The evolution of primate general and cultural intelligence

There are consistent individual differences in human intelligence, attributable to a single 'general intelligence' factor, g. The evolutionary basis of g and its links to social learning and culture remain controversial. Conflicting hypotheses regard primate cognition as divided into specialized, independently evolving modules versus a single general process. To assess how processes underlying culture relate to one another and other cognitive capacities, we compiled ecologically relevant cognitive measures from multiple domains, namely reported incidences of behavioural innovation, social learning, tool use, extractive foraging and tactical deception, in 62 primate species. All exhibited strong positive associations in principal component and factor analyses, after statistically controlling for multiple potential confounds. This highly correlated composite of cognitive traits suggests social, technical and ecological abilities have coevolved in primates, indicative of an across-species general intelligence that includes elements of cultural intelligence. Our composite species-level measure of general intelligence, 'primate g(S)', covaried with both brain volume and captive learning performance measures. Our findings question the independence of cognitive traits and do not support 'massive modularity' in primate cognition, nor an exclusively social model of primate intelligence. High general intelligence has independently evolved at least four times, with convergent evolution in capuchins, baboons, macaques and great apes.     

Group Size Predicts Social but Not Nonsocial Cognition in Lemurs

The social intelligence hypothesis suggests that living in large social networks was the primary selective pressure for the evolution of complex cognition in primates. This hypothesis is supported by comparative studies demonstrating a positive relationship between social group size and relative brain size across primates. However, the relationship between brain size and cognition remains equivocal. Moreover, there have been no experimental studies directly testing the association between group size and cognition across primates. We tested the social intelligence hypothesis by comparing 6 primate species (total N = 96) characterized by different group sizes on two cognitive tasks. Here, we show that a species’ typical social group size predicts performance on cognitive measures of social cognition, but not a nonsocial measure of inhibitory control. We also show that a species’ mean brain size (in absolute or relative terms) does not predict performance on either task in these species. These data provide evidence for a relationship between group size and social cognition in primates, and reveal the potential for cognitive evolution without concomitant changes in brain size. Furthermore our results underscore the need for more empirical studies of animal cognition, which have the power to reveal species differences in cognition not detectable by proxy variables, such as brain size.     

The social nature of primate cognition

The hypothesis that the enlarged brain size of the primates was selected for by social, rather than purely ecological, factors has been strongly influential in studies of primate cognition and behaviour over the past two decades. However, the Machiavellian intelligence hypothesis, also known as the social brain hypothesis, tends to emphasize certain traits and behaviours, like exploitation and deception, at the expense of others, such as tolerance and behavioural coordination, and therefore presents only one view of how social life may shape cognition. This review outlines work from other relevant disciplines, including evolutionary economics, cognitive science and neurophysiology, to illustrate how these can be used to build a more general theoretical framework, incorporating notions of embodied and distributed cognition, in which to situate questions concerning the evolution of primate social cognition.     

Old world monkeys compare to apes in the primate cognition test battery

Understanding the evolution of intelligence rests on comparative analyses of brain sizes as well as the assessment of cognitive skills of different species in relation to potential selective pressures such as environmental conditions and social organization. Because of the strong interest in human cognition, much previous work has focused on the comparison of the cognitive skills of human toddlers to those of our closest living relatives, i.e. apes. Such analyses revealed that apes and children have relatively similar competencies in the physical domain, while human children excel in the socio-cognitive domain; in particular in terms of attention sharing, cooperation, and mental state attribution. To develop a full understanding of the evolutionary dynamics of primate intelligence, however, comparative data for monkeys are needed. We tested 18 Old World monkeys (long-tailed macaques and olive baboons) in the so-called Primate Cognition Test Battery (PCTB) (Herrmann et al. 2007, Science). Surprisingly, our tests revealed largely comparable results between Old World monkeys and the Great apes. Single comparisons showed that chimpanzees performed only better than the macaques in experiments on spatial understanding and tool use, but in none of the socio-cognitive tasks. These results question the clear-cut relationship between cognitive performance and brain size and--prima facie--support the view of an accelerated evolution of social intelligence in humans. One limitation, however, is that the initial experiments were devised to tap into human specific skills in the first place, thus potentially underestimating both true nonhuman primate competencies as well as species differences.     

Social learning and evolution: the cultural intelligence hypothesis

If social learning is more efficient than independent individual exploration, animals should learn vital cultural skills exclusively, and routine skills faster, through social learning, provided they actually use social learning preferentially. Animals with opportunities for social learning indeed do so. Moreover, more frequent opportunities for social learning should boost an individual's repertoire of learned skills. This prediction is confirmed by comparisons among wild great ape populations and by social deprivation and enculturation experiments. These findings shaped the cultural intelligence hypothesis, which complements the traditional benefit hypotheses for the evolution of intelligence by specifying the conditions in which these benefits can be reaped. The evolutionary version of the hypothesis argues that species with frequent opportunities for social learning should more readily respond to selection for a greater number of learned skills. Because improved social learning also improves asocial learning, the hypothesis predicts a positive interspecific correlation between social-learning performance and individual learning ability. Variation among primates supports this prediction. The hypothesis also predicts that more heavily cultural species should be more intelligent. Preliminary tests involving birds and mammals support this prediction too. The cultural intelligence hypothesis can also account for the unusual cognitive abilities of humans, as well as our unique mechanisms of skill transfer.     

Communicative roots of complex sociality and cognition

Mammals living in more complex social groups typically have large brains for their body size and many researchers have proposed that the primary driver of the increase in brain size through primate and hominin evolution was the selection pressures associated with sociality. Many mammals, and especially primates, use flexible signals that show a high degree of voluntary control and these signals may play an important role in forming and maintaining social relationships between group members. However, the specific role that cognitive skills play in this complex communication, and how in turn this relates to sociality, is still unclear. The hypothesis for the communicative roots of complex sociality and cognition posits that cognitive demands behind the communication needed to form and maintain bonded social relationships in complex social settings drives the link between brain size and sociality. We review the evidence in support of this hypothesis and why key features of cognitively complex communication such as intentionality and referentiality should be more effective in forming and maintaining bonded relationships as compared with less cognitively complex communication. Exploring the link between cognition, communication and sociality provides insights into how increasing flexibility in communication can facilitate the emergence of social systems characterised by bonded social relationships, such as those found in non‐human primates and humans. To move the field forward and carry out both within‐ and among‐species comparisons, we advocate the use of social network analysis, which provides a novel way to describe and compare social structure. Using this approach can lead to a new, systematic way of examining social and communicative complexity across species, something that is lacking in current comparative studies of social structure.     

Human cognitive ecology: an instructive framework for comparative primatology

In this review, research on human cognitive ecology is compared with studies of the cognitive ecologies of apes-especially the common chimpanzee. The objective was to assess the feasibility of extending an activity-theory framework developed in studies of humans to an integrated approach for studying the cognitive accomplishments and skills of other primates living in the wild. Six generalizations were abstracted from studies of humans: 1) Social and material environments are arranged to facilitate production. 2) Human activity is shaped by conceptual and cultural principles that provide underlying logic for working knowledge and practice. 3) Schemata (multimodal, mental representations of procedures, strategies, and techniques) govern performance in a domain. 4) Working knowledge, skills, and social identities are co-constructed in communities of practice. 5) Rehearsal improves skilled performances, from which reputations as well as material products are derived. 6) Planning and emergence are in productive tension in human practices. These generalizations are applied to findings in the literature regarding the behavior of chimpanzees and other apes in the wild to assess the potential utility of a situated-activity approach for comparative studies of primate cognition. It is argued in the Discussion that schemata constitute a common core of higher primate intelligence. Planning, emergence, and alterations of the environment to facilitate production further characterize human and chimpanzee or gorilla behaviors to varying degrees. Less apparent in the nonhuman-primate literature is evidence of governing principles, rehearsal, and skill-based reputations or identities entailing theories of mind. Nonetheless, recent observations in the wild suggest that further research is warranted to explore the rudiments of each of these components to enhance our understanding of the ecology of primate cognition and its evolutionary history.     

Taxonomic counts of cognition in the wild

In 1985, Kummer & Goodall pleaded for an ecology of intelligence and proposed that innovations might be a good way to measure cognition in the wild. Counts of innovation per taxonomic group are now available in hundreds of avian and primate species, as are counts of tactical deception, tool use and social learning. Robust evidence suggests that innovation rate and its neural correlates allow birds and mammals to cope better with environmental change. The positive correlations between taxonomic counts, and the increasing number of cognitive and neural measures found to be associated with ecological variables, suggest that domain general processes might be more pervasive than previously thought in the evolution of intelligence.     

Machiavellian intelligence

The hypothesis that intelligence is an adaptation to deal with the complexity of living in semi-permanent groups of conspecifics, a situation that involves the potentially tricky balance of competition and cooperation with the same individuals, has been influential in recent theorizing about human mental evolution. It is important to distinguish among distinct versions of this general idea, for they predict different cognitive consequences and apply to different species of animal. Empirical support is strong in primates for links between (i) social complexity based on evolved tactics that require a good memory for socially relevant information, (ii) neocortical enlargement, and (iii) size of social groupings. However, the evolution of computational thought and the ability to understand other individuals' intentions are not well explained as products of selection for Machiavellian intelligence. Quite different explanations may therefore be required for increases in intelligence that occurred at different times in human ancestry.     

The human socio-cognitive niche and its evolutionary origins

Hominin evolution took a remarkable pathway, as the foraging strategy extended to large mammalian prey already hunted by a guild of specialist carnivores. How was this possible for a moderately sized ape lacking the formidable anatomical adaptations of these competing 'professional hunters'? The long-standing answer that this was achieved through the elaboration of a new 'cognitive niche' reliant on intelligence and technology is compelling, yet insufficient. Here we present evidence from a diversity of sources supporting the hypothesis that a fuller answer lies in the evolution of a new socio-cognitive niche, the principal components of which include forms of cooperation, egalitarianism, mindreading (also known as 'theory of mind'), language and cultural transmission, that go far beyond the most comparable phenomena in other primates. This cognitive and behavioural complex allows a human hunter-gatherer band to function as a unique and highly competitive predatory organism. Each of these core components of the socio-cognitive niche is distinctive to humans, but primate research has increasingly identified related capacities that permit inferences about significant ancestral cognitive foundations to the five pillars of the human social cognitive niche listed earlier. The principal focus of the present study was to review and integrate this range of recent comparative discoveries.     

The slow process: A hypothetical cognitive adaptation for distributed cognitive networks

Human cognitive evolution is characterized by two special features that are truly novel in the primate line. The first is the emergence of "mindsharing" cultures that perform cooperative cognitive work, and serve as distributed cognitive networks. The second is the emergence of a brain that is specifically adapted for functioning within those distributed networks, and cannot realize its design potential without them. This paper proposes a hypothetical neural process at the core of this brain adaptation, called the "slow process". It enables the human brain to comprehend social events of much longer duration and complexity than those that characterize primate social life. It runs in the background of human cognitive life, with the faster moving sensorimotor interface running in the foreground. Most mammals can integrate events in the shorter time zone that corresponds to working memory. However, very few can comprehend complex events that extend over several hours (for example, a game or conversation) in what may be called the "intermediate" time zone. Adult humans typically live, plan, and imagine their lives in this time range, which seems to exceed the capabilities of our closest relatives, bonobos and chimpanzees. In summary, human cognition has both an individual and a collective dimension. Individual brains and minds function within cognitive-cultural networks, or CCNs, that store and transmit knowledge. The human brain relies on cultural input even to develop the basic cognitive capacities needed to gain access to that knowledge in the first place. The postulated slow process is a top-down executive capacity that evolved specifically to manage the cultural connection, and handle the cognitive demands imposed by increasingly complex distributed systems.     

Social intelligence, human intelligence and niche construction

This paper is about the evolution of hominin intelligence. I agree with defenders of the social intelligence hypothesis in thinking that externalist models of hominin intelligence are not plausible: such models cannot explain the unique cognition and cooperation explosion in our lineage, for changes in the external environment (e.g. increasing environmental unpredictability) affect many lineages. Both the social intelligence hypothesis and the social intelligence-ecological complexity hybrid I outline here are niche construction models. Hominin evolution is hominin response to selective environments that earlier hominins have made. In contrast to social intelligence models, I argue that hominins have both created and responded to a unique foraging mode; a mode that is both social in itself and which has further effects on hominin social environments. In contrast to some social intelligence models, on this view, hominin encounters with their ecological environments continue to have profound selective effects. However, though the ecological environment selects, it does not select on its own. Accidents and their consequences, differential success and failure, result from the combination of the ecological environment an agent faces and the social features that enhance some opportunities and suppress others and that exacerbate some dangers and lessen others. Individuals do not face the ecological filters on their environment alone, but with others, and with the technology, information and misinformation that their social world provides.     

Natural pedagogy as evolutionary adaptation

We propose that the cognitive mechanisms that enable the transmission of cultural knowledge by communication between individuals constitute a system of 'natural pedagogy' in humans, and represent an evolutionary adaptation along the hominin lineage. We discuss three kinds of arguments that support this hypothesis. First, natural pedagogy is likely to be human-specific: while social learning and communication are both widespread in non-human animals, we know of no example of social learning by communication in any other species apart from humans. Second, natural pedagogy is universal: despite the huge variability in child-rearing practices, all human cultures rely on communication to transmit to novices a variety of different types of cultural knowledge, including information about artefact kinds, conventional behaviours, arbitrary referential symbols, cognitively opaque skills and know-how embedded in means-end actions. Third, the data available on early hominin technological culture are more compatible with the assumption that natural pedagogy was an independently selected adaptive cognitive system than considering it as a by-product of some other human-specific adaptation, such as language. By providing a qualitatively new type of social learning mechanism, natural pedagogy is not only the product but also one of the sources of the rich cultural heritage of our species.     

Investigating cognitive genetics and its implications for the treatment of cognitive deficit

Cognitive impairment in the elderly, caused by either normal ageing process or dementia, is an increasing problem in developed countries that has enormous social and economic considerations. Research investigating the genetic basis of cognition is a new and rapidly developing field that may aid in the development of new treatments for age-related cognitive deficit. Over the past 6 years, a number of quantitative trait loci (QTLs) have been associated with cognitive functioning in humans including loci within the genes catechol- o -methyltransferase, brain-derived neurotrophic factor, muscle segment homeobox 1, serotonin transporter 2A (HTR2A), cholinergic muscarinic receptor 2, cathepsin D, metabotrophic glutamate receptor and most recently the class II human leukocyte antigens. Unfortunately, inconsistency within the literature, which is a hallmark of almost all association studies investigating complex diseases and traits, is casting doubt as to which genes are truly associated with cognition and which are a result of Type 2 error. This review will highlight implicated intelligence QTLs, examine the probable reasons for the current discrepancies between reports and discuss the potential advantages that may be procured from the study of cognitive genetics.     

Social games between bonobos and humans: evidence for shared intentionality?

Triadic social games are interesting from a cognitive perspective because they require a high degree of mutual social awareness. They consist of two agents incorporating an object in turn-taking sequences and require individuals to coordinate their attention to the task, the object, and to one another. Social games are observed commonly in domesticated dogs interacting with humans, but they have received only little empirical attention in nonhuman primates. Here, we report observations of bonobos (Pan paniscus) engaging in social games with a human playmate. Our behavioral analyses revealed that the bonobos behaved in many ways similar to human children during these games. They were interested in the joint activity, rather than the play objects themselves, and used communicative gestures to encourage reluctant partners to perform their role, suggesting rudimentary understanding of others' intentions. Our observations thus may imply that shared intentionality, the ability to understand and shares intention with other individuals, has emerged in the primate lineage before the origins of hominids.     

Cooperation and the evolution of intelligence

The high levels of intelligence seen in humans, other primates, certain cetaceans and birds remain a major puzzle for evolutionary biologists, anthropologists and psychologists. It has long been held that social interactions provide the selection pressures necessary for the evolution of advanced cognitive abilities (the 'social intelligence hypothesis'), and in recent years decision-making in the context of cooperative social interactions has been conjectured to be of particular importance. Here we use an artificial neural network model to show that selection for efficient decision-making in cooperative dilemmas can give rise to selection pressures for greater cognitive abilities, and that intelligent strategies can themselves select for greater intelligence, leading to a Machiavellian arms race. Our results provide mechanistic support for the social intelligence hypothesis, highlight the potential importance of cooperative behaviour in the evolution of intelligence and may help us to explain the distribution of cooperation with intelligence across taxa.     

The coevolution of innovation and technical intelligence in primates

In birds and primates, the frequency of behavioural innovation has been shown to covary with absolute and relative brain size, leading to the suggestion that large brains allow animals to innovate, and/or that selection for innovativeness, together with social learning, may have driven brain enlargement. We examined the relationship between primate brain size and both technical (i.e. tool using) and non-technical innovation, deploying a combination of phylogenetically informed regression and exploratory causal graph analyses. Regression analyses revealed that absolute and relative brain size correlated positively with technical innovation, and exhibited consistently weaker, but still positive, relationships with non-technical innovation. These findings mirror similar results in birds. Our exploratory causal graph analyses suggested that technical innovation shares strong direct relationships with brain size, body size, social learning rate and social group size, whereas non-technical innovation did not exhibit a direct relationship with brain size. Nonetheless, non-technical innovation was linked to brain size indirectly via diet and life-history variables. Our findings support ‘technical intelligence’ hypotheses in linking technical innovation to encephalization in the restricted set of primate lineages where technical innovation has been reported. Our findings also provide support for a broad co-evolving complex of brain, behaviour, life-history, social and dietary variables, providing secondary support for social and ecological intelligence hypotheses. The ability to gain access to difficult-to-extract, but potentially nutrient-rich, resources through tool use may have conferred on some primates adaptive advantages, leading to selection for brain circuitry that underlies technical proficiency.     

Mental rehearsal in great apes (Pan troglodytes and Pongo pygmaeus) and children

The ability to rehearse possible future courses of action in the mind is an important feature of advanced social cognition in humans, and the "social brain" hypothesis implies that it might also be a feature of primate social cognition. We tested two chimpanzees, six orangutans and 63 children aged 3-7 years on a set of four puzzle boxes, half of which were presented with an opportunity to observe the box before being allowed to open it ("prior view"), the others being given without an opportunity to examine the boxes before handling them ("no prior view"). When learning effects are partialled out, puzzle boxes in the "prior view" condition were opened significantly faster than boxes given in the "no prior view" condition by the children, but not by either of the great apes. The three species differ significantly in the speed with which they opened boxes in the "no prior view" condition. The three species' performance on this task was a function of relative frontal lobe volume, suggesting that it may be possible to identify quantitative neuropsychological differences between species.     

Functionally referential signals: A promising paradigm whose time has passed

Finding the evolutionary origins of human language in the communication systems of our closest living relatives has, for the last several decades, been a major goal of many in the field of animal communication generally and primate communication specifically. 1 - 4 The so‐called “functionally referential” signals have long been considered promising in this regard, with apparent parallels with the semantic communication that characterizes language. The once‐prominent idea that functionally referential signals are word‐like, in that they are arbitrary sounds that refer to phenomena external to the caller, has largely been abandoned. 5 However, the idea that these signals may offer the strongest link between primate communication and human language remains widespread, primarily due to the fact the behavior of receivers indicates that such signals enable them to make very specific inferences about their physical or social environment. Here we review the concept of functional reference and discuss modern perspectives that indicate that, although the sophistication of receivers provides some continuity between nonhuman primate and human cognition, this continuity is not unique to functionally referential signals. In fact, because functionally referential signals are, by definition, produced only in specific contexts, receivers are less dependent on the integration of contextual cues with signal features to determine an appropriate response. The processing of functionally referential signals is therefore likely to entail simpler cognitive operations than does that of less context‐specific signals. While studies of functional reference have been important in highlighting the relatively sophisticated processes that underlie receiver behavior, we believe that the continued focus on context‐specific calls detracts from the potentially more complex processes underlying responses to more unspecific calls. In this sense, we argue that the concept of functional reference, while historically important for the field, has outlived its usefulness and become a red herring in the pursuit of the links between primate communication and human language. © 2012 Wiley Periodicals, Inc.     

Opinion: the neural basis of human moral cognition

Moral cognitive neuroscience is an emerging field of research that focuses on the neural basis of uniquely human forms of social cognition and behaviour. Recent functional imaging and clinical evidence indicates that a remarkably consistent network of brain regions is involved in moral cognition. These findings are fostering new interpretations of social behavioural impairments in patients with brain dysfunction, and require new approaches to enable us to understand the complex links between individuals and society. Here, we propose a cognitive neuroscience view of how cultural and context-dependent knowledge, semantic social knowledge and motivational states can be integrated to explain complex aspects of human moral cognition.