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.     

Cultural transmission and social control of human behavior

Humans have developed the capacity to approve or disapprove of the behavior of their children and of unrelated individuals. The ability to approve or disapprove transformed social learning into a system of cumulative cultural inheritance, because it increased the reliability of cultural transmission. Moreover, people can transmit their behavioral experiences (regarding what can and cannot be done) to their offspring, thereby avoiding the costs of a laborious, and sometimes dangerous, evaluation of different cultural alternatives. Our thesis is that, during ontogeny, the evaluative communication (approval/disapproval) between parents and offspring is substituted by other evaluative communications among peers, like individuals of the same generation. Each person belongs to a reference social group with individuals that interact more intensively. Humans have developed psychological mechanisms that enable cultural transmission by being receptive to parental advice as well as their reference social group. The selective pressure that promoted these new evaluative interactions arose to facilitate the establishment of efficient cooperative relationships. In short, the social control of behavior is essential to understand human cultural transmission.     

Social learning among Congo Basin hunter-gatherers

This paper explores childhood social learning among Aka and Bofi hunter-gatherers in Central Africa. Existing literature suggests that hunter-gatherer social learning is primarily vertical (parent-to-child) and that teaching is rare. We use behavioural observations, open-ended and semi-structured interviews, and informal and anecdotal observations to examine the modes (e.g. vertical versus horizontal/oblique) and processes (e.g. teaching versus observation and imitation) of cultural transmission. Cultural and demographic contexts of social learning associated with the modes and processes of cultural transmission are described. Hunter-gatherer social learning occurred early, was relatively rapid, primarily vertical under age 5 and oblique and horizontal between the ages of 6 and 12. Pedagogy and other forms of teaching existed as early as 12 months of age, but were relatively infrequent by comparison to other processes of social learning such as observation and imitation.     

The Significance of Non-vertical Transmission of Phenotype for the Evolution of Altruism

My aim in this paper is to demonstrate that a very simple learning rule based on imitation can help to sustain altruism as a culturally transmitted pattern or behaviour among agents playing a standard prisoner’s dilemma game. The point of this demonstration is not to prove that imitation is single-handedly responsible for existing levels of altruism (a thesis that is false), nor is the point to show that imitation is an important factor in explanations for the evolution of altruism (a thesis already prominent in the existing literature). The point is to show that imitation contributes to the evolution of altruism in a particular way that is not always fairly represented by evolutionary game theory models. Specifically, the paper uses a simple model to illustrate that cultural transmission includes mechanisms that do not transmit phenotype vertically (i.e. from parent to related offspring) and that these mechanisms can promote altruism in the absence of any direct biological propensity favouring such behaviour. This is a noteworthy result because it shows that evolutionary models can be built to explicitly reflect the contribution of non-vertical transmission in our explanations for the evolution of altruism among humans and other social species.     

Cultural niche construction and human evolution

Organisms frequently choose, regulate, construct and destroy important components of their environments, in the process changing the selection pressures to which they and other organisms are exposed. We refer to these processes as niche construction. In humans, culture has greatly amplified our capacity for niche construction and our ability to modify selection pressures. We use gene‐culture coevolutionary models to explore the evolutionary consequences of culturally generated niche construction through human evolution. Our analysis suggests that where cultural traits are transmitted in an unbiased fashion from parent to offspring, cultural niche construction will have a similar effect to gene‐based niche construction. However, cultural transmission biases favouring particular cultural traits may either increase or reduce the range of parameter space over which niche construction has an impact, which means that niche construction with biased transmission will either have a much smaller or a much bigger effect than gene‐based niche construction. The analysis also reveals circumstances under which cultural transmission can overwhelm natural selection, accelerate the rate at which a favoured gene spreads, initiate novel evolutionary events and trigger hominid speciation. Because cultural processes typically operate faster than natural selection, cultural niche construction probably has more profound consequences than gene‐based niche construction, and is likely to have played an important role in human evolution.     

Success-biased social learning: Cultural and evolutionary dynamics

Success bias is a social learning strategy whereby learners tend to acquire the cultural variants of successful individuals. I develop a general model of success-biased social learning for discrete cultural traits with stochastic payoffs, and investigate its dynamics when only two variants are present. I find that success bias inherently favors rare variants, and consequently performs worse than unbiased imitation (i.e. random copying) when success payoffs are at least mildly stochastic and the optimal variant is common. Because of this weakness, success bias fails to replace unbiased imitation in an evolutionary model when selection is fairly weak or when the environment is relatively stable, and sometimes fails to invade at all. I briefly discuss the optimal strength of success bias, the complicated nature of defining success in social learning contexts, and the value of variant frequency as an important source of information to social learners. I conclude with predictions regarding the prevalence of success bias in different behavioral domains.     

Social learning and teaching in chimpanzees

There is increasing evidence that some behavioural differences between groups of chimpanzees can be attributed neither to genetic nor to ecological variation. Such differences are likely to be maintained by social learning. While humans teach their offspring, and acquire cultural traits through imitative learning, there is little evidence of such behaviours in chimpanzees. However, by appealing only to incremental changes in motivation, attention and attention-soliciting behaviour, and without expensive changes in cognition, we can hypothesise the possible emergence of imitation and pedagogy in evolutionary history.     

Cultural evolution: implications for understanding the human language faculty and its evolution

Human language is unique among the communication systems of the natural world: it is socially learned and, as a consequence of its recursively compositional structure, offers open-ended communicative potential. The structure of this communication system can be explained as a consequence of the evolution of the human biological capacity for language or the cultural evolution of language itself. We argue, supported by a formal model, that an explanatory account that involves some role for cultural evolution has profound implications for our understanding of the biological evolution of the language faculty: under a number of reasonable scenarios, cultural evolution can shield the language faculty from selection, such that strongly constraining language-specific learning biases are unlikely to evolve. We therefore argue that language is best seen as a consequence of cultural evolution in populations with a weak and/or domain-general language faculty.     

Learning the ecological niche

A cornerstone of ecological theory is the ecological niche. Yet little is known about how individuals come to adopt it: whether it is innate or learned. Here, we report a cross-fostering experiment in the wild where we transferred eggs of blue tits, Cyanistes caeruleus, to nests of great tits, Parus major, and vice versa, to quantify the consequences of being reared in a different social context, but in an environment otherwise natural to the birds. We show that early learning causes a shift in the feeding niche in the direction of the foster species and that this shift lasts for life (foraging conservatism). Both species changed their feeding niches, but the change was greater in the great tit with its less specialized feeding behaviour. The study shows that cultural transmission through early learning is fundamental to the realization of ecological niches, and suggests a mechanism to explain learned habitat preference and sympatric speciation in animals.     

When in Rome,do as the Romans do: the coevolution of altruistic punishment,conformist learning,and cooperation

We model the coevolution of behavioral strategies and social learning rules in the context of a cooperative dilemma, a situation in which individuals must decide whether or not to subordinate their own interests to those of the group. There are two learning rules in our model, conformism and payoff-dependent imitation, which evolve by natural selection, and three behavioral strategies, cooperate, defect, and cooperate, plus punish defectors, which evolve under the influence of the prevailing learning rules. Group and individual level selective pressures drive evolution.We also simulate our model for conditions that approximate those in which early hominids lived. We find that conformism can evolve when the only problem that individuals face is a cooperative dilemma, in which prosocial behavior is always costly to the individual. Furthermore, the presence of conformists dramatically increases the group size for which cooperation can be sustained. The results of our model are robust: they hold even when migration rates are high, and when conflict among groups is infrequent.     

The evolution of social learning rules: Payoff-biased and frequency-dependent biased transmission

Humans and other animals do not use social learning indiscriminately, rather, natural selection has favoured the evolution of social learning rules that make selective use of social learning to acquire relevant information in a changing environment. We present a gene-culture coevolutionary analysis of a small selection of such rules (unbiased social learning, payoff-biased social learning and frequency-dependent biased social learning, including conformism and anti-conformism) in a population of asocial learners where the environment is subject to a constant probability of change to a novel state. We define conditions under which each rule evolves to a genetically polymorphic equilibrium. We find that payoff-biased social learning may evolve under high levels of environmental variation if the fitness benefit associated with the acquired behaviour is either high or low but not of intermediate value. In contrast, both conformist and anti-conformist biases can become fixed when environment variation is low, whereupon the mean fitness in the population is higher than for a population of asocial learners. Our examination of the population dynamics reveals stable limit cycles under conformist and anti-conformist biases and some highly complex dynamics including chaos. Anti-conformists can out-compete conformists when conditions favour a low equilibrium frequency of the learned behaviour. We conclude that evolution, punctuated by the repeated successful invasion of different social learning rules, should continuously favour a reduction in the equilibrium frequency of asocial learning, and propose that, among competing social learning rules, the dominant rule will be the one that can persist with the lowest frequency of asocial learning.     

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.     

Cultural transmission can inhibit the evolution of altruistic helping

The study of culturally inherited traits has led to the suggestion that the evolution of helping behaviors is more likely with cultural transmission than without. Here we evaluate this idea through a comparative analysis of selection on helping under both genetic and cultural inheritance. We develop two simple models for the evolution of helping through cultural group selection: one in which selection on the trait depends solely on Darwinian fitness effects and one in which selection is driven by nonreproductive factors, specifically imitation of strategies achieving higher payoffs. We show that when cultural variants affect Darwinian fitness, the selection pressure on helping can be markedly increased relative to that under genetic transmission. By contrast, when variants are driven by nonreproductive factors, the selection pressure on helping may be reduced relative to that under genetic inheritance. This occurs because, unlike biological offspring, the spread of cultural variants from one group to another through imitation does not reduce the number of these variants in the source group. As a consequence, there is increased within-group competition associated with traits increasing group productivity, which reduces the benefits of helping. In these cases, selection for harming behavior (decreasing the payoff to neighbors) may occur rather than selection for helping.     

How copying affects the amount, evenness and persistence of cultural knowledge: insights from the social learning strategies tournament

Darwinian processes should favour those individuals that deploy the most effective strategies for acquiring information about their environment. We organized a computer-based tournament to investigate which learning strategies would perform well in a changing environment. The most successful strategies relied almost exclusively on social learning (here, learning a behaviour performed by another individual) rather than asocial learning, even when environments were changing rapidly; moreover, successful strategies focused learning effort on periods of environmental change. Here, we use data from tournament simulations to examine how these strategies might affect cultural evolution, as reflected in the amount of culture (i.e. number of cultural traits) in the population, the distribution of cultural traits across individuals, and their persistence through time. We found that high levels of social learning are associated with a larger amount of more persistent knowledge, but a smaller amount of less persistent expressed behaviour, as well as more uneven distributions of behaviour, as individuals concentrated on exploiting a smaller subset of behaviour patterns. Increased rates of environmental change generated increases in the amount and evenness of behaviour. These observations suggest that copying confers on cultural populations an adaptive plasticity, allowing them to respond to changing environments rapidly by drawing on a wider knowledge base.     

Inheritance of optimal foraging behaviour in Columbian ground squirrels

Summary I examined the potential inheritance of the ability of Columbian ground squirrels (Spermophilus columbianus) to select an optimal diet. I calculated the diet that would maximize daily energy intake for each of 21 adult females and their litters, using a linear programming optimization model for each individual. The absolute value of the difference between an individual's predicted optimal diet and observed diet (deviation from an optimal diet) was used as a measure of an individual's foraging ability. The foraging ability of individuals was consistent over time and in different foraging environments, so I considered foraging ability to be a potentially heritable trait.Inheritance was determined from correlations of mother and offspring foraging ability. I experimentally removed some mothers just as they weaned their offspring so that offspring could not be influenced by their mother while learning to forage, while leaving the other mothers to raise their litters normally. In both cases, offspring strongly resembled their mother in foraging ability. However, offspring with mothers absent exhibited significantly larger deviations from their optimal diet. Offspring with mothers absent appeared to imitate their mother's diet during lactation, and this tendency partially explained their greater deviation. Consequently, offspring appear to inherit the ability to forage optimally from their mother, perhaps through observational learning or imitation. There may also be a genetic basis to foraging ability, but uncontrolled maternal effects in the experiment prevent a proper test for it.     

Social learning in birds and its role in shaping a foraging niche

We briefly review the literature on social learning in birds, concluding that strong evidence exists mainly for predator recognition, song, mate choice and foraging. The mechanism of local enhancement may be more important than imitation for birds learning to forage, but the former mechanism may be sufficient for faithful transmission depending on the ecological circumstances. To date, most insights have been gained from birds in captivity. We present a study of social learning of foraging in two passerine birds in the wild, where we cross-fostered eggs between nests of blue tits, Cyanistes caeruleus and great tits, Parus major. Early learning causes a shift in the foraging sites used by the tits in the direction of the foster species. The shift in foraging niches was consistent across seasons, as showed by an analysis of prey items, and the effect lasted for life. The fact that young birds learn from their foster parents, and use this experience later when subsequently feeding their own offspring, suggests that foraging behaviour can be culturally transmitted over generations in the wild. It may therefore have both ecological and evolutionary consequences, some of which are discussed.     

The ethological analysis of imitation

Theorists and experimental researchers have long debated whether animals are able to imitate. A variety of definitions of imitation have been proposed to describe this complex form of social learning. Experimental research on imitation has often been hampered by either a too loose 'anthropomorphic' approach or by too narrow 'behaviourist' definitions. At present neither associative nor cognitive theories are able to offer an exhaustive explanation of imitation in animals. An ethological approach to imitation offers a different perspective. By integrating questions on function, mechanism, development and evolution one can identify possible directions for future research. At present, however, we are still far from developing a comprehensive theory of imitation. A functional approach to imitation shows that, despite some evidence for imitative learning in food processing in apes, such learning has not been shown to be involved in the social transmission of either tool-use skills or communicative signals. Recently developed procedures offer possible ways of clarifying the role of imitation in tool use and visual communication. The role of imitation in explorative play in apes is also investigated and the available data suggest that copying during play might represent a behavioural homologue of human imitation. It is proposed that the ability to copy the behaviour of a companion is under a strong genetic influence in many social species. Many important factors have not been examined experimentally, e.g. the effect of the demonstrator, the influence of attention and memory and the ability to generalize. The potential importance of reinforcement raises the possibility that copying abilities serving divergent functions might be partly under the control of different mechanisms.     

A theoretical investigation of the role of social transmission in evolution

This paper contains an investigation of the interaction between protocultural processes in animals, generated by social learning and the processes of biological evolution. It addresses the question of whether mechanisms of social learning and transmission can play an evolutionary role by allowing learned patterns of behavior to spread through animal populations, in the process changing the selection pressures acting on them. Simple models of social transmission and gene-meme coevolution are developed to investigate three hypotheses related to the role of social transmission in animal evolution. Simulations using the models suggest that social transmission would have to be particularly stable and be associated with estremely strong selection, if it were to result in the fixation of alleles. A more likely hypothesis is that social transmission might allow animals to respond adaptively to novelty in their environment, rendering a genetic response unnecessary, or only partially necessary. Socially transmitted traits appear to spread sufficiently rapidly, relative to changes in gene frequency, that it would be quite feasible for a socially transmitted response to an environmental change to occur, preempting a genetic response. Social transmission is probably more likely to slow down evolutionary rates than to speed them up through changing selection pressures. However, cultural and evolutionary processes are likely to interact in complex ways, and a “behavioral drive” effect cannot be ruled out.     

Introduction. Cultural transmission and the evolution of human behaviour

The articles in this theme issue seek to understand the evolutionary bases of social learning and the consequences of cultural transmission for the evolution of human behaviour. In this introductory article, we provide a summary of these articles (seven articles on the experimental exploration of cultural transmission and three articles on the role of gene-culture coevolution in shaping human behaviour) and a personal view of some promising lines of development suggested by the work summarized here.     

Social selection parapatry in Afrotropical sunbirds

The extent of range overlap of incipient and recent species depends on the type and magnitude of phenotypic divergence that separates them, and the consequences of phenotypic divergence on their interactions. Signal divergence by social selection likely initiates many speciation events, but may yield niche‐conserved lineages predisposed to limit each others’ ranges via ecological competition. Here, we examine this neglected aspect of social selection speciation theory in relation to the discovery of a nonecotonal species border between sunbirds. We find that Nectarinia moreaui and Nectarinia fuelleborni meet in a ～6 km wide contact zone, as estimated by molecular cline analysis. These species exploit similar bioclimatic niches, but sing highly divergent learned songs, consistent with divergence by social selection. Cline analyses suggest that within‐species stabilizing social selection on song‐learning predispositions maintains species differences in song despite both hybridization and cultural transmission. We conclude that ecological competition between moreaui and fuelleborni contributes to the stabilization of the species border, but that ecological competition acts in conjunction with reproductive interference. The evolutionary maintenance of learned song differences in a hybrid zone recommend this study system for future studies on the mechanisms of learned song divergence and its role in speciation.