Social learning of a communicative signal in captive chimpanzees

The acquisition of linguistic competency from more experienced social partners is a fundamental aspect of human language. However, there is little evidence that non-human primates learn to use their vocalizations from social partners. Captive chimpanzees (Pan troglodytes) produce idiosyncratic vocal signals that are used intentionally to capture the attention of a human experimenter. Interestingly, not all apes produce these sounds, and it is unclear what factors explain this difference. We tested the hypothesis that these attention-getting (AG) sounds are socially learned via transmission between mothers and their offspring. We assessed 158 chimpanzees to determine if they produced AG sounds. A significant association was found between mother and offspring sound production. This association was attributable to individuals who were raised by their biological mother-as opposed to those raised by humans in a nursery environment. These data support the hypothesis that social learning plays a role in the acquisition and use of communicative vocal signals in chimpanzees.     

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.     

A word in the hand: action, gesture and mental representation in humans and non-human primates

The movements we make with our hands both reflect our mental processes and help to shape them. Our actions and gestures can affect our mental representations of actions and objects. In this paper, we explore the relationship between action, gesture and thought in both humans and non-human primates and discuss its role in the evolution of language. Human gesture (specifically representational gesture) may provide a unique link between action and mental representation. It is kinaesthetically close to action and is, at the same time, symbolic. Non-human primates use gesture frequently to communicate, and do so flexibly. However, their gestures mainly resemble incomplete actions and lack the representational elements that characterize much of human gesture. Differences in the mirror neuron system provide a potential explanation for non-human primates' lack of representational gestures; the monkey mirror system does not respond to representational gestures, while the human system does. In humans, gesture grounds mental representation in action, but there is no evidence for this link in other primates. We argue that gesture played an important role in the transition to symbolic thought and language in human evolution, following a cognitive leap that allowed gesture to incorporate representational elements.     

Fever from the forest: prospects for the continued emergence of sylvatic dengue virus and its impact on public health

The four dengue virus (DENV) serotypes that circulate among humans emerged independently from ancestral sylvatic progenitors that were present in non-human primates, following the establishment of human populations that were large and dense enough to support continuous inter-human transmission by mosquitoes. This ancestral sylvatic-DENV transmission cycle still exists and is maintained in non-human primates and Aedes mosquitoes in the forests of Southeast Asia and West Africa. Here, we provide an overview of the ecology and molecular evolution of sylvatic DENV and its potential for adaptation to human transmission. We also emphasize how the study of sylvatic DENV will improve our ability to understand, predict and, ideally, avert further DENV emergence.     

Cross-species transmission of CWD prions

Prions cause fatal neurodegenerative diseases in humans and animals and can be transmitted zoonotically. Chronic wasting disease (CWD) is a highly transmissible prion disease of wild deer and elk that affects cervids over extensive regions of the United States and Canada. The risk of cross-species CWD transmission has been experimentally evaluated in a wide array of mammals, including non-human primates and mouse models expressing human cellular prion protein. Here we review the determinants of cross-species CWD transmission, and propose a model that may explain a structural barrier for CWD transmission to humans.     

Economic behaviours among non-human primates

Do we have any valid reasons to affirm that non-human primates display economic behaviour in a sufficiently rich and precise sense of the phrase? To address this question, we have to develop a set of criteria to assess the vast array of experimental studies and field observations on individual cognitive and behavioural competences as well as the collective organization of non-human primates. We review a sample of these studies and assess how they answer to the following four main challenges. (i) Do we see any economic organization or institutions emerge among groups of non-human primates? (ii) Are the cognitive abilities, and often biases, that have been evidenced as underlying typical economic decision-making among humans, also present among non-human primates? (iii) Can we draw positive lessons from performance comparisons among primate species, humans and non-humans but also across non-human primate species, as elicited by canonical game-theoretical experimental paradigms, especially as far as economic cooperation and coordination are concerned? And (iv) in which way should we improve models and paradigms to obtain more ecological data and conclusions? Articles discussed in this paper most often bring about positive answers and promising perspectives to support the existence and prevalence of economic behaviours among non-human primates.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Introduction: integrating genetic and cultural evolutionary approaches to language

The papers in this special issue of Human Biology address recent research in the field of language evolution, both the genetic evolution of the language faculty and the cultural evolution of specific languages. While both of these areas have received increasing interest in recent years, there is also a need to integrate these somewhat separate efforts and explore the relevant gene-culture coevolutionary interactions. Here we summarize the individual contributions, set them in the context of the wider literature, and identify outstanding future research questions. The first set of papers concerns the comparative study of nonhuman communication in primates and birds from both a behavioral and neurobiological perspective, revealing evidence for several common language-related traits in various nonhuman species and providing clues as to the evolutionary origin and function of the human language faculty. The second set of papers discusses the consequences of viewing language as a culturally evolving system in its own right, including claims that this removes the need for strong genetic biases for language acquisition, and that phylogenetic evolutionary methods can be used to reconstruct language histories. We conclude by highlighting outstanding areas for future research, including identifying the precise selection pressures that gave rise to the language faculty in ancestral hominin species, and determining the strength, domain specificity, and origin of the cultural transmission biases that shape languages as they pass along successive generations of language learners.     

Evolution of modern humans: evidence from nuclear DNA polymorphisms.

Previously we have described studies of the evolution of modern humans based upon data for classical genetic markers and for nuclear DNA polymorphisms. Such polymorphisms provide a different point of view regarding human evolution than do mitochondrial DNA sequences. Here we compare revised dates for major migrations of anatomically modern humans, estimated from archaeological data, with separations suggested by a genetic tree constructed from classical marker allele frequencies. Analyses of DNA polymorphisms have now been extended and compared with those of classical markers; genetic trees continue to support the hypothesis of an initial African and non-African divergence for modern humans. We have also begun testing non-human primates for a set of human DNA polymorphisms. For most polymorphisms tested so far, humans share a single allele with other primates; such shared alleles are likely to be ancestral. Populations living in humid tropical environments have significantly higher frequencies of ancestral alleles than do other populations, supporting the hypothesis that natural selection acts to maintain high frequencies of particular alleles in some environments.     

The sound of one-hand clapping: handedness and perisylvian neural correlates of a communicative gesture in chimpanzees

Whether lateralization of communicative signalling in non-human primates might constitute prerequisites of hemispheric specialization for language is unclear. In the present study, we examined (i) hand preference for a communicative gesture (clapping in 94 captive chimpanzees from two research facilities) and (ii) the in vivo magnetic resonance imaging brain scans of 40 of these individuals. The preferred hand for clapping was defined as the one in the upper position when the two hands came together. Using computer manual tracing of regions of interest, we measured the neuroanatomical asymmetries for the homologues of key language areas, including the inferior frontal gyrus (IFG) and planum temporale (PT). When considering the entire sample, there was a predominance of right-handedness for clapping and the distribution of right- and left-handed individuals did not differ between the two facilities. The direction of hand preference (right- versus left-handed subjects) for clapping explained a significant portion of variability in asymmetries of the PT and IFG. The results are consistent with the view that gestural communication in the common ancestor may have been a precursor of language and its cerebral substrates in modern humans.     

Modeling Coevolution between Language and Memory Capacity during Language Origin

Memory is essential to many cognitive tasks including language. Apart from empirical studies of memory effects on language acquisition and use, there lack sufficient evolutionary explorations on whether a high level of memory capacity is prerequisite for language and whether language origin could influence memory capacity. In line with evolutionary theories that natural selection refined language-related cognitive abilities, we advocated a coevolution scenario between language and memory capacity, which incorporated the genetic transmission of individual memory capacity, cultural transmission of idiolects, and natural and cultural selections on individual reproduction and language teaching. To illustrate the coevolution dynamics, we adopted a multi-agent computational model simulating the emergence of lexical items and simple syntax through iterated communications. Simulations showed that: along with the origin of a communal language, an initially-low memory capacity for acquired linguistic knowledge was boosted; and such coherent increase in linguistic understandability and memory capacities reflected a language-memory coevolution; and such coevolution stopped till memory capacities became sufficient for language communications. Statistical analyses revealed that the coevolution was realized mainly by natural selection based on individual communicative success in cultural transmissions. This work elaborated the biology-culture parallelism of language evolution, demonstrated the driving force of culturally-constituted factors for natural selection of individual cognitive abilities, and suggested that the degree difference in language-related cognitive abilities between humans and nonhuman animals could result from a coevolution with language.     

Rhesus monkeys correctly read the goal-relevant gestures of a human agent

When humans point, they reveal to others their underlying intent to communicate about some distant goal. A controversy has recently emerged based on a broad set of comparative and phylogenetically relevant data. In particular, whereas chimpanzees (Pan troglodytes) have difficulty in using human-generated communicative gestures and actions such as pointing and placing symbolic markers to find hidden rewards, domesticated dogs (Canis familiaris) and silver foxes (Urocyon cinereoargenteus) readily use such gestures and markers. These comparative data have led to the hypothesis that the capacity to infer communicative intent in dogs and foxes has evolved as a result of human domestication. Though this hypothesis has met with challenges, due in part to studies of non-domesticated, non-primate animals, there remains the fundamental question of why our closest living relatives, the chimpanzees, together with other non-human primates, generally fail to make inferences about a target goal of an agent's communicative intent. Here, we add an important wrinkle to this phylogenetic pattern by showing that free-ranging rhesus monkeys (Macaca mulatta) draw correct inferences about the goals of a human agent, using a suite of communicative gestures to locate previously concealed food. Though domestication and human enculturation may play a significant role in tuning up the capacity to infer intentions from communicative gestures, these factors are not necessary.     

Words as alleles: connecting language evolution with Bayesian learners to models of genetic drift

Scientists studying how languages change over time often make an analogy between biological and cultural evolution, with words or grammars behaving like traits subject to natural selection. Recent work has exploited this analogy by using models of biological evolution to explain the properties of languages and other cultural artefacts. However, the mechanisms of biological and cultural evolution are very different: biological traits are passed between generations by genes, while languages and concepts are transmitted through learning. Here we show that these different mechanisms can have the same results, demonstrating that the transmission of frequency distributions over variants of linguistic forms by Bayesian learners is equivalent to the Wright–Fisher model of genetic drift. This simple learning mechanism thus provides a justification for the use of models of genetic drift in studying language evolution. In addition to providing an explicit connection between biological and cultural evolution, this allows us to define a ‘neutral’ model that indicates how languages can change in the absence of selection at the level of linguistic variants. We demonstrate that this neutral model can account for three phenomena: the s-shaped curve of language change, the distribution of word frequencies, and the relationship between word frequencies and extinction rates.     

Genomic signatures of diet-related shifts during human origins

There are numerous anthropological analyses concerning the importance of diet during human evolution. Diet is thought to have had a profound influence on the human phenotype, and dietary differences have been hypothesized to contribute to the dramatic morphological changes seen in modern humans as compared with non-human primates. Here, we attempt to integrate the results of new genomic studies within this well-developed anthropological context. We then review the current evidence for adaptation related to diet, both at the level of sequence changes and gene expression. Finally, we propose some ways in which new technologies can help identify specific genomic adaptations that have resulted in metabolic and morphological differences between humans and non-human primates.     

Failure to detect simian immunodeficiency virus infection in a large Cameroonian cohort with high non-human primate exposure

Hunting and butchering of wildlife in Central Africa are known risk factors for a variety of human diseases, including HIV/AIDS. Due to the high incidence of human exposure to body fluids of non-human primates, the significant prevalence of simian immunodeficiency virus (SIV) in non-human primates, and hunting/butchering associated cross-species transmission of other retroviruses in Central Africa, it is possible that SIV is actively transmitted to humans from primate species other than mangabeys, chimpanzees, and/or gorillas. We evaluated SIV transmission to humans by screening 2,436 individuals that hunt and butcher non-human primates, a population in which simian foamy virus and simian T-lymphotropic virus were previously detected. We identified 23 individuals with high seroreactivity to SIV. Nucleic acid sequences of SIV genes could not be detected, suggesting that SIV infection in humans could occur at a lower frequency than infections with other retroviruses, including simian foamy virus and simian T-lymphotropic virus. Additional studies on human populations at risk for non-human primate zoonosis are necessary to determine whether these results are due to viral/host characteristics or are indicative of low SIV prevalence in primate species consumed as bushmeat as compared to other retroviruses in Cameroon.     

Rank and relationships in the evolution of spoken language

If evolutionary benefits associated with language were predominantly referential, as many theorists assume, then there must have been a preparatory stage in which an 'appetite' for information, not evident in the other primates, developed. To date, no such stage has been demonstrated. The problem dissipates, however, if it is assumed that language emerged from a function more nearly shared with other primates. An obvious candidate is displaying. Here I argue that performative functions associated with oral sound-making provided initial pressures for vocal communication by promoting rank and relationships. These benefits, I suggest, facilitated conflict avoidance and resolution, collaboration, and reciprocal sharing of needed resources. By valuing the performative applications of language, which continue in modern humans, one can more easily derive speech from the social-vocal behaviours of non-human primates, providing greater continuity in accounts of linguistic evolution     

Self domestication and the evolution of language

We set out an account of how self-domestication plays a crucial role in the evolution of language. In doing so, we focus on the growing body of work that treats language structure as emerging from the process of cultural transmission. We argue that a full recognition of the importance of cultural transmission fundamentally changes the kind of questions we should be asking regarding the biological basis of language structure. If we think of language structure as reflecting an accumulated set of changes in our genome, then we might ask something like, “What are the genetic bases of language structure and why were they selected?” However, if cultural evolution can account for language structure, then this question no longer applies. Instead, we face the task of accounting for the origin of the traits that enabled that process of structure-creating cultural evolution to get started in the first place. In light of work on cultural evolution, then, the new question for biological evolution becomes, “How did those precursor traits evolve?” We identify two key precursor traits: (1) the transmission of the communication system through learning; and (2) the ability to infer the communicative intent associated with a signal or action. We then describe two comparative case studies—the Bengalese finch and the domestic dog—in which parallel traits can be seen emerging following domestication. Finally, we turn to the role of domestication in human evolution. We argue that the cultural evolution of language structure has its origin in an earlier process of self-domestication.     

A parasite-driven wedge: infectious diseases may explain language and other biodiversity

Parasite–host coevolutionary races are spatially variable across species' or human cultural ranges. Assortative sociality, biased toward local conspecifics, and limited dispersal (philopatry) in humans and other organisms can be adaptive through reduced contact with dangerous contagions harbored by distant/non-local conspecifics. These factors can generate cultural or population divergence. Thus, parasites are like a wedge driving groups apart through their effective creation of anticontagion behaviors. If this proposition is correct, then biological diversity should positively correlate with parasite diversity. Here we show that the worldwide distribution of indigenous human language diversity, a form of biodiversity, is strongly, positively related to human parasite diversity indicative of a legacy of parasite-mediated diversification. The significant pattern remains when potential confounds are removed. The pattern too is seen in each of the six world regions and is not confounded by regional differences in their history of colonization and conquest. We hypothesize that variation in limited dispersal and assortative sociality with conspecifics in response to the worldwide spatial variation in pathogen diversity provides a fundamental mechanism of population divergence explaining many important aspects of the geographic patterns of biodiversity. This hypothesis has broad implications for a diversity of research topics including language diversity, cultural evolution, speciation, phylogeny and biogeography.     

Two sources of meaning in infant communication: preceding action contexts and act-accompanying characteristics

How do infants communicate before they have acquired a language? This paper supports the hypothesis that infants possess social–cognitive skills that run deeper than language alone, enabling them to understand others and make themselves understood. I suggested that infants, like adults, use two sources of extralinguistic information to communicate meaningfully and react to and express communicative intentions appropriately. In support, a review of relevant experiments demonstrates, first, that infants use information from preceding shared activities to tailor their comprehension and production of communication. Second, a series of novel findings from our laboratory shows that in the absence of distinguishing information from preceding routines or activities, infants use accompanying characteristics (such as prosody and posture) that mark communicative intentions to extract and transmit meaning. Findings reveal that before infants begin to speak they communicate in meaningful ways by binding preceding and simultaneous multisensory information to a communicative act. These skills are not only a precursor to language, but also an outcome of social–cognitive development and social experience in the first year of life.