19 evolutionary origins of great ape intelligence: an

19 • Evolutionary origins of great ape intelligence:an integrated viewANNE E. RUSSON 1 AND DAVID R. BEGUN 2

1Psychology Department, Glendon College of York University, Toronto2Anthropology Department, University of Toronto, Toronto

Among the great apes that once ranged the forests ofthe Old World, only four species survive. Their evolu-tionary history reveals a huge range of morphologicaland behavioral diversity, all of which must be consid-ered successful adaptations in their own time. Some ofthese attributes (large brains, sclerocarp and hard-objectfeeding, frugivory, folivory, gigantism, terrestriality, andsuspensory positional behavior) survive in modern greatapes. Our questions are: what combination of behav-iors and attributes characterized the ancestor of livinggreat apes? what was the significance of this suite offeatures for cognition? and how did it arise in evolu-tion? To that end, we offer our model of a distinct greatape cognition along with its biological underpinningsand environmental challenges, then attempt to trace theevolutionary origins of this ensemble of features.

COGNITION

All living great apes express a distinctive grade of cog-nition intermediate between other nonhuman primatesand humans. Their cognition normally reaches rudi-mentary symbolic levels, where symbolic means usinginternal signs like mental images to stand for referentsor solving problems mentally. It supports rudimentarycognitive hierarchization or metarepresentation to levelsof complexity in the range of human 2 to 3.5 year olds,but not beyond (in this volume, see Blake, Chapter 5,Byrne, Chapter 3, Parker, Chapter 4, Russon, Chapter 6,Yamakoshi, Chapter 9).

Great apes’ high-level cognitive achievements aregeneralized in that they manifest system wide andrelatively evenly across cognitive domains (Russon,Chapter 6, this volume). Evolutionary reconstructions,however, have typically fixed on specific high-level abil-ities, singly or in combination, such as self-concept orintelligent tool use (see Russon, Chapter 1, this volume).

While the challenges these abilities address may haveprovided the evolutionary impetus to enhancing greatape cognition, evolutionary reconstructions have moreto explain than these. No single ability, combination ofabilities, or cognitive domain encompasses what setsgreat ape cognition apart. In the physical domain,great apes do use tools in ways that require theirgrade of cognition (Yamakoshi, Chapter 9, this volume)but they devise equally complex manual techniques(Byrne, Chapter 3, this volume) and solve equallycomplex spatial problems (Hunt, Chapter 10, Russon,Chapter 6, this volume). They show exceptionally com-plex social cognition in social routines, scripts, andfission–fusion flexibility, as well as in imitation, teaching,self-concept, perspective-taking, deception, and pre-tense (in this volume see Blake, Chapter 5, Parker,Chapter 4, Russon, Chapter 6, van Schaik et al.,Chapter 14, Yamagiwa, Chapter 12). Their communi-cation reaches rudimentary symbolic levels, even con-sidering only strictly defined gestures and language(Blake, Chapter 5, this volume), as does their logico-mathematical cognition (e.g., analogical reasoning, clas-sification, quantification) (e.g., Langer 2000; Thomp-son & Oden 2000). The latter has not figured inevolutionary reconstructions but perhaps it should.Enhanced logico-mathematical capacities offer impor-tant advantages; classification and quantification, forexample, may aid in managing great apes’ broad dietsand social exchange (Russon 2002), and analogical rea-soning may support limited cognitive interconnections(see below). Others have also emphasized generalizedfeatures of great apes’ cognitive enhancements (in thisvolume, Byrne, Chapter 3, Parker, Chapter 4, Russon,Chapter 6, van Schaik et al., Chapter 11, Yamakoshi,Chapter 9). Features our contributors identify includeregular, sequential plans of many actions, hierarchi-cal organization, bimanual role differentiation, complex

Copyright Anne Russon and David Begun 2004.

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Russon, A. E. & Begun, D. R. (2004). The evolutionary origins of great ape intelligence. In A. E. Russon & D. R. Begun (ed.), The Evolution of Great Ape Intelligence, pp. 353-368. Cambridge, UK: Cambridge University Press.

354 A. E. RUSSON & D. R. BEGUN

event representations, scripts and routines, and coordi-nating more components in solving a task.

Individual great apes can also interconnect abili-ties from different domains to solve a single problem oruse one ability to facilitate another (Russon, Chapter 6,this volume). This is an important source of cognitivepower because it enables solving multifaceted problemsand boosts problem-specific abilities. It is not commonlyrecognized in great ape cognition but evidence for itsrole in exceptionally complex achievements in the wild,for example Taı chimpanzees’ cooperative hunting, sug-gests that it should. It is important in evolutionary per-spective because it is a plausible source of the “fluidity ofthought” or “multiple intelligences working together”that stands out in humans. Its appearance in great apesties well with evidence that some of their species-typicalproblems require coordinating abilities across cognitivedomains, for example adjusting foraging strategies associal needs, feeding needs, and their interactions fluc-tuate (Yamagiwa, Chapter 12, this volume). It also speaksto claims that only humans have this capacity.

Great apes’ cognitive achievements appear to beproducts of generative systems, i.e., systems that con-struct problem-specific cognitive structures to suit theparticular challenges encountered. Their skills in stonenut cracking (Inoue-Nakamura & Matsuzawa 1997), lan-guage (Miles 1991; Miles, Mitchell & Harper 1996),and classification (Langer 1996) all show construc-tive processes. Models characterizing great ape cog-nition in terms of centralized constructive processeslike hierarchization or hierarchical mental construc-tion take this position (Byrne 1995; Gibson 1993).Hierarchization is especially important because hier-archical cognitive systems may be intrinsically gener-ative (Gibson 1990; Rumbaugh, Washburn & Hillix1996). Generativity helps explain several ostensiblyanomalous features of great ape cognition that haveincited debate – notably, achievement variability acrossindividuals, tasks, rearing/testing conditions, and com-munities, and “atypical” abilities that emerge withspecial rearing. If great apes’ cognitive systems are gen-erative, these “anomalies” may simply be normal expres-sions of generative cognitive systems.

Development is a defining feature of primate cog-nition. Distinctive in great apes is prolonging cognitivedevelopment beyond infancy and emergence of theirdistinctively complex achievements during juvenility(Parker & McKinney 1999). Prolonged cognitive devel-opment probably relates to their more complex social

and ecological challenges compared with other anthro-poid primates (Byrne, Chapter 3, Parker, Chapter 4,van Schaik et al., Chapter 11, Yamagiwa, Chapter 12,Yamakoshi, Chapter 9, this volume) coupled with thelonger time they need to grow their exceptionally largebrains (Ross, Chapter 8, this volume). Great apes’enhanced cultural potential (e.g., more powerful sociallearning, greater social tolerance) is considered essentialto their cognitive development, underlining how diffi-cult these challenges must be. Even with larger brainsand more time to learn, immature great apes need moresophisticated and extensive social support than otheranthropoid primates.

Many cognitive features believed critical to homininevolution are then shared by great apes, including sym-bolism, generativity, and cognitive fluidity as well asspecific abilities like complex tool use and manufac-ture, mental representation of absent items, perspectivetaking, cooperative hunting, food sharing, and symboliccommunication. While great apes share these featuresonly to rudimentary symbolic levels, these achievementsare significant comparatively. Rudimentary symbolismin particular has been taken as an exclusively human leapforward in cognitive evolution. If great apes share thiscapacity, however, it must have evolved with ancestralhominids.

BIOLOGICAL BASES OF GREATAPE COGNITION

The brain

Efforts to establish what in the brain confers high cogni-tive potential have focused on brain size because it pre-dicts many other brain features (e.g., structures, gyrifi-cation, organization). The picture for great apes remainsunclear because all available size measures are prob-lematic as indices of cognitive potential and samplesof great ape brains have typically been very small (seeBegun & Kordos, Chapter 14, MacLeod, Chapter 7,Ross, Chapter 8, this volume). As larger samples arebecoming available, within-species variation is appear-ing to be extensive, so the many published findings basedon small samples must now be treated as suggestive.These limitations in mind, modern great ape brains sug-gest the following cognitive characterization.

Great apes brains appear to follow a distinctively“ape” design (MacLeod, Chapter 7, this volume). Allapes, compared with other nonhuman anthropoids,

Evolutionary origins of great ape intelligence 355

show more complex cerebral convolutions and an aug-mented neocerebellum. The neocerebellum connectsextensively with the cerebral cortex, and primarilythrough it the cerebellum contributes to cognitive pro-cesses such as planning complex motor patterns, visuo-spatial problem solving, and procedural learning. Thesecognitive processes support skills apes need as suspen-sory frugivores, for example spatial memory, mapping,and complex manipulation. A large sample of primatebrains also suggests that apes may have disproportion-ately larger brains for their body size than other anthro-poids; this finding is tentative and runs counter tostandard views, but it is consistent with these structuraldistinctions (see MacLeod, Chapter 7, Ross, Chapter 8,this volume). A distinctive ape brain is also consistentwith apes’ distinctive life histories: living apes have dis-proportionately prolonged immaturity with delay con-centrated in the juvenile period (Ross, Chapter 8, thisvolume); fossil hominoids may have shared this pattern(Kelley 1997, Chapter 15, this volume).

Great apes’ higher cognitive potential over lesserapes, system wide, may well be a function of absolutelylarge brain size and its allometric effects on morphology.Large brains provide more “extra” neurons for cognition(Gibson, Rumbaugh & Beran 2001; Rumbaugh 1995).Lesser apes’ brains resemble great ape brains morpho-logically but resemble typical anthropoid brains in abso-lute size (Begun, Chapter 2, this volume), and do notshow these cognitive enhancements. Large brains arealso more extensively interconnected; this may enablemore complex cortical processing by enabling parallelprocessing and distributed networks, and so enhanceproblem solving via simultaneous processing in mul-tiple areas of the cortex and their connecting structures(Gibson 1990). This fits well with great apes’ capacity forsolving complex problems by interconnecting multiplecognitive structures.

Many specific brain features that distinguish greatapes can also be explained by their brains’ absolutelylarge size (e.g., greater lateralization, neocortex expan-sion, specialized areas). Even if these features owe prin-cipally to larger brain size, they can translate into impor-tant differences in cognitive potential. Brain structuresthat increase in size with increases in overall brain sizedo so at differential rates. Structures implicated in cog-nition (e.g., neocortex, cerebellum) typically increase athigher rates, so they come to represent a larger per-centage of the brain in larger-brained species. For thisreason great apes have relatively larger neocerebellar

structures, magnifying the cognitive advantages of anape cerebellum. This cerebellar advantage may con-tribute to handling the more severe tasks that greatapes face as extremely large-bodied suspensory pri-mates. Large brain size also increases demands on cere-bral cortical connectivity that, in humans, may havefavored neocortical reorganization towards lateraliza-tion and locally specialized functional units (Deacon1990; Hopkins & Rilling 2000). Great ape brains, allweighing over 250 g, appear to be large enough to experi-ence similar effects: they show two specialized structuresimplicated in sophisticated communication, a planumtemporale and spindle neurons of the anterior cingulatecortex, which are otherwise found only in humans. Thatthe allometric effects of large brain size likely broughtspecialized structures along with greater interconnect-edness may be related to the co-occurrence of problem-specific and interconnected cognitive structures in greatapes and humans.

Life histories

Life history traits are fundamental attributes of a species’biology that govern the pattern of maturation from con-ception to death (e.g., gestation period, age at weaning,maturation rate – age of female first reproduction, inter-birth interval, longevity). These traits typically occur inpackages that fall roughly along a continuum of fast–slow rates of life. They correlate highly with body andbrain size, but some taxa depart dramatically from thepredicted life history–body size relationship. For theirbody sizes, primates have greatly protracted life his-tories with notably delayed maturation compared withmost other mammals. Links between the brain and lifehistories may suggest broader biological factors associ-ated with high cognitive potential. Reasons for specificscaling factors are typically explored by assessing linksamong ecological, brain, and life-history features.

Anthropoid brain size is linked with delayed matu-ration, in particular prolonged juvenility. Anthropoidsmay then make tradeoffs against juvenile growth rates tosupport their large brains, diverting energy away frombody growth to support the brain. Even after removingbody size effects, juvenility appears to be further pro-longed relative to body size in apes. Great apes may dothe same thing to a greater degree. Slower body growthprobably affects juveniles, even though most primatebrain growth occurs in infancy, because caregivers with-draw support at weaning (Ross, Chapter 8, this volume).


Juveniles’ immature foraging skills and the slow rate atwhich great apes learn, added to withdrawal of care-giver nutritional subsidies, can only prolong the periodin which their energy intake does not meet the energeticneeds of supporting the brain and body growth. Espe-cially in apes, prolonged juvenility may be best explainedas an unavoidable but bearable cost imposed by largebrains, rather than as directly adaptive (Ross, Chapter 8,van Schaik et al., Chapter 11, this volume). No clear linksoccur between the brain and life history in great apes asa distinct group (Ross, Chapter 8, this volume).

Body size

There is no question about great ape body sizes – all areexceptionally large for primates – or about correlationsbetween their large body size and their large brain size(Ward et al., Chapter 18, this volume). Yet the reasonsfor this relationship are unresolved: direct cause–effectin one direction or the other, parallel adaptations to otherselection pressures, or byproducts of selection on relatedfactors.

Because brains scale to body size, ratios betweenthe two have been used to index a species’ “encephaliza-tion,” the extent to which its brain has increased in cog-nitive potential, by assessing its enlargement beyond thesize predicted by its body size. By these measures, greatapes appear no more encephalized than other anthro-poids: their brains are not relatively larger given theirbody size, even if they are absolutely larger (but seeMacLeod, Chapter 7, this volume). This has promptedsome to suggest that body size is the driving evolution-ary adaptation and that great apes’ large brains are mereside effects of their large bodies (e.g., see MacLeod,Chapter 7, this volume). Analyses that simply seek to“remove body size effects” implicitly take this view.Brain–body mass relationships are much more com-plex than such corrections suggest (Begun & Kordos,Chapter 14, Ward et al., Chapter 18, this volume) andno acceptable method has yet been developed to appor-tion relative percentages of brain mass related directly tobody mass and to selection for absolutely bigger brains.

ENVIRONMENTAL PRESSURESON COGNITION

Establishing the function and evolution of complexcognition and its biological underpinnings involves

exploring related behavioral challenges. Behavioral chal-lenges affecting modern great apes are often used tosuggest evolutionary selection pressures that may haveshaped their cognitive enhancement. Their counter-parts in evolutionary history are inferred from indi-rect indices, for example diet from dental morphology.Ecological challenges that primarily tap physical cog-nition include diet/foraging (Parker & Gibson 1979),diverse “technical” difficulties (Byrne 1997), and ar-boreality (Povinelli & Cant 1995). Social challenges,which tap both social and communicative cognition,involve both competition and cooperation (e.g., Byrne &Whiten 1988; Parker 1996; van Schaik et al., Chapter 11,this volume). In light of our characterization of great apecognition and contributions to this volume, we recon-sider these challenges.

Ecological challenges

Food is considered a primary limiting ecological factorof primate populations because of its sparse distribu-tion and anti-predator defenses (Yamagiwa, Chapter 12,this volume). Features considered to challenge cognitioninclude eclectic frugivory, very large dietary repertoiresand correspondingly large ranges, and essential “tech-nically difficult” foods. Interest in difficult foods hasfocused on embedded foods, especially those that elicittool use, but foods protected by other defenses suchas barbs or noxious chemicals and obtained manuallypresent comparable cognitive challenges (e.g., Byrne &Byrne 1991, 1993; Russon 1998; Stokes & Byrne 2001).The distribution of tool use in the wild (chimpanzeesand orangutans) probably reflects opportunity and notdifferential hominid cognitive potential. Bonobos andgorillas can both use tools when opportunities arise.

Fallback foods on which great apes rely during fruitscarcities are often difficult to obtain. This may be espe-cially true of the fallback foods on which orangutans andchimpanzees rely, some of which elicit use of foragingtools in the wild (Yamakoshi 1998; Yamagiwa, Chapter12, this volume). Seasonal fruit scarcities also prob-ably contribute to great apes’ extremely broad dietaryrepertoires and their flexibility in using individual foods.Cognitively, the latter may require interpreting localindices of change to detect the availability of particularfoods, given that great apes inhabit the tropics where sea-sonal change can be irregular. The last common ances-tor (LCA) was also a generalized frugivore that may also


have consumed hard foods needing preparation priorto ingestion and inhabited seasonal forest habitats thatprobably imposed periodic fruit scarcities. By implica-tion, the same dietary pressures affecting modern greatapes also affected the LCA: seasonality, dietary breadth,and the need for fallback foods.

Arboreal locomotion and navigation, two spatialproblems, present extreme cognitive challenges to greatapes because of their extremely large bodies and for-est habitats. Navigating large ranges effectively and effi-ciently may require mapping skills sophisticated enoughto calculate routes and distances mentally. Povinelli andCant (1995) hypothesized that the great apes’ work-it-out-as-you-go, non-stereotypic modes of arboreal loco-motion, for example cautious clambering and gap cross-ing, require minds with the representational capacity tofigure in the self. These “cognitive” positional modesare neither shared among nor unique to all living greatapes, however (Gebo, Chapter 17, Hunt, Chapter 10,this volume). They are prominent in orangutans andlesser apes but not African great apes. They could haveinfluenced great ape cognitive evolution if the LCA wasa large arboreal clamberer but this is uncertain, per-haps even unlikely (Gebo, Chapter 17, this volume).Povinelli and Cant suggested Oreopithecus as a modelof that ancestor, with the requisite large size and bodyplan for arboreal clambering. Oreopithecus was other-wise very unlike other hominids, however (e.g., folivo-rous versus frugivorous, unusually small brained), andprobably represents an isolated adaptation to a refugiumrather than great apes’ ancestral condition (see Begun &Kordos, Chapter 14, Gebo, Chapter 17, Potts, Chapter13, Singleton, Chapter 16, this volume). Even if arboreallocomotion demands complex cognition in orangutans,there is little to indicate that it does, or did, in the greatape lineage.

Social challenges

Primate social life is recognized as having high poten-tial for cognitive complexity. It is puzzling about greatapes that they use more complex cognition than otheranthropoids to solve social problems, but the problemsthemselves are not obviously more complex. Their socialunit sizes are well within the range of other anthropoids,their demographic composition is no more complex, andfew if any more complex social phenomena are known(van Schaik et al., Chapter 11, this volume). To add to

the puzzle, great ape species differ widely in their socialsystems but are very similar in cognitive potential.

Van Schaik et al. propose social challenges in greatapes that may help explain their enhanced social cog-nition: fission–fusion tendencies with individuals outof contact with conspecifics for lengthy periods andforaging females solitary; relatively high subordinateleverage leading to less rigid dominance and enhancedsocial tolerance; greater intrasexual bonds with non-kin,and extensive flexibility in social organization and affil-iation. These are clearly shared by chimpanzees andorangutans, and perhaps by the other species. Mostare consequences of large size and exceptionally slowlife histories, which reduce vulnerability to predators,increase vulnerability to hostile conspecifics, increasethe potential for contest competition (especially forfemales and in species unable to switch to high-fiber fall-back foods), and favor non-kin bonding. They requiremore complex cognition to handle greater flexibility insocial relations and interactions and in the interplayamong a more complex array of labile factors (e.g., bal-ance rivalry with interdependence, or social with pre-dation or foraging pressures). Rejoining conspecificsafter lengthy absences increases needs for sophisticatednavigation, distance communication, and renegotiat-ing relationships. Two examples of complex commu-nication in wild great apes concern rejoining compan-ions: tree drumming (Boesch & Boesch-Achermann2000) and placing indicators of travel direction (Savage-Rumbaugh et al. 1996). Higher subordinate leverage,less rigid dominance, and enhanced social tolerance arelikely to improve opportunities for social learning, cul-tural transmission, and more flexible use of eye con-tact (Yamagiwa, Chapter 12, this volume). Similar socialcomplexities also occur in some monkeys (capuchins,some macaques), however, so alone they cannot explainthe enhanced cognition seen in great apes.

Great ape sociality should be affected by dietbecause social groups must adjust to ecological condi-tions. Effects probably differ more in great apes thanin other anthropoids because of great apes’ broad, tech-nically difficult, and seasonally varying diet (Yamagiwa,Chapter 12, this volume). Social foraging strategies dur-ing fruit scarcities, when dietary and social competi-tion pressures are at their worst, expose these effects.Significant to cognition is that great ape foraging groupschange as a function of food availability, although pat-terns differ between species depending in part on the


preferred type of fallback food. This is consistent withsuggestions that fission–fusion in Pan functions to allowflexibility in handling challenges that vary over timeand space (Boesch & Boesch-Achermann 2000), greatape life allows and requires facultative switches betweensolitary and gregarious foraging (van Schaik et al., Chap-ter 11, this volume), and ephemeral activity subgroupsshow exceptional flexibility relative to ecological con-ditions (Parker, Chapter 4, this volume). All great apesthen share the challenge, as a normal circumstance, ofcomplex problems wherein pressures from two distinctcognitive domains interact.

EVOLUTIONARY RECONSTRUCTIONS

The origin of great ape cognitive capabilities is to befound in the Miocene, when the great apes originatedand diversified. Here, we examine the evidence of brainsize and morphology, life history, body size, positionalbehavior, diet, and environment in ancestral hominoidsas they relate to the evolution of great ape intelligence.Patterns are summarized in Table 19.1.

Ecology: habitat and diet

The local habitats of early Miocene hominoids weremost likely warm, moist forests in tropical and sub-tropical zones that enjoyed low seasonality and cli-matic stability (Andrews, Begun & Zylstra 1997; Potts,Chapter 13, this volume). Soft fruit, their dietary main-stay (Singleton, Chapter 16, this volume), would havebeen available year-round, albeit patchily distributedspatially and temporally.

Hominid emergence in the late middle Miocene,14–12 Ma, coincides with increasing climatic fluctua-tion, especially increasing seasonality (Potts, Chapter 13,this volume). This may have restricted soft fruit avail-ability for several months annually, at least in someregions. The earliest Eurasian hominoid, Griphopithecus,which is more modern in dental anatomy than Proconsul,shows for the first time a fully developed suite of mastica-tory characters indicative of hard-object feeding (Gulec& Begun 2003; Heizmann & Begun 2001; Singleton,Chapter 16, this volume). The ability of the ancestors ofhominids to exploit hard objects may have allowed theirexpansion into Eurasia at the end of the early Miocene, asa way of avoiding competition with the many frugivoresmaking the same trip northward (Heizmann & Begun

2001). In later hominids, the ability to exploit theseresources may have served as an important parachuteduring times of scarcity in more seasonal environmentswhen soft fruits, generally preferred by hominids, aremore difficult to find. Greater seasonality is indicated inboth Europe and Asia in the late Miocene, suggestingfruit scarcities with hard objects serving as fallback foodsin some taxa. Sivapithecus is often reconstructed as hav-ing had an essentially soft fruit diet based on microwear(Teaford & Walker 1984), although morphologically itshared many features with hard-object feeders (thickenamel, low, rounded cusps, large molars, thick, massivemandibles), suggesting an ability to exploit hard objectswhen needed. Dryopithecus was not a hard-object feederand may have lived in less seasonal environments thanSivapithecus (Andrews et al. 1997; Begun 1994; Single-ton, Chapter 16, this volume; Potts, Chapter 13, this vol-ume). However, seasonality was probably greater in envi-ronments inhabited by Dryopithecus than in most earlyMiocene hominoid environments, and evidence of theanterior dentition suggests enhanced abilities for pre-ingestive processing of embedded foods (Begun 1992).Either way, late Miocene hominids probably extendedtheir frugivory with fallback foods during fruit scarcities.Their large body size may also represent a response toincreased seasonality because it enhances energy-storingcapacities for surviving periods of fruit scarcity (Knott1998; Yamagiwa, Chapter 12, this volume). Living greatapes show similar dietary breadth. Species differ in howthey adjust to fruit scarcities, but all share the overallpattern of relying on fallback foods. Orangutans andchimpanzees use “hard” fallback foods (e.g., embed-ded, barks, pith), perhaps analogous to Sivapithecus, andgorillas and bonobos lean to folivory (although bono-bos appear to enjoy especially rich habitats abundantwith THV, which may or may not serve as fallbackfoods), possibly more similar to the Dryopithecus strat-egy. These environmental pressures and species traitsimply considerable cognitive–behavioral adaptation, allin the direction of increased flexibility or adaptability(Potts, Chapter 13, this volume).

The latest Miocene experienced cooling, drying,and more pronounced seasonality, causing a worldwideshift from moist, warm forest to drier, open grass-land and a corresponding shift in vegetation (Cerlinget al. 1997; Potts, Chapter 13, this volume). Effectson hominids’ preferred habitats, moist warm forests,include shrinkage, fragmentation, and retreat. Preferred

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foods would have been available in smaller patches andmore dispersed in distribution, an ecological situationless suitable to large-bodied hominid foragers – espe-cially in groups. Hominid presence is indicated in iso-lated moist forest and swamp refuges and forest–openwoodland mosaics, suggesting they tracked their pre-ferred habitats where possible. Overall, their presencewas increasingly restricted southward (Begun 2001,2002; Harrison & Rook 1997; Potts, Chapter 13, thisvolume).

Fewer hominids are known in the fossil record ofthe late Miocene after the last occurrence of Dryopithe-cus and Sivapithecus between about 9.5 and 7 Ma. Theyappear to have become extinct locally while their descen-dants may have moved south at this time (Begun 2001).In Europe, the most ecologically specialized hominidsare known from this time. Oreopithecus from Tuscanyhad an exceptionally small brain, well-developed sus-pensory positional behavior and highly folivorous diet,while Ouranopithecus was among the largest of theMiocene hominids and had a specialized hard-food diet.It is also most likely during this time that the ancestorsof the African apes and humans arrived in Africaand that gorillas shortly thereafter diverged from thechimpanzee–human clade. Recent evidence from Thai-land suggests that orangutan ancestors may have firstappeared in Southeast Asia at this time as well (Chaima-nee et al. 2003). These patterns overall also suggest habi-tat tracking, i.e., maintaining established habitat andfruit preferences (Potts, Chapter 13, this volume).

In the Plio-Pleistocene, worldwide climate wasmarked by strong arid–moist and temperature oscil-lations, wider climatic fluctuation, instability, pro-found habitat variability, and arid–monsoon seasonal-ity (Potts, Chapter 13, this volume). Hominids wouldhave experienced increased episodic disturbance, intra-annual variability in food availability, and repeated forestcontraction–expansion and fragmentation–coalescence.Predictable effects include impoverished habitat in sizeand quality, even greater variability in food availabilityand abundance, changing species communities, chang-ing competitor and predator patterns, and variable pop-ulation densities (Potts, Chapter 13, this volume). Plio-Pleistocene pressures likely led to further diversificationof strategies to augment capacities for handling unpre-dictable habitat instabilities. Gorillas shifted towardsfolivory, especially for fallback foods, smaller ranges,and reduced foraging complexity. Chimpanzees shifted

to greater omnivory, including increased meat con-sumption, and use of savanna habitats. Bonobos main-tained forest habitats and increased THV consumption.Orangutans maintained earlier diets and remained intropical moist forests of southeast Asia, which persistedin large blocks on Borneo and Sumatra until this cen-tury. Hominins became increasingly dependent on ter-restrial resources and developed a variety of approaches(megadontia, tools) to maximize dietary breadth andecological flexibility.

The brain

Great apes’ distinctive brains seem be defined by theirlarge absolute size and hominoid morphology. Recon-structing their evolutionary origins comes down to whenand why these features evolved. This exercise remainshampered by the dearth of fossil material on ancestralapes, especially crania.

Proconsulids, early Miocene stem hominoids, wererelatively unspecialized pronograde quadrupeds butwere distinguished from primitive anthropoids by theirlarge size, taillessness, powerful appendages, and brainswith a few hominoid features (Begun & Kordos, Chapter14, this volume; Kelley 1997, Chapter 15, this volume;Ward et al. 1991, Chapter 18, this volume). The earlyhominids, Dryopithecus in Europe and Sivapithecus inSouth Asia, are either known or supposed on indirectbut solid grounds to have had brain sizes in the rangeof modern great apes; where known, their endocastsshow greater resemblances to modern hominids thando Proconsul endocasts (Begun & Kordos, Chapter 14,this volume). Sivapithecus neurocrania are not known.For Dryopithecus, partial neurocrania yield brain sizeestimates at the low end in absolute size but at the highend relative to body mass compared with the ranges formodern great apes. The fact that great apes with brainsranging from 280 to 700 cc, or humans with brains rang-ing from 1000 to 2000 cc, have not been shown to differ incognitive capacity could be taken to indicate that there isa loose causal relationship between brain mass and cog-nitive capacity (Kelley, Chapter 15, this volume). On theother hand, the fact that there is no overlap in brain massbetween monkeys and great apes or between great apesand humans suggests that normal brain mass minimain each taxon represent thresholds for cognitive changebeyond which cognition is not affected, until the nextthreshold is attained. If this is the case, and absolutely


large brains are what generate great apes’ grade of cogni-tion, then the rubicon represented by Dryopithecus andthe smallest extant great apes (280–350 cc) evolved in thelate middle Miocene with Dryopithecus and Sivapithecus.The emergence of the hominid-sized brain is associ-ated with increasing seasonality, seasonal fruit scarcities,and frugivorous diet enhanced with hard foods. Thoughthere are indications of hominid-like cerebral reorga-nization in Dryopithecus, its endocast is distinct fromthat of extant hominids so it is not clear whether theirbrains provided equivalent cognitive potential. At a min-imum however, the cognitive potential of late Miocenehominids spans the considerable gap between great apesand other nonhuman primates, probably coming closerto the former.

The Plio-Pleistocene is likely to have exerted fur-ther selection pressures on hominid cognition given itsnegative effects of great ape habitats. Brain size has notchanged, but organizational differences between extantand Miocene hominids probably occurred at this time(Begun & Kordos, Chapter 14, Potts, Chapter 13, thisvolume). The most telling findings from the fossil recordmay be that (1) partial de-coupling of size and mor-phology is a common feature in the evolution of catar-rhine brains, and (2) hominoid brain evolution is highlydiverse, with reduction in some lineages and increasesin others. Some lineages experience brain mass loss inconnection with body mass reduction (e.g., Hylobates)or independent of body mass change (e.g., Oreopithe-cus). The pattern of brain size diversity in fossil greatapes more closely matches broad patterns of diet than ofsize (Begun & Kordos, Chapter 14, this volume), espe-cially frugivory extended (seasonally) with challengingfallback foods. Brain size has been surprisingly stable inhominid evolution until Homo, despite dramatic changesand diversity in body mass, diet, positional behavior, andecological conditions. It may be that a hominoid brainsize at least 250 g represents a rubicon that generateshominid levels of cognitive and behavioral complexity.Conversely, although large bodies do not always implylarge brains in hominoids, large brains always co-occurwith large bodies.

Body size and life history

Fossil hominids were predominantly large bodied butsomewhat smaller than living great apes. The smallestDryopithecus (female D. laietanus and D. brancoi) was

probably smaller on average than the smallest livinggreat apes, the smallest females possibly weighing about20 kg (Begun, Chapter 2, Ward et al., Chapter 18, thisvolume). The smallest Sivapithecus, female S. punjabicus,probably ranged from close to Dryopithecus in body sizeto as large as the smallest living hominids. Other clearlyhominid taxa such as Ouranopithecus, other species ofSivapithecus, and Lufengpithecus are in the size range oflarge chimpanzees and small gorillas; so is Morotopithe-cus, though it is less clearly a great ape. The LCA wastherefore almost certainly large compared with most pri-mates. Hylobatids are small bodied, but this is probablya result of secondary reduction in size compared withthe common hominoid ancestor (Begun, Chapter 2, thisvolume). The range of body sizes in the proconsulids isbroad and overlaps with the hominids.

In addition to being the size of an extant greatape, Sivapithecus and Dryopithecus M1 emergence ageestimates suggest life history prolongation roughlyequivalent to that of modern great apes (Kelley 1997,Chapter 15, this volume). The stem hominoids Proconsuland Afropithecus may show the first signs of life historyprolongation. Proconsul may have been intermediatebetween hominids and non-hominids in M1 emergenceage (Kelley 1997, Chapter 15, this volume), althoughBegun & Kordos (Chapter 14, this volume) and Kelley(Chapter 15, this volume) both also find Proconsul tobe equivalent to Papio in M1 emergence and brain size.Afropithecus may have been within the great ape rangesfor M1 emergence and brain size (Kelley & Smith, 2003;Kelley, Chapter 15, this volume). However, in our viewthe poorly preserved neurocranium of Afropithecus ten-tatively suggests a somewhat smaller brain than in a simi-larly sized chimpanzee, which would be consistent withthe lower end of the range of estimates of M1 emer-gence and brain size provided by Kelley (Chapter 15, thisvolume). Either way, the implication is that prolongedimmaturity emerged with the hominoids but becamemore clearly prolonged as brain size increased with thefirst hominids, because of energetic constraints, socialconstraints, or both. There is likely a complex inter-relationship among life history, body mass, and bodysize that has yet to be fully understood in vertebrates ingeneral (Ward et al., Chapter 18, this volume).

Sociality

Characterizing sociality in the LCA is a highly spec-ulative exercise resting exclusively on indirect indices.


Several features of great ape sociality result from largesize and exceptionally slow life histories, both of whichcharacterize early hominids (many Chapters in this vol-ume). If, as argued for living great apes, large size andslow life histories give impetus to these social features,then hominids should share them. All great apes butno lesser apes also share fission–fusion tendencies thatare affected by fruit scarcities and fallback foods; earlyhominids likely experienced similar dietary pressures, sothey too may have had a fission–fusion form of sociality.

The main influence on female sociality, foodavailability, depends on fallback foods in great apes(Yamagiwa, Chapter 12, this volume). In chimpanzeesand orangutans, which rely on similar hard fallbackfoods, females restrict their social grouping during fruitscarcities and increase it during periods of abundance.In gorillas and bonobos, which have more folivorous fall-back patterns, females grouping patterns remain morestable. The main influence on male sociality, access tofemales, is primarily shaped by sexual dimorphism ingreat apes. In highly dimorphic orangutans and gorillas,males tend to be solitary and corral females for mat-ing. In less dimorphic chimpanzees and bonobos, malesassociate with one another via dominance ranking sys-tems. In early hominids, challenging fallback foods co-occur with high sexual dimorphism (Begun, Chapter 2,Singleton, Chapter 16, Ward et al., Chapter 18, this vol-ume), so their social systems may have resembled theorangutan’s, perhaps in less dispersed form. Attributesinclude polygynous mating systems with solitary malesattempting to monopolize multiple females or femaleranges, male dominance based on size, and female asso-ciations waxing and waning with the seasons.

DISCUSSION

Stem hominoids lived in moist tropical forest habi-tat with low seasonality, and probably exhibited dedi-cated frugivory, social complexity commensurate withfrugivory, polygynous social structures with relativelyhigh male–male competition, life histories with some-what prolonged immaturity, brains mostly of anthro-poid size and design, and body mass somewhere in therange between monkeys and great apes (10–25 kg). Fromthis starting point and considering the many factors dis-cussed in this book, we suggest the following patternsand processes in the evolution of great ape intelligence(Figure 19.1).

Ecology

Compared with the first hominoids, the first well-knownfossil hominids, Dryopithecus and Sivapithecus, inhab-ited middle to late Miocene moist tropical forests withgreater seasonality, frugivory extended in the directionof challenging foods, polygyny/high male–male compe-tition, life histories with prolonged immaturity and pro-longed juvenility, and larger bodies and brains reachinginto the modern great ape range. The greater season-ality combined with incorporation of hard or otherwisechallenging foods in the diet suggests a dietary shifttowards adding fallback foods requiring pre-ingestivepreparation as diet supplements during fruit scarcities.Increased absolute brain size indicates increased cog-nitive potential. Altogether, this suggests that seasonal-ity resulted in a more cognitively challenging diet thatfavored larger brains. Ecological pressures on hominidsintensified under the increasingly seasonal and unpre-dictable conditions of the latest Miocene and Plio-Pleistocene. Their effects on cognitive evolution wereperhaps constrained by habitat tracking, with the greatapes adopting a more conservative ecological approachand the hominins exploiting more radically differentenvironments.

Brain–Body–Sociality

In the anthropoid/hominoid phylogenetic context,hominid large brain and body size likely co-occurredwith slow life histories, prolonged immaturity, lowerpredation risk, higher vulnerability to hostile con-specifics, stronger relations with non-kin, high subordi-nate leverage, and relaxed dominance. Which came firstis neither interesting intellectually nor a useful questionprocessually. We will never know, and these variableswere probably a package as soon as they appeared inearly hominids.

Socially, this package is consistent with unusuallyflexible fission–fusion tendencies and enhanced socialtolerance (van Schaik et al., Chapter 11, this volume).The former would have favored larger brains for morecomplex social problem-solving; the latter may havefurther boosted cognition by enhancing conditions forsocio-cultural learning. Some social intelligence mod-els argue for an “arms race” in cognition, once cog-nitive solutions to social problems take hold, becausecompeting successfully depends on outwitting increas-ingly savvy conspecifics (e.g., Ward et al., Chapter 18,


Figure 19.1. Factors implicated in the evolution of great ape intel-ligence. Early hominids are distinguished from early hominoidsmostly by body and brain size and slowed growth. Ecologicalchanges may have been the catalyst for a feedback reaction betweenlarger bodies and slower growth on the one hand and ecologicalchallenges on the other. Which response typical of extant hominids

came first may never be known, and may not even be important.The combination of characters is unique to hominids. While auto-catalytic, directionality is not inevitable, as we see in the exam-ples of hominoids that have smaller brains and presumably lessintelligence.

this volume). Biological and ecological variables exertsimilar dynamic effects, and in concert with social pres-sures they feed back and contribute to further cognitiveevolution.

Additional pressures between the brain and social-ity may have arisen through prolonging juvenility, whichhas been linked with their large brains’ higher energydemands (Kelley, Chapter 15, Ross, Chapter 8, this vol-ume). Prolongation increases vulnerability for juveniles,who are handicapped by poor foraging skills and smallsize. Learning foraging skills is exceptionally slow anddifficult because of great apes’ difficult diets; complexskills for obtaining their most difficult foods, some ofthem fallback foods, may not be mastered until nearadulthood. Juveniles’ poor foraging skills and slow learn-ing essentially extend their dependency, aggravating

pressures on caregivers, especially mothers. These pres-sures have been linked with enhancing apprenticeship(e.g., imitation, teaching) as a means of speeding theirskill acquisition (e.g., Parker 1996).

Body–diet–brain

Brain size correlates with diet more closely than withbody size (Begun & Kordos, Chapter 14, this volume).Large bodies are none the less linked with diet. Thehominid combination of body size, diet, and brain sizeprobably aggravated cognitive challenges.

Hominids, exceptionally large bodied, would haverequired more and/or better food than smaller-bodiedhominoids, although not proportional to their greatersize because of their lower metabolic rates. Fruit


specialists’ diets are typically diversified because fruitsare energy rich but poor in important nutrients likeproteins and fat; hominids in particular are too largeto be dedicated frugivores, and at some point theydiversified their diets to include foods richer in proteinand fat (Waterman 1984; Yamagiwa, Chapter 12, thisvolume). Whenever large body size appeared betweenstem hominoids and early hominids, broadening thediet was one probable avenue of obtaining more food.Compared with stem hominoids, early hominid den-tition indicates expanding beyond soft fruits to eclec-tic frugivory or additional hard foods. If modern greatapes are any index, their broader diets increased cogni-tive challenges by increasing foraging complexity, whichincreases memory load and the range and complexity ofskills needed to locate and obtain food.

Large brains, with their high energetic costs, favorbetter-quality diets (e.g., meat in hominins). Non-fruitfoods are generally differently distributed and morehighly defended against predators than fruits. Effectson behavior include broadening and/or shifting foragingranges and foraging skill repertoires; this increases thevariety and especially the complexity of foraging skills,which translates into greater cognitive challenges. Inhominids, then, improving diets to support large brainslikely generated new pressures to enlarge the brain evenmore. In other words, hominid diets and large brainsmay have generated their own dietary cognitive armsrace.

Diet–SocialityHominid diets and sociality mutually affect one another,as shown by great apes’ foraging strategies during sea-sonal fruit scarcities. Foraging strategies are affected byboth fruit scarcities (through females) and social pres-sures (through male competition). For cognition, thisis the sort of intertwined tangle of complex social andecological demands that requires interconnected cogni-tion, that is, handling diverse demands in one integratedsolution; it is a recurrent feature of normal great ape life.Potts, Chapter 13, and Ward et al., Chapter 18, this vol-ume also recognize this situation.

This myriad of interdependent biological, social,and ecological factors affecting intelligence in hominidsis complicated beyond our ability to discern first causesor prime movers. We do know, however, that theseattributes co-occur only in hominids. Some of themoccur in other mammals, but never all together and never

to the degree expressed in hominids. First causes maythen be less important to present day outcomes thanchanges induced by multiple interdependencies amongthese factors.

It is also probable that in the evolution of hominidbrains, this attribute package entailed “arms races”involving both ecological (dietary) and social pressures.Arms races are always constrained by initial conditions.As Ward et al., Chapter 18, this volume note, withina taxon individuals compete mainly with conspecifics.Pressures on a hominid come from other hominids intheir ecological and social context. Given their differentevolutionary trajectories, arms races in different social,biological, and evolutionary contexts should producedifferent outcomes. This is the reason we do not seemonkeys, even capuchins and baboons, as intelligent asgreat apes and humans. Monkeys experience differentecological conditions and do not need to be as intelli-gent as great apes to compete with other monkeys. Forthe hominids, diet and moist tropical forests are goodcandidates for constraints. The great apes never reallygot out of the fruit market and that may have limitedtheir capacity to take in enough energy to enlarge theirbrains beyond some ceiling. Their persistent tracking ofmoist tropical forests would impose other constraints ontheir adaptation, especially given ever-dwindling forestsize and productivity. The possibility that some sort ofsystemic equilibrium sets in is suggested by the distinct“grades” of intelligence and brain–body size scaling pat-terns that are evident within the primates, as opposed tocontinuous gradation.

CONCLUSIONS

Our interpretation of available evidence is that the evo-lution of a great ape grade of intelligence involved a webof factors, causally interrelated and mutually adjusted.Constituent pressures and traits may have affected oneanother in spiraling or arms race fashion before reach-ing the particular combination seen in the hominids.Great ape adaptation constitutes an integrated pack-age of cognitive–behavioral–social–morphological traitsdovetailed to a particular constellation of ecological andsocial pressures and possibilities, rather than an assem-blage of individual traits adapted independently to spe-cific pressures. Their cognitive system, one componentof this package, was shaped by all these traits and shapedall these traits in turn.


Many cognitive enhancements taken as key homininadaptations are now recognized in great apes, andwere probably present in the common ancestor of allhominids. While these cognitive enhancements do notreach human levels in any great ape, they none the lesspoint to the ancestral condition of hominid cognition.These include enhancements to individual cognitiveabilities (e.g., distance communication, mental repre-sentation of distant entities, spatio-temporal mapping,adaptability to novel and variable situations, attribut-ing others’ perspectives, tool manufacture and use, foodsharing, cooperative hunting) as well as to central-ized processes (e.g., rudimentary symbolism, generativ-ity, multiple intelligences working together). Evidenceoffered here indicates that these cognitive enhancementsare part and parcel of a biological package that evolvedwith the great apes, including larger brains, larger bod-ies, and extended life histories, in concert with the pack-age of socio-ecological pressures they faced and created.This is consistent with other recent findings, for examplethat cultures in orangutans and chimpanzees show com-plexities previously thought possible only in humans(van Schaik et al. 2003; Whiten et al. 1999).

The cognitive achievements of humans originatedas cognitive responses in fossil great apes to increas-ingly difficult life in the evolving sub-tropical forests ofEurasia. The unique cognitive adaptations of homininsevolved in response to the more severe challenges (for anape) of more open forested or grassland ecological set-tings, and are mere elaborations of the cognitive adap-tations of their great ape ancestors. In other words, theorigin of the human cognitive capacity makes sense onlyin the light of great ape cognitive evolution.

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