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.     

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.     

Understanding primate brain evolution

We present a detailed reanalysis of the comparative brain data for primates, and develop a model using path analysis that seeks to present the coevolution of primate brain (neocortex) and sociality within a broader ecological and life-history framework. We show that body size, basal metabolic rate and life history act as constraints on brain evolution and through this influence the coevolution of neocortex size and group size. However, they do not determine either of these variables, which appear to be locked in a tight coevolutionary system. We show that, within primates, this relationship is specific to the neocortex. Nonetheless, there are important constraints on brain evolution; we use path analysis to show that, in order to evolve a large neocortex, a species must first evolve a large brain to support that neocortex and this in turn requires adjustments in diet (to provide the energy needed) and life history (to allow sufficient time both for brain growth and for 'software' programming). We review a wider literature demonstrating a tight coevolutionary relationship between brain size and sociality in a range of mammalian taxa, but emphasize that the social brain hypothesis is not about the relationship between brain/neocortex size and group size per se; rather, it is about social complexity and we adduce evidence to support this. Finally, we consider the wider issue of how mammalian (and primate) brains evolve in order to localize the social effects.     

Introduction: Current studies on primate socioecology and evolution

Primate socioecology is being dramatically transformed as new studies are undertaken in Madagascar and the New World. Simultaneously, the incorporation of primate studies in a broader framework of theory in behavioral ecology promises to more intelligently inform anthropology's traditional concerns with primate and hominid evolution.     

Age at first molar emergence in early Miocene Afropithecus turkanensis and life-history evolution in the Hominoidea

Among primates, age at first molar emergence is correlated with a variety of life history traits. Age at first molar emergence can therefore be used to broadly infer the life histories of fossil primate species. One method of determining age at first molar emergence is to determine the age at death of fossil individuals that were in the process of erupting their first molars. This was done for an infant partial mandible of Afropithecus turkanensis (KNM-MO 26) from the approximately 17.5 Ma site of Moruorot in Kenya. A range of estimates of age at death was calculated for this individual using the permanent lateral incisor germ preserved in its crypt, by combining the number and periodicity of lateral enamel perikymata with estimates of the duration of cuspal enamel formation and the duration of the postnatal delay in the inception of crown mineralization. Perikymata periodicity was determined using daily cross striations between adjacent Retzius lines in thin sections of two A. turkanensis molars from the nearby site of Kalodirr. Based on the position of the KNM-MO 26 M(1)in relation to the mandibular alveolar margin, it had not yet undergone gingival emergence. The projected time to gingival emergence was estimated based on radiographic studies of M(1)eruption in extant baboons and chimpanzees.The estimates of age at M(1)emergence in KNM-MO 26 range from 28.2 to 43.5 months, using minimum and average values from extant great apes and humans for the estimated growth parameters. Even the absolute minimum value is well outside the ranges of extant large Old World monkeys for which there are data (12.5 to <25 months), but is within the range of chimpanzees (25.7 to 48.0 months). It is inferred, therefore, that A. turkanensis had a life history profile broadly like that of Pan. This is additional evidence to that provided by Sivapithecus parvada (Function, Phylogeny, and Fossils: Miocene Hominoid Evolution and Adaptations, 1997, 173) that the prolonged life histories characteristic of extant apes were achieved early in the evolutionary history of the group. However, it is unclear at present whether life-history prolongation in apes represents the primitive catarrhine pace of life history extended through phyletic increase in body mass, or whether it is derived with respect to a primitive, size-adjusted life history that was broadly intermediate between those of extant hominoids and cercopithecoids. Life history evolution in primates as a whole may have occurred largely through a series of grade-shifts, with the establishment of fundamental life-history profiles early in the histories of major higher taxa. These may have included shifts that were largely body mass dependent, as well as those that occurred in the absence of significant changes in body mass.     

Cooperation and human cognition: the Vygotskian intelligence hypothesis

Nicholas Humphrey's social intelligence hypothesis proposed that the major engine of primate cognitive evolution was social competition. Lev Vygotsky also emphasized the social dimension of intelligence, but he focused on human primates and cultural things such as collaboration, communication and teaching. A reasonable proposal is that primate cognition in general was driven mainly by social competition, but beyond that the unique aspects of human cognition were driven by, or even constituted by, social cooperation. In the present paper, we provide evidence for this Vygotskian intelligence hypothesis by comparing the social-cognitive skills of great apes with those of young human children in several domains of activity involving cooperation and communication with others. We argue, finally, that regular participation in cooperative, cultural interactions during ontogeny leads children to construct uniquely powerful forms of perspectival cognitive representation.     

The evolution of brain size and intelligence in man

The brain size of hominids has increased approximately threefold during the evolution of the hominids fromAustralopithecus toHomo sapiens. It is proposed that the principal reason for this increase is that larger brains conferred greater intelligence, and greater intelligence conferred a selection advantage. A number of anthropologists have difficulty accepting this thesis because they believe that brain size is not associated with intelligence in man. Evidence is reviewed, and new evidence from two studies is presented, to show that brain size as measured by head size is positively correlated with intelligence as measured by intelligence tests. On two recent samples statistically significant correlations of .21 and .30 were obtained between estimates of brain size and IQ. It is considered that brain size is positively associated with intelligence in man and that this is the major reason for the increase in brain size of the hominids during the last 3.2 million years.     

Studies of primate protein variation and evolution: Microelectrophoretic detection

Genetic variation at 16 protein and enzyme loci in Cercopithecus aethiops and several other primate species has been surveyed, using cellulose acetate microelectrophoresis. Resolution of several standard variant proteins is comparable to that achieved on starch gel or polyacrylamide gel. Although both intraspecific and interspecific variation was observed for some loci, the data generally support the concept that extracellular proteins are more likely to be polymorphic within a species, while intracellular proteins generally vary between species, if at all. These methodologies are particularly appropriate for screening multiple-locus variation in large numbers of samples; their relevance to studies of molecular evolution and evaluation of theories of kin selection is discussed.This research was supported in part by California State Agricultural Experiment Station Funds to the University of California, Berkeley, and the Wenner Gren Foundation.     

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.     

Built to last: The structure,function, and evolution of primate dental enamel

The teeth of every primate, living and extinct, are covered by a hard, durable layer of enamel. This is not unique: Almost all mammals have enamel-covered teeth. In addition, all of the variations in enamel structure that occur in primates are also found in other groups of mammals. Nevertheless, the very complexity of enamel and the variation we see in it on the teeth of living and fossil primates raise questions about its evolutionary significance. Is the complex structure of primate enamel adaptive? What, if anything, does enamel structure tell us about primate phylogeny? To answer these questions, we need to look more closely at the characteristics of prismatic enamel in primates and at the distribution of those characteristics, both in relation to our knowledge of primate dental function and feeding ecology and from a phylogenetic perspective.     

Middle Eocene primate tarsals from China: implications for haplorhine evolution

We describe tarsal remains of primates recovered from the Middle Eocene (approximately 45 mya) Shanghuang fissures in southern Jiangsu Province, China. These tarsals document the existence of four higher-level taxa of haplorhine primates and at least two adapid species. The meager and poorly preserved adapid material exhibits some similarities to European adapines like Adapis. The haplorhine primates are divided into two major groups: a "prosimian group" consisting of Tarsiidae and an unnamed group that is anatomically similar to Omomyidae; and an "anthropoid group" consisting of Eosimiidae and an unnamed group of protoanthropoids. The anthropoid tarsals are morphologically transitional between omomyids (or primitive haplorhines) and extant telanthropoids, providing the first postcranial evidence for primates which bridge the prosimian-anthropoid gap. All of the haplorhines are extremely small (most are between 50-100 g), and the deposits contain the smallest euprimates ever documented. The uniqueness of this fauna is further highlighted by the fact that no modern primate community contains as many tiny primates as does the fauna from Shanghuang.     

Leopard predation and primate evolution

Although predation is an important driving force of natural selection its effects on primate evolution are still not well understood, mainly because little is known about the hunting behaviour of the primates' various predators. Here, we present data on the hunting behaviour of the leopard (Panthera pardus), a major primate predator in the Tai; forest of Ivory Coast and elsewhere. Radio-tracking data showed that forest leopards primarily hunt for monkeys on the ground during the day. Faecal analyses confirmed that primates accounted for a large proportion of the leopards' diet and revealed in detail the predation pressure exerted on the eight different monkey and one chimpanzee species. We related the species-specific predation rates to various morphological, behavioural and demographic traits that are usually considered adaptations to predation (body size, group size, group composition, reproductive behaviour, and use of forest strata). Leopard predation was most reliably associated with density, suggesting that leopards hunt primates according to abundance. Contrary to predictions, leopard predation rates were not negatively, but positively, related to body size, group size and the number of males per group, suggesting that predation by leopards did not drive the evolution of these traits in the predicted way. We discuss these findings in light of some recent experimental data and suggest that the principal effect of leopard predation has been on primates' cognitive evolution.     

Ecology dictates the value of memory for foraging bees

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The nature and evolution of intelligence in orangutans (Pongo pygmaeus)

Orangutans share many intellectual qualities with African great apes and humans, likely because of their recent common ancestry. They may also show unique intellectual adaptations because of their long evolutionary divergence from the African lineage. This paper assesses orangutan intelligence in light of this evolutionary history. Evidence derives from observations of juvenile ex-captive orangutans reintroduced to free forest life by the Wanariset Orangutan Reintroduction Project, East Kalimantan, Indonesia. The intellectual qualities shared by great apes and humans point to a distinct “great ape” intelligence with hierarchization as a pivotal cognitive mechanism. Evolutionary reconstructions jibe with this view and suggest that technically difficult foods may have been key selection pressures. Orangutans should then show hierarchical intelligence when obtaining difficult foods. Evidence on ex-captive orangutans' techniques for processing difficult foods concurs. Intellectual qualities distinct to orangutans may owe to arboreal travel pressures; in particular arboreality may aggravate foraging problems. Evidence confirms that ex-captive orangutans' techniques for accessing difficult foods located arboreally are intellectually complex—i.e. they show hierarchization. These findings suggest other factors probably important to understanding great ape and orangutan forms of intelligence and their evolutionary origins.     

Genetics and the evolution of primate enamel thickness: a baboon model

The thickness of mammalian tooth enamel plays a prominent role in paleontology because it correlates with diet, and thicker enamel protects against tooth breakage and wear. Hominid evolutionary studies have stressed the importance of this character for over 30 years, from the identification of "Ramapithecus" as an early Miocene hominid, to the recent discovery that the earliest hominids display molar enamel intermediate in thickness between extant chimpanzees and Australopithecus. Enamel thickness remains largely unexplored for nonhominoid primate fossils, though there is significant variation across modern species. Despite the importance of enamel thickness variation to primate evolution, the mechanisms underlying variation in this trait have not yet been elucidated. We report here on the first quantitative genetic analysis of primate enamel thickness, an analysis based on 506 pedigreed baboons from a captive breeding colony. Computed tomography analysis of 44 Papio mandibular molars shows a zone of sufficiently uniform enamel thickness on the lateral surface of the protoconid. With this knowledge, we developed a caliper metric measurement protocol for use on baboon molars worn to within this zone, enabling the collection of a data set large enough for genetic analyses. Quantitative genetic analyses show that a significant portion of the phenotypic variance in enamel thickness is due to the additive effects of genes and is independent of sex and tooth size. Our models predict that enamel thickness could rapidly track dietary adaptive shifts through geological time, thus increasing the potential for homoplasy in this character. These results have implications for analyses of hominoid enamel thickness variation, and provide a foundation from which to explore the evolution of this phenotype in the papionin fossil record.     

New views on primate origins

Most primates live in trees, and many of them have strikingly human-like hands and faces. Scientists who study primate evolution agree that these two facts must be connected in some way. The details, however, are a matter of debate. Early theories explained the human-like peculiarities of primates simply as arboreal adaptations. More recent accounts have traced the origins of these peculiarities to more specific ways of arboreal life, involving leaping locomotion, shrub-layer foraging, visually guided predation on insects, or fruit-eating.     

The influence of developmental environment on the evolution of olfactory foraging behaviour in procellariiform seabirds

The evolutionary origins of foraging behaviour by procellariiform seabirds (petrels, albatrosses and shearwaters) are poorly understood. Moreover, proximate factors affecting foraging ecology, such as the influence of environment on the development of sensory systems, have yet to be addressed. Here, we apply comparative methods based on current procellariiform phylogenies to identify associations between sensory modalities and the developmental environment that may underlie the evolution of complex foraging behaviour. We postulate that, for burrow-nesting species, smell is likely to dominate the sensory world of the developing chick. Alternatively, for ground-nesting species, chicks receive exposure to a range of visual, auditory and olfactory cues. We employ maximum likelihood to test models of correlated trait evolution between nesting habit and olfactory foraging style and to reconstruct the ancestral states of these characters when coded as binary states. Our results suggest that nesting behaviour has evolved in conjunction with foraging style. Based on this analysis, we propose that nesting on the surface was a life-history innovation that opened up a new developmental environment with profound effects on the foraging ecology of procellariiform seabirds.     

Correlated evolution of herbivory and food chemical discrimination in iguanian and ambush foraging lizards

To efficiently locate and assess foods, animal sensory capacitiesand behavioral discriminations based on them must be appropriatefor the diet and method of hunting. In lizards, actively foraginginsectivores identify animal prey using lingually sampled chemicalcues, but ambush foragers do not. Among plant eaters derivedfrom active foragers, plant chemical discrimination is addedto prey chemical discrimination, resulting in correlated evolutionof plant diet and plant chemical discrimination. Here I presentcomparative evidence on the relationships between plant dietand food chemical discrimination in Iguania, which consistsprimarily of ambush foragers and is one of two major lizardclades, and for ambushing lizards in general. Comparative analysesconducted using phylogenetic methods show that (1) all but onespecies of omnivore studied exhibited both prey and plant chemicaldiscrimination, whereas ambush foragers exhibited neither; (2)significant correlated evolution occurred between plant dietand plant chemical discrimination in Iguania and in omnivoresand herbivores derived from ambush foragers; and (3) correlatedevolution has occurred between prey and plant chemical discriminationin Iguania and, more generally, in taxa derived from ambushforagers. These results are explained by selection on planteaters to assess the nutritional value and possible toxicityof plants and by continued consumption of some animal prey evenin herbivores combined with freedom from factors that selectagainst prey chemical discrimination in ambush foragers.