Journal of Human Evolution 51 (2006) 480e489

Evolution of brain size and juvenile periods in primates

Robert Walker a,*, Oskar Burger a, John Wagner a, Christopher R. Von Rueden b
a
Department of Anthropology, University of New Mexico, Albuquerque, NM 87131, USA
b
Department of Anthropology, University of CaliforniaeSanta Barbara, Santa Barbara, CA 93106, USA
Received 12 May 2005; accepted 20 June 2006

Abstract

This paper assesses selective pressures that shaped primate life histories, with particular attention to the evolution of longer juvenile periods
and increased brain sizes. We evaluate the effects of social complexity (as indexed by group size) and foraging complexity (as indexed by per-
cent fruit and seeds in the diet) on the length of the juvenile period, brain size, and brain ratios (neocortex and executive brain ratios) while
controlling for positive covariance among body size, life span, and home range. Results support strong components of diet, life span, and pop-
ulation density acting on juvenile periods and of home range acting on relative brain sizes. Social-complexity arguments for the evolution of
primate intelligence are compelling given strong positive correlations between brain ratios and group size while controlling for potential con-
founding variables. We conclude that both social and ecological components acting at variable intensities in different primate clades are impor-
tant for understanding variation in primate life histories.
Ó 2006 Elsevier Ltd. All rights reserved.

Keywords: Brain size; Neocortex ratio; Age at first reproduction; Comparative analysis; Juvenile primates; Life-history evolution; Socioecology

Introduction traits are posited to be directly related to encephalization in

the primate order in general and in great apes in particular
Primate life histories tend to be characterized by rather long (Kaplan et al., 2000; Deaner et al., 2003). Our interest here
subadult periods (Pereira and Fairbanks, 1993; Leigh, 2001), is to evaluate different competing ideas, namely social versus
long life spans (Austad and Fischer, 1992; Hakeem et al., foraging complexity, on the evolution of slow primate life
1996), slow growth rates (Leigh and Park, 1998), slow fertility histories. Based on previous analyses (e.g., Sawaguchi,
rates (Charnov and Berrigan, 1993), and large absolute and 1992; Dunbar, 1996; Barton, 1999), but including more eco-
relative brain sizes (Rilling and Insel, 1999) compared to other logical variables, our general prediction is that various mea-
mammalian orders. At the extreme are wild chimpanzee sures of relative brain size, in addition to age at first
females with an age at first reproduction of about 13 years reproduction as a proxy for the end of the growth period,
(Sugiyama, 2004) and natural-fertility hunter-gatherers that will be positively associated with indices of social and forag-
begin to reproduce around 19 years of age (Marlowe, 2005). ing complexity within and across primate clades.
Chimpanzees, humans, and other large primates grow nearly Long juvenile periods are often interpreted as necessary to
an order of magnitude slower than other mammals of similar develop the sophisticated cognitive capacities requisite in
size (Case, 1978; Walker et al., 2006). These ‘‘slow’’ life-history complex socioecologies (Bogin, 1999; Kaplan et al., 2000).
In support of this idea are strong relationships among longer
juvenile periods in primates and various measures of relative
* Corresponding author. Tel.: þ1 505 277 3054.
brain size (Barton, 1999). Longer juvenile periods and in-
E-mail addresses: robwal@unm.edu (R. Walker), oskar@unm.edu (O.
Burger), wagner@unm.edu (J. Wagner), vonrueden@umail.ucsb.edu (C.R.
creased learning are consistent with a social-complexity
Von Rueden). model, which is further supported by strong positive associa-
URL: http://www.unm.edu/wrobwal tions between relative brain-size measures and primate group

0047-2484/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jhevol.2006.06.002
 R. Walker et al. / Journal of Human Evolution 51 (2006) 480e489 481

sizes (Dunbar, 2003). In the same vein as Barton (1999), we of this model point to the complex techniques employed by
focus on multiple regressions that allow us to simultaneously human hunters, who integrate many sources of information
examine brain-size variation explained by diet and group within a large area to locate many types of prey and to utilize
size. The availability of additional ecological variables, such a wide range of techniques to capture prey once located (Kaplan
as home range from studies of wild primates, further et al., 2000). Chimpanzees also utilize a range of complex hunt-
strengthens our ability to separate independent predictors of ing techniques (Mitani and Watts, 1999), and the great apes, in
brain size and age at first reproduction (Kaplan et al., 2003). general, are capable of elaborate tool use for foraging (Boesch
We pay special attention to differences between Old and and Boesch, 1990; McGrew, 1992; Fox et al., 1999; Yamakoshi,
New World primates in recognition of the fact that different 2004; Russon and Begun, 2004) and execute complex
selective pressures may be more or less important in different sequences for extracting food from plants (Byrne and Byrne,
primate clades. Our goal is to evaluate the relative effects of 1991, 1993). However, some primates are as adept at foraging
social complexity (as indexed by group size) and foraging as juveniles as they are as adults (Watts, 1988; Pereira and
complexity (percent fruit and seeds) on brain size and brain Fairbanks, 1993; Janson and van Schaik, 1993).
ratios (e.g., neocortex and executive brain ratios). We are also Interpreting the brain and higher cortical functions as adap-
interested in selection for longer juvenile periods given the sug- tations for negotiating social interactions within large-group
gestion that these have likely coevolved with larger relative settings has been widely discussed (Jolly, 1966; Humphrey,
brain measures (e.g., the nonvisual neocortex; Joffe, 1997). 1976; Whiten and Byrne, 1988; Byrne and Whiten, 1988;
Alexander, 1989; Dunbar, 1993, 1998, 2003; Byrne, 1995;
Brain evolution Kummer et al., 1997; Whiten and Byrne, 1997; Heyes,
1998; Barton, 1999; Flinn et al., 2005) and offers an alterna-
The ultimate explanation for the evolution of large relative tive (or perhaps complementary) scenario leading to primate
brain sizes in primates remains unresolved. In particular, the encephalization. The central supposition of social-brain sce-
neocortex of many primates has undergone sizable expan- narios or ‘‘Machiavellian’’ intelligence is that higher cognitive
sion, reaching its most extreme form in humans (Rilling functions evolved in response to selective pressures arising
and Insel, 1999). The neocortex is generally associated from social interactions with conspecifics and specifically
with multimodal integration, planning, inhibition, innovation, the ability to use and manipulate social information. Monkeys
cognitive memory, and higher-order information processing are capable of rapid social learning and deception (Byrne and
(Keverne et al., 1996; Joffe and Dunbar, 1997). A number Whiten 1988), while the great apes are further capable of
of hypotheses have been put forth to account for cerebral ex- theory of mind, the reasoning about the beliefs and desires
pansion in primate lineages. Epiphenomenal and develop- of others (Call and Tomasello, 1998).
mental models have interpreted brain size as a by-product In hominoids, particularly chimpanzees and humans, the in-
of large body size (Finlay et al., 2001) or as resulting from fluence of intergroup competition on social organization has
certain nutritional conditions (Broadhurst et al., 2002), been emphasized (Manson and Wrangham, 1991). Competi-
respectively. In this paper, we focus on models that address tion among subpopulations can result in coalitionary arms
potential selective pressures leading to primate cortical races, producing larger and necessarily more complex social
expansion, namely the cognitive demands associated with ex- groups (Alexander, 1989). The ability to navigate within in-
ploiting a skill-intensive foraging niche (Parker and Gibson, creasingly larger social arenas filled with equally sophisticated
1977) and the sociocognitive competencies of living in large conspecifics may have provided an autocatalytic mechanism
social groups (Humphrey, 1976). by which social intelligence rapidly increased. Social models
Selective pressures related to foraging have long been can be criticized on grounds that they do not account for qual-
suspected to play a role in the evolution of intelligence. This itative differences among primate grades, nor do they ade-
argument centers on cognitive challenges associated with se- quately address overcoming the costs associated with living
curing high-quality (nutrient-dense) but difficult-to-acquire in large groups. These costs may in turn depend on ecological
food sources, which may be ephemeral and require detailed conditions highlighting the probable interaction of social and
mental maps to track and locate across time and space (Parker ecological factors on primate life histories.
and Gibson, 1977; Clutton-Brock and Harvey, 1980; Harvey A challenge to students of primate life-history evolution is
and Krebs, 1990; Parker and McKinney, 1999). For example, to develop tests that evaluate foraging and social explanations
the greater cognitive abilities in frugivorous compared to foliv- for the evolution of long juvenile growth periods and large
orous primates may reflect the greater challenges associated brains. In this paper, we develop a series of multiple regres-
with foraging for ripe fruit versus a nearly constant supply sions that examine the relative effects of group size and per-
of leaves (Milton, 1981). Additionally, more nutritionally cent fruit and seeds in the diet on age at first reproduction
dense, higher-quality foods are required to support metaboli- and brain size while addressing interrelationships with home
cally expensive neural tissue (Milton, 2003). As such, the shift range and longevity. The models allow us to separate direct
in hominin diet to higher-quality but more difficult-to-acquire (perhaps causal) effects from indirect effects acting through
resources would have required learning skill-intensive extrac- spurious correlations with other life-history and socioecologi-
tive techniques, thereby producing longer juvenile-learning cal variables. In this manner we are able to simultaneously
periods and larger brains (Kaplan et al., 2000). Proponents evaluate social- and foraging-complexity hypotheses and
482 R. Walker et al. / Journal of Human Evolution 51 (2006) 480e489

estimate the relative importance of each for the evolution of [neocortex / (whole brain  neocortex); Dunbar, 1992], (2)
primate brain sizes and juvenile periods within and across neocortex ratio that adjusts for the cerebellum [neocortex /
clades. (whole brain  cerebellum  neocortex); Reader and Mac-
Donald, 2003], (3) nonvisual neocortex ratio [(neocortex 
Materials and methods V1) / (whole brain  neocortex); Joffe, 1997], (4) nonvisual
neocortex ratio that adjusts for the cerebellum [(neocortex 
Comparative analysis V1) / (whole brain  cerebellum  neocortex)], and (5)
executive brain ratio [(neocortex þ striatum) / (mesencepha-
Comparative data can be used to better understand the se- lon þ diencephalon); Reader and Laland, 2002]. The best
lective pressures acting on brain size and juvenile periods. measure of relative brain size is still debated (Barton, 1999;
The analyses reported here used a primate data base contain- Deaner et al., 2000), but we included ratios that exclude the
ing female age at first reproduction (months), brain weight cerebellum to avoid the problem that larger neocortices could
(g), maximum life span (years), body size (kg), maximum be driven by diminished cerebella (Reader and MacDonald,
home range (km2), percent fruit and seeds in the diet, and av- 2003). The brain ratios were taken from Reader and
erage group size. The data base was compiled from second- MacDonald (2003), who relied principally on the primate
ary sources (Barton, 1999; Harvey et al., 1987; Smith and brain-component volumes (corrected for species-typical
Jungers, 1997; Kappeler and Pereira, 2003) with an emphasis values) of Stephan and colleagues (1970, 1981, 1988).
on primary field data where available (Kaplan et al., 2003; Unfortunately, the available sample size for different brain
see http://www.unm.edu/%7Ehkaplan/pnas/primatedatabase. ratios was only 23e33 primate species depending on the ra-
xls for data and information sources). In various analyses, tio, which is small for the assumptions of ordinary least
we used a total of 67 primate species (11 strepsirrhines, 19 squares regression. Small sample size is also a problem for
New World monkeys, 30 Old World monkeys, and 7 homi- the regression analyses conducted within Old and New
noids, excluding humans) for which values for each of the World monkeys. Therefore, we calculated p-values for our
seven characteristics listed above were available. Where pos- parameter estimates using resampling with replacement, or
sible, we performed analyses within New World and Old bootstrapping, techniques (Efron, 1979; Yu, 2003) with a Pas-
World monkeys but were not able to do so for the hominoids cal program. The original data distributions were resampled
and strepsirrhines, given small sample sizes. Therefore, in with replacement in 10,000 bootstrap replications for each
our all-primate analyses we included all 67 species. Analyses independent variable while holding the other variables con-
(unreported) show that omission of the strepsirrhines from stant. The p-value was defined as the proportion of iterations
the all-primate sample does not significantly alter our main in which the slope fitted to random data was absolutely larger
conclusions. than the slope through the observed data (Davison and
The data were analyzed with species as independent data Hinkley, 1997). Contrary to the recommendations of some
points and using independent contrasts, which adjust for phy- (Deaner et al., 2000), we found similar or often better
logenetic effects (Nunn and Barton, 2001) because closely model results for all the brain ratios when they were log-
related species may be similar simply because they share a re- transformed, but this could be partially a function of
cent ancestor (Felsenstein, 1985; Garland et al., 1992; Losos, resampling, which is less affected by distributions of the
1999). The independent contrasts module of PDTREE by Gar- original data (Mitchell-Olds and Shaw, 1987).
land and colleagues (1993, 1999; Garland and Ives, 2000),
used primarily with the phylogenetic tree and branch lengths Results
of Smith and Cheverud (2002) and secondarily from Purvis
(1995), was used to construct independent contrasts. These Age at first reproduction
were analyzed and graphed using SPSS software and Pascal
(see below). All variables were log-transformed (base 10) We report results in three related sections of dependent
prior to analysis. Diagnostics available in PDTREE were ex- variablesdlength of the juvenile period, brain size, and brain
amined to ensure homoscedasticity in residuals and that ratios. First, age at first reproduction, which approximates the
branch lengths were statistically appropriate. cessation of the growth period (at least for females), was re-
gressed on body size, group size, life span, and the ecological
Other relative brain-size measures or ‘‘brain ratios’’ variables. Group size has a strong positive effect on longer ju-
venile periods in Old World monkeys and across the primate
Since body size can change independently of brain size order (Table 1). Home range has a negative effect on age at
(Willner, 1989; Deacon, 1990), it has been suggested that var- first reproduction for Old World monkeys. This interesting
ious brain ratios are preferable to using whole-brain or brain- but difficult to interpret result was also mentioned by Deaner
component size while controlling for body size (Dunbar, and colleagues (2003). Taken together these results (positive
1998). Brain ratios are relative measures of brain volume for group size and negative home-range effect) imply that age at
areas of higher cognitive functions (i.e., neocortex) scaled to first reproduction in Old World monkeys is later when popula-
the remainder of the brain or a more ancestral brain region. tion density is high given that log (population density) w log
We used the following brain ratios: (1) neocortex ratio (group size)  log (home range).
 R. Walker et al. / Journal of Human Evolution 51 (2006) 480e489 483

Table 1 learning periods needed for more complex foraging skills,

Multiple-regression models of age at first reproduction (dependent variable) though this relationship does not appear to hold for New
for 1) Platyrrhini, 2) Cercopithecidae, and 3) all primates (including Hominoi-
dea and Strepsirrhini)
World monkeys.
Model Species as data Independent contrasts
points Brain size
b p b p b p
We performed similar analyses with brain size as the de-
1) New World monkeys (n ¼ 19)
(Intercept) (No Intercept) pendent variable. In New World monkeys, relative brain size
Body size 0.723 0.001 0.575 0.035 0.492 0.058 is best predicted by maximum life span regardless of whether
Group size* L0.307 0.034 0.442 0.078 species values or independent contrasts were used as data
Life span 0.308 0.058 0.498 0.076 0.366 0.171 points (Table 2). This pattern does not hold, however, in Old
Home range* 0.295 0.043 0.357 0.247
World monkeys, in which diet is a strong predictor with spe-
Fruit þ seed 0.146 0.327 0.159 0.449 0.060 0.738
Density 0.250 0.390 cies as data points, but home range is the strong predictor
with independent contrasts. This intraorder variation between
2) Old World monkeys (n ¼ 30)
(Intercept) (No Intercept)
Old and New World monkeys makes analyses of a composite
Body size 0.660 0.002 0.214 0.109 0.068 0.532 primate data base challenging because there is likely to be
Group size* 0.940 <0.001 0.495 0.001 a blurring of grade shifts when analyzing across clades
Life span 0.114 0.519 0.185 0.186 0.343 0.036 (Martin, 2003; Martin et al., 2005). It raises the red flag that
Home range* L1.155 <0.001 L0.550 0.002 important selective effects may be different across primate
Fruit þ seed 0.109 0.546 0.366 0.143 0.464 0.118
Density 0.319 0.044
clades. Unfortunately, small numbers of hominoids and strep-
sirrhines prohibit analyses within these clades. Allman and
3) All primates (n ¼ 66)
colleagues (1993) found a positive association between life
(Intercept) (No Intercept)
Body size 0.672 <0.001 0.146 0.185 0.126 0.263 span and brain mass while controlling for body size within
Group size* 0.011 0.907 0.329 0.006 haplorhines but not within strepsirrhines. We confirm this
Life span 0.396 <0.001 0.297 0.007 0.385 <0.001 relationship for New World monkeys since only home range
Home range* 0.171 0.193 L0.355 0.006 (and not life span) is more strongly associated with brain
Fruit þ seed 0.053 0.424 0.379 <0.001 0.411 <0.001
size in Old World monkeys.
Density 0.278 0.015
Group size and life span are strong predictors of relative
Notes: All variables were log-transformed prior to analysis. Standardized
brain size across primates. However, adjusting for phylogeny
regression coefficients, b, and resampling-generated p-values ( p < 0.05 are
in bold) are given for regressions in which species values were treated as causes these effects to diminish and home range becomes the
data points and for those in which independent contrasts were used as data single most important predictor. In most of our results, we
points. *Denotes potential problem with collinearity, i.e., the home-range/
group-size effects do not hold with omission of one or the other. Log(density) Table 2
equals log(group size)  log(home range). Multiple regression models of brain size (dependent variable) for 1) New
World monkeys, Old World monkeys, and 3) all primates
One might suspect that this effect may be driven by col- Model Species as data points Independent contrasts
linearity between group size and home range (Deaner b p b p
et al., 2000) because both effects drop out when the other 1) New world monkeys (n ¼ 19)
variable is omitted. However, if we collapse group size and (Intercept) (No Intercept)
home range into a single population density variable, the re- Body size 0.767 <0.001 0.787 0.003
sult is strong and positive on longer juvenile periods and Group size 0.038 0.514 0.101 0.300
Life span 0.224 0.007 0.199 0.073
avoids the problem of collinearity. One interpretation is
Home range 0.092 0.117 0.122 0.153
that higher resource competition is associated with higher Fruit þ seed 0.012 0.828 0.134 0.293
population density, which leads to longer periods of growth
2) Old World monkeys (n ¼ 30)
and is consistent with risk-aversion in juvenile primates (Intercept) (No Intercept)
(Janson and van Schaik, 1993). In the upcoming regression Body size 0.891 <0.001 0.667 <0.001
models, either home range or group size is a significant Group size 0.065 0.352 0.132 0.108
parameter (but not both simultaneously) and so we no longer Life span 0.056 0.426 0.062 0.290
need to invoke population density as a method to avoid Home range 0.087 0.208 0.359 0.003
Fruit þ seed 0.159 0.049 0.002 0.948
collinearity problems.
Longevity tends to be strongly associated with age at first 3) All primates (n ¼ 67)
(Intercept) (No Intercept)
reproduction within and across primate clades (Table 1).
Body size 0.812 <0.001 0.780 <0.001
This result supports one of the most salient predictions of Group size 0.083 0.035 0.015 0.822
life-history theory that higher adult mortality selects for earlier Life span 0.178 <0.001 0.084 0.168
reproduction (Harvey and Zammuto, 1985; Stearns, 1992; Home range 0.002 0.969 0.191 0.009
Charnov, 1993). Additionally, the effect of diet on juvenile Fruit þ seed 0.043 0.102 0.054 0.334
periods shows some support for an ecological model of longer Notes: See Table 1.
484 R. Walker et al. / Journal of Human Evolution 51 (2006) 480e489

found consistency between models using species as data Deaner et al., 2003). This result suggests that juvenile periods
points and models using independent contrasts. The two big- and brain size may not have been subjects of strong and direct
gest exceptions are the brain-size models in Table 2 for Old coevolution (Leigh, 2004).
World monkeys and all primates. Given the problem of One problem with using relative brain size (residuals of log
a large number of closely related cercopithecines in Old brain size by log body size) as a dependent variable is that
World monkeys, which is ameliorated with phylogenetic these measures appear incongruent with field study results
analysis, we lean towards putting more confidence in the that show high levels of cognitive complexity in great apes
independent-contrast results (but see Martin et al., 2005). (Russon and Begun, 2004; Ross, 2004). Out of a list of 100
Thus, given these results, there is little evidence in support primates, gorillas rank 86th, chimpanzees 57th, and orangu-
of the social-complexity model for the evolution of longer tans 39th on the scale of highest-to-lowest relative brain
juvenile periods and larger relative brain sizes in primates size, whereas capuchin and squirrel monkeys take up the top
or within monkey clades. Results better support an ecological ranks after humans. Therefore, alternative neural measures
component acting on larger brain size through larger home may better index higher cognitive abilities.
ranges (Fig. 1). However, this result is not found in the
brain-ratio analyses, where group size is consistently the Brain ratios
strongest predictor (see below).
We omitted age at first reproduction from the brain-size A series of regressions were performed with other relative
model and brain size from the age-at-first-reproduction model. brain measures that we call brain ratios. Five brain ratios
Age at first reproduction does show some association with were examined as functions of body size, group size, longev-
brain size when entered as another independent variable. How- ity, home range, and diet using species values as data points
ever, we believe that the length of the juvenile period is best and independent contrasts (Tables 3e7). Age at first reproduc-
considered a choice (dependent) variable, as it is one of the tion was omitted from most brain-ratio models due to near-
most important life-history decisions an organism faces. The zero partial correlations with all except for the two nonvisual
advantage of this method is that we can test for coevolution neocortex ratios, in which the relationship is strong and posi-
between brain size and juvenile periods. The correlation of tive (Joffe, 1997). We report the results of a total of ten regres-
the age-at-first-reproduction residuals from Table 1 with sion procedures (five ratios each with species values and
the brain residuals from Table 2 is positive (r ¼ 0.376, contrasts). Group-size and life-span effects are invariably pos-
p ¼ 0.002, n ¼ 67) using species values as individual data itive. Importantly there is a rough convergence of the different
points. However, within New World monkeys, there is no models across all five ratios with species values as data points
relationship between brain size and age-at-first-reproduction and independent contrasts.
residuals, and with independent contrasts, the relationship be- Following the results of Deaner and colleagues (2000),
comes negative and nonsignificant (r ¼ 0.206, ¼ 0.107, most of the brain ratios used here show strong relationships
n ¼ 66). Therefore, primates fail the strong test for an associ- with body size, rendering any bivariate analyses ignoring
ation between brain size and age at first reproduction (cf. this important confounding variable suspect. Moreover, in
each of the ten models, group size is one of the strongest pre-
dictors. This pattern is surprisingly robust given the mostly
Residuals of brain size by body size contrasts

0.08
spurious correlations documented for group size and brain
0.06 size in Table 2. Life span is an important predictor of execu-
0.04
tive-to-brainstem ratio and is positive in the other regressions,
though it tends to be weaker than group size. Home range
0.02
shows a modest correlation with neocortex ratio, but like per-
0.00 cent fruit and seeds in the diet, it is never significantly differ-
-0.02
ent from zero in any of the ten brain-ratio models. Therefore,
-0.04
Table 3
-0.06 Multiple-regression model of neocortex ratio (dependent variable) for primates
-0.08
of all grades
Model Species as data points Independent contrasts
-0.10
-0.6 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8 1.0 1.2 b p b p
Residuals of max home range by body size contrasts
All primates (n ¼ 32)
Fig. 1. Relationship between the independent contrasts of brain size and max- (Intercept) (No Intercept)
imum home range after removing the statistical effect of body size on each Body size 0.267 0.013 0.313 0.131
(n ¼ 66 nodes for primates of all grades; r2 ¼ 0.1863). A stronger effect is vis- Group size 0.405 0.001 0.320 0.039
ible within Old World monkeys (Table 2). Using an alternative body-size data Life span 0.285 0.007 0.115 0.612
base (Kappeler and Pereira, 2003) to calculate home-range residuals gives Home range 0.086 0.412 0.293 0.095
essentially identical results, indicating that the relationship is not spuriously Fruit þ seed 0.067 0.547 0.016 0.907
driven by errors in body sizes that affect both variables. Notes: See Table 1.
 R. Walker et al. / Journal of Human Evolution 51 (2006) 480e489 485

Table 4 Table 6
Multiple-regression models of neocortex ratio without cerebellum (dependent Multiple-regression model of nonvisual neocortex ratio without the cerebellum
variable) for primates of all grades (dependent variable) for primates of all grades
Model Species as data points Independent contrasts Model Species as Independent contrasts
b p b p data points

All primates (n ¼ 33) b p b p b p

(Intercept) (No Intercept) All primates (n ¼ 23)
Body size 0.402 <0.001 0.504 0.009 (Intercept) (No Intercept)
Group size 0.311 0.002 0.263 0.074 Body size 0.266 0.011 0.561 0.010 0.311 0.042
Life span 0.318 0.001 0.149 0.405 Group size 0.332 0.003 0.362 0.013 0.378 0.008
Home range 0.051 0.586 0.181 0.269 Life span 0.373 0.001 0.382 0.098 0.192 0.251
Fruit þ seed 0.032 0.743 0.054 0.714 Home range 0.101 0.296 0.022 0.824 0.051 0.667
Notes: See Table 1. Fruit þ seed 0.053 0.605 0.045 0.637 0.059 0.626
Age at first 0.478 0.004
reproduction
we conclude that brain ratios are much more strongly related Notes: See Table 1.
to social complexity, as opposed to foraging or ecological
complexity.
independently explain variation in brain size (Barton, 1999)
The final step in the analysis compared observed human
and neocortex ratio (Dunbar, 1996). On the other hand, our re-
ratios to those expected for a primate of our size and adjusting
sults are consistent with those of Kaplan and colleagues
for a long human life span and a typical human group size.
(2003). Here, group size affects brain size indirectly through
Using the regressions in Tables 3e7, we calculated expected
its positive associations with longevity and home range, often
human values with liberal estimates of body size (65 kg),
omitted in studies that detect correlations between brain size,
life span (120 yr), and group size (n ¼ 150). Observed human
diet, and group size. In our analyses, there is a strong relation-
values are considerably higher than those expected from the
ship between relative brain size and home range (Fig. 1). The
nonhuman primate regressions (Table 8). For example, the hu-
default expectation of a relationship between group size and
man nonvisual neocortex ratios and the executive-to-brainstem
brain size was not supported, potentially because relative brain
ratio are three to four times larger than expected. Observed
size is not a good measure of intelligence given that selection
chimpanzee values are also high, as are those for other apes.
acts on body size independently of brain size (case in point,
gorilla). Importantly, group size is most strongly and consis-
Discussion tently related to all of the various brain ratios.
Most of the results presented here are concordant with pre-
After addressing problems with collinearity associated with vious comparative analyses. For example, Dunbar (1993,
group size and home range, we conclude that diet and life span 1998, 2003) found a significant correlation between neocortex
are the best predictors of longer juvenile periods, tentatively ratio and group size within and across primate grades (see also
supporting a foraging-complexity model. However, neither Deaner et al., 2000). Kaplan and colleagues (2003) also dem-
group size nor percent fruit and seeds in the diet have signif- onstrated that, across primates, the neocortex (with the rest of
icant effects on relative brain size. This result contrasts with brain weight entered as an instrument) correlates most
previous work supporting a correlation between brain size strongly with group size. We find that the executive-to-brain-
and diet across primates (Clutton-Brock and Harvey, 1980; stem and other neocortex ratios also tend to correlate more
Foley and Lee, 1992), including studies in which multiple strongly with group size than with any ecological variable.
regression was used to demonstrate that diet and group size Our three main variables of interestdlength of the juvenile
period, brain size, and brain ratiosdappear to be driven by
Table 5 different socioenvironmental factors, namely diet/life span
Multiple-regression model of nonvisual neocortex ratio (dependent variable)
for primates of all grades
Table 7
Model Species as Independent contrasts
Multiple-regression model of executive-to-brainstem ratio (dependent vari-
data points
able) for primates of all grades
b p b p b p
Model Species as data points Independent contrasts
All primates (n ¼ 23)
b p b p
(Intercept) (No Intercept)
Body size 0.142 0.211 0.420 0.060 0.077 0.587 All primates (n ¼ 30)
Group size 0.389 0.003 0.453 0.009 0.474 0.003 (Intercept) (No Intercept)
Life span 0.359 0.004 0.376 0.174 0.115 0.542 Body size 0.403 <0.001 0.586 <0.001
Home range 0.136 0.225 0.012 0.999 0.027 0.810 Group size 0.231 0.007 0.328 0.008
Fruit þ seed 0.086 0.495 0.083 0.474 0.060 0.660 Life span 0.400 <0.001 0.340 0.017
Age at first 0.656 0.001 Home range 0.094 0.226 0.045 0.733
reproduction Fruit þ seed 0.007 0.930 0.035 0.776
Notes: See Table 1. Notes: See Table 1.
486 R. Walker et al. / Journal of Human Evolution 51 (2006) 480e489

Table 8 ages at first reproduction in particular primate taxa. Ecological

Comparison between observed brain ratios in humans and those expected from and social hypotheses can be difficult to separate because de-
primate regressions (chimpanzee brain ratios are included for comparison)
velopment of higher cortical function for one purpose can be
Brain ratio Pan troglodytes Homo sapiens applied in other domains. For example, long juvenile learning
Predicted Observed periods can serve the dual purpose of mastering skills needed
Neocortex ratio 2.4e3.2 2.2 3.1e4.1 to compete in adult social arenas (e.g., mating and social-
Neocortex ratio without 4.5e6.2 3.5 5.3e9.3 maneuvering) and also to master complicated foraging tasks
cerebellum (e.g., frugivory and carnivory).
Nonvisual neocortex ratio 3.1 1.4 4.0
Nonvisual neocortex ratio 5.9 2.3 9.1
An interesting test case is the sympatric fruit-eating spider
without cerebellum monkey and the more folivorous howler monkey. It has been
Executive-to-brainstem ratio 31.8 13.7 58.5 suggested that the spatiotemporal demands for locating ripen-
ing fruit relative to a ubiquitous supply of leaves has led to the
evolution of a spider-monkey brain about twice the size of that
(Table 1), home range (Fig. 1), and group size (Tables 3e7), of a howler monkey (Milton, 1981). Spider monkeys exhibit
respectively. We could not find a convincing link between a complex fission-fusion social system (Symington, 1990),
the residuals of age at first reproduction and those of brain also seen in chimpanzees, which perhaps has selected for in-
size. Moreover, most of the brain ratios did not exhibit an as- creased cognitive capacity in contrast to howler monkeys.
sociation with age at first reproduction, with the exception of Dunbar (2003) suggests that complex fission-fusion social re-
the nonvisual neocortex ratio with and without the cerebellum, lationships, created by a combination of ripe-fruit foraging and
where the correlations with longer juvenile periods are quite large community sizes, have driven intelligence (and nonvisual
strong. This finding is consistent with the results of Joffe’s neocortical expansion) in hominoids.
(1997) study, who found strong relationships between various It is possible that certain primate socioecologies select for
measures of the length of the juvenile period and the non- increases in brain size based more on social demands, whereas
visual neocortex ratio. In sum, there may be a suite of semi- others tend to promote larger brains because of foraging com-
independent effects of socioenvironmental parameters on plexities (including tool use), leading to the weak correlations
different aspects of primate life histories, namely diet/life among diet, group size, and brain size demonstrated in this
span/ juvenile period, home range/ brain size, and group study. Across the primate order, there is mixed evidence for
size/ brain ratios. The links among these different effects the coevolution of larger brains, longer juvenile periods, and
are surprisingly weak, which cautions against any all- longer life spans (Charnov and Berrigan, 1993; Kaplan and
encompassing coevolutionary argument for slower primate Robson, 2002; Kaplan et al., 2003). The specifics of social
life histories. The few examples of links across these different and/or ecological pressures are likely to vary across the pri-
relationships are age at first reproduction/ nonvisual neocor- mate order, especially when comparing phylogenetic grades
tex ratio and life span/ executive-to-brainstem ratio. (Sawaguchi, 1992). Indeed, we found that life span appears
to be a more important determinant of brain size in New World
Social, ecological, or socioecological? monkeys, whereas home range is more important in Old World
monkeys. This difference potentially relates to complete ar-
The strong positive effect of home range on brain size may boreality in the New World monkeys and the larger body
support an ecological foundation underlying larger brain size. size and terrestrial strategies among Old World species.
However, larger home ranges may also introduce increased so- Following the patterns documented here, human life-
cial complexity at the intergroup level through more contact history characteristics appear qualitatively similar, yet the
with other groups of conspecifics. Regardless, home range specifics of selection pressures involved since the human-
does covary strongly with both longevity and group size and chimpanzee split remain unresolved. Evaluating the marginal
should be included as a potential confounding variable in benefits of social versus foraging returns to investment in brain
any regression. Otherwise, one runs the risk that the omission size (Dunbar, 2003) between closely related taxa appears to be
of home range confounds the true relationship between group an especially informative avenue for future investigations. An-
size and brain size or some brain ratio. The positive associa- alyzing what humans and other primates are doing during the
tion between group size and longevity creates a similar effect long juvenile period and how this translates into adult behavior
whereby omission of longevity increases the correlation be- and fitness benefits should also prove valuable (Altmann,
tween group size and brain size. Because of strong covariance 1998; Walker et al., 2002; Maestripiere and Ross, 2004).
among the variables of interest and consequent risk of obtain- Many cognitive and motor skills are gained quickly during
ing spurious results, multiple regression methods are often childhood, but not mastered as easily if the learning process
preferable to bivariate correlations that only control for body begins later (e.g., language; Kim et al., 1997). Documenting
size. This admonition is a most important consideration sensitive periods of time when the brain is primed for the
when overall brain size is the dependent variable. learning of important life skills (e.g., foraging and social tasks;
We suggest that associations between group size and rela- Bock, 1995, 2002) can elucidate how selective pressures have
tive brain size are spurious. It is probable that there exists shaped cognitive architecture. Substantial neurophysiological
more than one causal pathway to larger brain size and later changes that occur into young adulthood (e.g., Cabana et al.,
 R. Walker et al. / Journal of Human Evolution 51 (2006) 480e489 487

1993; Pujol et al., 1993; Benes et al., 1994; Pfefferbaum et al., Boesch, C., Boesch, H., 1990. Tool use and tool making in wild chimpanzees.
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the analyses and interpretations. A National Science Founda- Chicago, pp. 233e265.
tion Graduate Fellowship to RW funded some of this research. Deaner, R.O., Nunn, C.L., van Schaik, C.P., 2000. Comparative tests of pri-
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