Download Postreproductive Life Predicted by Primate Patterns

Journal of Gerontology: BIOLOGICAL SCIENCES
2000, Vol. 55A, No. 4, B201–B209
Copyright 2000 by The Gerontological Society of America
Postreproductive Life Predicted by Primate Patterns
Debra S. Judge1 and James R. Carey2
Departments of 1Anthropology and 2Entomology, University of California at Davis.
Regression analyses of primate life spans on recently revised female body and brain masses of Old World primates predict a human life span of between 72 years and 91 years—estimates that exceed the age of human menopause (and prior estimates) by well over 20 years. The life spans predicted from body and brain sizes in the early
Homo suggest that postreproductive life spans predate Homo sapiens. Among anthropoid primates, residual longevity after body and brain effects are controlled is greatest for Homo and for the New World monkeys of the genus Cebus. Body and brain masses predict a 25-year life span for Cebus, although recorded life spans exceed 50
years. Cebus are geographically widespread, have a female-bonded social organization convergent with Old
World monkeys, and are primarily frugivorous, though the diet is heavily supplemented with vertebrate prey.
Regressions of phylogenetically independent contrasts indicate that body mass and brain mass relationships to
longevity remain significant when phylogeny is controlled and that brain mass is a more robust predictor than
body mass. These data are new in terms of the completeness of species representation, more reliable body masses,
presentation of various comparison group regressions, and control for phylogenetic independence.
T
O what extent is human longevity explained as a function of primate origin, body size, and brain size rather
than as a function of modern ability to manipulate environment and self? Determining whether contemporary longevity is “extreme” on an evolutionary timescale requires a
comparison with hominid ancestors and within the broader
framework of our primate ancestors. Humans are relatively
large-bodied mammals, and larger mammals tend to live
longer than the smaller bodied (1). After controlling for
body mass, one can explain some of the residual human longevity by the fact that humans are primates and primates
live longer than other comparably sized mammals (2–4).
Some of this potential for long life may be attributable to
the relatively larger brains of primates (5,6).
Primates have the capacity for life spans that exceed predictions based on their body size (7,8). The majority of primates are small to midsized (0.1–93 kg, with the vast majority weighing less than 10 kg), yet life spans of 20–30 years
and more are not uncommon. The morphology, life history,
and socioecology of primates are relatively well documented. Just as primates generally exceed the average life
span predicted for mammals of their body size, body size
accounts for a large proportion of the within-order variation
in life span as well. Adult female body weight explains 63%
of the variation in life span among genera (Figure 1). The
positive relationship of longevity to body size within the order is not typical of all mammalian orders (8; and our unpublished data).
From an evolutionary perspective, postreproductive life
spans are anomalous. Thus the human female pattern of reproductive cessation in the fifth decade has intrigued evolutionary biologists for decades (9,10). A postreproductive
life span may increase the survivorship of last-born young
when juvenile periods are prolonged (11). Where more than
two generations overlap, older females may subsidize the
growth and development of more distant kin such as grandoffspring (12–14). This should apply particularly when females remain in their natal group while males disperse, as
groups of females will be related. The presence of a grandmother more than halved the probability of mortality of captive vervet monkey infants (15). Female gelada baboons
who form coalitions, first with their mothers and later with
their own daughters, experience late life increases in rank
and lifetime fitness that exceed the benefits of other coalitions (16). Attempts to model natural selection for postreproductive survival or to document this process have yielded
mixed success (17, 18). Recent demographic data on baboons and lions found no differences in survival and reproductive success associated with the presence of grandmothers (19). Both species live in groups of related females and
their immature offspring with in-migrating males; however,
neither species is particularly long lived for its order and
thus may not be the most appropriate test case.
Brain size is correlated with both body size and life span
in mammals as a whole (6) and within the Primate order
(20–22). Relative brain size and relative life span (residual
brain and life span after controlling for body mass) are reported to be highly correlated (2, n ⫽ 73 species; 22, n ⫽ 72
species). However, the body mass measurements on which
these correlations are based appear to have numerous errors
(23), and the use of species-level data exacerbates problems
of nonindependence.
We examine 133 species of primates for evidence of relatively long life span, relate longevity to body mass values
and adult brain size, and examine the human life span relative to extant primates and estimates for early hominids.
Convergence in socioecological characteristics of the primates exhibiting “hyperlongevity” adds support for hypotheses relating adult longevity to cooperative behavior (e.g.,
allomaternal care or cooperative hunting), perhaps through
kin selection.
METHODS AND MATERIALS
Life span records, life history measures, and socioecological variables for 133 species of primates representing all
major taxa form the database (Table 1). Adult female body
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JUDGE AND CAREY
Figure 1. Adult female body mass and life spans for 53 genera of
primates (r ⫽ .817, p ⬍ .001, r2adj ⫽ .660). Regression performed on
genera; symbols indicate superfamilies.
mass was taken from the recent carefully corrected and referenced compilations of Smith and Jungers (23) rather than
the earlier, and reportedly problematic, values of Harvey
and colleagues (21). Life spans were gleaned from a variety
of sources (we began with 21, 24 and updated by using 22
and the primary primate literature). Record life spans are
available for many more species of primates than are life
expectancies. Whereas life expectancy is the result of interactions between organisms and their immediate environment
and strongly reflects exogenous mortality, record life spans
of primates are generally obtained under captive conditions
with good to excellent husbandry and reflect endogenous
mortality. For broadly comparative purposes across taxa,
where it is the underlying rate of aging that is of interest,
record life spans minimize noise that is due to cohort and period effects relative to comparisons based on life expectancy
(25). That record observations are more conservative can be
illustrated by noting that during the Twentieth Century, the
female life expectancy at birth in the United States increased
from 49 to 79 years (⫹61%), whereas the model maximum
increased by less than 7.6% from 105 to 113 (26).
Regressions are performed on the log-transformed values
for record life span, adult female body mass (in kilograms ⫹ 1
to avoid negative log values and to allow comparisons with
recently published work on primate life span), and adult
brain mass. Life span predictions using adult female body
mass differed from those computed using adult female body
mass ⫹ 1 kg by less than 1 year (0.8–1.3 years), and differences in the predictions were not significantly related to
phylogenetic group or to body size. Species specific measures are averaged to obtain estimates for 36 genera of anthropoid primates and 16 genera of prosimians. Using
generic averages reduces bias that is due to sample composition and to the pseudo-independence of species as data points
(27). Conservative human values of a 50-kg female body
mass, 1250-g brain mass, and the 65-year life span derived
from observations of the !Kung people of Botswana (28) are
used in regressions. Predicted life span values are computed
by using the case deletion method—the predicted life span
for each taxon is computed by an equation that excludes its
observed value.
This study expands previous work on relationships of
body mass, brain, and life span by expanding the scope of
species included, avoiding problematic data sources that
have inflated relationships previously reported in the literature, and correcting for phylogenetic nonindependence among
data points while maintaining taxonomic variation. Phylogenetic nonindependence occurs when a data set includes a
large number of values for closely related taxa. Two characteristics may be highly correlated not because they are replicated responses to evolutionary pressures, but because they
co-occur in an ancestor antecedent to all the species included in the analyses. To reduce the likelihood of such spurious correlations, the group phylogeny is used to pinpoint
independent comparisons between sister taxa. Thus, sister
species may provide one comparison point; the average for
their genus may then be compared with that of a sister genus, etc. It is the standardized differences (or contrasts) between variable values for the independent comparisons of
sister taxa that are input into the regression (29). We use the
Comparative Analysis by Independent Contrasts (CAIC)
program developed by Purvis and Rambaut (for a detailed
description of the analytical process, see 30). Rather than
each taxon providing a value in the regression, each contrast
between paired taxa provides one datum. This procedure allows for the assessment of quantitative and dichotomous
traits. The question then is the extent to which contrasts in
states between these paired taxa change together. These regressions of phylogenetically independent contrasts are used
to validate the quantitative relationships of primate body
mass and brain mass to longevity and to place human longevity in a broader quantitative context. The CAIC program
provides phylogenetically controlled assessments of trait correlations but is not used directly in predictive computations.
For this reason, human life span predictions are derived
based on 53 primate genera, 36 genera of catarrhine primates, and the six genera of apes, respectively.
There is a lack of consensus regarding the appropriate regression models for allometric comparisons (e.g., 27, 31).
We have used least-squares regression because it produces
residuals that are intuitively sensible and will produce a
conservative estimate of predicted values for large-bodied
species (including humans). Predicted life span values are
the adjusted predictions—those values predicted when the
data point (in this case the genus) is excluded from the
equation. Human life span predictions based on adult female body mass and brain mass from anthropoid, catarrhine, and hominoid reference groups are presented. Regressions were performed by using SPSS for Windows
programs.
RESULTS
Body Size Life Span Predictions
The adjusted predicted human life span (when humans are
excluded from building the equation), as derived from linear
POSTREPRODUCTIVE LIFE PREDICTED BY PRIMATE PATTERNS
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Table 1. Average Life Spans, Adult Female Body Masses, and Brain Masses for Primate Genera
Mass
Infraorder
Family
Genus
Life Span (y)*
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Prosimii
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Platyrrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Catarrhini
Loridae
Loridae
Loridae
Loridae
Galagonidae
Galagonidae
Lemuridae
Lemuridae
Lemuridae
Lemuridae
Megaladapidae
Cheirogaleidae
Cheirogaleidae
Cheirogaleidae
Indridae
Daubentoniidae
Tarsiidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Callimiconidae
Callithricidae
Callithricidae
Callithricidae
Callithricidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Hylobatidae
Hylobatidae
Pongidae
Pongidae
Pongidae
Hominidae
Arctocebus
Loris
Nycticebus
Perodicticus
Galago
Otolemur
Eulemur
Hapalemur
Lemur
Varecia
Lepilemur
Phaner
Cheirogaleus
Microcebus
Propithecus
Daubentonia
Tarsius
Alouatta
Aotus
Ateles
Brachyteles
Cacajao
Callicebus
Cebus
Chiropotes
Lagothrix
Pithecia
Saimiri
Callimico
Callithrix
Cebuella
Leontopithecus
Saguinus
Allenopithecus
Cercocebus
Cercopithecus
Colobus
Erythrocebus
Macaca
Mandrillus
Miopithecus
Nasalis
Papio
Presbytis
Pygathrix
Theropithecus
Trachypithecus
Hylobates
Symphalangus
Gorilla
Pan
Pongo
Homo
13.0
15.0
20.0
26.0
14.6
15.0
27.8
12.4
28.7
19.0
12.0
12.0
16.4
14.1
19.1
23.3
12.5
22.4
22.5
33.2
30.0
20.1
25.3
45.9
17.5
30.0
19.6
21.0
17.9
16.2
18.1
24.7
15.8
23.0
26.5
25.4
27.3
23.9
28.9
39.2
30.9
21.0
33.4
20.0
25.0
28.0
26.1
35.6
38.0
54.0
53.4
58.7
65.0
Female
(kg)†
0.31
0.19
0.49
0.84
0.24
0.73
1.8
1.1
2.2
3.51
0.62
0.46
0.3
0.1
4.3
2.5
0.11
5.3
0.9
8.2
8.1
2.8
0.9
2.5
2.5
7.0
2.0
0.7
0.5
0.4
0.1
0.6
0.5
3.2
5.7
3.2
8.1
6.5
6.4
12.7
1.1
9.8
12.4
7.4
8.4
11.7
6.0
5.9
10.7
71.5
33.5
35.8
50.0
Brain (g)‡
7.7
6.7
10.0
14.3
5.6
N/A
24.1
11.8
25.6
34.2
9.5
7.3
4.1
1.8
31.9
45.2
3.9
56.6
18.2
110.5
120.1
73.3
19.0
78.1
53.0
96.4
34.8
24.4
10.8
7.9
4.2
12.9
9.6
62.5
107.6
69.8
79.5
106.6
89.2
156.0
37.7
94.2
171.8
104.0
108.5
131.9
65.5
115.2
121.7
505.9
410.3
413.3
1250.0
*Life spans are generally captive life spans and were taken from Harvey and colleagues (21) and then updated according to various sources cited in Rowe
(24) and from Hakeem and colleagues (22).
†Original adult female body masses are from Smith and Jungers (23); means are the back-transformed mean log masses for species within each genus.
‡Original brain masses from Harvey and colleagues (21) and Rowe (24).
regressions of log-transformed life span and adult female
body weights (⫹ 1 kg) of 53 primate genera, is 51 years:
log 10 L = 1.175 + 0.317 ( log 10 M ),
(1)
where L is the longest observed life span in years and M is
the adult female body mass ⫹ 1 k (r ⫽ .817, n ⫽ 53 genera;
p ⬍ .001, r2adj ⫽ .660). Cebus, a genus of New World monkey, is the only statistical outlier in the sample (Figure 1).
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JUDGE AND CAREY
Excluding the prosimians, which Martin (32) argued represent a significantly different evolutionary trajectory, results in the following relationship:
log 10 L = 1.235 + 0.267 [ log 10 ( M ) ]
(2)
and decreases the adjusted human life span prediction to 47
years (r ⫽ .771, n ⫽ 36 genera; p ⬍ .001, r2adj ⫽ .582). Curiously, this equation for anthropoid genera is almost exactly the same as that derived by Austad and Fischer (2) for
77 species of primates including the prosimians. Excluding
the prosimians results in the expected increased intercept
and decreased slope (Figure 2). The relationship of life span
and body mass in anthropoid primates predicts a life span
that is roughly equal to the age by which most extant human
females experience menopause and exceeds the age of noticeable fertility decline (33). The adult female body masses
of anthropoid primate genera are positively correlated with
life span when phylogenetic relationships are controlled, although r is somewhat reduced (r ⫽ .540, p ⫽ .007).
With the standard human values noted above, residual
life spans are longer for Cebus monkeys than for humans.
The ratio of observed to the adjusted expected in Cebus is 2;
a roughly equivalent human average would be 94 years. The
Cebus weigh 2–4 kg, and there are multiple records of these
monkeys living well over 40 years. New World monkeys
have evolved independently of the hominid lineage for approximately 45 million years, indicating that the evolution
of hyperlongevity in Cebus is independent of that in the
hominid line. The earliest fossils that may distinguish Cebus
from its sister genus Saimiri date from approximately
10,000 years ago, and yet Cebus are the most widespread
genus of New World monkeys (34).
Incorporating Brain Size Into Predictions
Primate brain size is correlated with body size and with
longevity. The relationships between anthropoid body and
brain mass (Figure 3; independent contrasts r ⫽ .711, p ⬍
.001) and between brain mass and longevity (Figure 4; independent contrasts r ⫽ .661, p ⬍ .001) are sustained when
Figure 2. Adult female body mass and life spans for 36 genera of
anthropoid primates (r ⫽ .771, p ⬍ .001, r2adj ⫽ .582).
Figure 3. Adult brain mass and body mass for 36 genera of anthropoid primates.
phylogenetic relationships are controlled. Using the most
recently available body mass and life span data, and controlling for the effects of adult female body mass and congeneric data points, we find only a trend of relationship between relative brain mass and relative life span among
anthropoid genera (Figure 5):
LS = 0.0018 + 0.193 ( RB )
(3)
(LS and RB are the adjusted residual life spans and brain
masses, respectively, after body mass is controlled; n ⫽ 36,
r2adj ⫽ .075, p ⫽ .058). The largest deviation between the
observed and adjusted predicted brain size occurs in Cebus
monkeys. The observed brain size is more than twice the expected; the conservative human value of 1250 g is 1.92
times larger than that predicted by body size. A 1396-g human brain would equal the Cebus’ encephalization quotient
(ratio of observed to predicted brain mass)—a not unusual
human brain mass. Miopithecus has the largest relative brain
size and an unusual longevity for an Old World monkey.
Incorporating brain mass into the equation predicting life
span results in a multivariate relationship:
Figure 4. Anthropoid primate life span by log brain mass.
POSTREPRODUCTIVE LIFE PREDICTED BY PRIMATE PATTERNS
Figure 5. Residual values of adult brain weight regressed on adult
female body weight and of life span regressed on adult body weight
for 34 genera of anthropoid primates (n ⫽ 36, r2adj ⫽ .075, p ⫽ .058).
The resulting values indicate the relationship of brain and life span
after that portion explained by body weight is excluded.
log 10 L = 1.037 + 0.045 ( log 10 M ) + 0.202B,
(4)
where L and M are defined as above and B is the brain mass
in grams ( p ⱕ .001, r2adj ⫽ .615). This results in an extension of the adjusted predicted human life span to 52.4 years.
Responding to the colinearity of brain and body mass, we
regressed life span on body mass and the encephalization
quotient (EQ)
log 10 L = 1.235 + 0.267 ( log 10 M ) + 0.180 EQ
t = 7.333, 1.907
p = ⬍.001, .065
(5)
n⫽ 36 genera, r2adj ⫽ .613, p ⬍ .001), yielding in an adjusted predicted human life span of 52.7 years. The leastsquares method produces a conservative estimate of the
slope. When phylogeny is controlled, brain mass is a stronger predictor of life span than is body size (contrast for body
mass b ⫽ 0.066, T ⫽ 0.766, p ⫽ .449; contrast for brain
mass b ⫽ 0.193, T ⫽ 3.043, p ⫽ .005). It is clear that New
World monkeys predominate in the lower end of the mass
range and Old World groups in the upper end. Excluding the
New World genera yields the following equation:
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Figure 6. Observed and predicted life spans (by body weight and
relative brain size; case deletion) for 20 genera of Old World primates.
(n ⫽ 6 genera, r2adj ⫽ .900, p ⫽ .015) and an adjusted predicted human life span of 82.3 years (Figure 7). Given human phylogenetic history, adult female body mass, and
brain mass, a life span of 72 or more years is not exceptional, and life spans of nine to ten decades under good conditions are predicted.
DISCUSSION
The lowest predicted human life span (52 years) exceeds
the observed life spans of other great apes and the period of
severely reduced fertility in apes and humans (33). The predictions generated from catarrhine primates exceed the age
of menopause in extant women by at least 20 years; they
also exceed the observed longevity of extant hunter–gatherers (often assumed to reflect “premodern” potential). This
suggests that a life span exceeding that of the female reproductive system is part of a phylogenetic legacy rather than a
modern development related to uniquely human cultural innovations. Although this contradicts the idea that postreproductive life span is an artifact of modern cultural conven-
log 10 L = 0.701 – 0.049 ( log 10 M ) + 0.402 ( log 10 B )
t = – 0.318 , 2.476
(6)
p = .755, .024
for the relationship between body and brain mass for catarrhine primates (n ⫽ 20 genera of Old World monkeys and
apes; r2adj ⫽ .679, p ⬍ .001). The predicted human life span
is 72 years and the adjusted prediction for human life span
is 91 years (Figure 6). Including only the apes to generate
the relationship yields the following relationship:
log 10 L = 1.104 + 0.072 ( log 10 M ) + 0.193 ( log 10 B )
t = 0.871, 2.355
(7)
p = ⬍.001, .065
Figure 7. Observed lifespan of Hominoidea (n ⫽ 6 genera) by
body and brain mass predicted life span (case deletion).
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JUDGE AND CAREY
tions, it does not address whether selection proceeded to
reduce reproductive life span (i.e., the evolution of early reproductive cessation; 11, 19) or to extend life span beyond
some set reproductive limit.
The great apes have absolutely long lives and exceed the
life span expected by body and brain size. However, the
closest relatives of humans (Gorilla and Pan) are exceeded
in their positive deviation from the expected by five other
catarrhine genera (see Table 2), and no Old World nonhuman genus approaches the positive deviation from expected
life span demonstrated by the New World monkeys of the
genus Cebus. Cebus exhibit life spans that rival those of
chimpanzees, even though chimp females are roughly 15
times larger. The 23-year Cebus life span predicted by body
size alone is extended to only 25 years (a 9% increase)
when brain size is incorporated, which underestimates Cebus longevity by more than 20 years. Cebus are the most
geographically widespread of New World monkeys and
show convergent evolution in social structure to Old World
monkeys (35). They have a fruit-based diet with a heavy
meat component obtained through predation on both invertebrates and vertebrates (36).
Contrary to the hypothesis that capacity for prolonged
life span should evolve where exogenous mortality is low
(2, 37), Cebus monkeys are important prey to human and
avian predators (38, 39). As frugivores/omnivores, Cebus
exploit food sources that juveniles require time to learn to
find, capture, and process—a trait that has been associated
with slower than expected juvenile growth patterns (40).
However, when food sources require experience to find and/
or manipulate (41), prolonged dietary subsidization from
older (related) group members may be selectively advantageous. This is central to one formulation of the “grandmother hypothesis” (see, e.g., 14, 42). Recent findings that
Cebus are cooperative hunters of vertebrate prey (36) both
adds to the benefits that might accrue to younger animals
from sharing by older group members and underscores the
benefits of age and experience in successful foraging.
Generally, mammalian females live longer than conspecific males. Allman and colleagues (43) suggested that primates with predominantly paternal care exhibited a male
survival advantage. Unfortunately, the number of species
for which sex-specific survivorship is available is small.
Several of the species documented are closely related phylogenetically, and male parental care appears more to be associated with no difference between the sexes rather than
male-biased survivorship (only the Owl monkey—Aotus—
showed a statistically significant male advantage). Additionally, the effects of paternal care were not separated from
those of reduced male–male competition in monogamous
mating systems. These authors note that they have not taken
into account cooperative interactions among caregivers of
the same sex (43; p. 6868).
Cebus social organization is based on philopatric (and
therefore related) females, their offspring, and one or few
immigrant adult males. Though numbers of resident adult
males may vary, females in larger groups have higher reproductive success than females in smaller groups. Researchers
have reported allomaternal nursing in wild Cebus; other
(unrelated and sometimes juvenile) female members of the
Table 2. Residual Life Span After Adult Female Body and Adult
Brain Masses Are Included In the Predictive Equation
Residuals
Family
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Callimiconidae
Callithricidae
Callithricidae
Callithricidae
Callithricidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Hylobatidae
Hylobatidae
Pongidae
Pongidae
Pongidae
Hominidae
Genus
Anthropoid*
Catarrhine†
Hominoid‡
Alouatta
Aotus
Ateles
Brachyteles
Cacajao
Callicebus
Cebus
Chiropotes
Lagothrix
Pithecia
Saimiri
Callimico
Callithrix
Cebuella
Leontopithecus
Saguinus
Allenopithecus
Cercocebus
Cercopithecus
Colobus
Erythrocebus
Macaca
Mandrillus
Miopithecus
Nasalis
Papio
Presbytis
Pygathrix
Theropithecus
Trachypithecus
Hylobates
Symphalangus
Pongo
Gorilla
Pan
Homo
⫺0.08123
0.05048
0.02908
⫺0.02342
⫺0.14850
0.09943
0.25944
⫺0.17510
⫺0.00154
⫺0.07956
0.11588
⫺0.00185
⫺0.02044
0.13018
0.13314
⫺0.05271
⫺0.06752
⫺0.06182
⫺0.03273
⫺0.03119
⫺0.11020
⫺0.01003
0.06425
0.13786
⫺0.17216
⫺0.01670
⫺0.19087
⫺0.09790
⫺0.07253
⫺0.02720
0.06573
0.07544
0.10654
0.10460
0.15096
0.09132
⫺0.03353
⫺0.05732
⫺0.00733
0.02374
⫺0.09969
0.02135
0.07199
0.23377
⫺0.13881
⫺0.02040
⫺0.17373
⫺0.07636
⫺0.05423
0.03346
0.07174
0.10147
0.06264
0.06231
0.11192
⫺0.14434
⫺0.0316
⫺0.0065
⫺0.0857
0.01
0.0586
⫺0.1024
*Deleted residuals calculated from an equation including all anthropoid
primate genera; n ⫽ 36.
†Deleted residuals calculated from an equation including only the Old
World monkeys and apes; n ⫽ 20 genera.
‡Deleted residuals calculated from an equation including only the apes;
n ⫽ 6 genera.
group sometimes suckle from lactating females (44, 45). Although Cebus are not cooperative breeders in the sense of
the delayed reproduction and carrying behavior of the Callitrichidae, they do cooperate facultatively. Convergences of
Cebus and Homo in extreme relative longevity suggest the
importance of further research on the interactions of older
Cebus females with their daughters and other females as well
as detailed information on late life ovarian function. Postreproductive periods that are two standard deviations greater
than an average interbirth interval for the majority of females
were documented only in humans and chimps; however, Cebus were not one of the 14 species examined (33).
The observed hunter–gatherer life span used herein underperforms the expected. Based on catarrhine primate patterns, human life spans into the tenth decade are within a
reasonable range of observed life spans based on weight and
POSTREPRODUCTIVE LIFE PREDICTED BY PRIMATE PATTERNS
B207
Figure 8. Open ovals, rectangles, and triangles are longevity estimates based on anthropoid subfamily values for body and brain mass regressions; filled ovals, rectangles, and triangles are based on extant hominoid values adapted from Hammer and Foley (48). Open cups are estimates
from hominoid body and brain regressions and closed cups are based on catarrhines body and brain mass regressions (this paper).
brain size. No matter which regressions are used, extant
traditional human life spans do not exceed the relative divergence above the expected of at least one other phylogenetically independent genus. The 105-year-old maximum
observed in a sample of 1,000 obituaries in contemporary
Los Angeles (22) is remarkably close to what would be expected based on the primate patterns (where the number of
observations are roughly the same order of magnitude).
Humans are survivors of a much richer assemblage of
hominid species that existed as recently as 2 million years
ago, and more precise estimates might be derived from trajectories of hominid ancestors than from extant anthropoids.
McHenry (46) inferred life span from estimates of body size
by using relationships between bone measures and body
size in extant hominoids (Great Apes) to infer the body
weights of ancestral hominids. This procedure yields estimates of female body weight in Australopithecus (3 and 4
million years ago) between 29 and 34 kg (male 40–48 kg),
and the use of published body weight and life span relationships for primate subfamilies (5) yields a life span of 42–44
years. For Homo habilis (2.4–1.6 million years ago) McHenry
estimated a 43-year life span. Female body weight in Homo
erectus (1.7–0.7 million years ago), is estimated to have increased to 52 kg while sexual size dimorphism decreased
(males ⫽ 63 kg), and life span based on body size is estimated at 50 years (47). We have found that using the body
masses from Smith and Jungers (23) reduces the estimated
life spans somewhat.
Hammer and Foley (48) incorporated body and raw brain
size estimates from fossil crania to predict early hominid
longevity, using a multivariate OLS regression of the log
body weight and brain volume (Figure 8). Estimates based
on regressions of anthropoid primate subfamilies (5) or limited to extant apes indicate a major increase in longevity
from the 52–56 years of H habilis to the 60–63 years for H
erectus between roughly 1.7 and 2 million years ago. Their
predicted life span for small-bodied H sapiens is 66–72
years. From a catarrhine comparison group, our prediction
is 72 years (91 years when H sapiens is excluded from the
predicting equation).
For early hominids to live as long or longer than predicted was probably extremely rare; the important point is
that the basic catarrhine design resulted in a primate with
the potential to survive long beyond a mother’s ability to
birth young. Notably, Hammer and Foley’s predicted life
span of H habilis exceeds the age of menopause in extant
women by only 7 to 11 years, whereas that of H erectus exceeds menopause by 15–18 years. This suggests that postmenopausal survival is not an artifact of modern life style
(49) but may have originated between 1 and 2 million years
ago, coincident with the radiation of hominids out of Africa.
This lends support to Hawkes and colleagues’ earliest posited timing of the evolution of postreproductive life (14).
The rapid increase in longevity noted in H erectus is interesting in light of suggestions that H erectus but not H habilis is more likely closer related to H sapiens than to the australopiths (50).
Evolutionarily significant human data are mixed. Paleodemographic studies of small samples of human remains report very few individuals surviving to old age, whereas data
on contemporary hunter–gatherers consistently indicate the
presence of adults of 65⫹ years of age, even in habitats that
are clearly marginal (e.g., 28). Twenty-five percent of adult
Ache women survive to 70 years (51), and among other
South American groups, 18% (Yanomamo) to 22% (Hiwi)
of adult women exceed 65 years (42). Hawkes and colleagues (13) demonstrate that the product of Hadza grandmothers’ gathering subsidizes the weight gain of grandchil-
B208
JUDGE AND CAREY
dren between weaning and adolescence (when primate young
are most vulnerable to starvation). The grandmother’s inclusive fitness is increased during a time when she is no longer
able to successfully reproduce herself. This new formulation is important because it takes cessation of reproduction
(menopause) as a hominoid given and attempts to explain
selection for prolonged longevity by means of kin selection.
Kaplan (42) has demonstrated quantitatively that in contrast
to adolescents, “old” individuals of both sexes in several
traditional hunter–gatherer and horticultural groups are net
resource providers. Although it is possible that extant “traditional” groups are unreliable demographic models for
early hominid populations, it is also possible that archeological studies are less likely to retrieve the fossil remains of
the most frail individuals—those most likely to die while
migrating or otherwise absent from a base camp.
Centenarian humans are not out of the scope of primate
longevity, especially given the large numbers of human observations (i.e., high numbers increase the probability of sampling the extreme right tail of the distribution). This suggests
that life spans beyond the age of human female menopause
are not necessarily artifacts of modern lifestyles. Furthermore, Cebus monkeys exhibit relative life span potentials
similar to humans and are convergent in traits such as a relatively large brain, generalized ability to exploit a wide range
of ecological niches over a broad geographical distribution,
fruit-based diet with cooperative hunting of vertebrate prey,
and polygynous mating systems. Whether human ancestors
were male or female philopatric is unresolved. If human ancestors had the potential for 72-year life spans and postreproductive life for 1–2 million years, one might wonder why
prolonging the life span to 100 years under modern conditions of ecological release has not been easier.
Acknowledgments
We thank Drs. Alexander Harcourt, Sarah Blaffer Hrdy, Henry
McHenry and Kelly Stewart for discussion and comments on earlier drafts
of the manuscript. Three anonymous reviewers provided comments and
questions that improved the manuscript. Our thanks to Dr. Andy Purvis, Department of Biology, Imperial College at Silwood Park for the primate phylogeny used by the CAIC program. This research was supported by Grant
AG-08761 from the National Institute of Aging.
Address correspondence to D. S. Judge, Department of Anthropology,
University of California at Davis, Davis, CA 95616. E-mail: dsjudge@
ucdavis.edu
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Received February 3, 1999
Accepted September 17, 1999
Decision Editor: Jay Roberts, PhD