Unity in diversity: Lessons from macaque societies

Unity in Diversity: Lessons From Macaque SocietiesBERNARD THIERRY

The macaque radiation is as old as the hominin radiation, approximately 7 mil-lion years. After Homo, Macaca has the widest geographical range among pri-mates, and both of these genera are present in tropical and temperate regionsas well. Whereas the single extant representative of the genus Homo divergedthrough processes of cultural diversification, extant species of macaquesemerged through processes of evolutionary diversification. Macaque societiesare characterized by profound unity and great diversity, and can best bedescribed as variations on the same theme. To understand macaque variationand adaptation, we must take into account the processes that insure the persist-ence of their societies across generations and environments.

We presently recognize 22 speciesin the macaque genus distributedinto several lineages (Box 1). On onehand, macaques share the same ba-sic patterns of grouping and disper-sal. They are semiterrestrial primatesthat form multimale, multifemalegroups that permanently containboth adult males and females withoffspring. The adult sex ratio is bi-ased toward females. Neighboringgroups have overlapping home

ranges. Most males disperse andperiodically transfer from one groupto another. Most females stay intheir natal group and maintainenduring relationships with their rel-atives, constituting matrilines thatlead to the coexistence of severalgenerations in the same group.Whereas the dominance status ofmales varies through their lifetimes,following shifts in their competitiveabilities, the positions of females inhierarchies remain quite stableowing to kin-based alliances.

On the other hand, the diversityreported in the relationships of indi-vidual macaques appears to beunmatched among nonhuman pri-mates. Macaques display varyingdegrees of dominance asymmetryand preference for kin. Affiliativebehaviors are developed in some spe-cies and limited in others. There arestriking disparities in maternal con-trol over offspring across species.Mating patterns range from regularchanges in sexual partners to pro-longed female guarding by males.

A commonly unstated assumptionis that the components of a social or-ganization can be modified sepa-rately to fulfill fitness requirements.An organization is an integratedwhole, a change in one component is

liable to induce changes in others.1,2

We may take advantage of the diver-sity of macaque societies to investi-gate correlations between behavioraltraits. To explain diversity, main-stream evolutionary thinking focuseson natural selection as the preemi-nent driving force behind adaptativeprocesses. It deals with the mutabil-ity of livings beings to explain howthey cope with the requirements ofan ever-changing environment.3 Thisapproach shaped the study of pri-mate social organization during thelast three decades, allowing us to for-mulate and test specific hypothesesabout the adaptive function ofbehaviors. Nowadays, there is grow-ing interest in the stability or, moreexactly, the robustness of livingbeings. They preserve their state ofadaptation by protecting the dynam-ics of developmental and functionalsystems against potentially disruptivefactors.3–5 To make sense of varia-tions, we must be able to specify theconstraints that shape an organiza-tion and exert strong stabilizingselection on its components.From the start of modern prima-

tology, the study of behavioral varia-tion in macaques has produced anumber of scientific discoveries. Welearned that early mother-infant sep-aration induces irreversible psycho-logical damages in the developingindividual, that kinship has over-whelming structural effects on socialrelationships, and that acquiredchanges may be socially transmittedfrom one generation to the next, giv-ing rise to traditions. The followingdecades delivered further lessons, themost remarkable of which haveemphasized the robustness of pri-mate societies and their underpin-nings: (1) Social relations remain

ARTICLES

Bernard Thierry is Research Director atthe Departement Ecologie, Physiologieand Ethologie (IPHC), Centre Nationalpour la Recherche Scientifique, Univer-site Louis Pasteur, Strasbourg, France.His research focuses on social organiza-tion and information transmission in non-human primates. He is the lead editor ofthe volume Macaque Societies: A Modelfor the Study of Social Organization, withcoeditors Mewa Singh and WernerKaumanns, published in 2004 by Cam-bridge University Press. E-mail: [email protected]

Key words: social style; correlated variation;

robustness; constraint; epigenesis; phylogeny;

Macaca

VVC 2007 Wiley-Liss, Inc.DOI 10.1002/evan.20147Published online in Wiley InterScience(www.interscience.wiley.com).

Evolutionary Anthropology 16:224�238 (2007)

Box 1. Species, PhyleticLineages and GeographicalDistribution of the Genus

Macaca

Macaques constitute a monophy-letic group of the cercopithecine sub-family. The fossil record indicatesthat they colonized Eurasia 5 to 6million years ago via the Near East.They then branched into several phy-letic lineages that have been identi-fied from morphological and molecu-lar evidence.6–11 We distinguish threemain lineages of extant macaques,corresponding to three dispersalwaves in Asia. The silenus lineagehas the most disjunct geographicaldistribution, indicating an early dis-persal. Only the pigtailed macaquehas a large distribution range. Theliontailed macaque is found in theevergreen forests of southern India.The other species of the lineageinhabit the Sulawesi and MentawaiIslands. The sinica lineage has amoderately fragmented distributionin southern Asia and is thought to bethe second lineage to have dispersed.Four of its species are found in tropi-cal and subtropical continental areas,while the fifth species, the toquemacaque, lives on Sri Lanka. Themost broadly and continuously dis-tributed lineage is fascicularis, whichis likely to be the third lineage tohave dispersed. The longtailed maca-que is present in equatorial and trop-ical regions; the other three speciesare found in subtropical and temper-ate Asia. The taxonomic position oftwo further species remains debated.The Barbary macaque, which lives inthe montane forests of North Africa,is the most ancient taxon of the ge-nus. It is alternatively classified as ei-ther being the only member of itsown species group or one belongingto the silenus-sylvanus lineage. Thestumptailed macaque inhabits broad-leaf evergreen forests of southernAsia. It is either ascribed to its ownspecies group or included in the sin-ica-arctoides lineage.6,7,9

ARTICLES Macaque Societies 225

226 Thierry ARTICLES

consistent despite individual plastic-ity; (2) variation is circumscribed toa limited number of social styles; (3)linkages between behavioral traitsarise at any level of organization; (4)cross-species contrasts are betterexplained by phylogeny than by ecol-ogy; (5) evolutionary transformationdepends on a balance between exter-nal and internal determinants; (6)mating patterns are largely inde-pendent from social styles. I willreview them in turn to examine howadaptation trades off against robust-ness in primate societies.

CONSISTENCY OF SOCIALRELATIONS: THE CASE OF THE

RHESUS MACAQUE

The social organization of eachspecies of nonhuman primates seemsto gravitate to some norm.12,13 Twoalternative viewpoints have longsince been suggested for the extentto which societies are variable.Observed regularities led some tobelieve that ‘‘the genetic potential ofsome nonhuman species may indeedbe restricted to one type of societywhich environmental change wouldhardly alter.’’1 The fluctuations ob-served in demographic patterns andbehavior rates led others to wonderwhether there exists ‘‘such thing as a‘normal social structure’ for a givenspecies.’’14

There is no better example thanthe rhesus macaque for use in exam-ining the possible extent of variationin social behaviors of nonhuman pri-mates. This is the most extensivelystudied monkey and also the mostadaptable. In the laboratory, rhesusmacaques are able to cope with mul-tiple experimental conditions, includ-ing outer space. In the wild, they arefound from 708E longitude in Af-ghanistan to 1208E longitude inChina. They live in diverse habitats:tropical, temperate, and subalpineforests, tidal areas, arid lands,regions of human settlement, andeven urban zones (Fig. 1).15,16 Theirdiet is exceptionally flexible. They aremainly folivorous in the deciduousforests of the Himalayan foothills,but appear to be largely frugivorousin other habitats. Rhesus macaques

are well adapted to ecologically dis-turbed zones. As humans clear for-ests they adjust their diet to includecultivated crop plants.16 Group sizeusually ranges between 20 and 40individuals, but can be as large as100–200 individuals. Home-rangeareas also vary widely, fluctuatingbetween some hectares and 20 km2

according to ecological resources.15

Experimental changes in the avail-ability of social partners may affectthe quality of individuals’ social inter-actions and development. Amonggroup-living rhesus macaques, adultmales show little interest in infantsand rarely affiliate with them. None-theless, when a wild-born male ispair-housed with an infant, he devel-ops a strong bond with that infantand will groom and play with it.17 Inthe absence of mothers, there ispotential for males and infants toform affiliative relationships. Inexperiments where young rhesusmacaques were co-housed withslightly older stumptailed macaques,the conciliatory tendencies of the for-mer were multiplied threefold, stabi-lizing at levels comparable to those ofthe latter.18

The study of free-ranging groupsof rhesus macaques introduced onthe Caribbean island of Cayo San-tiago has shown that the rates of off-spring rejection of females are simi-lar to those of their own mother.19

There is intergenerational transmis-sion of mothers’ rearing style. Cross-fostering experiments have demon-strated that abusive behaviors to-ward offspring may be transmittedfrom mothers to daughters throughexperience.20,21 Maternal behavioradditionally depends on demo-graphic factors. The number of non-relatives in proximity to infantsincreases with the size of groups. Insmaller groups, mothers spend lesstime monitoring their infants andare less restrictive regarding theirmoves and social contacts.22 Theseeffects have an impact on the devel-opmental trajectory of individuals byinfluencing the degree of exclusivityof the mother-offspring bond and theextent of immatures’ social networks.

Variation may also originate fromgenetic diversity. A fair amount ofheritability has been documented in

the temperament of individuals. Tem-perament is trait-like; that is, indivi-duals display stable behavioral dispo-sitions across different situationsthroughout their lives.23 Geneticanalyses in infant rhesus macaqueshave revealed high heritabilities ofanxiety-related behaviors like inhibi-tion and distress responses.24,25 Tem-perament characteristics have biolog-ical correlates; a wealth of data dem-onstrate that high impulsivity andaggressiveness are related to reducedserotonin activity. Serotonin is a neu-rotransmitter involved in control ofthe neurohormonal stress axis. Stud-ies of rhesus macaques have shownthat low levels of serotonin are asso-ciated with a consistent suite of be-havioral tendencies that includes im-pulsive risk-taking, unrestrainedaggression, and lack of submission.Low-level males additionally havetendencies toward social isolation,early dispersal, frequent wounding,and heightened mortality rates,whereas low-level females, thoughthe most protective mothers, never-theless experience higher rates ofinfant loss.26–28

Interindividual differences in cen-tral serotonin turnover are undergenetic influence. There is polymor-phism at the promoter region of agene encoding the serotonin trans-porter protein. Two main alleles ofthe gene, S and L, have been identi-fied. The S allele is associated withless efficient serotonin promotion,meaning that, in rhesus macaques,as in humans,20 different genotypesproduce individuals with differentlevels of impulsivity. Interestingly,the rearing environment modulatesthe phenotypic expression of thegene. In peer-reared subjects, indi-viduals carrying the S allele consis-tently present lower serotonin con-centrations. However, mother-rearedsubjects display normal concentra-tion levels regardless of whether ornot they possess the S allele. Therearing environment seems to bufferthe infant from the potentially nega-tive effects of the allele on serotoninmetabolism.29

The buffering effect of the socialmilieu may explain a paradoxical les-son learned from the study of rhesusmacaques. Despite the extensive plas-


ticity reported for individuals, theirsocial relations follow consistent pat-terns. In any of the places wherethey have been studied, we see theintractable and aggressive tempera-ment that drives rhesus macaques tothreaten others at the slightest prov-ocation, using the stare open-mouthfacial display; subordinates performa silent bared-teeth response thatspecifically expresses submission andreveals strong dominance asymmetryin social relationships. Most contestsare unidirectional; that is, theattacked individuals flee or submitwithout any attempt to counter theiraggressor.30,31 Measuring the propor-tion of reconciliations betweenmature females and unrelated part-ners regularly yields values below10%.32,33 Mothers exert close controlover the social interactions of theirinfant. Adult females and immaturesexhibit strong preference for mater-nal kin. The degree of relatedness isa main predictor of affiliation, domi-nance, and support.34,35 Whenevermatrilines are large enough, the sup-port of relatives in contests producesstrict rules of rank inheritanceamong adult females:36–38 (1)Females inherit their mother’s rankrelative to others; (2) they hold rankjust below their mothers; (3) youngerdaughters dominate their elder sis-

ters. Dominance ranks correspondinversely with age within matrilinesbecause mothers and sisters chooseto help their youngest relatives.These traits form what may be calledthe ‘‘social style’’ of rhesus macaques,something like a behavioral arche-type.

With regard to mating patterns,Carpenter39 described the ‘‘norm ofsexual activities for Macaca mulatta’’as early as 1942. He pinpointed thecommunicative signals associatedwith copulation, the increase inaggression during the mating season,and the relationship between maledominance and consortship. He alsoidentified more peculiar patterns,such as that receptive females matewith a succession of males and thatdominant males disrupt the consortsof lower-ranking males by threaten-ing the females rather than theirrivals. Subsequent reports repeatedlycorroborated the accuracy of Carpen-ter’s first account.40,41

By experimentally modifying socialdensity, we can significantly alter thefrequencies or durations of behaviorslike aggression and social groom-ing.32,42,43 In contrast to this, thequality of social interactions showslittle range in variation. The form ofthe interactions in which an individ-ual is involved is, by nature, heavily

dependent on the behavior of part-ners. When comparing rhesus maca-ques living in different environments,variables such as the proportion ofreconciled conflicts, as well as pat-terns of support and contact regula-tion between mother and infant, showrelatively limited fluctuations.19,32,42–45 As once noted by Richard,38 simi-larities in the social organization ofthe provisioned groups of Cayo San-tiago and the wild populations of thePakistan forests are more strikingthan their differences.Social style has a learned compo-

nent. Some behavior patterns may betransmitted to the next generation, asillustrated by the social inheritance ofdominance rank and maternal behav-ior. In light of these facts, we mightexpect to find cultural effects in socialstyles, that is, social patterns, wouldcontinuously change through timeand consistently differ betweengroups. We do not actually know ofany examples of such an effect. If cul-tural evolution is identified by the ir-reversible drift it produces, we haveno evidence for cultural evolutionamong macaques. Socially acquiredbehaviors represent fluctuations inthe system, which periodically returnsto initial conditions.46 Indeed, with-out what is called the ratchet effect,socially transmitted changes cannotaccumulate over time.47 Moreover,there are no hints that macaqueswould become abnormal if they failedto learn the social knowledgeacquired by previous generations. Anatural experiment made by StephenSuomi (personal communication)nicely illustrates this point. In 1973 heestablished a breeding colony by gath-ering eight 6-month-old peer-rearedrhesus macaques. Each of them hadbeen removed from its mother atbirth and was hand-reared in a nurs-ery for the first month of life. Theinfants were then allowed to interactwith peers for two hours a day untilsix months of age. Thereafter, theywere put together to form a breedinggroup. In less than three decades, thegroup expanded to more than onehundred individuals. The outcome is,today, a multigenerational troopmaintained in semi-free ranging con-ditions at the NIH Animal Center inPoolesville, Maryland. The group

Figure 1. A subgroup of rhesus macaques sitting on the rooftop of a building in thesacred city of Vrindavan, India. The species is present in a wide variety of environments,including towns and cities, where it lives commensally with humans (photo by R. Seitre).


Box 2. Contrasts in Patterns of Conflict Resolution

The study of reconciliation pro-vides a standardized tool for com-paring social relations in macaques.Reconciliation is defined as a posi-tive contact occurring after conflictbetween former opponents. Toquantify reconciliations, one oppo-nent is followed during a 10-minutepostconflict period (PC). Then a 10-minute matched-control period (MC)is conducted on the same individualon the next possible observationday.48 By matching PC and MC,each pair of former opponents isclassified as ‘‘attracted’’ if contactbetween individuals occurs earlier oronly in the PC, ‘‘dispersed’’ if con-tact occurs earlier or only in the MC,or ‘‘neutral’’ if contact occurs at thesame time or did not occur in thePC and MC. The conciliatory tend-ency is calculated as the number ofattracted minus the number of dis-persed pairs, divided by the totalnumber of PC-MC pairs. The datacollected by three research teamsduring the last twenty years showthat conciliatory tendencies wereconsistently below 20% in some

species, and rated around 50% ormore in other species (Fig. A).33

Statistical analyses first showedthat several traits related to the re-solution of conflicts display corre-lated variation. Species cannot beconsidered as independent units,however, since they may share traitsthrough common ancestry. There-fore, the method of independentcontrasts49 was used in a secondstep to control for phylogeneticrelatedness. It showed that associa-tions between traits were still con-sistent. In particular, rates of explicitphysical contacts (for example,mounts and clasps) were more ele-vated in species characterized byhigher conciliatory tendencies (Fig.B), supporting the view that suchcontacts are instrumental in promot-ing reconciliation. Another significantassociation was found betweenthe percentage of counter-aggres-sion and kin-bias in reconciliation;preference for kin was greater inspecies characterized by a lowernumber of protests and counter-attacks in conflicts (Fig. B). This

result is consistent with the hypothe-sis that the occurrence of coalitionscreates a causal link between levelsof dominance asymmetry and kinbias in female macaques. Whenmost coalitions involve relatives, thedominance status of individualsdepends primarily on the power ofthe kin subgroup to which theybelong. This increases rank differen-ces between nonrelatives and fur-ther develops kin coalitions, gener-ating group networks based onstrong hierarchies. In contrast, whenkin-bias is less pronounced, coali-tions involving nonrelatives are morecommon. Dominance appears to bemore a question of individual attrib-utes and the individual retains somedegree of freedom with regard topower networks. Dominance rela-tionships remain balanced amonggroup members and close ties existeven between nonrelatives. A con-sequence of the connection be-tween dominance asymmetry anddegree of kin preference is that envi-ronmental factors cannot separatelyact on either of these two traits.

Figure B. Associations between counter-aggression and kin bias (above), and be-tween conciliatory tendency and explicitcontact (below).33 Regression analysesused independent contrasts computedfrom thephylogenyprovided in Purvis.50

Figure A. Mean conciliatory tendencies in fifteen captive populations of macaquesrepresenting nine species of macaques.33 To standardize data, only dyadic conflictsoccurring between pairs of unrelated females (older than 3.5 years) and between pairsof females and unrelated juveniles (between 1.5 and 3.5 years of age) were taken intoaccount.


exhibits the normal social organiza-tion of rhesus macaques, includingall of the species-typical behavior pat-terns regarding communication, aggr-ession, affiliation, dominance, kinshipand socialization. Even if their rela-tionships were not normal at the start,individuals deprived of the experienceof previous generations succeeded increating a social organization thatconverged toward the archetypal styleof their species.

SOCIAL STYLES AS COVARIANTSETS OF TRAITS

Strong nepotism and dominancehierarchies were once believed to betypical of the entire macaque genus, ifnot other primate families.51,52 Subse-quent studies showed that these fea-tures were, in fact, those characteriz-ing the two better-known representa-tives of the genus, the rhesus macaqueand its sister species, the Japanesemacaque. Other macaques actuallydepart, to varying degrees, from themulatta/fuscata archetype. In the lat-ter two species, conflicts are unidirec-tional, high-intensity aggression iscommon, and reconciliations are notfrequent.32,53–58 Quantitative analyseshave shown quite different patterns ofaggression and response to aggressionin Sulawesi macaques (Tonkean,crested, and moor macaques). A ma-jority of their conflicts are bidirec-tional, and most aggressive actsinduce protest or retaliation. Aggres-sion is generally of low intensity.Measuring conciliatory tendenciesyields high values, around 50% amongunrelated partners (Box 2).31,54,57,59,60

Other macaques are located inter-mediately between previous speciesregarding patterns of aggression andreconciliation. Longtailed and pig-

tailed macaques are most similar torhesus and Japanese macaques,whereas stumptailed, Barbary, lion-tailed, and bonnet macaques aremost comparable to the Sulawesimacaques.61 When measuring differ-ent populations of the same species,conciliatory tendencies fall within anarrow range of variation, indicatingthat they reflect species-typical socialstyles (Box 2).32,33,42,56,58,61–63 I haveproposed to arrange macaque speciesalong a 4-grade scale mainly basedon patterns of aggression and recon-ciliation (Table 1).61 Species fromgrades 3 and 4 display higher ratesof tension-reducing contacts than doothers. The meaning of the silentbared-teeth display consistentlyvaries along the scale. In macaquesfrom grades 1 and 2, subordinatesuse it to express submission, for-mally acknowledging their lower sta-

tus relative to higher-ranking conspe-cifics. In grade-3 species like Barbaryand liontailed macaques, the samedisplay may either have a positivemeaning or express submissionaccording to contexts. In speciesfrom grade 4, formal indicators ofsubordination are absent; the bared-teeth display signals the sender’speaceful intentions like a smile(Fig. 2).61,64

The degree of kin-bias in socialrelationships covaries with patternsof aggression and dominance. Thedegree to which females prefermaternal relatives for contact, socialgrooming, and coalition is less pro-nounced in the third than in the firsttwo grades34,53,55,65,66 and kin-bias isstill weaker in Sulawesi macaques(grade 4).52,67,68 The socializationprocess also contributes to the spe-cies social style. Except for the high-

TABLE 1. Tentative Scaling of Macaque Social Styles (modified from Thierry61)a.

Grade 1 Grade 2 Grade 3 Grade 4

Rhesus macaque Longtailed macaque Stumptailed macaque Tonkean macaqueJapanese macaque Pigtailed macaque Barbary macaque Moor macaque(Taiwan macaque) (Assamese macaque) Liontailed macaque Crested macaque

(Tibetan macaque) Bonnet macaque (Muna-Butung macaque)(Toque macaque) (Booted macaque)

(Heck’s macaque)(Gorontalo macaque)(Siberut macaque)

a Social tolerance increases from left (grade 1) to right (grade 4). The least known species are indicated in brackets.

Figure 2. Silent bared-teeth displays among males in semi-free ranging Tonkean maca-ques, Strasbourg Primate Center, France. Baring the teeth serves to initiate affiliative inter-actions in all Sulawesi macaques (photo by B. Thierry).


est-ranking females, mothers in thefirst two grades are protective oftheir infants, frequently retrievingthem, restricting their interactionsmostly to relatives. The amount ofcare provided by females other thanthe mother is limited. By contrast,mothers belonging to species fromthe other two grades are permissive;many females in the group may han-dle infants from an early age.61

Although we lack quantitative dataabout female rank acquisition inmost macaque species, we know thatin longtailed macaques (grade 2)rank acquisition follows the inheri-tance rules described in rhesus andJapanese macaques. However, rankreversals between mothers anddaughters are not uncommon.69 InBarbary macaques (grade 3), daugh-ters often outrank older mothers andfemales are usually subordinate totheir older sisters.66,70 In Tonkeanmacaques (grade 4), rank reversal ofmothers and daughters is not rareand the rule of youngest ascendancydoes not apply (Thierry, unpublisheddata).The 4-grade scale may be used

as a periodic table that allows forfalsifiable predictions to be made(Table 1). A few traits may be usedto predict others. Several expecta-tions of the covariation hypothesishave already been verified, includingthe permissive mother style ofstumptailed macaques,71 the moder-ate female kin-bias of Barbary maca-ques,65 the high proportion of retalia-tion of Muna-Butung macaques,72

and the elevated conciliatory tend-ency of bonnet macaques.73 Directinterspecific comparisons have beencarried out for only a limited sampleof species, groups, and traits, how-ever, and intraspecific variabilitycalls for caution.61 While it is easy togroup those species that fit into ei-ther the first or the fourth grade, it ismore difficult to group intermediatespecies. Recent studies indicate thatAssamese and Tibetan macaquesbelong to grade 2. They confirm thattheir patterns of aggression, reconcil-iation, and dominance consistentlycovary, with the caveat that they dis-play tension-reducing behaviors aliketo species from grades 3 and 4.74,75

Although each species is assigned to

one grade, a more accurate picturewould represent the various studypopulations of each species as a clus-ter of points centered on one modallocation.

Stating that the components ofmacaque societies are arranged in alimited subset of social stylesamounts to saying that large parts ofthe macaque sociospace remainunoccupied. This is the second les-son to be drawn from the study ofmacaques. Sociospace may bedefined as the set of forms that aparticular kind of social organizationmay take. It is described by all possi-ble combinations in the values of theparameters characterizing the socialorganization. By acknowledging afamily of established styles, it is pos-sible to identify an empirical socio-space defined by the variation of be-havioral traits. The question thenarises why some social styles do notexist in macaques, such as thosecharacterized by strong dominanceasymmetry and weak preference forkin, or low conciliatory tendency andregular infant handling by groupmembers. To answer this question,we have to look at the processes re-sponsible for the coupling of traits.

SOURCES OF LINKAGES BETWEENBEHAVIORAL TRAITS

Identifying the connections amongconstituent parts of a biological sys-tem is a notoriously tricky task. Itmay involve genetic and acquiredcomponents. For example, severalprocesses may account for the asso-ciation found between levels ofaggression and maternal protective-ness among macaques.2 Reducedserotonin activity may yield bothheightened aggression and low ratesof infant rejection by the mother.Alternatively, elevated risks ofaggression may lower rejection ratesthrough an increase in maternal anx-iety. Mothers from the first twogrades live in a social milieu charac-terized by intense aggression andmarked hierarchies, and they restricttheir infant’s interactions. A thirdprocess may also take place. Anxietyis a trait of temperament. If its varia-tion range differs between species,

this may result in interspecific dis-parities in infant rejection rates.Regular interspecific variation has

been shown in the temperament ofmacaques. They differ in response tostress and novelty as measured byarousal, alarm, and explorationbehavior, corticosteroids or heartrate.61,76 Species from grades 3 and 4are less easily aroused than are spe-cies from grades 1 and 2. Such varia-tions in behavioral responses havemeaningful biological correlates.Higher aggression intensity is associ-ated with lower serotoninergic activ-ity in rhesus compared with pigtailedmacaques.77 Also, tolerant macaques(stumptailed, Barbary, and Tonkeanmacaques) are mostly monomorphicfor serotoninergic genes, while moreintolerant macaques (pigtailed, long-tailed, and rhesus macaques) appearto be polymorphic. Moreover, poly-morphism regarding the serotoningene transporter includes the S alleleonly in rhesus macaques. Naturally,we cannot expect that a limited num-ber of alleles accounts for the fullspectrum of behavioral variationsreported in macaques, but theseresults do point out a genetic influ-ence on interspecific variation.78 Wehave evidence of the neurochemicaland genetic basis of further cross-spe-cies differences in anxiety-relatedbehaviors.78,79 Such findings shouldbe considered the first steps towardunraveling the genetic underpinningsof macaque temperament.Links between traits may originate

from two main mechanisms, com-mon source or interaction betweenconstituent parts of the system. Suchmechanisms may arise at differentlevels: genome, individual phenotype,and social phenotype.2 An exampleof a common source is gene pleio-tropy; a single gene locus affects avariety of traits, producing multiplecorrelated effects. For instance, lowrates of serotonin are responsible fora broad behavioral syndrome asreported in rhesus macaques. Somecorrelations may be an outcome ofthe systemic variation of a singlehormone or neurotransmitter actingon several targets, but variationsmay also affect the distribution andresponsiveness of targets. At the levelof individual temperament, impulsiv-


ity, aggressivity, and lack of submis-sion are likely to be different facetsof one and the same dimension,23

meaning that they cannot be sepa-rated. At the social level, a singletemperament dimension may pro-duce a range of various outputsdepending on the context. Thoseassociated with lower serotoninergicactivity may engage in social isola-tion, early dispersal, and heightenedmaternal protectiveness.Slight differences in the tempera-

ment of individuals may yield signifi-cant variations in individual behav-iors and social relationships.13,23 Byacting on behavioral propensitiesand response thresholds, selectiveprocesses can shift social styles fromone part of the macaque sociospaceto another. Hemelrijk80 was able togenerate self-organized patterns thatresemble those found in macaquesby implementing simple rules ofattraction and competition in a mul-tiagent model. She demonstratedthat a quantitative shift in aggressionintensity leads to correlated changesin spatial cohesion and conflictasymmetry.Various linkages stem from social

interactions. Individuals’ behaviorsmay complement or reinforce oneanother, or oppose and even excludeone another. Tactical considerationsindicate that competitors’ readinessto struggle for a resource depends onthe risk they incur. If the risk ofbeing wounded in a conflict is ele-vated, the better tactic for the weakerindividual is to submit or flee ratherthan to counterattack the opponent.Conversely, when the dominancegradient is low, the threatened indi-vidual can easily retaliate, forcingthe adversary to avoid potentiallydangerous attacks. In animals able touse graded threats, if a high propor-tion of retaliations in conflictsresulted in frequent biting andwounding, it would represent poortactics. This explains why intensityin aggression, asymmetry of conflict,and submission patterns are covary-ing traits in macaques.2 On onehand, asymmetric conflicts and highrisk of injury inhibit the occurrenceof affiliative contacts between oppo-nents. On the other hand, uncer-tainty about outcomes creates room

for negotiation. Appeasement behav-iors reduce the probability of conflictescalation by allowing informationexchange,81 which may account forthe correlation found between ratesof explicit contacts and proportionsof reconciliations (Box 2).

A third lesson from macaques isthat linkages underpinning societiesmay arise at any level of organiza-tion. An important consequence ofthis is that some traits representbyproducts of others. The matrilinealstructuring of dominance relation-ships in rhesus and Japanese maca-ques (that is, females ranking belowtheir mothers and age-reversed rankorder among sisters) may beregarded as an incidental side effectof the support given to relatives,which is quite exclusive comparedwith that reported in more tolerantspecies. Similarly, cross-species dif-ferences in rates of infant handlingby group members appear to bederived from variations in motheringstyle. Regardless of the motives ofindividuals trying to interact withinfants, their access to infants is afunction of the mother’s protective-ness. She shapes her offsprings’social network by selectively allowingor preventing others from approach-

ing (Fig. 3). From this perspective,there is no need to provide a particu-lar adaptive explanation for theoccurrence of low or high rates ofinfant handling.2

ECOLOGICAL ANDPHYLOGENETIC CORRELATES

In order to unravel the origins ofcross-species differences in the socialstyles of macaques, we must examinetheir evolutionary past. There is aconsensus that social organizationpatterns in primates are linked to thecharacteristics of the environment inwhich they have evolved. But howdeterministic the influence of theenvironment is remains an openquestion. The predominant socioeco-logical model assumes that predationpressures compel female primates tolive in groups, while the distributionof resources subsequently determinesthe strength of feeding competitionwithin and between groups, thusshaping the nature of social relation-ships.82–84 Does this model accountfor the interspecific variationobserved in macaque social styles?In a recent review, Menard85 exam-ined the fit between theoretical

Figure 3. A mother lets another female handle her infant in semi-free ranging Barbarymacaques, Kintzheim, France. Infant handling and caretaking by individuals other thanthe mother is especially frequent in the species (photo by B. Thierry).


expectations and what we knowabout the ecology of wild popula-tions of macaques. She concludedthat available data on habitats andmodes of exploitation by macaques‘‘do not indicate any consistent fea-tures of known ecological conditionsfor each species that appear to becorrelated with their characteristicdominance styles.’’ In the tropics, forinstance, macaques mainly dependon clumped foods like fruits,whereas in more temperate areasBarbary, rhesus, and Japanese maca-ques heavily rely on more evenly dis-tributed seeds, buds, leaves, andherbs. From the assumption that lev-els of within-group contest competi-tion are weak when high-rankingfemales cannot monopolize food, themodel predicts that the latter threespecies should display tolerant rela-tionships.85 Quite to the contrary,rhesus and Japanese macaques sharethe same ‘‘despotic’’ social style; onlyBarbary macaques exhibit relaxeddominance relationships (Table 1).The socio-ecological model additio-nally states that species undergoingstrong between-group competitionshould display more tolerant socialrelationships than do those not fac-ing such competition. High-rankingfemales should accept a more equalexploitation of resources in exchangeof the help of low-ranking females incommunal defense against othergroups.83,84 Here again, the model isnot supported by the results of fieldresearch.85 The rates of aggressivebetween-group encounters do notdiffer between tolerant and intoler-ant macaques, and low levels ofbetween-group competition arereported in females from tolerantspecies such as bonnet and moormacaques.86,87

Whereas related primate taxa oftencluster together based on ecologicalvariables,88 the ecological preferen-ces of macaques appears weakly con-nected with their phylogenetic rela-tions.8,16 The development of statisti-cal comparative methods49 has madeit possible to test the occurrence ofhistorical effects on social organiza-tion patterns. It was found that Cer-copithecine monkeys typically sharetraits like female philopatry and kin-relations.89 Study of the macaque

genus further showed that its threemain phyletic lineages have a differ-ent distribution on the 4-grade scaleand that variations in social stylecorrelate with phylogeny.2,87,90 Bytracing each of the traits on the phy-logenetic tree of macaques, it is pos-sible to recognize the most ancientstates and reconstruct the typicalancestral organization of macaques.The resulting set of traits closelymatches grade 3 on the scale, whichmay be tentatively considered as theancestral state.90 The fact that Bar-bary and liontailed macaques arelocated in grade 3 reinforces the pre-

vious finding since these two speciescome closest to the root of the phylo-genetic trees established from mor-phological and molecular data. Theother species of the first lineage havediverged, moving either to grade 4(Sulawesi macaques) or grade 2 (pig-tailed macaques). Members of thesecond lineage have remained ongrade 3 or drifted to grade 2. Thethird lineage evolved toward grades 1and 2. The location of every lineageis mostly restricted to two grades inthe scale. This means that the coreof the species-typical system of socialrelationships underwent limitedchanges during several hundreds ofthousands of years and even millionsof years in some species.

In a recent study we used datafrom several species to test correla-

tions between the proportion ofcounter-aggression and traits relatedto reconciliation, conciliatory tend-ency, degree of preference for kin,and proportion of explicit physicalcontacts leading to the reunion ofprevious opponents.33 The analysisshowed that several traits additio-nally displayed correlated evolution-ary changes even after controllingfor phylogeny (Box 2). This confirmsthe occurrence of internal connec-tions responsible for the clustering ofbehavioral traits. The importance oflinkages between traits challengeequilibrium models based on directassociations between traits and theenvironment. Another lesson frommacaques is that social organizationis underdetermined by environmen-tal factors.

BALANCE BETWEEN EXTERNALAND INTERNAL DETERMINANTS

We cannot explain macaque diver-sity by considering environmentalpressures and linkages between traitsseparately. Any evolutionary explana-tion must account for the fact thatmacaque social styles are quite stablepackages of integrated behavioraltraits. To account for phyletic stasis(that is, the absence of evolutionarychanges), one classically resorts tophylogenetic inertia. Present traitswould have been selected for in thepast under conditions different fromthose of today and would persistacross environmental changes beca-use of the time lag in adapta-tions.66,85 Phylogenetic inertia is theblack hole of socioecological theory;it spares functional hypotheses at theexpense of reasons lost in the past.91

Moreover, calling on species lag saysnothing about the forces at work. Westill have to specify whether the ab-sence of changes is produced by alack of effective selection or becauseof stabilizing selection.92

Linkages between traits are notjust slave proximate mechanismsunder the command of ultimate fac-tors. They act as constraints thatreduce the probability of trade-offsfor evolutionary changes.3,4,93

Employing the word ‘‘constraint’’conveys the message that structural

The importance oflinkages between traitschallenge equilibriummodels based on directassociations betweentraits and theenvironment. Anotherlesson from macaques isthat social organizationis underdetermined byenvironmental factors.


and functional linkages channel theadaptive pathways open to biologicalsystems by ‘‘constraining’’ their mu-tability. This view advocates a trans-formational approach, which investi-gates how organizational propertiesmay shape the transformation of bio-logical systems throughout history.94

We may alternatively describe opti-mization models as ‘‘models underconstraints’’ that aim to unraveltrade-offs endowed with a higher fit-ness. This second view promotes anequilibrium approach by focusing onthe counterbalancing actions of fac-tors liable to drive changes. For thelast two decades, misunderstandingsabout the definition of constraintswas a primary cause of controversybetween the proponents of the equi-librium (‘‘functionalist’’) and thetransformational (‘‘structuralist’’) para-digms.94,95

It should be apparent that bothapproaches complement each other.A game-theory model developed byMatsumura and Kobayashi96 helpsto clarify this point. To account forthe outcomes of contests over resour-ces, they proposed three possible tac-tics for opponents with unequalfighting abilities: (1) hawk, escalatefighting until injury or opponentretreats; (2) dove, display but retreatif opponent escalates; (3) retaliator,start by displaying but escalate if op-ponent escalates. The main parame-ters of the model are the resourcevalue (V), the cost of injury (D), andthe probability of winning the con-tests (x). The implementation of thismodel reveals that several strategiesare evolutionarily stable: hawkagainst dove, dove against dove,hawk against hawk, and retaliatoragainst retaliator. Moreover, differ-ent strategies may co-exist for thesame values of V, D, and x, whichsignifies that strategies are notmerely determined by ecological con-ditions.96 The use of an optimalitymodel thus indicates that aggressionintensity and conflict asymmetry arefunctionally related traits and thatthey are partly disconnected fromthe environment as seen in maca-ques. Alternative strategies may beregarded as different fitness peaks inan adaptive landscape. A classical ex-planation is that evolutionary path-

ways lead species to occupy differentpeaks. It is difficult for them to reacha peak of higher fitness because ofthe low-fitness valleys surroundingthe peaks. Linkages between traitshave arisen throughout historyand they are not easily broken byselection.

The same device may be functionalat one organization level and act as aconstraint at another. This is a fifthlesson from macaques, applicable tothe study of other societies. Notethat this was already known to beapplicable to the biology of organ-isms. ‘‘Constraint’’ is a relative con-

cept.3 It remains meaningless if wedo not specify a null model of evolu-tion regarding the trait considered.The null model states how traitswould evolve in the absence of con-straint; we commonly define it as theadaptation to external pressures.3,4,93

From this viewpoint, a constraint isa mechanism that limits the evolu-tionary response of traits to externalselective pressures acting at a givenorganizational level.3 A correlate isthat selection has an internal compo-nent that results from the fitnessconsequences of trait variation asdetermined by the dynamics of bio-

logical systems. It maintains therobustness of systems by eliminatingthe disrupting variations that wouldcorrespond to low payoffs for indi-viduals. The concept of constraintcaptures those causal mechanismsthat produce stabilizing selectionand are less dependent on the exter-nal environment.Like organisms, societies result

from a balance between organiza-tional and environmental pressures.Each individual in a society submitsto the consequences of these twocomponents of selection. Organiza-tional pressures arise from social dy-namics. We may resort to gamemodels to explore frequency-depend-ent strategies and understand whysome behaviors are favored or dis-carded. We may also employ the lan-guage of constraints or trade-offs toexplain that a change in one traitinduces a change in another. Thecrucial point is that the wheels of thesocial machinery exert strong stabi-lizing selection that opposes theadaptative changes possibly requiredby the ecological milieu. Evolution-ary transformation depends on a bal-ance between the respective strengthof external pressures and stabilizingprocesses. Theory predicts that themore numerous the interconnectionsbetween the components of a system,the more limited the optima open tothe system and the greater theirnumber,97 which may account forthe various social styles observed inmacaques.A difficulty that arises when con-

sidering behavioral phenotypes isthat we may choose to considereither the ecological milieu (abioticand biotic, excluding conspecifics) orboth the ecological and the socialmilieu as the external environment,which influences the scope of poten-tial constraints. Aware that therequirements of sexual selection mayconflict with ecological pressures,behavioral ecologists included sexualselection among the external forcesliable to shape primate social organi-zation.84,98,99 By recognizing thedifferent outcomes of selection com-ponents, we may be close to reconcil-ing the transformational and equilib-rium approaches for studying pri-mate societies.

The crucial point is thatthe wheels of the socialmachinery exert strongstabilizing selection thatopposes the adaptativechanges possiblyrequired by theecological milieu.Evolutionarytransformation dependson a balance betweenthe respective strengthof external pressuresand stabilizingprocesses.


QUASI-INDEPENDENCE OFMATING PATTERNS

A main assumption in socioecologyis that the exploitation of environ-mental resources by females deter-mines grouping patterns, whereasmales follow this distribution tocompete for mating access.82,100 Pat-terns of mating competition fluctuatebetween two extremes in maca-ques.101 In mate guarding, an adultmale closely follows and mates witha fertile female over a period of sev-eral days, excluding other malesfrom reproduction. This tactic isbased on contest competition andonly dominant males can use it. Thepressure exerted by males leaves lit-tle room for female mate choice. Thesecond pattern is opportunistic mat-ing, in which associations betweenmales and females do not last formore than hours or even minutes.Competition is typically scramble,but it also involves some contestcomponent; males regularly shift fromone fertile female to another, andmay also supplant a lower-rankingmale from the proximity of a female.Conversely, a female may expressmate preferences, refusing to copulatewith a male and accepting another,

even a lower-ranking one.41,102 Amajor variable determining matingcompetition is the operational sex ra-tio, or the number of fertilizablefemales relative to the number of sex-ually active males.100 For males,reproductive success depends on theirability to monopolize access tofemales. When only a few females areovulating at the same time, high-rank-ing males tend to mate guard anddominance rank functions as a queuefor mating opportunities; if there is asingle peri-ovulatory female, only thefirst-ranking male is able to mate.When many females cycle synchro-nously, however, no male can monop-olize reproduction and opportunisticmating becomes the primary tactic.

In multimale groups, the opera-tional sex ratio may change accord-ing to the number of perio-ovulatoryfemales. A primary source of varia-tion is the more or less periodic na-ture of reproduction in macaques,which entails broad interspecific dif-ferences in the mating system. Intropical species where reproductionoccurs year round, there is usuallyno more than one fertilizable femalein a group at any given time. Thispromotes long-lasting periods ofmate guarding by top-ranking males

in, for example, liontailed, Tonkean,and crested macaques (Fig. 4).101 Incontrast, there is an annual breedingseason for species living in temperateregions. Strong environmental sea-sonality entrains the synchrony ofreproductive cycles. This way,females secure adequate resourcesduring the good season, when theirnutritional needs are highest. Mostreproductive females cycle duringthe fall within a two- to three-monthperiod, which favors opportunisticmating.41,101,102 Lengthy guardingcan coexist with opportunistic mat-ing depending on the operational sexratio. Not surprisingly, this is espe-cially common in species experienc-ing limited seasonality, such as long-tailed and pigtailed macaques. Sincethere can be one or several peri-ovu-latory females at any given time,female defendability is quite change-able. The duration and exclusivity ofassociations between sexes is vari-able too. It is worth adding thatexclusive mate guarding by top-rank-ing males prevails in any specieseach time that the number of avail-able mates decreases to two peri-ovu-latory females or just one, which fre-quently occurs in small groups. InJapanese macaques, when the num-ber of simultaneously cyclingfemales decreases, the time spent bysubordinate males in proximity tothem decreases103 and dominantmales sire more offspring.104

Paternity analyses show that tropi-cal macaques are characterized by ahigh male reproductive skew; that is,top-ranking males father a dispropor-tionate number of progeny.102,105

This has far-reaching consequencesfor the life history of males who can-not reproduce unless they acquire ahigh dominance status. This favorshigh-risk tactics for rank acquisi-tion.101,106 At some point in their life-time, adult males face a go or no-godecision. They must aggressivelychallenge top-ranking males anddefeat them to gain access to females.In comparison, the reproductive skewremains low among male seasonalbreeders.102,105 Because no male hascomplete control over mating access,the door is open to alternative matingtactics. Being dominant is just one ofthem. Subordinates may practice

Figure 4. Female mate guarding in wild crested macaques, Tangkoko Dua Saudara Na-ture Reserve, Sulawesi, Indonesia. The female presents her hindquarters to the male. Heranogenital swelling has not yet reached its maximal size. The male closely follows thefemale during days. His high rank allows him to keep rivals away until the end of thefemale’s fertile period (photo by A. Engelhardt).


‘‘sneak copulations’’; they go out ofthe view of high-ranking males tosurreptitiously mount females. Malesalso compete by ‘‘endurance rivalry’’;some may forego reproductive oppor-tunities because of the high energeticexpenditures incurred by long peri-ods of mating competition.41,103 Fur-thermore, females have room tocounter male coercion and pursuetheir own interests. The point of in-terest here is that seasonally breedingmales can produce a fair amount ofprogeny without necessarily acquir-ing a top-rank position. Except insmall groups, severe fighting betweenadult males is rare. Most of themincrease in dominance rank with ageand tenure in a group.101,106

Contrary to what may be expected,the correlation between male domi-nance rank and the number of pro-geny is not weaker in more tolerantspecies.61,102 For instance, the repro-ductive skew is significantly higherin stumptailed macaques (grade 3)and Tonkean macaques (grade 4)than in rhesus and Japanese maca-ques (grade 1). This is a further les-son learned from the study of maca-ques. Patterns of mating competitionappear to be quasi-independent fromsocial style. Dominance relationshipshave more influence on reproductivesorting in year-round breeders withlimited dominance asymmetry thanin seasonal breeders with strongdominance asymmetry. When a sin-gle fertile female is available at atime, males directly reach the go orno-go decision point regardless ofthe nature of their social bonds.Social styles and mating systemserve as two different modules inmacaque social organization.Phylogenetic analyses have revealed

that species-typical social styles und-erwent limited changes over longperiods of time.2,90 The plasticity ofreproductive patterns contrasts withsuch stability. Macaque populationshave more than once experienced achange between warm and temperateclimate during recent geological time.Not only does switching between sea-sonal and aseasonal reproductionprobably represent a simple adapta-tion regarding hormonal processes, italso suggests that individuals mayshift from one tactic to another

depending on circumstances. Theselective pressures responsible for themaintenance of social styles appearslargely independent from those expr-essed in mating competition.

The overwhelming effects of repro-ductive periodicity on reproductiveskew raises questions about themeaning of cross-species differencesin social style and particularly fordominance asymmetry. It seems thatonly males able to outrank rivalshave progeny under the tropics whilevariability in reproductive successremains limited in temperateregions. Environmental seasonality isa contingent factor on the evolution-ary path of macaques; individualscannot help but cope with variablesorting rules. It may be asked inwhich relative proportions the viabil-ity conditions attached to socialstyles and the conditions of repro-ductive competition affect the repre-sentation of individuals in the nextgenerations. If the periodicity ofreproduction modulates the strengthof sexual selection, it would influencethe genetic structure of social groups.While offspring have different fathersin temperate regions, a strong age-cohort effect should be found in thetropics, with all members of the samegeneration being paternal half-siblings.We do not know what could be the ev-olutionary consequences of such dis-parities in sibship.

PROSPECT

Over time, primatology has gonethrough stages similar to those inother fields of research. It began withdescriptive explanations and thenevolved to testing theoretical explana-tions.51,107 A pending question is towhat extent we may progress to afinal, synthetic stage where the mod-els proposed to explain different phe-nomena would become special casesof a general theory. Although prima-tologists cannot hope to reach unifi-cation levels similar to thoseachieved by the so-called exact scien-ces, the embedding of their studysubjects in biological evolutionallows them to foster a more deter-ministic project than their socialanthropologist fellows.51 The veryhistorical dimension of the evolution-

ary process puts some limits on thisproject, however. Macaques teach usthat the evolutionary pathways ofprimate societies are more complexthan was previously thought. Theirbehavioral patterns cannot bereduced exclusively to the action ofecological and sexual selection pres-sures. We must introduce explana-tions for stability to the picture.Aware that primate societies are co-determined by internal and externalfactors, we have to investigate thestrength of the linkages holding themup and the ability of adaptive pro-cesses to break them up.

ACKNOWLEDGMENTS

I thank S. Suomi and A. Engel-hardt for valuable inputs, C. Abeggfor drawing the maps, and M. Dindofor language advice. I am grateful toR. Seitre, C. Abegg, A. Engelhardt,M. J. Hsu, A. Sinha, N. Herrenschmidt,N. Priston, Operation Wallacea andN. Rowe (Pictorial guide to the livingprimates) for providing photographs.

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Books Received

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� Filler, A. G. (2007). The UprightApe: A New Origin of the Spe-cies. 286 pp. Franklin Lakes:Career Press. ISBN 978-1-56414-933-6. $24.99 (cloth).

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xiii þ 256 pp. New York: Harper

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� Goldenberg, L. (2007). Little

People and a Lost World. 112

pp. Minneapolis: Twenty-First

Century Books. ISBN 978-0-

8225-5983-2. $30.60 (cloth).

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chiavellian Intelligence. 198 pp.

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Documents

Unity in diversity: Lessons from macaque societies