Variation in primate decision-making under uncertainty and the roots of human economic behaviour

Uncertainty is a ubiquitous component of human economic behaviour, yet people can vary in their preferences for risk across populations, individuals and different points in time. As uncertainty also characterizes many aspects of animal decision-making, comparative research can help evaluate different potential mechanisms that generate this variation, including the role of biological differences or maturational change versus cultural learning, as well as identify human-unique components of economic decision-making. Here, we examine decision-making under risk across non-human primates, our closest relatives. We first review theoretical approaches and current methods for understanding decision-making in animals. We then assess the current evidence for variation in animal preferences between species and populations, between individuals based on personality, sex and age, and finally, between different contexts and individual states. We then use these primate data to evaluate the processes that can shape human decision-making strategies and identify the primate foundations of human economic behaviour.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Evolutionary causes and consequences of consistent individual variation in cooperative behaviour

Behaviour is typically regarded as among the most flexible of animal phenotypic traits. In particular, expression of cooperative behaviour is often assumed to be conditional upon the behaviours of others. This flexibility is a key component of many hypothesized mechanisms favouring the evolution of cooperative behaviour. However, evidence shows that cooperative behaviours are often less flexible than expected and that, in many species, individuals show consistent differences in the amount and type of cooperative and non-cooperative behaviours displayed. This phenomenon is known as ‘animal personality’ or a ‘behavioural syndrome’. Animal personality is evolutionarily relevant, as it typically shows heritable variation and can entail fitness consequences, and hence, is subject to evolutionary change. Here, we review the empirical evidence for individual variation in cooperative behaviour across taxa, we examine the evolutionary processes that have been invoked to explain the existence of individual variation in cooperative behaviour and we discuss the consequences of consistent individual differences on the evolutionary stability of cooperation. We highlight that consistent individual variation in cooperativeness can both stabilize or disrupt cooperation in populations. We conclude that recognizing the existence of consistent individual differences in cooperativeness is essential for an understanding of the evolution and prevalence of cooperation.     

Exploring the effects of working for endowments on behaviour in standard economic games

In recent years, significant advances have been made in understanding the adaptive (ultimate) and mechanistic (proximate) explanations for the evolution and maintenance of cooperation. Studies of cooperative behaviour in humans invariably use economic games. These games have provided important insights into the mechanisms that maintain economic and social cooperation in our species. However, they usually rely on the division of monetary tokens which are given to participants by the investigator. The extent to which behaviour in such games may reflect behaviour in the real world of biological markets--where money must be earned and behavioural strategies incur real costs and benefits--is unclear. To provide new data on the potential scale of this problem, we investigated whether people behaved differently in two standard economic games (public goods game and dictator game) when they had to earn their monetary endowments through the completion of dull or physically demanding tasks, as compared with simply being given the endowment. The requirement for endowments to be 'earned' through labour did not affect behaviour in the dictator game. However, the requirement to complete a dull task reduced cooperation in the public goods game among the subset of participants who were not familiar with game theory. There has been some effort to test whether the conclusions drawn from standard, token-based cooperation games adequately reflect cooperative behaviour 'in the wild.' However, given the almost total reliance on such games to study cooperation, more exploration of this issue would be welcome. Our data are not unduly worrying, but they do suggest that further exploration is needed if we are to make general inferences about human behaviour from the results of structured economic games.     

Maternal Oxytocin Is Linked to Close Mother-Infant Proximity in Grey Seals (Halichoerus grypus)

Maternal behaviour is a crucial component of reproduction in all mammals; however the quality of care that mothers give to infants can vary greatly. It is vital to document variation in maternal behaviour caused by the physiological processes controlling its expression. This underlying physiology should be conserved throughout reproductive events and should be replicated across all individuals of a species; therefore, any correlates to maternal care quality may be present across many individuals or contexts. Oxytocin modulates the initiation and expression of maternal behaviour in mammals; therefore we tested whether maternal plasma oxytocin concentrations correlated to key maternal behaviours in wild grey seals (Halichoerus grypus). Plasma oxytocin concentrations in non-breeding individuals (4.3 ±0.5 pg/ml) were significantly lower than those in mothers with dependent pups in both early (8.2 ±0.8 pg/ml) and late (6.9 ±0.7 pg/ml) lactation. Maternal plasma oxytocin concentrations were not correlated to the amount of nursing prior to sampling, or a mother’s nursing intensity throughout the dependant period. Mothers with high plasma oxytocin concentrations stayed closer to their pups, reducing the likelihood of mother-pup separation during lactation which is credited with causing starvation, the largest cause of pup mortality in grey seals. This is the first study to link endogenous oxytocin concentrations in wild mammalian mothers with any type of maternal behaviour. Oxytocin’s structure and function is widely conserved across mammalian mothers, including humans. Defining the impact the oxytocin system has on maternal behaviour highlights relationships that may occur across many individuals or species, and such behaviours heavily influence infant development and an individual’s lifetime reproductive success.     

Insights into neural mechanisms and evolution of behaviour from electric fish

Both behaviour and its neural control can be studied at two levels. At the proximate level, we aim to identify the neural circuits that control behaviour and to understand how information is represented and processed in these circuits. Ultimately, however, we are faced with questions of why particular neural solutions have arisen, and what factors govern the ways in which neural circuits are modified during the evolution of new behaviours. Only by integrating these levels of analysis can we fully understand the neural control of behaviour. Recent studies of electrosensory systems show how this synthesis can benefit from the use of tractable systems and comparative studies.     

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’.     

Dynamics to Equilibrium in Network Games: Individual Behavior and Global Response

Various social contexts can be depicted as games of strategic interactions on networks, where an individual’s welfare depends on both her and her partners’ actions. Whereas much attention has been devoted to Bayes-Nash equilibria in such games, here we look at strategic interactions from an evolutionary perspective. To this end, we present the results of a numerical simulations program for these games, which allows us to find out whether Nash equilibria are accessible by adaptation of player strategies, and in general to identify the attractors of the evolution. Simulations allow us to go beyond a global characterization of the cooperativeness at equilibrium and probe into individual behavior. We find that when players imitate each other, evolution does not reach Nash equilibria and, worse, leads to very unfavorable states in terms of welfare. On the contrary, when players update their behavior rationally, they self-organize into a rich variety of Nash equilibria, where individual behavior and payoffs are shaped by the nature of the game, the social network’s structure and the players’ position within the network. Our results allow to assess the validity of mean-field approaches we use to describe the dynamics of these games. Interestingly, our dynamically-found equilibria generally do not coincide with (but show qualitatively the same features of) those resulting from theoretical predictions in the context of one-shot games under incomplete information.     

Genetic composition of social groups influences male aggressive behaviour and fitness in natural genotypes of Drosophila melanogaster

Indirect genetic effects (IGEs) describe how an individual''s behaviour—which is influenced by his or her genotype—can affect the behaviours of interacting individuals. IGE research has focused on dyads. However, insights from social networks research, and other studies of group behaviour, suggest that dyadic interactions are affected by the behaviour of other individuals in the group. To extend IGE inferences to groups of three or more, IGEs must be considered from a group perspective. Here, I introduce the ‘focal interaction’ approach to study IGEs in groups. I illustrate the utility of this approach by studying aggression among natural genotypes of Drosophila melanogaster. I chose two natural genotypes as ‘focal interactants’: the behavioural interaction between them was the ‘focal interaction’. One male from each focal interactant genotype was present in every group, and I varied the genotype of the third male—the ‘treatment male’. Genetic variation in the treatment male''s aggressive behaviour influenced the focal interaction, demonstrating that IGEs in groups are not a straightforward extension of IGEs measured in dyads. Further, the focal interaction influenced male mating success, illustrating the role of IGEs in behavioural evolution. These results represent the first manipulative evidence for IGEs at the group level.     

Physiological mechanisms for food-hoarding motivation in animals

The study of ingestive behaviour has an extensive history, starting as early as 1918 when Wallace Craig, an animal behaviourist, coined the terms ‘appetitive’ and ‘consummatory’ for the two-part sequence of eating, drinking and sexual behaviours. Since then, most ingestive behaviour research has focused on the neuroendocrine control of food ingestion (consummatory behaviour). The quantity of food eaten, however, is also influenced by the drive both to acquire and to store food (appetitive behaviour). For example, hamster species have a natural proclivity to hoard food and preferentially alter appetitive ingestive behaviours in response to environmental changes and/or metabolic hormones and neuropeptides, whereas other species would instead primarily increase their food intake. Therefore, with the strong appetitive component to their ingestive behaviour that is relatively separate from their consummatory behaviour, they seem an ideal model for elucidating the neuroendocrine mechanisms underlying the control of food hoarding and foraging. This review focuses on the appetitive side of ingestive behaviour, in particular food hoarding, attempting to integrate what is known about the neuroendocrine mechanisms regulating this relatively poorly studied behaviour. An hypothesis is formed stating that the direction of ‘energy flux’ is a unifying factor for the control of food hoarding.     

Balancing costs and benefits in primates: ecological and palaeoanthropological views

Maintaining the balance between costs and benefits is challenging for species living in complex and dynamic socio-ecological environments, such as primates, but also crucial for shaping life history, reproductive and feeding strategies. Indeed, individuals must decide to invest time and energy to obtain food, services and partners, with little direct feedback on the success of their investments. Whereas decision-making relies heavily upon cognition in humans, the extent to which it also involves cognition in other species, based on their environmental constraints, has remained a challenging question. Building mental representations relating behaviours and their long-term outcome could be critical for other primates, but there are actually very little data relating cognition to real socio-ecological challenges in extant and extinct primates. Here, we review available data illustrating how specific cognitive processes enable(d) modern primates and extinct hominins to manage multiple resources (e.g. food, partners) and to organize their behaviour in space and time, both at the individual and at the group level. We particularly focus on how they overcome fluctuating and competing demands, and select courses of action corresponding to the best possible packages of potential costs and benefits in reproductive and foraging contexts.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Environmental transmission of a personality trait: foster parent exploration behaviour predicts offspring exploration behaviour in zebra finches

Consistent behavioural differences among individuals are common in many species and can have important effects on offspring fitness. To understand such ‘personality’ variation, it is important to determine the mode of inheritance, but this has been quantified for only a few species. Here, we report results from a breeding experiment in captive zebra finches, Taeniopygia guttata, in which we cross-fostered offspring to disentangle the importance of genetic and non-genetic transmission of behaviour. Genetic and foster-parents’ exploratory type was measured in a novel environment pre-breeding and offspring exploratory type was assessed at adulthood. Offspring exploratory type was predicted by the exploratory behaviour of the foster but not the genetic parents, whereas offspring size was predicted by genetic but not foster-parents’ size. Other aspects of the social environment, such as rearing regime (uni- versus biparental), hatching position, brood size or an individual''s sex did not influence offspring exploration. Our results therefore indicate that non-genetic transmission of behaviour can play an important role in shaping animal personality variation.     

A dynamic over games drives selfish agents to win–win outcomes

Understanding human institutions, animal cultures and other social systems requires flexible formalisms that describe how their members change them from within. We introduce a framework for modelling how agents change the games they participate in. We contrast this between-game ‘institutional evolution’ with the more familiar within-game ‘behavioural evolution’. We model institutional change by following small numbers of persistent agents as they select and play a changing series of games. Starting from an initial game, a group of agents trace trajectories through game space by navigating to increasingly preferable games until they converge on ‘attractor’ games. Agents use their ‘institutional preferences'' for game features (such as stability, fairness and efficiency) to choose between neighbouring games. We use this framework to pose a pressing question: what kinds of games does institutional evolution select for; what is in the attractors? After computing institutional change trajectories over the two-player space, we find that attractors have disproportionately fair outcomes, even though the agents who produce them are strictly self-interested and indifferent to fairness. This seems to occur because game fairness co-occurs with the self-serving features these agents do actually prefer. We thus present institutional evolution as a mechanism for encouraging the spontaneous emergence of cooperation among small groups of inherently selfish agents, without space, reputation, repetition, or other more familiar mechanisms. Game space trajectories provide a flexible, testable formalism for modelling the interdependencies of behavioural and institutional evolutionary processes, as well as a mechanism for the evolution of cooperation.     

Individual behaviour in firebugs (Pyrrhocoris apterus)

The concept of animal personalities has recently become of major interest as researchers began to wonder why animals within a given population show consistent behaviour across situations and contexts, what led to the evolution of such behavioural inflexibility and what mechanisms might underlie the phenomenon. A recent model explains individual differences in a population as the result of trade-off between present and future reproduction. We tested this model on the two wing morphs, i.e. short-winged (brachypterous) and long-winged (macropterous) specimens of the firebug (Pyrrhocoris apterus). Since it has been already demonstrated that the two wing morphs differ in their life-history strategies, this species is an ideal subject to test whether the specimens with different life-history strategies have different personalities as well. The results show that individuals behave consistently over time and across contexts, meaning observed bugs do have personalities. We also have found that in females, the two wing morphs have different personalities supporting the theoretical predictions, i.e. winged ones, which are supposed to have lower future reproductive value, are braver and more exploratory. We found no difference between the morphs in males. Differences in reproductive investment might explain this discrepancy between the sexes.     

Taking a Comparative Approach: Analysing Personality as a Multivariate Behavioural Response across Species

Animal personality, repeatable behaviour through time and across contexts, is ecologically and evolutionarily important as it can account for the exhibition of sub-optimal behaviours. Interspecific comparisons have been suggested as important for understanding the evolution of animal personality; however, these are seldom accomplished due, in part, to the lack of statistical tools for quantifying differences and similarities in behaviour between groups of individuals. We used nine species of closely-related coral reef fishes to investigate the usefulness of ecological community analyses for the analysis of between-species behavioural differences and behavioural heterogeneity. We first documented behavioural carryover across species by observing the fishes' behaviour and measuring their response to a threatening stimulus to quantify boldness. Bold fish spent more time away from the reef and fed more than shy fish. We then used ecological community analysis tools (canonical variate analysis, multi-response permutation procedure, and permutational analysis of multivariate dispersion) and identified four 'clusters' of behaviourally similar fishes, and found that the species differ in the behavioural variation expressed; some species are more behaviourally heterogeneous than others. We found that ecological community analysis tools are easily and fruitfully applied to comparative studies of personality and encourage their use by future studies.     

Cognitive neuroscience of human social behaviour

We are an intensely social species--it has been argued that our social nature defines what makes us human, what makes us conscious or what gave us our large brains. As a new field, the social brain sciences are probing the neural underpinnings of social behaviour and have produced a banquet of data that are both tantalizing and deeply puzzling. We are finding new links between emotion and reason, between action and perception, and between representations of other people and ourselves. No less important are the links that are also being established across disciplines to understand social behaviour, as neuroscientists, social psychologists, anthropologists, ethologists and philosophers forge new collaborations.     

Can We Predict Personality in Fish? Searching for Consistency over Time and across Contexts

The interest in animal personality, broadly defined as consistency of individual behavioural traits over time and across contexts, has increased dramatically over the last years. Individual differences in behaviour are no longer recognised as noise around a mean but rather as adaptive variation and thus, essentially, raw material for evolution. Animal personality has been considered evolutionary conserved and has been shown to be present in all vertebrates including fish. Despite the importance of evolutionary and comparative aspects in this field, few studies have actually documented consistency across situations in fish. In addition, most studies are done with individually housed fish which may pose additional challenges when interpreting data from social species. Here, we investigate, for the first time in fish, whether individual differences in behavioural responses to a variety of challenges are consistent over time and across contexts using both individual and grouped-based tests. Twenty-four juveniles of Gilthead seabream Sparus aurata were subjected to three individual-based tests: feed intake recovery in a novel environment, novel object and restraining and to two group-based tests: risk-taking and hypoxia. Each test was repeated twice to assess consistency of behavioural responses over time. Risk taking and escape behaviours during restraining were shown to be significantly consistent over time. In addition, consistency across contexts was also observed: individuals that took longer to recover feed intake after transfer into a novel environment exhibited higher escape attempts during a restraining test and escaped faster from hypoxia conditions. These results highlight the possibility to predict behaviour in groups from individual personality traits.     

Emotions as infectious diseases in a large social network: the SISa model

Human populations are arranged in social networks that determine interactions and influence the spread of diseases, behaviours and ideas. We evaluate the spread of long-term emotional states across a social network. We introduce a novel form of the classical susceptible–infected–susceptible disease model which includes the possibility for ‘spontaneous’ (or ‘automatic’) infection, in addition to disease transmission (the SISa model). Using this framework and data from the Framingham Heart Study, we provide formal evidence that positive and negative emotional states behave like infectious diseases spreading across social networks over long periods of time. The probability of becoming content is increased by 0.02 per year for each content contact, and the probability of becoming discontent is increased by 0.04 per year per discontent contact. Our mathematical formalism allows us to derive various quantities from the data, such as the average lifetime of a contentment ‘infection’ (10 years) or discontentment ‘infection’ (5 years). Our results give insight into the transmissive nature of positive and negative emotional states. Determining to what extent particular emotions or behaviours are infectious is a promising direction for further research with important implications for social science, epidemiology and health policy. Our model provides a theoretical framework for studying the interpersonal spread of any state that may also arise spontaneously, such as emotions, behaviours, health states, ideas or diseases with reservoirs.     

Evolutionary mechanisms in behaviour: An intraspecific genetic approach

The study of the evolutionary mechanisms in behaviour and of the biological grounds of individual variability may be based on the comparative phylogenetic approach or on an intraspecific genetic analysis. The discontinuous behavioural progression evident across species is due to the assumption that the phylogenetic “scale” may be adopted in place of the phylogenetic trees and to the fact that today's existing species have evolved in parallel and may not be used to represent an evolutionary sequence. However, despite the existence of different motor and perceptual abilities the comparative approach has shown that many analogies exist between some basic brain mechanisms across species.The existence of outstanding individual differences within the same species must be regarded as a powerful potential tool since quantitative differences between the behaviours of different individuals belonging to the same species might later result in qualitatively different phenotypes. By using different strains and mutations of mice and different genetic approaches it has been possible to assess the mode of inheritance, to calculate estimates of heritability and of the number of segregating units for different behavioural traits ranging from avoidance to maze learning and activity. The existence of clear genetic correlations between some of these behavioural patterns has also allowed the identification of some single-gene mutants affecting these traits and the characterization of a gene responsible for a major effect on activity. This psychogenetic approach shows that there are behaviour differences which are the products of evolutionary adaptive processes and that the knowledge of the genetic systems that underlie these differences is a basic step for understanding the brain mechanisms in Man.     

First evidence for heritable variation in cooperative breeding behaviour

Understanding the evolution of complex social behaviours, such as cooperative breeding, is a fundamental problem in evolutionary biology, which has attracted much theoretical and empirical interest. Variation within and between species in the frequency of helping behaviour has been typically associated with variation in direct costs and benefits due to ecological constraints, or with indirect fitness payoffs (i.e. kin selection). Here, we provide the first evidence that individual variation in cooperative behaviour within a natural population also has a heritable component. Using a seven-generation pedigree in a wild population of western bluebirds (Sialia mexicana), we show significant heritable variation for the propensity to help rather than breed, as well as for the probability of having a helper at the nest. We also document a strong positive relationship between a bird's lifespan and its prospect of receiving help when breeding, in accordance with earlier comparative studies across species. These findings provide useful insights into the possible mechanisms which have led to the evolution of cooperative breeding and other social systems.     

Virtual bargaining: a theory of social decision-making

An essential element of goal-directed decision-making in social contexts is that agents'' actions may be mutually interdependent. However, the most well-developed approaches to such strategic interactions, based on the Nash equilibrium concept in game theory, are sometimes too broad and at other times ‘overlook’ good solutions to fundamental social dilemmas and coordination problems. The authors propose a new theory of social decision-making—virtual bargaining—in which individuals decide among a set of moves on the basis of what they would agree to do if they could openly bargain. The core principles of a formal account are outlined (vis-à-vis the notions of ‘feasible agreement’ and explicit negotiation) and further illustrated with the introduction of a new game, dubbed the ‘Boobytrap game’ (a modification on the canonical Prisoner''s Dilemma paradigm). In the first empirical data of how individuals play the Boobytrap game, participants'' experimental choices accord well with a virtual bargaining perspective, but do not match predictions from a standard Nash account. Alternative frameworks are discussed, with specific empirical tests between these and virtual bargaining identified as future research directions. Lastly, it is proposed that virtual bargaining underpins a vast range of human activities, from social decision-making to joint action and communication.