a hipotese do cerebro social kevin dunbar

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ARTICLES

The Social Brain HypothesisRobin I.M. Dunbar

The concensus view has tradition-ally been that brains evolved to pro-cess i nformation of ecological rel-evance. This view, however, ignores animportant consideration: Brains are

exceedingly expensive both to evolveand to maintain. The adult humanbrain weighs about 2% of body weightbut consumes about 20% of total en-ergy intake.2 In the light of this, it isdifficult to justify the claim that pri-mates, and especially humans, needlarger brainsthan other species merelyto do the same ecological job. Claimsthat primate ecological strategies i n-

volve more complex problem-solv-ing3,4 are plausible when applied to

the behaviors of particular species,such astermite-extraction bychimpan-zees and nut-cracking by Cebu s mon-keys, but fail to explain why allprimates, including those that are con-ventional folivores, require larger brainsthan thoseof all other mammals.

An alternative hypothesis offeredduring the late 1980s was that pri-mates’ large brains reflect the compu-

tational demands of the complex so-cial systems that characterize theorder.5,6 Pri ma facie, this suggestionseems plausible: There is ample evi-dence that primate social systems aremore complex than those of otherspecies. These systems can be shownto involve processes such as tacticaldeception5 and coalition-formation,7,8

which are rare or occur only in sim-pler forms in other taxonomic groups.Because of this, the suggestion wasrapidly dubbed theM achiavellianintel-ligencehypothesis, although there is agrowing preference to call it thesocialbrain hypothesis.9,10

Plausible asit seems, thesocial brainhypothesis faced a problem that wasrecognized at an early date. Specifi-cally, what quantitative empirical evi-dencethere was tended to favor oneorthe other of the ecological hypoth-eses,1 whereas the evidence adducedin favor of the social brain hypothesiswas, at best, anecdotal.6 In this article,I shall first show how we can testbetween the competing hypothesesmore conclusively and then considersome of the implications of the social

brain hypothesis for humans. Finally,I shall briefly consider some of theunderlying cognitivemechanismsthatmight beinvolved.

TESTING BETWEEN ALTERNATIVE

HYPOTHESES

To test between the competing hy-potheses, we need to force thehypoth-eses into conflict in such a way thattheir predictions are mutually contra-dictory. This allows the data to dis-

criminate unequivocally betweenthem. In the present case, we can dothis by asking which hypothesis bestpredicts the differences in brain sizeacross the primate order. To do so, weneed to identify the specific quantita-tivepredictions made by each hypoth-esis and to determine an appropriatemeasure of brain size.

The four classes of hypotheses thathave been put forward to explain pri-mate brain evolution are epiphenom-enal, developmental, ecological, andsocial in orientation (Table 1). Theepiphenomenal and developmental hy-potheses share the assumption thatevolution of thebrain (or brain part) isnot a consequence of external selec-tion pressures but rather simply aconsequence of something to do withthe way biological growth processesareorganized.The epiphenomenal hy-potheses thus argue that brain evolu-tion is a mere byproduct of body sizeevolution, and that brain part size is,in turn, a byproduct of total brainevolution.11

The developmental versions differonly in that they provide a more spe-cific mechanism by presuming thatmaternal metabolic input is the criti-cal factor influencing brain develop-ment. This claim is given credibility bythe fact that the bulk of brain growthin mammals occurs prenatally. In-deed, it appears to be the completionof brain development that precipitatesbirth in mammals, with what littlepostnatal brain growth occurs beingcompleted by the time an infant isweaned. From this, the conclusion isdrawn that brain evolution must beconstrained by the spare energy, overandaboveher basal metabolic require-ments, that the mother has to channelinto fetal development.12–14 Some evi-dence in support of this claim comesfrom the fact that frugivorous pri-mates have larger adult brains relative

Robin Dunbar is Professor of EvolutionaryPsychology and Behavioural Ecology atthe University of Liverpool, England. Hisresearch primarily focuses on the behav-ioral ecology of ungulates and human andnonhuman primates, and on the cognitivemechanisms and brain components thatunderpin the decisions that animals make.He runsa large research group, withgradu-ate students working on many differentspecies on four continents.

Key Words: brain size, neocortex, social brainhypothesis, social skills, mind reading, primates

Conventional wisdom over the past 160 years in the cognitive and neurosciences

has assumed that brains evolved to process factual information about the world.

Most attention has therefore been focused on such features as pattern recognition,

color vision, and speech perception. By extension, it was assumed that brains

evolved to deal with essentially ecological problem-solving tasks. 1

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to body size than do folivorous pri-mates.1 This has been interpreted asimplying that frugivores have a richerdiet than folivores do and thus havemore spare energy to divert into fetalgrowth. L arge brains are thus seen asa kind of emergent epigenetic effect of sparecapacity in thesystem.

Both kinds of explanations sufferfrom the problem that they ignore afundamental principle of evolutionarytheory, which is that evolution is theoutcome of the balancebetween costsandbenefits. Becausethecost of main-taining a large brain is so great, it isintrinsically unlikely that large brainswil l evolve merely because they can.Largebrains will evolve only when theselection factor in their favor is suffi-cient to overcome thesteep cost gradi-ent. Developmental constraints areun-doubtedly important, but rather thanbeing causal their role is that of aconstraint that must be overcome if larger brains areto evolve. In addition,Pagel and H arvey15 have shown that

the energetic arguments do not addup: P recocial mammals do not havehigher metabolic rates than do altri-cial mammals despite the fact thatthey have neonatal brain sizes thatare, on average, twice as large. Wetherefore do not need to consider ei-

ther epiphenomenal or developmentalhypotheses any further in the contextof this article.

This does not necessarily mean thatthese explanations are wrong. Bothkinds of explanation may be true inthe sense that they correctly identifydevelopmental constraints on braingrowth, but they do not tell us whybrains actually evolved as they did. They may tell us that if you want toevolve a large brain, then you mustevolve a large body in order to carrytheenergetic costs of doing so or a diet

that ensures sufficient energy to pro-vide for fetal brain development. Nosuch allometric argument can everimply that you have to evolve a largebrain or a large body. The large brainor brain part is a cost that animalsmust factor into their calculationswhen considering whether or not alargebody or a largebrain is a sensiblesolution to a particular ecologicalproblem. Shiftsto more energy-rich ormore easily processed diets may beessential precursors of significant in-creases in brain or brain part size.2

This would explain why frugivoreshave larger brains than folivores doand why hominids have larger brainsthan great apes do.

This leaves us with just two classesof hypotheses, the ecological and thesocial. At least three versions of theformer can be identified, which I willterm the dietary, mental maps, andextractive foraging hypotheses. I n es-sence, these argue, respectively, that

primatespecies will need larger brainsif (i) they arefrugivorousbecausefruitsare more ephemeral and patchy intheir distribution than leaves are, andhence require more memory to find;(ii) they have larger ranges becauseof the greater memory requirements of large-scale mental maps; or (iii) theirdiet requires them to extract resourcesfrom a matrix in which they are em-bedded (e.g., they must remove fruitpulp from a case, stimulate gum flowfrom a tree, extract termites from atermitarium, or hunt species that are

cryptic or behave evasively).For obvious reasons, I used theper-

centageof fruit in thediet as an appro-priateindex for thedietary hypothesis.I used the size of the range area andthelength of theday journey asalterna-tive indices for the mental mappinghypothesis, though I present the dataonly for thefirstof thesehere. Thefirstindex correspondsto thecasein whichanimals have to be able to manipulateinformation about the locations of re-sources relative to themselves in aEuclidean space (an example would

be the nut-cracking activities of the Taı̈ chimpanzees16); the second corre-sponds to the possibility that the con-straint lies in theneeds of some aspectof inertial navigation. The extractiveforaging hypothesisis less easy to char-acterize in quantitative terms becausethere is no objective measure of thedegree to which diets vary i n theirextractiveness. However, Gibson4 pro-vided a classification of primate spe-cies i nto four categories of diet thatdiffer in their degree of extractiveness.We can test this hypothesis by askingwhether there is a consistent variationin brain size among these four catego-ries, with the species having the moreextractive diets having larger brainsthan those with the less extractivediets.

Finally, we need an index of socialcomplexity. In my original analyses, Iused social group size as a simplemeasure of social complexity. Althoughat best rather crude, this measurenonetheless captures oneaspect of the

TABLE 1. Hypotheses Used to Explain the

Evolution of Large Brains in Primates

Hypothesis Sources

A. Epiphenomenal

hypotheses

1. Large brains (or brain parts)

are an unavoidable conse-

quence of having a largebody (or brain) 11, 70

B. Ecological hypotheses

2. Frugivory imposes higher

cognitive demands than

folivory does 1, 65

3. Brain size constrains the size

of the mental map: 1

(a) constraint on size of

home range

(b) constraint on inertial

navigation (day journey

length)

4. Extractive foraging

hypothesis 3, 4

C. Social hypotheses 5. Brain size constrains size of

social network (group size):

6, 71,

72

(a) constraint on memory

for relationships

(b) constraint on social skills

to manage relationships

D. Developmental

hypotheses

6. Maternal energy con-

straints determine energy

capacity for fetal brain

growth

12, 13

46, 55,

73

Because the cost of

maintaining a large brainis so great, it is

intrinsically unlikely that

large brains will evolvemerely because they

can. Large brains will

evolve only when the

selection factor in theirfavor is sufficient to

overcome the steep costgradient.

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complexity of social groups, the factthat information-processing demandscan be expected to increase as thenumber of relationships involved in-creases. M ore importantly, perhaps,this measure has the distinct merit of being easily quantified and widelyavailable. Although it is possible toconceive of a number of better mea-sures of social complexity, the appro-priate data are rarely available formore than oneor two species.

The second problem concerns themost appropriate measure of brainevolution. Hitherto, most studieshaveconsidered the brain as a single func-tional unit. This view has been rein-forced byF inlayandDarlington,11 whoargued that theevolution in brain partsize closely correlates with the evolu-tion of total brain size and can beexplained simply in terms of allome-tric consequences of increases in totalbrain size. However, Finlay and Dar-lington failed to consider thepossibil-ity that changes in brain size mightactually be driven by changes in itsparts rather than in the whole brain. This is especially true of the neocor-tex, for its volumeaccounts for 50% to80% of total brain volumein primates. Thus, changes in the volume of theneocortex inevitably have a large di-rect effect on apparentchangein brainvolume that may bequiteunrelated tochanges in other brain components. This point is given weight by the factthat Fi nlay and Darlington themselves

showed that neocortex size is an expo-nential function of brain size, whereasother brain componentsare not.

Finlay and Darlington11 notwith-standing, there is evidence that brainevolution has not been a history of simple expansion in total volume.Rather, brain evolution has been mo-saic in character, with both the rateand the extent of evolution havingvaried between components of thesys-tem. M acL ean17 pointed out manyyearsago that primatebrain evolutioncan be viewed in terms of three majorsystems (his concept of the triunebrain). These systems correspond tothe basic r eptili an brain (hind- andmidbrain systems), the mammalianbrain (palaeocortex, subcortical sys-tems), and theprimatebrain (broadly,the neocortex). A more importantpoint, perhaps, is that variations canbe found within these broad catego-ries in the rates at which differentcomponents expanded, which, in atleast some cases, have been shown tocorrelatewith ecological factors.10Par-tialling out the effects of body size onthe size of brain components suggeststhat the story may be more complexthan Finlay and Darlington11 sup-posed, with some remodeling of braingrowth patterns occurring in thetran-sitions between insectivores, prosim-ians, and anthropoids.18

The important point in the presentcontext is that, asPassingham19 noted,relative to the more primitive parts of

the brain such as the medulla, theneocortexshowsdramatic andincreas-ing expansion across the range of pri-mates (Fig. 1). The neocortex is ap-proximately the same size as themedulla in insectivores; however, it isabout 10 times larger than the me-

dulla in prosimians and 20–50 timeslarger in the anthropoids, with thehuman neocortex being as much as105 times thesizeof themedulla.

This suggests that rather than look-ing at total brain size, as previousstudieshavedone, weshould in fact beconsidering the brain system, namelythe neocortex, that has been mainlyresponsible for the expansion of theprimate brain. From the point of viewof all the hypotheses of primate brainevolution, this makes sense: The neo-

cortex is generally regarded as beingthe seat of those cognitive processesthat we associate with reasoning andconsciousness, and therefore may beexpected to be under the most intenseselection from the need to increase orimprovethe effectivenessof thesepro-cesses.

One additional problem needs to beresolved. In his seminal study of brainevolution, J erison20 argued that brainsize can beexpected to vary with bodysize for no other reason than funda-mental allometric relationshipsassoci-ated with the need to manage thephysiological machinery of the body.What is of interest, he suggested, isnot absolute brain size, but the sparebrain capacity over and above thatneeded to manage body mechanisms.

Figure 1. Neocortex volume as a ratio of medulla volume in different groups of primates (after

Passingham19). Source: Stephan et al29

. . . brain evolution has

not been a history ofsimple expansion in total

volume. Rather, brain

evolution has beenmosaic in character,

with both the rate and

the extent of evolution

having varied betweencomponents of the

system.

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For this reason, J erison derived hisencephalization quotient. All subse-quent studies have used body size astheappropriatebaselineagainst whichto measure relativedeviations in brainsize. However, a problem has sinceemerged: Brain size is determined

early in development and, comparedto many other body systems, appearsto be highly conservative in evolution-ary terms. As a result, body size canoften changedramatically bothontoge-netically across populations in re-sponse to local environmental condi-tions21 and phylogenetically22,23

without corresponding changes inbrain size. This is particularly con-spicuous in thecase of phyletic dwarfs(e.g., calli trichids and perhaps mod-ern humans andhylobatids22) and spe-cies in which body size may have

increased in response to predationpressure following the occupation of more open terrestrial habitats (e.g.,papionids24).

The labili ty of body size thereforemakes it a poor baseline, though onethat probably is adequate for analyseson the mouse-elephant scale. Conse-quently, it is necessary to find an inter-nally moreconsistent baseline for taxo-nomically fine-grained analyses.Willner22 suggested that either molartooth size or brain size may be suit-able because both are developmen-

tally conservative. Becausewe arecon-cerned with brain part size, someaspect of brain size seems the mostappropriate.

At this point, threeoptionsareavail-able. Onei s to compare theneocortex,the brain part of interest, with thewhole brain; the second is to use therest of thebrain other than the part of interest; the third is to use some lessvariable primitive component of thebrain, such as the medulla, as a base-line. Two options are in turn availableas mechanisms for controlling forbrain size in each of these cases. Oneis to use residuals from a commonregression line against the baseline(e.g., theresidual of neocortex volumeon total brain volume or medula vol-ume). Theother choiceis to useratios.

We have considered and tested allthese options10,24 (see Box 1). The re-sults are virtually identical irrespec-tive of which measure i s used. Oneexplanation for this may be that allthesemeasuresactually indexthesame

thing, absolute neocortex size, mainlybecause the neocortex i s such a largecomponent of the primate brain. In-deed, the use of absolute neocortexsize produces results that are similarto thoseobtained from relativized indi-ces of neocortex volume.24,25 This

makes some sense in computationalterms: As Byrne26 has pointed out, a10% increasein the processing capac-ity of a small computer is worth agreat deal less in information-process-ing terms than is a 10% increase in alarge computer. Although residualsfrom a common regression line wouldconventionally be considered the saf-est measure, and have been used inmany recent analyses,27,28 I shall con-

tinue to use my original ratio indexbecause it provides the best predictor(see Box 1).

Finally, it is now widely appreciated

thatcomparativeanalyses need to con-

trol for the effects of phylogeneticinertia. Closely related species can be

expected to have similar values for

many anatomical and behavioral di-

mensions merely by virtue of having

inherited them from a recent common

ancestor. In such cases, plotting raw

data would result in pseudoreplica-

tion, artificially inflating the sample

size by assuming that closely related

speciesare actually independent evolu-

tionary events. The ways of dealing

with this problem include plotting

means for higher taxonomic units,per-

forming nested analyses of variance

using phylogenetic levels as factors,

comparing matched pairs of species,

andmaking independent contrasts that

control directly for phylogeny. Each

method has its own advantages and

disadvantages, but the first and third

procedures are particularly associated

with loss of information and small

sample sizes. I shall use the first and

last method, the last because it allows

individual species to becompared, but

the first because it allows grade shifts

within data sets to be identified (a

problem that independent-contrasts

methods have difficulty dealing with).

I shall take the genus as a suitable

basis for analysis becausegenera typi-cally represent different reproductive

or ecological radiations and thus are

more likely to constitute independent

evolutionary events.

The resulting analyses arerelatively

straightforward: Figure 2 presents the

datafor neocortex ratio for theanthro-

poid primate species in the data base

of Stephan, Frahm, and Baron.29 Neo-

cortex size, however measured, does

not correlate with any index of the

ecological hypotheses, but does corre-

late with social group size. Similarfindings were reported by Sawaguchi

and K udo,30 who found that neocortex

size correlated with mating system in

primates. Barton and Purvis31 have

confirmed that using both residuals of

neocortex volume on total brain vol-

ume and the method of independent

contrasts yields the same result. Both

Barton10 and T. J offe (unpublished)

have repeated the analyses using the

medulla as the baseline for compari-

son. M ore importantly, Barton and

Purvis31 have shown that while rela-tive neocortex volume correlates with

group size but not the size of the

ranging area, the reverse i s true of

relative hippocampus size. A correla-

tion between range area and hippo-

campus sizeis to be expected because

of hippocampal involvement in spatial

memory.32,33 This correlation demon-

strates that it is not simply total brain

sizethati simportant (apotential prob-lem, given the overwhelming size of

The neocortex isgenerally regarded as

being the seat of thosecognitive processes that

we associate with

reasoning andconsciousness, and

therefore may be

expected to be underthe most intense

selection from the needto increase or improvethe effectiveness of

these processes.



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the primate neocortex). M oreover, itpoints to the specific involvement of the neocortex.

The validity of this relationshipcould be tested directly by using it topredict group sizes in a sample of

species for which brain volumetricdata were not available in the originalsample of Stephan, Frahm, and

TABLE 2. Stepwise Regression Analysis

of Indices of Brain Component Volume

as Predictors of Group Size in

Anthropoid Primates, Based on

Independent Contrasts Analysis*

Independent Variable t P

Absolute brain volume 1.69 0.107

Residual of brain volume

on body mass 0.91 0.371Absolute telencephalon

volume 1.72 0.101

Residual of telen-

cephalon volume on

body mass 0.61 0.546

Residual of telen-

cephalon volume on

brain volume 1.69 0.107

Absolute neocortex

volume 1.70 0.104

Residual of neocortex

volume on body mass 0.56 0.583

Residual of neocortex

volume on brain

volume 1.60 0.136Neocortex ratio (against

rest of brain) 3.79 0.001

*Sample: 24 species of anthropoid pri-

mates from Stephan, Frahm, and

Baron.29

Box 1. How to Measure Brains

R. Dunbar and Tracey H. Joffe

The different ways of measuring

relative brain size have raised doubts

as to the most appropriate technique

to use.65 Many researchers have pre-

ferred to use residuals from the com-

mon regression line of best fit for the

data set concerned. This provides a

measure of the extent to which brain

(or brain part) volume deviates from

what would be expected for an aver-

age member of the relevant taxon of

the appropriate size. Although ratios

have been used to compare the rela-

tive size of brain components,29,66 this

has been criticized on the grounds

that trade-offs within the brain may

mean that a given index simply mea-

sures total brain size (or the size of a

brain part) and thus does not remove

the effects of absolute size. Ratios

may also be prone to autocorrelation

effects, especially when the baseline

is taken to be the whole brain and, as

in the case of the neocortex, the part in

question is a major volumetric compo-

nent of the brain.

Although there are likely to be

some trade-offs of this kind within the

brain, the fact that neocortex volume

increases progressively across the pri-

mate order suggests that such con-straints are less likely to have a signifi-

cant effect on a ratio measure. Of

course the residuals procedure is itself

a ratio: Encephalization-type indices

are calculated as actual volume di-

vided by predicted volume (which,

when data are logged, becomes the

conventional actual minus predicted

values). Thus, ratio measures per se

may not be the problem. Rather, the

substantive objection is whether or not

a ratio partials out the allometric ef-

fects of body size. In fact, it seems that

neocortex ratios are not correlatedwith the basal brain (i.e., brain volume

excluding the neocortex) within major

taxonomic groups (unpublished analy-

ses). Consequently, this criticism has

less force than it might appear to have

on first sight. Moreover, any index that

uses the whole brain as its base is

likely to suffer from autocorrelation

effects. Because the neocortex is such

a large proportion of the brain in pri-

mates, residuals of neocortex from

total brain size may simply be a mea-

sure of neocortex plotted against it-

self.

To consider the problem in more

detail, we ran a stepwise regression

analysis on the 24 species of anthro-

poid primates, including humans, on

the data base of Stephan, Frahm, and

Baron,29 with group size as the depen-

dent variable and nine indices of rela-

tive brain or brain-part volume as inde-

pendent variables. In addition toneocortex ratio, these included total

brain volume as well as telencephalon

and neocortex volume, each taken as

absolute volume and as a residual

from both body mass and brain vol-

ume. All variables were log10-trans-

formed for analysis. In both cases,

neocortex ratio was selected as the

variable of first choice. We carried out

both regressions on generic plots and

independent contrast analyses. For

the contrasts analysis, the best fit

least-squares regression equation

through the origin was:

Contrast in log10 (group size) 3.834

* Contrast in log10 (neocortex ratio)

(r 2 0.395, F 1,22 15.39,

P 0.001).

With all other variables held constant,

none of the other eight indices made a

significant contribution to the variabil-

ity in group size in either analysis.

Table 2 gives the results for the inde-

pendent contrasts analysis.

Neocortex ratio is thus the singlemost powerful predictor of group size

in these species. While the biological

significance of this variable remains

open to interpretation, the fact that it

provides the best predictor, indepen-

dently of all other confounding mea-

sures, suggests that more detailed

consideration needs to be given to its

significance and meaning. It may be,

for example, that body size, rather

than being a determinant20 is simply a

constraint on neocortex size: A spe-

cies can evolve a large neocortex only

if its body is large enough to provide

the spare energy capacity through

Kleiber’s relationship for basal meta-

bolic rate to allow for a larger than

average brain. This interpretation is

implied by the Aiello and Wheeler2

‘‘expensive tissue hypothesis.’’It would

also be in line with Finlay and Darling-

ton’s11 claim that in mammals the evo-

lution of brain-part size is driven, devel-

opmentally at least, by the evolution of

the whole brain, thus generating very

tight correlations between brain-part

size and total brain size.



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Baron.29 I did this by exploiting thefact that neocortex ratios can be pre-dicted from total brain volume,34 aresult that, in fact, follows directlyfrom the Finlay and Darlington11 find-ings. The result was a significant fitbetween predicted neocortex ratio andobserved mean group size for a sam-ple of 15 New and Old World monkeyspecies.35

Barton27 noted that the originalanalyses of Dunbar24 seemed to implythat variation in neocortex size wasmuch greater than variation in groupsize in the prosimians. Using Dun-bar’s24 data on group size, Barton sug-gested that the relationship betweenneocortex and group size did not ap-ply in the case of prosimians. How-ever, the data on prosimian groupsizes in this sample suffered from apaucity of data, particularly for thenocturnal species. Because many of theseare described as semi-solitary, itwas conservatively assumed in theDunbar24 database that their groupsize was one. M ore recent field studieshave produced markedly improved es-

timates of the sizes of social groupsand, in the case of the semi-solitaryspecies, daytime nest groups.36 Re-analysis of the data for prosimiansusing these improved estimates of so-cial group size suggests that thesespecies do in fact adhere to the samerelationship between neocortex andgroup size as that which pertains forother primates.25 M ore importantly,the regression line for this taxon isparallel to, but shifted to the left of,that for other anthropoid primates(Fig. 3).

This relationship has now beenshown to hold for at least four othermammalian orders: bats,10 carnivoresand insectivores,37,38 and odontocetecetaceans.39,40 In the case of the insec-tivores, the data points are shifted farto theleft of those for the primates, asmight be expected of a taxonomicgroup that is considered to bebroadlyrepresentative of the ancestral mam-mals.37 However, the relationship isweak in this case, probably becauseestimates of group size are particu-larly uncertain for insectivores.

Surprisingly, the data for the carni-

vores map directly onto those for the

simian primates, that is, the regres-

sion lines for the two data sets do not

differ significantly. However,thecarni-

vores do not exhibit as widea range of

neocortex ratios or group sizes as do

anthropoid primates. The fact that theprosimians lie to the left of both these

taxonomic groupsimplies that thecar-

nivores represent an independent evo-

lutionary development alongthesameprinciples astheanthropoid primates,

thedifferencebeing that they just have

not taken it as far as primates have.

One reason for this may be that thecarnivore social world is olfaction-dominated rather than vision-domi-

nated, as in the case of the primates.

Barton10,27,41 has pointed out that the

shift to a diurnal lifestyle based on

color vision, perhaps initially diet-

driven, but leading to a shift into vi-

sion-based communication, may bethekey featurethat has spurred on the

dramatic development of the primate

neocortex.

Figure 2. Relative neocortex size in anthropoid primates plotted against (a) percentage of fruit in the diet, (b) mean home-range size scaled as

the residual of range size regressed on body weight (after Dunbar24), (c) types of extractive foraging (after Gibson4), and (d) mean group size.

((a), (b), and (d) are redrawn from Dunbar 24, Figures 6, 2 and 1, respectively; (c) is from Dunbar,35 Figure 2.)



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REFINING THE RELATIONSHIP

The social brain hypothesis impliesthat constraints on group size arisefrom the information-processing ca-pacity of the primate brain, and thatthe neocortex plays a major role inthis. However, even this proposal isopen to several interpretations as tohow the relationship is mediated. Atleast five possibilities can be usefullyconsidered. The constraint on groupsize could be a result of the ability torecognize and interpret visual signalsfor identifying either individuals ortheir behavior; limitations on memoryfor faces; the ability to remember whohas a relationship with whom (e.g., alldyadic relationships within the groupas a whole); the ability to manipulateinformation about a set of relation-ships;andthecapacity to processemo-tional information, particularly withrespect to recognizing and acting oncuesto other animals’emotional states. Theseare not all necessarily mutuallyexclusive, but they do identify differ-ent points in thecognitivemechanismthat might be thecrucial information-processing bottleneck.

Although visual mechanisms arelikely to be important for social inter-action, and may well have been the

initial kick for the evolution of largebrains in primates,10 it seems intrinsi-cally unlikely that the ultimate con-straint lies in the mechanisms of thevisual system itself.28 Although thereis a correlation between the relative

sizeof the visual cortex and group sizein anthropoid primates, thefit is muchpoorer, and theslopesignificantly shal-lower than that between thenonvisualneocortex and group size(r 2 0.31 vsr 2 0.61, respectively) (Fig. 4). Partialcorrelation analysis indicates that onlythe correlation for the nonvisual rela-tionship remains significant when theother component is held constant28

(though this is not true for prosim-ians25). A more important point is thatthe volume of the lateral geniculatenucleus, a major subcortical way sta-tion in visual processing, does notcorrelatewith groupsizeat all, indicat-ing that pattern recognition per se isunlikely to be the issue.28 It may be of some significance that the absolutesize of thevisual cortex seemsto reachan asymptotic value i n the great apeclade, whereas the nonvisual neocor-tex continues to increase in size. Oneinterpretation of this is that visualprocessing does not necessarily con-tinue to improve indefinitely as the

size of thecortical processingmachin-ery increases, at least relative to theopportunitycost of taking cortical neu-rons away from other cognitive pro-cesses.

It seems equally unlikely that theproblem lies with a pure memory con-

straint, though memory capacity obvi-ously mustimposesomekind of upperlimit on the number of relationshipsthat an animal can have. There arethree reasons for this claim. First, inhumans at least, memory for faces isan order of magnitude larger than thepredicted cognitive group size: Hu-mans are said to be able to attachnames to around 2,000 faces but havea cognitive group size of only about

150. Second, there is no intrinsic rea-

son to suppose that memory per se is

the issue. The social brain hypothesis

is about theability to manipulateinfor-

mation, not simply to remember it.

Third, and perhaps most significantly,memories appear to be stored mainly

in the temporal lobes,42 whereas re-

cent PE T scan studies implicate the

prefrontal neocortex, notably Brod-

man area 8, as the area for social skills

and, specifically, theory of mind.43

Frith44 has suggested that memories

and representations for objects or

events may involve interactions be-

tween several levels of the neocortex

depending on the kinds of operations

Figure 3. Mean group size plotted against neocortex ratio for individual genera, shown

separately for prosimian, simian, and hominoid primates. Prosimian group size data, from

Dunbar and Joffe,25 include species for which neocortex ratio is estimated from total brain

volume. Anthropoid data are from Dunbar.24 Simians: 1, Miopithecus; 2, Papio; 3, Macaca; 4,

Procolobus; 5, Saimiri; 6, Erythrocebus; 7, Cercopithecus; 8, Lagothrix; 9, Cebus; 10, Ateles; 11,

Cercocebus; 12, Nasalis; 13, Callicebus; 14, Alouatta; 15, Callimico; 16, Cebuella; 17, Saguinus;

18, Aotus; 19, Pithecia; 20, Callicebus. Prosimians: a, Lemur; b, Varecia; c, Eulemur; d, Propithe-

cus; e, Indri; f, Microcebus; g, Galago; h, Hapalemur; i, Avahi; j, Perodictus.

The social brainhypothesis implies thatconstraints on group size

arise from the

information-processingcapacity of the primate

brain, and that the

neocortex plays a majorrole in this. However,

even this proposal is

open to severalinterpretations as to how

the relationship is

mediated.



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involved. These interactions could oc-cur between the sensory and associa-tion cortices (perceiving an object),between the association and frontal

cortices (remembering an object), andamong all three (being aware of per-ceiving an object). It is worth notinginthis context that although social skillsarecommonly disrupted by damage tothe prefrontal cortex, memory forevents and peopleis not.42

It seems unlikely that emotional re-sponses per se are the substantiveconstraint. Although the correct emis-sion and i nterpretation of emotionalcues is of singular importance in themanagement of social relationships,45

there is little evidence that thesubcor-tical areas principally associated withemotional cuing (for example, theamygdala in the limbic system) corre-late in any way with social groupsize.28 Indeed, K everne, Martel, andNevison46 point out that there hasbeen progressivereduction in therela-tive sizes of the ‘‘emotional’’ centers inthe brain (the hypothalamus and sep-tum) in favor of the ‘‘executive’’ cen-ters (the neocortex and striate cortex)during pri mate evolution. They inter-

pret this in terms of a shift away fromemotional control of behavior to moreconscious, deliberatecontrol.

The only remaining alternative is

that the mechanisms involved lie i nthe ability to manipulate informationabout social relationships themselves. This claim is supported by six addi-tional lines of evidence that point tothe fundamental importance of socialskills in the detailed management of social relationships.

Onei s the fact that close analysis of the data on group size and neocortexvolumesuggests that there are, in fact,distinct grades even within theanthro-poid primates (Fig. 3). Apes seem to lieon a separategradefrom themonkeys,which in turn lie on a separate gradefrom theprosimians. The slopecoeffi-cients on these separate regressionlinesdo not differ significantly, but theintercepts do. It is as if apes requiremore computingpower to manage thesame number of relationships thatmonkeys do, and monkeys i n turnrequiremorethan prosimiansdo. Thisgradation corresponds closely to theperceived scaling of social complexity.

The second line of evidence is that

therates with which tactical deceptionare used correlate with neocortexsize.26 Species with large neocortexratios make significantly more use of tactical deception, even when the dif-ferential frequencies with which theselarge-brained species have been stud-

ied are taken into account. Third, Pawlowski, Dunbar, andLowen47 have shown that among po-lygamous primates the male rank cor-relation with mating success is nega-tively related to neocortex size(Fig. 5). This is just what we would predict if the lower ranking males of specieswith larger neocortices were able tousetheir greater computational capaci-ties to deploy more sophisticated so-cial skills, such as theuseof coalitionsand capitalizing on female matechoice, to undermine or circumvent

thepower-based strategies of thedomi-nant animals.

The fourth line of evidence is J of-fe’s48 demonstration that adult neocor-tex sizein primates correlates with thelength of the juvenile period, but notwith the length of gestation, lactation,or the reproductive life span, eventhough total brain size in mammalscorrelates with thelength of thegesta-tion period.49,50 This suggeststhat whatis most i mportant in the developmentof a large neocortex in primates is notthe embryological development of brain tissueper se, which is associatedmainly with gestation length, butrather the ‘‘software programming’’that occurs during the period of sociallearning between weaning and adult-hood.

Fifth, Kudo, Lowen, and Dunbar51

have shown that grooming cliquesize,a surrogate variable that indexes alli-

Figure 4. Independent contrasts in mean group size plotted against contrasts in the visual

cortex and the volume of the rest of the neocortex (nonvisual neocortex) for individual

anthropoid species. Note that the visual cortex is here defined as visual area V1; the nonvisual

cortex is the non-V1 volume of the neocortex and thus includes some higher order visual

processing components (e.g.,visual area V2). Unfortunately, thedata base of Stephan, Frahm,

and Baron29 doesnot allow usto define our measure ofthe nonvisual areaany more finely than

this. (Reprinted from Joffe and Dunbar,28 Fig. 1.)

. . . there is no intrinsicreason to suppose that

memory per se is the

issue. The social brainhypothesis is about the

ability to manipulate

information, not simply toremember it.



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ancesize, correlates rather tightly withrelative neocortex and social groupsize in primates, including humans(Fig. 6). The human data derive fromtwo samples: hair-care networksamong female bushmen52 and supportcliques among adults in the UnitedK ingdom.53 What is remarkableis howclosely the human data fit with thedata from other primate species.Grooming cliques of this kind invari-ably function as coalitions in primategroups. Coalitionsarefunctionally cru-cial to individuals within these groupsbecause they enable the animals tominimize thelevels of harassment andcompetition that they inevitably sufferwhen living in close proximity to oth-ers.54 Coalitions essentially allow pri-mates to manage a fine balancing actbetween keeping other individuals off their backs while at the same timeavoiding driving them away altogetherand thereby losing the benefits forwhich the groups formed in the firstplace. Theseresults can thus probablybe interpreted as a direct cognitivelimitation on the number of individu-als with which an animal can simulta-neously maintain a relationship of suf-

ficient depth that they can berelied onto provide unstinting mutual supportwhen one of them is under attack.Because this is the core process that

gives primatesocial groups their inter-nal structure and coherence, this canbe seen as a crucial basis for primatesociality.

Fi nally, K everne, Martel, and Nevi-son46 have suggested that the neocor-tex and striate cortex, those areas of

theprimate brain that are responsiblefor executive function, are under ma-ternally rather than paternally im-printed genes (i.e., genes that ‘‘know’’which parent they came from),whereas the converse is true for thelimbic system, those parts of thebrainmost closely associated with emo-tional behavior. They interpret this inrelation to the cognitive demands of the more intense social life of femalesin matrilineal female-bonded societ-ies.

IMPLICATIONS FOR HUMAN

GROUPS

The fact that the relationship be-tween neocortex size and what I willterm thecognitivegroup size holdsupso well in so many different taxonomicgroups raises the obvious question of whether or not it also applies to hu-mans. Wecan easily predict a valueforgroup sizein humans. Doingso,whichis simply a matter of using thehumanneocortex volume to extrapolate avalue for group size from the primate

Figure 5. Independent contrasts in the Spearman rank correlation (r s ) between male rank and

mating success plotted against contrasts in neocortex size for two different male cohort sizes (4

to 8, and 9 to 30 males) for individual species. The regression equations for the two cohort sizes

are significantly differentfrom b 0. Thespecies sampled are C. apella, P. entellus,C. aethiops,

M. fuscata, M. mulatta, M. radiata, M. arctoides, P. cynocephalus, P. anubis, P. ursinus, and P.

troglodytes. (Redrawn from Pawlowski, Dunbar, and Lowen,47 Fig. 1.)

Figure 6. Mean grooming clique size plotted against mean neocortex ratio for individual

primate genera. The square is Homo sapiens. Species sampled are L. catta, L. fulvus, Propithe-

cus, Indri, S. sciureus, C. apella, C. torquatus, A. geoffroyi, A. fusciceps, P. badius, P. entellus, P.

pileata, P. johnii, C. campbelli, C. diana, C. aethiops, C. mitis, E. patas, M. mulatta, M. fuscata,

M. arctoides, M. sylvana, M. radiata, P. anubis, P. ursinus, P. cynocephalus, P. hamadryas, T.

gelada, P. troglodytes, P. paniscus. (Redrawn from Kudo, Lowen, and Dunbar,51 Fig. 4a.)



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equation, produces a value in the or-der of 150. The real issue is whetherhumans really do go around in groupsof this size.

I dentifying the relevant level of grouping to measure in humans isdifficult because most humans live ina series of hierarchically inclusivegroups. This, in itself, is not especiallyunusual: Hi erarchically structuredgroups of this kind are characteristicof primates54 and may be typical of many mammals and birds.55 At leastin the case of the diurnal primates, itseems that, with a few notable excep-tions, the various species’ groupingpatterns exhibit an overt level of stabil-ity at roughly the sameposition in thehierarchy across a wide range of taxa.M oreover, because the various layersof this hierarchy appear to be inti-mately related to each other, probablythrough being part of a seriesof cause-and-consequence chains,51 it wouldnot matter which particular groupinglevel (for example, stable social group,

network, or grooming clique) wastaken to bethe grouping criterion.

The problem with respect to hu-mans is that it is difficult to identifywhich of the many potential groupinglevels is functionally or cognitivelyequivalent to the particular level of grouping that I happened to use forprimates. This difficulty is particularlyintrusive in this case because humanslivein a dispersed social system some-times referred to as a fission-fusionsystem. In order to get around thisproblem, I adopted the conversestrat-egy in my original analysis,56 askingwhether there was any group sizecon-sistently characteristic of humans thatwas of about the requisite size and, if so, whether its intrinsic psychologicalcharacteristics were similar to thosefound in primategroups.

Because of the structural complex-ity of postagricultural societies, I con-sidered only traditional hunter-gath-erer and small-scale horticulturalsocieties. Although census data on

such societies are limited, those thatare available suggest that there is in-deed a consistent group size in theregion of 150 individuals (Fig. 7). E x-cept among settled horticulturalists,where the village seems to be therelevant unit, this typically involves

theset of individuals from whom over-night camps are easily and regularlyformed. Such groups are not oftenconspicuous as physical entities (theydo not often appear together in oneplace at one time), but they do invari-ably have important ri tual functionsfor the individuals concerned. AmongAustralian aboriginals, for example,the relevant group is the clan, whichmeets from time to time in jamboreeswhere the rituals of life (marriagesand rites of passage) are enacted andtales of the old times are rehearsed to

remind everyone who they are andwhy they hold a particular relation-ship to each other. Indeed, this genu-inely seems to be the largest group of people who know everyone in thegroup as individuals at the level of personal relationships. Thi s is essen-tially the definition that holds in thecaseof primates.

A more extensive exploration of hu-man groups in other contextssuggeststhat groupings of this size are wide-spread and form an important compo-nent of all human social systems, be-

ing present in structures that rangefrom business organizations to thearrangement of farming communi-ties.56 Estimates of community sizefor two traditional farming communi-ties in the United States, H utteritesandan East Tennesseemountain com-munity, and of actual social networksizes (from small-worlds experiments)(shown astriangles on theright sideof Fig. 7) fit very closely within the rel-evant range of group sizes.

It is easy, of course, to play thenumerologist in this context by find-ing groups that fit whatever group sizeonewishes to promote. The importantfeature to note here, however, is thatthe various human groups that can beidentified in any society seem to clus-ter rather tightly around a series of values (5, 12, 35, 150, 500, and 2,000)with virtually no overlap in the vari-ance around these characteristic val-ues. They seem to represent points of stability or clustering in thedegrees of familiarity within the broad range of

Figure 7. Mean sizes for different types of groups in traditional human societies. Individual

societies are ordered along the bottom, with data for three main types of social groups

(overnight camps, clans or villages, and tribes). Societies include hunter-gatherer and settled

horticulturalists from Australia, Africa, Asia, and North and South America. The triangles give

mean group sizes for three contemporary United States samples: mean network size from

small-worlds experiments (N 2),67 mean Hutterite community size,68 and the size of an East

Tennessee mountain community.69 The value of 150 predicted by the primate neocortex size

relationship (from Fig. 1d) is indicated by the horizontal line, with 95% confidence intervals

shown as dashed lines.



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human relationships, from the mostintimateto themost tenuous.

COGNITIVE MECHANISMS

The suggestion that the mecha-nismsinvolved in theseprocesses maybe concerned with social skills raisesthe issue alluded to by the originalM achiavellian intelligencehypothesis,namely to what extent cognitively so-phisticated mechanismsconferring theability to ‘‘mind-read’’ might be in-volved. Tactical deception, in its strongsense, i mplies the ability to hold falsebeliefs and, thus, the presence of theability known as ‘‘theory of mind’’(ToM). Of course, tactical deception aspracticed by primates on a daily basismay not, as Byrne26 himself haspointed out, be quite as sophisticatedas first impressions suggest. A moreconventional behaviorist accountbased on simple associative learningcan i nvariably be given for almost allexamples reported in theliterature.

Nonetheless, convincing evidencesuggests that humans at least do use ToM in executing some of their moremanipulative social activities. Andwhilewe may not wish to attribute full ToM to all primates, at least circum-stantial evidence suggests that basic ToM is present i n great apes and thatmonkeys may aspire to a level thatByrne26 has described as level 1.5 in-tentionality (full ToM being level 2intentionality) (see Box 2). The differ-ence has been summed up rather

graphically by Cheney and Seyfarth’s57

observation that apes seem to be goodpsychologists in that they are good atreading minds, whereas monkeys aregood ethologists in that they are goodat reading behavior—or at least atmaking inferences about intentions inthe everyday sense, even i f not in the

philosophical senseof belief states.

Evidence that chimpanzees aspireto at least a basic form of ToM is

provided by their performance on ex-

perimental false-belief tasks.58–61 These

studies haveattempted to develop ana-

logues of the classic false-belief tasks

used with children.62 Though it is clear

that chimpanzees do not perform to

the level at which fully competent

children perform, O’Connell’s61 experi-

ments at least suggest that they can

perform at the level of children who

stand on the threshold of acquiring ToM. M ore importantly, chimpanzeesdo better than autistic adults, one of whose defining features is the lack of ToM, on thesametests.

That mind-reading, thebasis of ToM,is difficult to do has been shown byexperiments on normal adults testedon ‘‘advanced’’ ToM tasks, up to fifth-order intentionality.62 These data sug-gest that normal humans find tasks of greater than fourth-order intentional-

ity exceedingly hard to do. The higherror rates at theselevels do not reflecta memory retention problem: All sub- jects passthe tests that assess memoryfor the story line. M oreover, the samesubjects show considerable compe-tence on reasoning tasks that involvecausal chains of up to the sixth order. The difficulty seems genuinely to besomething to do with operating withdeeply embedded mental states.

One possibly significant observationin this context is that the visual andnonvisual components of the primate

neocortex do not increase isometri-cally. Although initially there is a moreor less linear increase in the visualarea V1 with increasingsizeof therestof the neocortex, this drops off withinthe great ape clade. From gorillasthrough humans, increases in the sizeof thevisual area progress moreslowlythan do increases in thesizeof therestof theneocortex.28 Weinterpret this asimplying that beyond a certain pointthe acuity of the visual system does

Box 2. A Beginner’s Guide to Intensionality

Computers can be said to know

things because their memories con-

tain information; however, it seems

unlikely that they know that they know

these things, in that we have no evi-

dence that they can reflect on their

states of ‘‘mind.’’ In the jargon of the

philosophy of mind, computers are

zero-order intensional machines. In-

tensionality (with an s) is the term

that philosophers of mind use to refer

to the state of having a state of mind

(knowing, believing, thinking, wanting,

understanding, intending, etc).

Most vertebrates are probably ca-

pable of reflecting on their states of

mind, at least in some crude sense:

they know that they know. Organisms

of this kind are first-order intensional.

By extension, second-order inten-

sional organisms know that someone

else knows something, and third-order

intensional organisms know that some-

one else knows that someone else

knows something. In principle, the se-

quence can be extended reflexively

indefinitely, although, in practice, hu-

mans rarely engage in more than

fourth-order intensionality in everyday

life and probably face an upper limit at

sixth-order (‘‘Peter knows that Jane

believes that Mark thinks that Paula

wants Jake to suppose that Amelia

intends to do something’’).

A minimum of fourth-order inten-

sionality is required for literature thatgoes beyond the merely narrative (‘‘the

writer wants the reader to believe that

character A thinks that character B

intends to do something’’). Similar abili-

ties may be required for science, since

doing science requires us to ask

whether the world can be other than it

is (a second-order problem at the very

least) and then ask someone else to

do the same (an additional order of

intensionality).

. . . apes seem to be

good psychologists inthat they are good atreading minds, whereas

monkeys are good

ethologists in that theyare good at reading

behavior . . .



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not increase linearly with size. Be-cause thetotal size of theneocortex islimited by embryological and ener-getic factors, this means that dispro-portionately more capacity can bededicated to nonvisual areas of theneocortex once the volume is above

the crucial threshold. This might ex-plain why apes appear to becapableof theadditional cognitive processing as-sociated with mind reading, whereasmonkeysarenot. It might also explainwhy humans are better at it than apes.

For humans, one important aspectof ToM concerns its relevance to lan-guage, a communication medium thatcrucially depends on understandinginterlocutors’ mental states or inten-tions. The kinds of metaphorical usesof language that characterize not onlyour rather telegraphic everyday ex-

changes (in which ‘‘you know what Imean?’’ is a common terminal clause)but also lies at the very heart of themetaphorical features of language. Asstudiesof pragmatics haveamply dem-onstrated,63 a great deal of linguisticcommunication is based on metaphor:Understanding the intentions behinda metaphor is crucial to successfulcommunication. Failureto understandthese intentions commonly results inconfusion or inappropriate responses.Indeed, without these abilities i t isdoubtful whether literature, notably

poetry, would be possible. Our conver-sations would be confined to the ba-nally factual; those fine nuances of meaning that create both theambigu-itiesof politenessand thesubtleties of public relations would not be pos-sible.64

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