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Primate longevity Its place in the mammalian scheme.

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American Journal of Primatology 28:251-261 (1992)
Primate Longevity: Its Place in the Mammalian Scheme
STEVEN N. AUSTAD’
AND
KATHLEEN E. FISCHER’
Harvard University,’ Department of Organismic and Evolutionary Biology, and ‘Department
of Organismic and Evolutionary Biology, The Biological Laboratories, Harvard University,
and Department of Anthropology, The Peabody Museum, Cambridge, Massachusetts
Data on captive longevity in 587 mammalian species were analyzed in
order to evaluate primate longevity in the context of general mammalian
life history patterns. Contrary to some recurrent claims in the literature,
we found that 1) primates are not the longest-lived mammalian order,
either by absolute longevity, longevity corrected for body size, or metabolic
expenditure per lifetime; 2) although relative brain size is highly correlated with longevity in primates, this is a n aberrant trend for mammals in
general, and other body organs account for a n even greater amount of
variation in longevity; and 3) there has been no progressive evolution of
increased longevity among the primate superfamilies. The exceptional
magnitude of primate longevity may, in keeping with evolutionary senescence theory, be due to a n evolutionary history of low vulnerability to
environmentally imposed death due to their body size, arboreal habit, and
propensity to live in social groups. 0 1992 Wiley-Liss, Inc.
Key words: longevity, b o d y size, brain size, evolution, metabolism
INTRODUCTION
The exceptional longevity of primates, especially humans, relative to other
mammals has had a major impact on scientific thought concerning the determinant(s) of animal life span [Sacher, 1959, 1975; Cutler, 1975, 19761. For instance,
primate longevity has contributed to the notion that brain size (or some specific
component of brain size such as cortex size or cerebro-cortical surface) and longevity are causally related [Sacher, 1959, 1975; Cutler, 1975; Mallouk, 1975; Weiss,
1981; Hofman, 19831. Second, it has been stated that primates exhibit a greater
energetic expenditure per unit body mass per lifetime than other mammals, and
this energetic longevity reflects greater metabolic efficiency [Cutler, 19781. Finally, it is commonly stated life span has been increasing through evolutionary
time [Schultz, 1969; Cutler, 1975; Bowden & Jones, 1979; Lovejoy, 1981; Hofman,
1984; Napier & Napier, 19851. These ideas arose primarily from the analysis of the
allometric relationship between a size variable (e.g., body mass, brain mass) and
maximum captive longevity for a species.
. Maximum captive longevity is likely to reveal a n important aspect of the rate
Received for publication May 11, 1992; revision accepted July 4, 1992.
Steven N. Austads current address is: Department of Biological Science, University of Idaho, Moscow,
ID 83843.Send reprint requests to him there.
0 1992 Wiley-Liss, Inc.
252 I Austad and Fischer
of aging, because it presumably reflects how long individuals can survive under
optimal conditions before dying due to senescence. The study of captive longevity
is therefore an indirect manner of studying aging.
We can see the importance of the first two aspects of primate longevity in
relation to general theories of aging, if we consider several of the historically
important theories. An enormously influential general theory of aging has been
the rate-of-living theory [Rubner, 1908; Pearl, 19281. Briefly, this idea posits that
an organism’s life span depends upon a genetically determined metabolic potential
and the rate at which that potential is expended. In its strong form, this notion
holds that related species, such as birds or mammals, have similar metabolic
potentials and consequently the diversity of life spans could be largely explained
by differences in metabolic rate [Sacher, 1959; Lindstedt & Calder, 19761. In its
more modern, weaker form, the theory holds that aging is an ineluctable consequence of imperfect physiochemical processes which ultimately lead to failure of
cellular constituents due to the accumulation of biochemical errors or to the gradual buildup of toxic metabolic byproducts [Sohal, 19761. However a major prediction of the theory remains that other things being equal, organisms with low
metabolic rates should outlive organisms with high metabolic rates. It is well
known that there is a general trend for maximum life span to allometrically increase, and mass-specific metabolic rate to allometrically decrease, with body size
among mammals [e.g., Sacher, 1959; Lindstedt & Calder, 1981; Calder, 19841. In
combination these trends tend to support the rate-of-living theory.
The idea that primates reputedly expend greater metabolic energy than other
mammals has led to the speculation that they are a special case among mammals
with some generalized physiological superiority, and that some unique primate
characteristic besides metabolic rate was causally related to this physiological
superiority [Sacher, 1959, 1975; Cutler, 1975; Mallouk, 1975; Weiss, 1981; Hofman, 19831. One glaringly obvious difference between primates and the rest of
mammals is their relative large brain size. Hence brain size was a prime candidate
for the source of primate longevity. A relatively large brain has been hypothesized
to confer longevity either because of the improved precision of physiological homeostasis it putatively mediates [Sacher, 19591, some substance vital to tissue
repair it secretes [Mallouk, 19751, or its specialized metabolic demands [Hofman,
19831. This theory would predict that if there has been a progressive evolutionary
increase in brain size, there would also be a progressive increase in life span.
A competing general theory is evolutionary aging, or senescence, theory
[Medawar, 1952; Williams, 19571. Evolutionary senescence theory attributes aging
to the declining strength of natural selection a t successive ages after sexual maturity. According to this idea, the power of natural selection to favor advantageous
alleles, or eliminate disadvantageous ones, wanes with the age a t which these
alleles are expressed. The waning of selection is due to environmental hazards
which dictate the probability that an animal will be alive at the time the trait is
expressed. Aging, then, is the genetic consequence of a) the accumulation of lateacting deleterious alleles which are nearly selectively neutral in their effects, and
b) positive selection for alleles with beneficial early-acting effects and deleterious
late-acting effects. This second mechanism has been called negative or antagonistic pleiotropy and could be manifested in traits, for instance, that favor a rapid rate
of early reproduction at the expense of later survival [Williams, 19571.
It is important to note that the rate at which natural selection declines with
age will be related to the degree of environmental hazard, i.e., the probability of
death which is unrelated to aging. Note also that this theory is one of physiological
design optimization, such that organisms may be engineered t o reproduce rapidly
Primate Longevity I 253
but not endure very long or the reverse. In any case, organisms’ aging rate should
be related t o their ecological history and the trade-offs between early and late
fitness. With respect to primates, evolutionary senescence theory suggests that
their exceptional life spans would be due t o an evolutionary history of low environmental hazard and slow early reproduction, and that other mammal groups
with similar histories should also exhibit exceptional longevity. Also according to
this theory, there is no reason to expect a progressive evolutionary increase in
longevity in any group.
In this study we will assess primate longevity, lifetime metabolic expenditure,
and relative brain size in light of the overall mammalian patterns. Previous studies on general patterns of mammalian life span have been performed using relatively few of the more than 4,300 species of extant mammals and approximately
180 living primate species [Corbet & Hill, 19911. Currently, data from many more
species are available. In addition, improved husbandry and record keeping in zoos
have substantially increased maximum longevity for less commonly kept species.
Analyses of more extensive data sets have overturned some of the conventional
wisdom from the past already [Prothero & Jurgens, 1987; Austad & Fischer, 19911
and we feel such an analysis is timely
MATERIALS AND METHODS
Our data base consists of body mass and maximum recorded longevity for 587
mammalian species, including 77 primates, gathered from standard secondary
sources [Anonymous, 1960; Flower, 1931; Crandall, 1964; Haltenorth & Diller,
1977;Jones, 1982; Nowak & Paradiso, 1983; Harvey et al., 19861,supplemented by
material from the primary literature and by personal correspondence with zoo
personnel, field biologists, and veterinarians. When several records of maximum
longevity were found, we selected the longest.
Nearly all the longevity data derive from captive populations with the exception of the bats, for which 82% (41150) of our species information comes from the
maximum recapture interval of individuals from banded wild populations. The
accuracy with which mark and recapture data reflects actual maximum longevity
of bats in the wild will depend upon banding intensity and the frequency of capture
attempts as well as on the length of the study. Consequently bat longevity is
probably substantially underestimated in all species studied only in the wild.
The data base does not represent all species for which information was available. Maximum captive longevity is likely to be misleadingly short if husbandry
techniques are inadequately developed. Therefore we did not use available data for
a species if we knew that a) breeding attempts in captivity had not been successful,
b) greater than 50%of individuals died during their first year in captivity, or c) the
author indicated that life span was probably shortened by captivity. Furthermore,
because maximum longevity will be strongly influenced by sample size a t small
numbers, we deleted species for which the sample of prospective life spans was
known to be less than ten.
Body mass was determined in several ways. Field measurements of body mass
always took priority over captive data if both were available. If only body mass
ranges were given, we used the arithmetic mean of those values. In highly sexually
dimorphic species, we used the arithmetic mean of male and female body mass. If
only maximum body mass was reported, we used 55% of that value, a convention
used by Prothero and Jurgens 119871 after finding it to be the ratio of mean to
maximum body mass reported for the Asian elephant.
McNab [1988] has compiled data on basal metabolic rate for 321 species, and
we added to this information on 18 additional species from the primary literature.
254 I Austad and Fischer
Both maximum life span and basal metabolic rate were available for 164 species.
Primate brain sizes are from Harvey, Martin, and Clutton-Brock [19871, and other
brain sizes are from Eisenberg 119811, Crile and Quiring 119401, and Pirlot and
Stephan 119701. Data on the mass of other body organs (spleen, liver, kidney, and
heart) are from Crile and Quiring 119401.
Using species as independent data points can confound analyses [Pagel and
Harvey 19881. Well-studied taxa, or those with many species, can dominate a
sample and bias the analyses. To prevent our sample from being dominated by
particular taxa for which many data points were available (e.g., Rodentia), we used
nested mean values for all higher level comparisons. That is, order means were
calculated from family means which were calculated from genus means which
were, in turn, calculated from species values. Taxonomy is from Corbet and Hill
[1991], and statistical analyses from Wilkinson [19901.
RESULTS
It is well known that mammalian longevity increases with body size [e.g.,
Rubner, 1908; Sacher, 19591. Our previous work, using LOWESS regression (robust locally-weighted sum of the squares, a statistical technique that reveals the
shape of the relationship between two variables by using the weighted average of
nearby values of the dependent variable to calculate expected values [Cleveland,
1979, 198111, has indicated that if all our species are included, the relationship
between the logarithms of body mass and maximum longevity is not even approximately linear. However, if bats and marsupials are deleted, the relationship becomes surprisingly linear [total 463 species, Austad & Fischer, 19911. The resulting regression line can be considered to yield the “expected longevity” for a
mammal of a particular body size. We call the ratio of actual to expected longevity
and longevity quotient (LQ),which gives the intuitively satisfying proportion of an
“average” mammal’s longevity which the species in question exhibits. LQ in our
data ranges from 0.14 (Australian water rat) to 5.39 (little brown bat).
Life Span of Primates Relative to Other Mammals
Primates are clearly among the longest-lived mammals. They exhibit the
fourth highest absolute longevity among the eighteen mammalian orders examined, and the third highest LQ (Table I). They are also clearly not the longest-lived
mammals for their body size. They are surpassed in this respect by the monotremes
(echnidas and duck-billed platypus) and the bats. Contrary to past assumptions
[e.g., Sacher, 19591,the tendency to hibernate or enter daily torpor is not correlated
with exceptionally long life among mammals, as shown by the fact that nonhibernating bats and marsupials are equally long-lived as related species that do not
hibernate or enter torpor [Jiirgens & Prothero, 1987; Austad & Fischer, 19911.
Multiplying mass-specific basal metabolic rate times maximum longevity
yields lifetime basal energy expenditure-a quantity which has been hypothesized
to be approximately constant throughout the mammals [Rubner, 1908; Sacher,
1959; Stahl, 1962; Cutler, 19761. Primates have the second highest lifetime energetic expenditure by this measure, but it is still significantly less than that of bats
= 0.02).
(Table I) (Tll = 2.297, Pone-tail
Organ Size and Longevity in Primates and Other Mammals
Primates have exceptionally large brains for their body size [Jerison, 19731,
and brain size has been implicated in their longevity [Sacher, 1959, 1975; Mallouk
1975; Cutler, 1976; Hofman, 19841. A convenient measure of brain size, corrected
for body size, is encephalization quotient (EQ), or the ratio of actual brain size to
Primate Longevity I 255
TABLE I. Mean Maximum Longevity, and Longevity Quotient (LQ), Encephalization
Quotient (EQ),and Lifetime Energy Expenditure (LEE) for 18 Mammalian Orders
[Taxonomy based on Corbet & Hill,19911
Order
Chiroptera
(bats)
Monotremata
(monotremes)
Primata
(monkeys & apes)
Dermoptera
(flying ‘‘lemurs”)
Edentata
(edentates)
Scandentia
(tree shrews)
Proboscidea
(elephants)
Carnivora
(carnivores)
Artiodactyla
(even-toed ungulates)
Tubulidentata
(aardvark)
Perissodactyla
(odd-toed ungulates)
Rodentia
(rodents)
Hyracoidea
(hyraxes)
Marsupialia
(marsupials)
Lagomorpha
(rabbits, hares)
Insectivora
(insectivores)
Pholidota
(pangolins)
Macroscelidea
(elephant-shrews)
Number of
species
Maximum
longevity (yr)
LQ
EQ
LEE
(kcal/g/life)
50
14.9
2.75
0.94
602
3
32.6
2.41
0.83
228
77
27.9
1.92
2.54
420
1
17.5
1.56
-
-
9
21.4
1.44
0.95
171
2
12.0
1.44
1.34
397
2
64.5
1.36
1.59
-
109
21.4
1.07
1.22
283
92
22.0
0.84
0.84
209
1
24.2
1.06
-
130
12
36.7
0.96
0.92
-
131
10.0
0.95
0.99
250
3
12.1
0.92
0.90
200
67
10.1
0.88
0.61
149
7
8.1
0.85
0.62
241
14
6.2
0.79
0.55
228
1
13.1
0.72
-
-
6
4.1
0.62
-
87
that expected from the general relation between mammalian body size and brain
size [Jerison, 19731.
The most complete analysis of the mammalian brain size-body size relation
was by Eisenberg and Redford, who assembled data on 547 mammalian species in
similar relative proportion to that actually represented among taxonomic orders
[Eisenberg, 19811. Using their formulation for EQ, we find that primates have by
far the largest brains among mammals (Table I). Furthermore, in primates EQ is
indeed significantly related to both maximum longevity (r = 0.656, N = 73, P <
< 0.001) and LQ (r = 0.621, P < < O.OOl), although this relationship explains less
than half of the variation and is highly leveraged by the outlying values for the
Hominoidea. The nonhominoid relationship remains statistically significant, but
256 I Austad and Fischer
TABLE 11. Correlations Between Encephalization Quotient (EQ) and Two Measures of
Longevity-Maximum Longevity and Longevity Quotient (LQ).P Values are Corrected
by a Sequential Bonferroni Technique for Simultaneous Tests [Rice, 19891.
Order
Artiodactla
Carnivora
Chiroptera
Insectivora
Marsupialia
Primata
Rodentia
EQ-LQ
Correlation (Pearson’s r)
EQ-maximum longevity
N
-0.512
-0.052
-0.125
-0.085
-0.097
0.621***
0.371
-0.672*
-0.438
0.066
-0.174
-0.329
0.656***
0.049
21
33
23
12
24
73
39
*P < 0.05.
***P << 0.0001.
is even looser (r = 0.506, N = 69, P < 0.001 and r = 0.478, P < 0.001, respectively).
On the other hand, primates are rather unusual in this relationship. Among
the seven other mammalian orders for which we have a reasonably sizable sample
(N 2 12), no other order has a similarly significant positive relationship between
EQ and LQ or EQ and maximum longevity, in fact most of the correlations are
negative, and the only other significant correlation ( A ~ t i o d ~ c t yisZ a~negative
)
one
(Table 11). Moreover, the mammalian groups with the highest LQs, monotremes
and bats, have EQs below the general mammalian average (mean = 0.83, N = 2
and mean = 0.85, N = 22, respectively). In fact, there is no correlation between
EQ and maximum longevity (r = 0.452, N = 14, P = 0.105) or LQ (r = 0.335, P
= 0.335) for the mammalian orders generally, or for all the nonprimate species
when considered individually (EQ-LQ, r = -0.002, N = 158, P = .998; EQmaximum longevity, r = 0.047, P = 562).
A second point is that other organ weights are also correlated with longevity
(Table 111). In fact in our data for nonprimate species, heart, liver, kidney, and
spleen sizes all show a stronger correlation with maximum longevity (or its logarithm) than does brain size.
Progressive Lengthening of Life in Primates
Do primates exhibit increased longevity throughout their history, as exemplified by extant forms that are considered to represent earlier stages in primate
evolutionary development as some have hypothesized [e.g., Schultz, 1969; Lovejoy,
1981]? This is an orthogenetic notion which implies that the longer ago a group
diverged from the direct ancestry of the hominids, the more reduced will be its
longevity.
The most straightforward manner in which to assess this notion is to look at
the relationship between body size and maximum longevity in each of the six
extant primate superfamilies (Lemuroidea, Lorisoidea, Tarsioidea, Ceboidea, Cercopithecoidea, and Hominoidea) [Koop et al., 19891. In absolute terms, mean longevity is clearly the greatest in the Hominoidea, second greatest in the Cercopithecoidea; the other four superfamilies are similar to one another, with no
discernible pattern relating divergence and longevity (Table IV). However, cercopithecoids and hominoids are also substantially larger than the other primate
groups. This size bias can be corrected by comparing LQ rather than absolute
values for longevity. While hominoids are still clearly the longest-lived group, the
Primate Longevity I 257
TABLE 111. Relationships Between Maximum Longevity and Organ Mass
for Nonprimates
Organ
Maximum longevity
Correlation (Pearson’s r)
Log (maximum longevity)
Brain
Heart
Liver
Kidney
Spleen
.579
.604
.639
,613
,677
,417
,428
.443
.446
.535
N
60
54
50
52
26
TABLE IV. Mean Body Mass, Maximum Longevity, Longevity Quotient, and Mean
Residuals From the Primate Log Maximum Longevity-Body Mass Regression in the Six
Monouhvletic Grouus of Primates
Grour,
Lemuroidea
Lorisoidea
Tarsioidea
Ceboidea
Cercopithecoidea
Hominoidea
Body mass (ka)
Longevity (yr)
LQ
Mean residuals
1.97
1.65
0.16
1.46
10.18
42.02
17.66
16.02
12.65
15.60
26.13
57.66
1.57
1.65
1.67
1.47
1.68
2.82
-0.340
0.006
0.042
-0.002
-0.013
0.102
other primate superfamilies share remarkably similar LQs, and there is certainly
no scala naturae, no trend toward decreasing longevity as relationships become
more distant from the hominoids.
An alternative approach to the same issue is to construct a primate-specific
regression line between log body mass and maximum longevity (Fig. 11, and to
analyze the residuals from this line. A one-way analysis of variance of these residuals by superfamily shows no significant differences between groups (F5,71=
1.115, P = 0.3601, and absolute values of the residuals show no trend for decreasing longevity as one diverges farther and farther from the hominid lineage (Table
IV).
DISCUSSION
Primates are indeed relatively long-lived mammals, but they are clearly not
the longest-lived either in absolute longevity or in longevity corrected for body
size. Relative brain size is correlated with maximum longevity within the primates, but this is apparently a primate idiosyncrasy, because a similar relationship is missing in the other mammalian orders or across the mammals generally.
Even within primates, the correlation between relative brain size and longevity is
not particularly tight and consequently brain size cannot be used to predict maximum longevity with any degree of confidence. Finally, although hominoids are
substantially longer-lived than the rest of the primates, both in relative and absolute terms, the other primate superfamilies have very similar LQs to one another.
The original implication of brain size in the aging process derived from the fact
that brain size was more closely correlated with maximum longevity than was
body size [Sacher, 19591. It is a well known, if often ignored, caveat in statistical
analysis that correlation does not imply causation regardless of the strength of the
correlation [Radinsky, 1982; Calder, 19841. The relationship between brain size
258 I Austad and Fischer
2.0
I
I
I
H
I
r
;k
v
~
1.7
.
U
d
5M
a
3
ti
1.4
B
1
Ei
.d
s
X
s
2
1B
B 4M
1.1
/
C
B
M M
0.8
-2
-1
0
1
2
3
Log Body Mass (kg)
Fig. 1. Maximum longevity as a function of body mass in the primates. Regression line: Log (maximum
longevity) = 1.238 + ,227dog (body mass). 9 = 0.562, +.x = 0.140. L, Lorimidea; M, Lemuroidea; T, Tarsioidea; B, Ceboidea; C, Cercopithecoidea;H, Hominoidea.
and longevity should provide yet another cautionary example of the reason for this
caveat, because larger data sets and more extensive analyses demonstrated that
other organs, such as the liver, were correlated at least as closely with maximum
longevity as brain size [Economos, 1980; Prothero & Jurgens, 19871. These results
suggest that organ mass may be a better indicator of overall body size than body
mass, and the relative magnitude of these correlations does not contain much
insight into factors governing longevity.
The reason for the general mammalian correlation between body size and
longevity isn’t clear, but it is not due to the relation between body size and basal
metabolic rate [Austad & Fischer, 19911. One current idea is that body size is a
surrogate variable which reflects vulnerability to environmental hazards or mortality risk [Read & Harvey, 1989; Austad & Fischer, 19911, a factor which life
history theory suggests is central to the evolution of life history characteristics
[e.g., Stearns, 1976; Charlesworth, 19801. According to this idea, larger animals
would, on average, be less susceptible to predators, and perhaps because of their
lower metabolic rate more resistant to food or water shortages. Resistance to environmentally imposed mortality of this nature should lead to the evolution of
retarded aging [Medawar, 1952; Williams, 1957; Hamilton, 19663.
By this reasoning, small organisms that for some special reason exhibit reduced vulnerability to environmental hazard should also exhibit long-for-size life
spans. Owing to their aerial habits, small, volant and gliding mammals (bats,
dermopterans, gliding marsupials, and “flying” squirrels) and birds are likely to be
at reduced risk from many forms of predation [Pomeroy, 19901 and should therefore show increased longevity. Gliding mammals, including marsupials, average
1.7 time the expected life span of nonflying eutherians [Austad & Fischer, 19911,
Primate Longevity / 259
while birds live about 2.4 times the mass-specific life span of eutherian mammals
[Lindstedt and Calder, 19761.
Historically, considerations of broad interspecific patterns of longevity have
led to insight into potential mechanisms through which aging might occur. The
rate-of-living theory, though now virtually discarded by biogerontologists [e.g.,
McCarter et al., 1985; Finch, 1990; Rose, 19911, has stimulated very productive
research into damaging by-products of normal metabolic processes. One such byproduct is the generation of highly reactive free oxygen radicals [Harman, 1962;
Halliwell & Gutteridge, 19851, which damage an array of cellular components from
membranes to nucleic acids. A second type of damaging by-product is the nonenzymatic attachment of glucose and other reducing sugars to proteins and nucleic
acids to form nonreversible “advanced glycosylation end-products” (AGE’S) [Cerami, 1985; Monnier, 19891.
What the diversity of mammalian life spans in the face of a variety of metabolic demands tells us is that a key to understanding mechanisms of aging is not
simply understanding these how these damaging by-products are generated, but
more importantly in understanding evolutionarily important mechanisms of defense against these by-products. The study of antioxidant defenses is well developed and currently a very active field of research [Halliwell & Gutteridge, 19851
and the study of anti-glycosylation defense systems is just beginning [Cerami et
al., 1987; Monnier et al., 19911.
One thing that the preceding analysis indicates is that primates such as humans are not the only animals with highly developed defenses against normal
metabolic damage. Indeed instead of focusing virtually all research effort into
anti-aging mechanisms on animal models such as laboratory rodents which have
demonstrably poor defenses, scientists might fruitfully turn to other organisms
with as effective, or even more effective, defense systems than humans. Unexploited animal models that would seemingly be ideal for this sort of research are
bats and birds.
In conclusion, our results show that primates’ exceptional longevity is not
anomalous, but is a pattern that fits into the larger context of the evolution of
mammalian life spans. The theories that 1) brain size is a determinant of maximum life span, 2) that life span has been increasing through evolutionary time
among primates, and 3) that metabolic efficiency and life-time energy expenditure
are determinants of maximum life span are not supported by our analyses. We
suggest that the exceptional primate longevity may be better explained as a result
of a generalized low mortality risk due to an arboreal habit and the propensity for
social grouping. Because primates have been the subjects of intensive, long-term
studies, they offer an ideal opportunity t o address some of the problems concerning
mammalian life history evolution.
ACKNOWLEDGMENTS
This work was supported in part by grants to S.N.A. from the Henry Rosovsky
Fund and Milton Fund of Harvard University and by U.S.N.I.H. grant AG0970001. We are grateful to C. Finch, J. Robinson, P. Waser, and R. Wrangham for
helpful comments on the text.
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