494 Opinion TRENDS in Cognitive Sciences Vol.7 No.11 November 2003 Primate cognition: from ‘what now?’ to ‘what if ?’ Louise Barrett1, Peter Henzi2 and Robin Dunbar1 1School of Biological Sciences, University of Liverpool, Biosciences Building, Crown St, Liverpool, UK L69 7ZB 2Behavioural Ecology Research Group, University of Natal, 4041 Durban, South Africa The ‘social brain’ hypothesis has had a major impact on unique features of human cognition, such as language the study of comparative cognition. However, despite a and metacognition [11]. strong sense, gained from both experimental and Here, we present a new hypothesis to explain the observational work, that monkeys and apes differ from differences between monkeys and apes, based on an each other, we are still no closer to understanding understanding of the ecological constraints under which exactly how they differ. We hypothesize that the dis- these animals operate. Specifically, we argue that the persed social systems characteristic of ape societies dispersed social systems (‘fission–fusion’ societies) in explains why monkeys and apes should differ cogni- which most (if not all) of the hominoids (apes and humans) tively. The increased cognitive control and analogical live can be viewed as cognitively more demanding social reasoning ability needed to cope with life in dispersed ‘market places’ than monkey groups. The demands of societies also suggests a possible route for human cog- navigating a more complex social landscape thus con- nitive evolution. This hypothesis is supported by beha- stituted a unique selection pressure among the ancestral vioural and neurobiological data, but we need more of apes for increased brain size and cognitive abilities. This both if we are to fully understand how our primate cou- ecologically-valid approach will, we hope, enable research- sins see the world. ers to uncover the cognitive differences that have, so far, been concealed. Primates have unusually large brains for body size. It is now widely recognized that this is mainly associated with The social market place their distinctive social skills (the ‘Machiavellian intelli- To date, the social brain hypothesis has focused on a general notion of social complexity (often indexed by group gence’ [1] or ‘social brain’ hypothesis’ [2,3]). Within the size) as a driving force in brain evolution [3] and has not primate array, however, there are significant differences in attempted to explain how the particular characteristics of competence – most strikingly between monkeys and apes species’ social structure are related to cognitive capacity. – both in general cognitive abilities and, more importantly, However, recent empirical work on non-human primates in social behaviour and sociocognitive skills. These [12–14], along with theoretical speculations on humans contrasts seem to parallel differences between species in [15], suggests that applying a ‘biological markets’ [16] key aspects of brain evolution [4–6]. framework to studies of primate sociality might help point However, despite extensive psychological experimen- the way to more informative experimental studies of tation, the exact nature of the cognitive differences monkey and ape cognition. The theory of biological between monkeys and apes are unclear [7], and the degree markets views animals as traders engaged in a mutually to which apes are capable of any form of metarepresenta- beneficial exchange of commodities. Individuals within a tional thought (whether socially-based or not) remains biological market attempt to maximize ‘profit’ (in terms of contentious [8,9]. We suggest that this is because the tests fitness) by selecting social partners that offer the best have not been exhaustive and/or the right kinds of tests value, with an exchange rate set by the supply and demand have not been performed. The latter could be because of the commodity in question. much of the work on social cognition has been anthropo- Unlike standard optimality models of decision making, centric, seeking to discover which human cognitive market models are inherently dynamic, recognizing that characteristics are shared by our simian cousins [10]. individuals’ decisions vary across time according to local Thesameistruefromaneurobiologicalperspective, circumstance. They are perfect for the analysis of social where the use of monkeys as a model species has decision-making because the social world is also inher- meant, again, that similarities between non-human ently dynamic: each individual has its own particular set of primates and humans have been highlighted at the desires and goals that might not coincide with those of expense of distinctive differences. It is only recently others and decisions therefore reflect an ongoing process of that researchers have begun to probe for neurobiolo- negotiation. gical differences that might be linked to the apparently Studies of baboons (Papio hamadryas ursinus) [12–13] and chimpanzees (Pan troglodytes) [14] have shown that Corresponding author: Louise Barrett ([email protected]). animals trade grooming as a ‘service’, either for its own http://tics.trends.com 1364-6613/$ - see front matter q 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.tics.2003.09.005 Opinion TRENDS in Cognitive Sciences Vol.7 No.11 November 2003 495 utilitarian value or for its value equivalent; moreover, true market effects can be found, with the duration of grooming 1000 (the ‘price paid’) varying in relation to the supply of particular commodities [13]. Viewing primate groups as market places allows us to refine the social brain 100 hypothesis because we can identify the key differences between ape and monkey market places and thus predict consequent differences in cognitive skills. 10 Mean group size Mean group A market for brain power In primate market places, individuals must track the price 1 0.1 1 10 of commodities and respond flexibly to changes in supply Neocortex ratio and demand. This agrees with the ‘Machiavellian intelli- gence’ hypothesis, in that sociality is assumed to drive TRENDS in Cognitive Sciences brain evolution. It differs, however, by assuming that Figure 1. Evidence for grades within the primate brain suggests that there may be animals have not been selected to cope with increasingly quantitative, or even qualitative, differences between monkey and ape social cog- elaborate strategies and counter-strategies, the goals of nition. When a measure of social complexity (in this case, group size) is plotted which are to ‘outwit’ the competition. Instead, it assumes against a measure of relative brain size (in this case, the ratio of neocortex volume to the volume of the rest of the brain), it is apparent that hominoids (apes and that the evolution of brain size and structure have been humans, orange squares) require more neural capacity to support a given group driven by a need to track fluctuations in commodity value. size than monkeys (pink circles) do, who in turn require more than prosimians Monitoring the market place is intrinsically complex (blue triangles). Each datapoint is a single genus. Humans are represented by the top right-hand square. because the value of a particular partner is contingent on the value of others. Each of these values can shift with whole. By contrast, the nature of spider monkey fission– changes in reproductive state, health, dominance and fusion is not well studied and could differ from apes in ongoing social behaviour. Those who are good value today important ways. If, however, their behaviour is truly ape- might not be so tomorrow. This constant state of flux like, then we have an ideal test case: we would predict that means that keeping tabs on the social market is very they manifest ape-like cognitive abilities – something that different from the other kinds of contingent monitoring is, perhaps, hinted at by the fact that they are one of the that primates must do, such as tracking fluctuations in most encephalized of the South American monkeys. fruit availability [17]. Fruits, unlike conspecifics, do not In fission–fusion societies, individuals see each other make decisions of their own in response to primate only at infrequent intervals, often weeks apart, yet each behaviour. This inherent contingency in primate market recognizes the members of its community and is capable of places thus selects for a ‘knowledge-based’ [18], rather maintaining long-standing relationships. In such systems, than strictly cue-based, understanding of others, as individuals must be able to represent mentally individuals evidence from monkeys and, to an even greater degree, that are not present and to retain and manipulate apes has shown [18]. Nevertheless, there remains a information about them for substantial periods of time, cognitive difference between monkeys and apes that, whereas there is no such pressure for these abilities to although poorly characterized, is apparent when compar- evolve in spatially and temporally stable monkey groups ing their performance on psychological tests [7,19–20].It where animals are only out of view for at most a few hours. is also apparent that there are distinct grades within the The computational load required to monitor and track brain data that point specifically to increased cognitive changes in a dispersed ape market place is therefore powers among the apes [3,6,21] (Figure 1). We suggest that significantly greater than when members of a group see these emerged because of a key difference in the market each other every day [6]. A salient point to note in this places of these two taxonomic groups. context is that humans also live in dispersed societies Whereas monkeys are all highly gregarious and live in based on fission–fusion dynamics [25]. cohesive groups in which individuals encounter every member of their group every day, the apes – in particular, Monitoring space and time the chimpanzee and orang-utan (Pongo pygmaeus) – live More importantly, in terms of monitoring the state of their in more fragmented societies as a result of food compe- social market place, animals need to recognize that the tition, which forces females to forage in small parties or absence of a particular individual can affect the relative alone [22].