and are seeking to explain. What needs ex- off favoring early fertility.
number of peas are controlled by neg- plaining is why age-specific fertility
atively correlated genes (antagonistic begins decreasing decades before
pleiotropy). Negative genetic correla- menopause. Menopause is simply the Historical and Cross-
tions can result in intertemporal phys- last event in the process of declining Populational Evidence of
iological trade-offs as well. Such is fertility. Whether menopause is the
thought to be the case with reproduc-
Early Fertility
result of selection for efficient early
tive senescence in human females: In support of the physiological trade-
reproduction or selection for a pos-
Pleiotropic genes are favored because off explanation, we find historical and
treproductive life span is exceedingly
they have positive effects at younger cross-population evidence of selection
difficult to tease apart. Indeed, if over-
ages, even though they have negative for early fertility in human populations.
lapping child care is the truly unique
effects later in life.10 –12,137 According In extant and historical natural-fertility
to evolutionary theories of senes- reproductive character in human fe- populations, total fertility rates vary
cence, such time-delayed antagonistic enormously, as do nutritional status
pleiotropy can exist because selection and mortality rates.16,87,138,139 Despite
against fitness-reducing traits weak- these differences, the pattern of age-
ens with age.5 Whether menopause is specific marital fertility remains re-
the result of selection for markably consistent across time and
THE PHYSIOLOGICAL TRADE- geographical boundaries, peaking
efficient early around age 25, then decreasing mono-
OFF
reproduction or tonically with the cessation of fertility,
Given semelgametogenesis, the rea- generally preceding menopause by
son for a physiological trade-off favor- selection for a several years (Fig. 3).140 This supports
ing efficient early reproduction is that postreproductive life the importance of a biological expla-
human female reproductive physiol- nation for reproductive cessation be-
ogy should be designed to maximize span is exceedingly fore menopause and for menopause
reproductive output early in life be- difficult to tease apart. itself.
fore the dwindling supply of oocytes Additional indication that the
jeopardizes hormonal support for
Indeed, if overlapping causes of the premenopausal cessa-
ovulation12,38,137 and to terminate fer- child care is the truly tion of fertility are physiological
tility before the negative conse- comes from analysis of age-specific
quences of “old eggs” predominate.10
unique reproductive apparent fecundabilities, or monthly
Selection might favor a longer repro- character in human probabilities of a recognized concep-
ductive life span in human females, females, both the tion. Based on data from Taiwanese
but selection for efficient early fertil- and Hutterite women and a statistical
ity, which results in decreased fertility adaptation and model, Wood and Weinstein141
and eventual sterility in later life, pro- physiological trade-off showed that apparent fecundability
vides greater lifetime reproductive begins to decline around age 25 years.
success. Selection for efficient early explanations are Declining coital rates are responsible
fertility is not about starting repro- applicable. for most of the yearly decrease in
duction early. In fact, the hypothesis apparent fecundability up to age
is silent regarding when reproduction 35.140,141 After age 35, biological
begins; what is at issue is the intensity causes take on major importance,
of reproduction early in the fertile life males, both the adaptation and phys- eventually totally predominating.16
span. In this scenario, as in the adap- iological trade-off explanations are The model suggests that the biological
tation theory, reproductive senes- portion of the decline stems from the
applicable. At any rate, these two ex-
cence is about stopping early. increasing risk of early fetal loss.140
planations share some of the same
The physiological trade-off explana- Further validation of the physiolog-
predictions: long postreproductive life
tion and the adaptation explanation ical trade-off explanation comes from
spans should be unique to human fe-
are not necessarily mutually exclu- Wood and colleagues.12,142 According
sive. Besides the fact that selection for males; prolonged fertility should have
to these investigators, the menstruat-
efficient early fertility can be con- fitness costs in the form of reduced ing life spans of women of all ages are
sidered an adaptation in its own offspring survival and fertility; and fit- characterized by periods of ovarian
right—for example, to accommodate ness benefits should be associated inactivity in which regular cycling
overlapping child care—antagonistic with reproductive cessation. Earlier, and, presumably, ovulation, do not
pleiotropy or a design trade-off could we saw that a long postreproductive occur because the production of ovar-
be the proximate mechanism creating life span is unique to human females, ian steroids is insufficient to maintain
a postreproductive life span if that but that the costs of prolonged fertility negative feedback on lutenizing hor-
were favored. The difference between and the benefits of reproductive cessa- mone and follicle-stimulating hor-ARTICLES Evolutionary Anthropology 51
mechanisms in humans and chimpan-
zees.12
Across mammals, females’ supply of
follicles at puberty scales allometri-
cally with species body size and life
span.15 To allow for the fact that the
number of follicles at puberty rises
more steeply with body weight than
with life span, and to insure a lifetime
supply, ovulation rates vary inversely
with size.15 At maturity, human fe-
males have the number of follicles
predicted by body weight, and there is
no evidence for a relatively high rate
of follicular attrition.15 In fact, there is
some evidence that longer-lived spe-
cies use follicles more conservative-
ly.15 Still, in other species senescence
and death usually precede depletion
of oocytes, whereas the postreproduc-
tive life span of human females is long
and universal.147 The questions, then,
are why does human fertility start to
decrease when women are in their
Figure 3. a) Comparison of age-specific marital fertility rates in natural fertility populations mid-twenties and terminate when
and b) age-specific marital fertility rates corrected for differences in total fertility rates. Raw they are around age 40, and why do
rates at each age are divided by the rate at age 20 to 24 years. (Redrawn from Wood16).
human females outlive their supply of
eggs? Leidy148 hypothesizes that “the
process of follicular atresia evolved as
mone, which is essential for ovula- semi-provisioned species such as Bar- integral to the process of sexual repro-
tion. The pattern of these “inactive bary macaques,143 olive baboons,144 duction and that the entire hominid
phases,” which increase in frequency lions,144 and East African elephants145 somatic lifespan was more amenable
and duration as menopause is ap- do, in fact, look very different from to change than was the process of
proached, is predictable from the age the human pattern.146 Instead of re- atresia” (p. 149). In my view, selection
pattern of follicular depletion, sug- sembling a left-skewed triangle with for efficient early reproduction is an
gesting that the characteristics of the fertility starting to decrease when fe- adaptation, accommodating pro-
follicular-depletion system determine males are in their mid-twenties, the longed offspring dependence and the
the distribution of inactive phases and age-specific fertility functions of ma- expedience of overlapping child care.
the probability of ovulatory cy- caques143 and elephants,145 are box- Indeed, I consider the physiological
cles.12,142 Wood, O’Connor, and Hol- like, with fertility remaining relatively trade-off favoring early fertility to be
man12 hypothesize that menopause constant over a relatively long period, the most powerful explanation of all.
evolved by antagonistic pleiotropy be- then terminating abruptly only a few In addition, although the proponents
cause of selection acting on the follic- years before maximum age at death of selection for early fertility do not
ular depletion system to maintain reg- (Fig. 4). For Mahale chimpanzees,71 address the value of the postreproduc-
ular ovarian cycles at young adult there is no correlation between fe- tive life span, a postreproductive pe-
ages. males’ age at last birth and length of riod, albeit a modest one at first,
interbirth interval [r ⫽ 0.09 ⫹ ⫺8.66, would have afforded a fitness advan-
N ⫽ 19], suggesting that noncaptive tage if it increased offspring survival.
Fertility in Other Mammals chimpanzees also have a box-like fer- That brings us back to the adaptation
The fact that biological factors in- tility pattern.91 Many similar exam- hypothesis.
volving a design trade-off and antago- ples can probably be adduced. In
nistic pleiotropy (or both) appear to addition, though some female nonhu- ARTIFACT OF LONGER LIFE
be responsible for the early reproduc- man primates living in captivity show
tive peak in human females is still in- age-specific fertility patterns similar
SPANS OR LIFE EXPECTANCIES
sufficient to explain menopause. One to those of humans, only among chim- I come to the explanation of meno-
must also show that fertility functions panzees do more than than 50% of pause as a by-product of long life span
of humans are different from those of females have a postreproductive life or increase in life expectancies. The
other mammals. One must show that span.83 The finding that chimpanzees elucidation here is that, given the phy-
human females are unique both in have menopause and a post reproduc- logenetic, physiological, and develop-
terms of their early fertility peak and tive lifespan if they live long enough is mental constraints of semelgameto-
long postreproductive life span. Fertil- consistent with the similarity between genesis, menopause is simply the
ity patterns for nonprovisioned or the follicular depletion patterns and result of human life spans and life ex-52 Evolutionary Anthropology ARTICLES
at least 3,000 years, and during most
of this time living conditions for most
women were certainly not very good.
This leaves us to explain why life span
exceeded reproductive capacity.
Females of other long-lived species
do not have menopause—recall ele-
phants, tortoises, and most whales,
which live to be 60, 80, and 90 years
old, respectively. According to Dia-
mond53 there “is nothing evolutionar-
ily inevitable about menopause from
the perspective of mammals in gen-
eral. Other species maintain fertility
and viable oocytes longer than hu-
mans” (p. 116). Human females use
up their supply of oocytes approxi-
mately half-way through the maxi-
mum life span.2 In contrast, follicular
depletion before the end of life is rare
in other female mammals.147 Females
in other mammalian species rarely
have postreproductive life spans;
when they do, these are relatively
short.2
According to evolutionary theories
of senescence, there should be no se-
lection for postreproductive individu-
als. Reproductive senescence is equiv-
alent to death.5 But no one is truly
postreproductive. As Williams5 put it,
no one is truly postreproductive until
the last child is self-sufficient. Dia-
mond53 goes further, stating that peo-
ple are never truly postreproductive if
they can influence the fitness of bio-
logical relatives. The notion that there
can be no selection against mutations
causing damaging effects in old peo-
ple because they are postreproductive
Figure 4. Age-specific fertility functions: a) Hutterite women, b) semi-free-ranging Barbary overlooks this fact. Especially in pre-
macaques, and c) East African elephants. Arrows indicate maximum age at death (re-
literate foraging societies, Diamond53
drawn from Robinson146; Paul, Keuster, and Podzuweit143; and Laws, Parker, and John-
stone144). notes, older folk are valued for their
ability to share their vast store of
knowledge, in particular their knowl-
pectancies increasing beyond the fe- for mothers and offspring. The arti- edge of matters concerning survival.
male’s supply of eggs or ability to sus- fact and adaptation explanations are Accordingly, older individuals, includ-
tain ovulatory cycles.13–17 not mutually exclusive either. If the ing postreproductive females, could
The physiological trade-off and ar- dissynchrony between reproductive have been valued even before the ori-
tifact explanations are not mutually and somatic senescence arose in hu- gin of spoken language, when com-
exclusive for two reasons. First, de- man females because selection for a munication still relied on vocaliza-
sign trade-offs and antagonistic postreproductive life span was greater tions, signs, and facial expressions.
pleiotropy would be the proximate than selection for longer fertility, This makes it possible that meno-
mechanisms preventing increases in menopause would be more adapta- pause is a very old trait indeed. As for
reproductive life span. Second, in- tion than artifact. how humans evolved longer life
creases in life span and life expectan- As an explanation for the origin of spans, Diamond49 suggests that per-
cies may be partly the result of selec- menopause, we can dismiss the hy- haps we live longer because we
tion for early fertility if reproductive pothesis that a postmenopausal life evolved better repair mechanisms as
effort released by the cessation of fer- span is the result of a recent increase we gained more control of our envi-
tility is directed toward increased so- in life expectancies due to improved ronment.
matic repair or if the cessation of sanitation and medical care. Some fe- If human females have the number
childbirth increases life expectancies males have lived past menopause for of follicles predicted for a mammal ofARTICLES Evolutionary Anthropology 53
our body weight at maturity, and if From a heritability estimate, we learn span now is significant because it
there is no evidence for a relatively about the maintenance of menopause changes the terms of the menopause
high rate of follicular attrition, despite from the stability of the mean age of debate. Previous investigation has fo-
the acceleration in atresia,15 why do menopause over the relatively recent cused on the socioecology of hunter-
we run out of oocytes prematurely? past—say, the last 2,000 years. We gatherers in an attempt to understand
According to Gosden and Telfer,15 the learn about the long-term mainte- the selection pressures of the environ-
odd thing about human females is nance of the trait from the amount of ment of evolutionary adaptedness.
that, based on body weight, allometry additive genetic variance (VA).152 The fact that there is presently a cost,
predicts a life span of only 30 years. As discussed earlier, the evidence, as many have suspected, means that
These researchers believe this consti- there is nothing peculiar to the forag-
though not conclusive, suggests that
tutes “a prima facie case for arguing ing way of life that makes premature
the age of menopause has remained
that menopause has arisen adventi- reproductive senescence adaptive.
relatively stable for a few thousand
tiously during evolution” due to in- This is not unexpected, given the pre-
years throughout the world, despite
creases in life span (p. 174). In con- ponderance of evidence suggesting
trast, Judge and Carey23 predict a tremendous socioeconomic and de- that reproductive patterns in human
human life span of 72 years based on mographic change. With no upward females are remarkably consistent
body and brain mass of a catarrhine secular trend in the mean age of across populations and time, regard-
comparison group. Observing that menopause and heritablities as large less of mode of subsistence.
this estimate exceeds average longev- as 40% to 60%,25–27 there are three The next question is whether sta-
ity in hunter-gatherers and the age of possible explanations. The first is that bilizing selection on the age of
menopause by at least 20 years, Judge menopause is weak or strong. Strong
and Carey suggest “that a lifespan ex- stabilizing selection is usually asso-
ceeding that of the female reproduc- ciated with low heritabilities, be-
tive system is part of the phylogenetic According to cause strong selection is generally
legacy rather than a modern develop- expected to reduce additive genetic
ment related to uniquely human cul-
evolutionary theories of variation.149,150,153,154; cf.151,155 (Un-
tural innovations” (p. B205). senescence, there der certain circumstances, however,
In the patriarch hypothesis Mar- should be no selection high heritability can remain in the
lowe17 posits that menopause is the presence of strong stabilizing selec-
by-product of selection for extension for postreproductive tion.151,156 –159) This implies that a
of maximum life span in males. The individuals. broad range of intermediate ages
life span of females co-evolved with of menopause is favored, and that
that of males, whereas commensurate Reproductive menstruating life span is not corre-
increases in female reproductive life senescence is lated with lifetime reproductive suc-
span were constrained by the deple- cess.149 In this case, menstruating
tion of viable oocytes. Without justify- equivalent to death. But life span would have a flat fitness
ing the postreproductive life span, the no one is truly profile, perhaps with selection only
artifact explanation is insufficient. against very early or very late meno-
However, menopause could be a re-
postreproductive. pause. Over much of its range, age of
sult of life span outlasting female re- menopause could be considered a
productive capacity if postreproduc- neutral trait. Weak stabilizing selec-
tive females had indirect reproductive tion on the age of menopause could
value. age of menopause has experienced be the result of selection for some
upward movement that we have not other trait that affects the age of
detected. Lack of evidence for a secu- menopause, such as selection for
Heritability in the Age of lar trend is not definitive. The second early fertility or a postreproductive
Menopause is that age of menopause is selectively life span. The nearly universal age at
Additional insight into the investi- neutral. The third is that age of meno- last birth of approximately 40 years,
gation of menopause and the adapta- pause is under some degree of stabi- regardless of median age of meno-
tion-versus-epiphenomenon debate is lizing selection. pause, is consistent with this notion.
provided by estimates of heritability High heritability and no discernible To me this represents further sup-
in the age of menopause because her- upward movement in the mean age of port for the hypothesis that meno-
itability provides information about menopause in the presence of improv- pause is an epiphenomenon of selec-
the history of selection on a trait.141–151 ing socioeconomic conditions sug- tion for efficient early reproduction.
Indeed, heritability estimates are par- gests a cost to prolonged fertility now, In this scenario, menopause is both
ticularly useful in this case because in modern industrialized and tradi- the result of selection for intensive
researchers have had to resort to a tional agricultural societies, which reproduction early in the fertile pe-
good deal of speculation about the or- supports the third option. By implica- riod to accommodate prolonged de-
igin of menopause, while empirical tion, this cost has existed since the pendence of offspring through over-
work on the maintenance of the trait domestication of plants and animals lapping child care and an adaptation
is hindered by the fact that meno- about 10,000 years ago. Finding a cost for more effective maternal invest-
pause is universal in our species. to prolonging female reproductive life ment, including a modest postrepro-You can also read
