Communication and the primate brain: insights from neuroimaging studies in humans, chimpanzees and macaques

Considerable knowledge is available on the neural substrates for speech and language from brain-imaging studies in humans, but until recently there was a lack of data for comparison from other animal species on the evolutionarily conserved brain regions that process species-specific communication signals. To obtain new insights into the relationship of the substrates for communication in primates, we compared the results from several neuroimaging studies in humans with those that have recently been obtained from macaque monkeys and chimpanzees. The recent work in humans challenges the longstanding notion of highly localized speech areas. As a result, the brain regions that have been identified in humans for speech and nonlinguistic voice processing show a striking general correspondence to how the brains of other primates analyze species-specific vocalizations or information in the voice, such as voice identity. The comparative neuroimaging work has begun to clarify evolutionary relationships in brain function, supporting the notion that the brain regions that process communication signals in the human brain arose from a precursor network of regions that is present in nonhuman primates and is used for processing species-specific vocalizations. We conclude by considering how the stage now seems to be set for comparative neurobiology to characterize the ancestral state of the network that evolved in humans to support language.     

On the Evolutionary Foundations of Language

New data on the cognitive capacities of other primates requires a reevaluation of our position on the nature of human language and the factors that led to its development. Pressures on the limited display system of the social primates may have made changes in the vocal tract anatomy of man associated with the development of upright posture of great selective importance. Human vocal tract anatomy may be at least as important as brain capacity in accounting for the origins of human language. An apparent upper age limit on efficient language acquisition in man leads to the "foreign accent" phenomenon. This may have been adoptively significant as a device which helped in the maintenance of a population structure in which rapid genetic change was possible. Embedding in language may represent a cognitive ability that is also reflected in the capacity for cultural variation, and may be extremely important in maintaining efficient population structure and in selecting for increasing intelligence.     

Infanticide and the evolution of pair bonds in nonhuman primates

Social relationships between adult males and females vary widely among mammals. In general, interactions between the sexes, particularly those of an affiliative nature, are associated with and, indeed, often limited to the period of copulation or female estrus.¹ Nevertheless, cohesive male-female bonds persist beyond estrus in some species, particularly nonhuman primates,² for reasons that remain largely obscure. Protection from male infanticide has been offered as a potential benefit to females of bonds with males in a variety of primates, including mountain gorillas and gibbons. Here I evaluate this hypothesis within a comparative framework that considers alternative costs and benefits of social relationships between the sexes.     

Concealing of facial expressions by a wild Barbary macaque (Macaca sylvanus)

Behavioural research on non-vocal communication among non-human primates and its possible links to the origin of human language is a long-standing research topic. Because human language is under voluntary control, it is of interest whether this is also true for any communicative signals of other species. It has been argued that the behaviour of hiding a facial expression with one’s hand supports the idea that gestures might be under more voluntary control than facial expressions among non-human primates, and it has also been interpreted as a sign of intentionality. So far, the behaviour has only been reported twice, for single gorilla and chimpanzee individuals, both in captivity. Here, we report the first observation of concealing of facial expressions by a monkey, a Barbary macaque (Macaca sylvanus), living in the wild. On eight separate occasions between 2009 and 2011 an adult male was filmed concealing two different facial expressions associated with play and aggression (“play face” and “scream face”), 22 times in total. The videos were analysed in detail, including gaze direction, hand usage, duration, and individuals present. This male was the only individual in his group to manifest this behaviour, which always occurred in the presence of a dominant male. Several possible interpretations of the function of the behaviour are discussed. The observations in this study indicate that the gestural communication and cognitive abilities of monkeys warrant more research attention.     

Grooming and group cohesion in primates: implications for the evolution of language

It is well established that allogrooming, which evolved for a hygienic function, has acquired an important derived social function in many primates. In particular, it has been postulated that grooming may play an essential role in group cohesion and that human language, as verbal grooming or gossip, evolved to maintain group cohesion in the hominin lineage with its unusually large group sizes. Here, we examine this group cohesion hypothesis and test it against the alternative grooming-need hypothesis which posits that rates of grooming are higher in species where grooming need (i.e. the motivation to groom for hygiene and its associated psychological reward) is more pronounced. This alternative predicts that the derived social function of grooming evolved mostly in those lineages that had the highest exposure to ectoparasites and dirt, i.e. terrestrial species. A detailed comparative analysis of 74 species of wild primates, controlling for phylogenetic non-independence, showed that terrestriality was a highly significant predictor of allogrooming time, consistent with the prediction. The predictions of the group cohesion hypothesis were not supported, however. Group size did not predict grooming time across primates, nor did it do so in separate intra-population analyses in 17 species. Thus, there is no comparative support for the group-cohesion function of allogrooming, which questions the role of grooming in the evolution of human language.     

Replacement female house sparrows regularly commit infanticide: gaining time or signaling status?

Although the killing of unrelated young (usually designed asinfanticide) has been typically considered a male behavior,recent research has shown that females may commit infanticideeven more frequently than do males. In rodents and primates,female infanticide represents a strategy associated to competitionfor resources or infant exploitation, but little is known aboutthe causes and reproductive consequences of the killing of conspecificsby females in other vertebrates. In the present article, I focuson infanticide committed by females that replace mates of territorialmales in a population of the house sparrow. I show that (1)replacement females regularly committed infanticide, (2) experiencedfemales committed infanticide more frequently than did novelfemales and tended to select polygynous males to take over theirnests, and (3) laying date and reproductive success after aterritory takeover did not differ between infanticidal and noninfanticidalfemales. These results seem to indicate that infanticide hasnot evolved in females because of the short-term reproductivebenefits it accrues to the perpetrator. I suggest that the killingof unrelated young by females relates to dominance status amongpotential female breeders and that this behavior benefits theperpetrators in terms of mate selection.     

The function and mechanism of vocal accommodation in humans and other primates

The study of non‐human animals, in particular primates, can provide essential insights into language evolution. A critical element of language is vocal production learning, i.e. learning how to produce calls. In contrast to other lineages such as songbirds, vocal production learning of completely new signals is strikingly rare in non‐human primates. An increasing body of research, however, suggests that various species of non‐human primates engage in vocal accommodation and adjust the structure of their calls in response to environmental noise or conspecific vocalizations. To date it is unclear what role vocal accommodation may have played in language evolution, in particular because it summarizes a variety of heterogeneous phenomena which are potentially achieved by different mechanisms. In contrast to non‐human primates, accommodation research in humans has a long tradition in psychology and linguistics. Based on theoretical models from these research traditions, we provide a new framework which allows comparing instances of accommodation across species, and studying them according to their underlying mechanism and ultimate biological function. We found that at the mechanistic level, many cases of accommodation can be explained with an automatic perception–production link, but some instances arguably require higher levels of vocal control. Functionally, both human and non‐human primates use social accommodation to signal social closeness or social distance to a partner or social group. Together, this indicates that not only some vocal control, but also the communicative function of vocal accommodation to signal social closeness and distance must have evolved prior to the emergence of language, rather than being the result of it. Vocal accommodation as found in other primates has thus endowed our ancestors with pre‐adaptations that may have paved the way for language evolution.     

Combinatorial Communication in Bacteria: Implications for the Origins of Linguistic Generativity

Combinatorial communication, in which two signals are used together to achieve an effect that is different to the sum of the effects of the component parts, is apparently rare in nature: it is ubiquitous in human language, appears to exist in a simple form in some non-human primates, but has not been demonstrated in other species. This observed distribution has led to the pair of related suggestions, that (i) these differences in the complexity of observed communication systems reflect cognitive differences between species; and (ii) that the combinations we see in non-human primates may be evolutionary pre-cursors of human language. Here we replicate the landmark experiments on combinatorial communication in non-human primates, but in an entirely different species, unrelated to humans, and with no higher cognition: the bacterium Pseudomonas aeruginosa. Using the same general methods as the primate studies, we find the same general pattern of results: the effect of the combined signal differs from the composite effect of the two individual signals. This suggests that advanced cognitive abilities and large brains do not necessarily explain why some species have combinatorial communication systems and others do not. We thus argue that it is premature to conclude that the systems observed in non-human primates are evolutionarily related to language. Our results illustrate the value of an extremely broad approach to comparative research.     

Increased breathing control: Another factor in the evolution of human language

Investigation into the evolution of human language has involved evidence of many different kinds and approaches from many different disciplines. For full modern language, humans must have evolved a range of physical abilities for the production of our complex speech sounds, as well as sophisticated cognitive abilities. Human speech involves free‐flowing, intricately varied, rapid sound sequences suitable for the fast transfer of complex, highly flexible communication. Some aspects of human speech, such as our ability to manipulate the vocal tract to produce a wide range of different types of sounds that form vowels and consonants, have attracted considerable attention from those interested in the evolution of language. 1 , 2 However, one very important contributory skill, the human ability to attain very fine control of breathing during speech, has been neglected. Here we present evidence of the importance of breathing control to human speech, as well as evidence that our capabilities greatly exceed those of nonhuman primates. Human speech breathing demands fine neurological control of the respiratory muscles, integrated with cognitive processes and other factors. Evidence from comparison of the vertebral canals of fossil hominids and those of extant primates suggests that a major increase in thoracic innervation evolved in later hominid evolution, providing enhanced breathing control. If that is so, then earlier hominids would have had quite restricted speech patterns, whereas more recent hominids, with human‐like breath control abilities, would have been capable of faster, more varied speech sequences.     

Sleep intensity and the evolution of human cognition

Over the past four decades, scientists have made substantial progress in understanding the evolution of sleep patterns across the Tree of Life. 1 , 2 Remarkably, the specifics of sleep along the human lineage have been slow to emerge. This is surprising, given our unique mental and behavioral capacity and the importance of sleep for individual cognitive performance. 3 - 5 One view is that our species' sleep architecture is in accord with patterns documented in other mammals. 6 We promote an alternative view, that human sleep is highly derived relative to that of other primates. Based on new and existing evidence, we specifically propose that humans are more efficient in their sleep patterns than are other primates, and that human sleep is shorter, deeper, and exhibits a higher proportion of REM than expected. Thus, we propose the sleep intensity hypothesis: Early humans experienced selective pressure to fulfill sleep needs in the shortest time possible. Several factors likely served as selective pressures for more efficient sleep, including increased predation risk in terrestrial environments, threats from intergroup conflict, and benefits arising from increased social interaction. Less sleep would enable longer active periods in which to acquire and transmit new skills and knowledge, while deeper sleep may be critical for the consolidation of those skills, leading to enhanced cognitive abilities in early humans.     

Two organizing principles of vocal production: Implications for nonhuman and human primates

Vocal communication in nonhuman primates receives considerable research attention, with many investigators arguing for similarities between this calling and speech in humans. Data from development and neural organization show a central role of affect in monkey and ape sounds, however, suggesting that their calls are homologous to spontaneous human emotional vocalizations while having little relation to spoken language. Based on this evidence, we propose two principles that can be useful in evaluating the many and disparate empirical findings that bear on the nature of vocal production in nonhuman and human primates. One principle distinguishes production-first from reception-first vocal development, referring to the markedly different role of auditory-motor experience in each case. The second highlights a phenomenon dubbed dual neural pathways, specifically that when a species with an existing vocal system evolves a new functionally distinct vocalization capability, it occurs through emergence of a second parallel neural pathway rather than through expansion of the extant circuitry. With these principles as a backdrop, we review evidence of acoustic modification of calling associated with background noise, conditioning effects, audience composition, and vocal convergence and divergence in nonhuman primates. Although each kind of evidence has been interpreted to show flexible cognitively mediated control over vocal production, we suggest that most are more consistent with affectively grounded mechanisms. The lone exception is production of simple, novel sounds in great apes, which is argued to reveal at least some degree of volitional vocal control. If also present in early hominins, the cortically based circuitry surmised to be associated with these rudimentary capabilities likely also provided the substrate for later emergence of the neural pathway allowing volitional production in modern humans.     

Origins,Diversity and Relationships of Lemurs

I review new evidence on origins and adaptive radiation of Malagasy lemurs, a remarkably diverse group containing 13% of living primate species. The number of recognized lemur species has increased significantly, partly due to research revealing specific subdivisions within known populations but mainly because of discovery of new populations through fieldwork. Some species feared to be extinct have also been rediscovered. Specific numbers have increased particularly in small-bodied, cryptic genera for which continued research will surely reveal even more species.Adaptative radiation of lemurs has been essentially confined to Madagascar. The high density of lemur species on that island, associated with very small geographical ranges, has major implications both for their evolutionary divergence and for conservation. Reconstructions of phylogenetic relationships among primates have been considerably enhanced by DNA sequence data. Sufficient data are now available from both nuclear and mitochondrial sequences to examine relationships among and within the major groups of living primates. Most studies have confirmed that lemurs constitute a monophyletic sister-group of the lorisiform clade and all exclude a specific relationship between cheirogaleids and lorisiforms repeatedly inferred from morphological evidence. However, some analyses indicate that the aye-aye may have branched away before the divergence between other lemurs and lorisiforms. DNA sequence analyses have also yielded a broad consensus for relationships between Eulemur, Hapalemur, Lemur and Varecia: Varecia branched away first, while Lemur is more closely related to Hapalemur than to Eulemur. As debate about phylogenetic relationships among lemurs and other primates seems to have been settled in favor of lemur monophyly (possibly excluding the aye-aye), only a single invasion of Madagascar is required; but it must still be explained how ancestral lemurs could have migrated there at an appropriate time. Separation between Madagascar and Africa was apparently complete by about 120 Ma, too far in the past for direct overland migration. A recent hypothesis suggested that uplifted land in the Mozambique Channel assisted colonization of Madagascar 26-45 Ma, seemingly agreeing with an estimated date of about 40 Ma for divergence of lemurs from other primates. However, mounting evidence suggests that divergence occurred significantly earlier. Because the earliest known fossil representatives of several modern orders of placental mammals (including primates) are dated no earlier than the early Tertiary, it is widely accepted that their divergence took place after the Cretaceous/Tertiary mass extinction. Yet the known fossil record can only yield minimum divergence times; if sampling is poor and/or biased there may be a considerable discrepancy between minimum and actual dates. There is, for example, virtually no known fossil record for lemurs in Madagascar and the earliest known representatives are subfossil lemurs, so in this case a direct reading of the fossil record would indicate that the lemurs first originated just a few thousand years ago! Examination of underestimation of times of origin because of poor sampling in the fossil record has confirmed previous suggestions that primates originated considerably earlier than generally believed. Several recent phylogenetic reconstructions based on DNA sequence data and using calibration dates derived from groups other than primates provide independent support for this inference. Overall, it now seems that primates originated at around 90 Ma rather than the 55 Ma indicated by direct reading of the known fossil record. Hence, colonization of Madagascar by lemurs would have taken place at about 80 Ma, double the date usually accepted, and should be interpreted in terms of contemporary continental relationships.     

The Development of Primate Raiding: Implications for Management and Conservation

Ecosystems and habitats are fast becoming human dominated, which means that more species, including primates, are compelled to exploit new human resources to survive and compete. Primate “pests” pose major management and conservation challenges. I here present the results from a unique opportunity to document how well-known individuals and groups respond to the new opportunity to feed on human foods. Data are from a long-term study of a single population in Kenya at Kekopey, near Gilgil, Kenya. Some of the naïve research baboons became raiders while others did not. I compare diet, activity budgets, and home range use of raiders and nonraiders both simultaneously, after the incursion of agriculture, and historically compared to the period before agriculture appeared. I present measures of the relative benefits (female reproduction) and costs (injuries, mortality, and survivorship) of incorporating human food into the diet and discuss why the baboons raid and their variations in raiding tendencies. Guarding and chasing are evaluated as control techniques. I also suggest conflict mitigation strategies by identifying the most likely options in different contexts. I end with a proposal for a rapid field assessment of human wildlife conflict involving primates.     

Left-hand Preference for a Complex Manual Task in a Population of Wild Siamangs (<Emphasis Type="BoldItalic">Symphalangus syndactylus</Emphasis>)

Many hypotheses have been proposed linking the emergence of lateralized activities—such as handedness—in primates, with hemispheric specialization and the evolution of complex communication such as human language. Although data to test these ideas are rapidly accumulating for many primate taxa, some species are still largely unexplored, especially under natural conditions. I present the first data on a population of wild siamangs (Symphalangus syndactylus), highly arboreal small apes. Preference for the left hand is shown both at the individual and population levels for a complex manual task: collecting and drinking water from tree holes. There was no difference in hand preference between males and females, and immature individuals showed more variable patterns than adults. These results are consistent with the postural origins theory, allow a new interpretation of the findings of comparable studies, and indicate a useful behavior for future investigations of laterality in wild primates.     

Textual self‐authorization

This article examines some of the pragmatic strategies by which certain texts render themselves and are rendered so authoritative as to legitimate representations of reality and the stolidity of the reality that lies behind them. My primary focus is on what I call indexical dramas (i.e. the pragmatic and meta‐pragmatic play) that support such self‐arrogating texts, particularly Scripture, as read by American Fundamentalists, and, to a lesser extent, the American Declaration of Independence and the United States Constitution. I argue that performatives and their uptake, including self‐arrogation, are dramatic events and that the attention given to their denouement – the performative utterance itself — masks the complex, at times contradictory, play of indexicals that constitute, or at least highlight, the very felicity conditions on which their success depends. In other words, the fragility of performatives is deflected by their denouement. Some of the defensive strategies that mask the fragility of textual self‐arrogation are: the establishment of the authority of the author of the performative; legitimation of sources of textual cohesiveness and hermeneutic practices; citationalism; its temporality; and perlocutionary effacement – the forgetting or ignoring, except in moments of crisis, of the fragility of performative acts and their uptake. I ask whether that forgetting enhances the illocutionary force of the target text over its history. I further suggest that Fundamentalists’ insistence on making their lives as biblical as possible gives performative force to their reading of Scripture.     

Social intelligence in the spotted hyena (Crocuta crocuta)

If the large brains and great intelligence characteristic of primates were favoured by selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in non-primate mammals living in large, elaborate societies in which social dexterity enhances individual fitness. The societies of spotted hyenas are remarkably like those of cercopithecine primates with respect to size, structure and patterns of competition and cooperation. These similarities set an ideal stage for comparative analysis of social intelligence and nervous system organization. As in cercopithecine primates, spotted hyenas use multiple sensory modalities to recognize their kin and other conspecifics as individuals, they recognize third-party kin and rank relationships among their clan mates, and they use this knowledge adaptively during social decision making. However, hyenas appear to rely more intensively than primates on social facilitation and simple rules of thumb in social decision making. No evidence to date suggests that hyenas are capable of true imitation. Finally, it appears that the gross anatomy of the brain in spotted hyenas might resemble that in primates with respect to expansion of frontal cortex, presumed to be involved in the mediation of social behaviour.     

Mixed‐species Groups of Marmosets and Tamarins Across a Gradient of Agroforestry Intensification

Polyspecific associations are commonly observed in social animals, including primates, and have been interpreted as adaptations either to improve access to resources or to provide protection against predators. Mixed‐species associations between Wied's marmosets (Callithrix kuhlii) and golden‐headed lion tamarins (Leontopithecus chrysomelas) have been documented, and are unique among Atlantic forest primates. Both species are endemic to southern Bahia where part of the forest has been converted into cacao agroforests, which have been subjected to management intensification. Tree density and canopy connectivity decrease in more intensively managed agroforests, potentially increasing predation risk and the frequency of mixed‐species groups between these primates. Here, we test this hypothesis using a standardized, large spatial‐scale data set obtained from camera‐trapping in 30 sites across an agroforestry landscape mosaic. As expected, the frequency of mixed‐species groups increased in more intensively managed agroforests, but only relative to the total number of records of tamarins. Our results highlight that the benefits of mixed‐species groups can be asymmetrical among species and variable across the landscape. They corroborate that predation avoidance is an important advantage of mixed‐species groups in callitrichids, especially for conspicuous species living in smaller groups, such as the tamarin. Despite the importance of agroforests to conservation, our results indicate that management intensification can increase predation risk for species of conservation concern. To maintain the conservation value of agroforests, management practices should be planned to avoid any loss of canopy connectivity, taking into account the biodiversity vs. productivity trade‐off associated with shade management.     

Sexual Size Dimorphism,Canine Dimorphism,and Male-Male Competition in Primates

Sexual size dimorphism is generally associated with sexual selection via agonistic male competition in nonhuman primates. These primate models play an important role in understanding the origins and evolution of human behavior. Human size dimorphism is often hypothesized to be associated with high rates of male violence and polygyny. This raises the question of whether human dimorphism and patterns of male violence are inherited from a common ancestor with chimpanzees or are uniquely derived. Here I review patterns of, and causal models for, dimorphism in humans and other primates. While dimorphism in primates is associated with agonistic male mate competition, a variety of factors can affect male and female size, and thereby dimorphism. The causes of human sexual size dimorphism are uncertain, and could involve several non-mutually-exclusive mechanisms, such as mate competition, resource competition, intergroup violence, and female choice. A phylogenetic reconstruction of the evolution of dimorphism, including fossil hominins, indicates that the modern human condition is derived. This suggests that at least some behavioral similarities with Pan associated with dimorphism may have arisen independently, and not directly from a common ancestor.     

Theory and method in studies of vigilance and aggregation

Predation is considered one of the most important selective pressures on free-ranging animals. Our understanding of it derives mainly from studies of individual vigilance (visual scanning of the surroundings beyond the immediate vicinity) and aggregation in prey. Vigilance bears a direct relationship to aggregation, because animals in groups may rely on associates for early warning of danger. This review addresses the relationship between vigilance and aggregation with particular attention to the prediction that individual vigilance declines with increasing group size. Contrary to most other animals studied, primates do not support the prediction. Exploring this, I examined the assumptions underlying vigilance theory in the light of primate behaviour. First I tested whether manual harvesting and upright processing of food as seen among primates might permit them to feed and scan simultaneously. I found no support for this idea. Next I examined the targets of primate vigilance and found that one component (within-group vigilance) might explain the differences between primates and other animals. Finally, I evaluated whether individual primates in large groups face a lower risk of predation than those in small groups. A conclusion was impossible, but by separating group-level from individual-level risk, I was able to identify several common circumstances in which group size would not predict individual risk or vigilance. These circumstances arose for primates and nonprimates alike. I concluded that the relationship of vigilance to aggregation is not straightforward. The absence of a group-size effect on vigilance among primates is probably due to functional differences in vigilance behaviour or safety in groups, not to methodological differences. Furthermore, future work on animal vigilance and aggregation must fully consider both the targets of glances, and the assumption that larger groups are safer from predators. I predict that animals will not relax vigilance in larger groups if conspecific threat increases with group size. Group size will not predict individual risk of predation nor individual vigilance rates when predators do not rely on surprise, or when predators select a small subset of highly vulnerable group members. Copyright 2000 The Association for the Study of Animal Behaviour.     

Pain and stress during childbirth and time of day

Twenty-nine women were asked to rate the pain and stress of their labors within 48 hours of childbirth. Significantly lower ratings of both pain and stress were associated with labors in which the second stage started at night. It is suggested that as with other primates, there are factors that predispose humans to giving birth at night.