Individual differences affect honest signalling in a songbird

Research in the past decade has established the existence of consistent individual differences or ‘personality’ in animals and their important role in many aspects of animal behaviour. At the same time, research on honest signalling of aggression has revealed that while some of the putative aggression signals are reliable, they are only imperfectly so. This study asks whether a significant portion of the variance in the aggression-signal regression may be explained by individual differences in signalling strategies. Using the well-studied aggressive signalling system of song sparrows (Melospiza melodia), we carried out repeated assays to measure both aggressive behaviours and aggressive signalling of territorial males. Through these assays, we found that aggressive behaviours and aggressive signalling were both highly repeatable, and moreover that aggressive behaviours in 2009–2010 predicted whether the birds would attack a taxidermic mount over a year later. Most significantly, we found that residual variation in signalling behaviours, after controlling for aggressive behaviour, was individually consistent, suggesting there may be a second personality trait determining the level of aggressive signalling. We term this potential personality trait ‘communicativeness’ and discuss these results in the context of honest signalling theories and recent findings reporting prevalence of ‘under-signalling’.     

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.     

Social enhancement can create adaptive,arbitrary and maladaptive cultural traditions

Many animals are known to learn socially, i.e. they are able to acquire new behaviours by using information from other individuals. Researchers distinguish between a number of different social-learning mechanisms such as imitation and social enhancement. Social enhancement is a simple form of social learning that is among the most widespread in animals. However, unlike imitation, it is debated whether social enhancement can create cultural traditions. Based on a recent study on capuchin monkeys, we developed an agent-based model to test the hypotheses that (i) social enhancement can create and maintain stable traditions and (ii) social enhancement can create cultural conformity. Our results supported both hypotheses. A key factor that led to the creation of cultural conformity and traditions was the repeated interaction of individual reinforcement and social enhancement learning. This result emphasizes that the emergence of cultural conformity does not necessarily require cognitively complex mechanisms such as ‘copying the majority’ or group norms. In addition, we observed that social enhancement can create learning dynamics similar to a ‘copy when uncertain’ learning strategy. Results from additional analyses also point to situations that should favour the evolution of learning mechanisms more sophisticated than social enhancement.     

Phenotypic variability in unicellular organisms: from calcium signalling to social behaviour

Historically, research has focused on the mean and often neglected the variance. However, variability in nature is observable at all scales: among cells within an individual, among individuals within a population and among populations within a species. A fundamental quest in biology now is to find the mechanisms that underlie variability. Here, we investigated behavioural variability in a unique unicellular organism, Physarum polycephalum. We combined experiments and models to show that variability in cell signalling contributes to major differences in behaviour underpinning some aspects of social interactions. First, following thousands of cells under various contexts, we identified distinct behavioural phenotypes: ‘slow–regular–social’, ‘fast–regular–social’ and ‘fast–irregular–asocial’. Second, coupling chemical analysis and behavioural assays we found that calcium signalling is responsible for these behavioural phenotypes. Finally, we show that differences in signalling and behaviour led to alternative social strategies. Our results have considerable implications for our understanding of the emergence of variability in living organisms.     

Further Explorations of the Facing Bias in Biological Motion Perception: Perspective Cues,Observer Sex,and Response Times

The human visual system has evolved to be highly sensitive to visual information about other persons and their movements as is illustrated by the effortless perception of point-light figures or ‘biological motion’. When presented orthographically, a point-light walker is interpreted in two anatomically plausible ways: As ‘facing the viewer’ or as ‘facing away’ from the viewer. However, human observers show a ‘facing bias’: They perceive such a point-light walker as facing towards them in about 70-80% of the cases. In studies exploring the role of social and biological relevance as a possible account for the facing bias, we found a ‘figure gender effect’: Male point-light figures elicit a stronger facing bias than female point-light figures. Moreover, we also found an ‘observer gender effect’: The ‘figure gender effect’ was stronger for male than for female observers. In the present study we presented to 11 males and 11 females point-light walkers of which, very subtly, the perspective information was manipulated by modifying the earlier reported ‘perspective technique’. Proportions of ‘facing the viewer’ responses and reaction times were recorded. Results show that human observers, even in the absence of local shape or size cues, easily pick up on perspective cues, confirming recent demonstrations of high visual sensitivity to cues on whether another person is potentially approaching. We also found a consistent difference in how male and female observers respond to stimulus variations (figure gender or perspective cues) that cause variations in the perceived in-depth orientation of a point-light walker. Thus, the ‘figure gender effect’ is possibly caused by changes in the relative locations and motions of the dots that the perceptual system tends to interpret as perspective cues. Third, reaction time measures confirmed the existence of the facing bias and recent research showing faster detection of approaching than receding biological motion.     

Gratefully Received,Gratefully Repaid: The Role of Perceived Fairness in Cooperative Interactions

It is well documented that people would remunerate fair behaviours and penalize unfair behaviours. It is argued that individuals’ reactions following the receipt of a gift depend on the perceived intentions of the donors. Fair intentions should prompt positive affect, like gratitude, triggering cooperative behaviours; while intended unfairness should trigger negative affect, like anger, fostering anti-social actions. It is, however, contended that when people lack information to infer others’ intention they may use ‘normative’ beliefs about fairness - what a typical fair individual ‘should’ do in these circumstances – to guide their behaviour. In this experiment we examined this assertion. We had 122 participants play a one-shot, double-anonymous game with half playing as potential helpers (P1s) and half as recipients (P2s). Whether a participant was a P1 or P2 was chance-determined and all participants knew this. P1s decided whether to help P2s and whether to make their help unconditional (no repayment needed) or conditional (full or ‘taxed’ repayment). P2s decided whether to accept the offer and whatever conditions attached but were blind to the list of helping options available to P1s. We anticipated that recipients would refer to the ‘injunctive norm’ that ‘fair people should help “for free” when it is only by chance that they are in a position to help’. Therefore, without knowing P1s’ different helping options, unconditional offers should be rated by recipients as fairer than conditional offers, and this should be linked to greater gratitude with greater gratitude linked to greater reciprocation. Path analyses confirmed this serial mediation. The results showed that recipients of unconditional offers, compared to conditional ones, interpreted the helpers’ motives as more helpful, experienced greater gratitude and were more eager to reciprocate. The behavioural data further revealed that, when given a latter option to default, 38% of recipients of conditional offers did so.     

Backtracking behaviour in lost ants: an additional strategy in their navigational toolkit

Ants use multiple sources of information to navigate, but do not integrate all this information into a unified representation of the world. Rather, the available information appears to serve three distinct main navigational systems: path integration, systematic search and the use of learnt information—mainly via vision. Here, we report on an additional behaviour that suggests a supplemental system in the ant''s navigational toolkit: ‘backtracking’. Homing ants, having almost reached their nest but, suddenly displaced to unfamiliar areas, did not show the characteristic undirected headings of systematic searches. Instead, these ants backtracked in the compass direction opposite to the path that they had just travelled. The ecological function of this behaviour is clear as we show it increases the chances of returning to familiar terrain. Importantly, the mechanistic implications of this behaviour stress an extra level of cognitive complexity in ant navigation. Our results imply: (i) the presence of a type of ‘memory of the current trip’ allowing lost ants to take into account the familiar view recently experienced, and (ii) direct sharing of information across different navigational systems. We propose a revised architecture of the ant''s navigational toolkit illustrating how the different systems may interact to produce adaptive behaviours.     

Affective responses in tamarins elicited by species-specific music

Theories of music evolution agree that human music has an affective influence on listeners. Tests of non-humans provided little evidence of preferences for human music. However, prosodic features of speech (‘motherese’) influence affective behaviour of non-verbal infants as well as domestic animals, suggesting that features of music can influence the behaviour of non-human species. We incorporated acoustical characteristics of tamarin affiliation vocalizations and tamarin threat vocalizations into corresponding pieces of music. We compared music composed for tamarins with that composed for humans. Tamarins were generally indifferent to playbacks of human music, but responded with increased arousal to tamarin threat vocalization based music, and with decreased activity and increased calm behaviour to tamarin affective vocalization based music. Affective components in human music may have evolutionary origins in the structure of calls of non-human animals. In addition, animal signals may have evolved to manage the behaviour of listeners by influencing their affective state.     

Escalation of aggressive vocal signals: a sequential playback study

Rival conspecifics often produce stereotyped sequences of signals as agonistic interactions escalate. Successive signals in sequence are thought to convey increasingly pronounced levels of aggressive motivation. Here, we propose and test a model of aggressive escalation in black-throated blue warblers, presenting subjects with two sequential and increasingly elevated levels of threat. From a speaker outside the territorial boundary, we initiated an interaction (low-threat level), and from a second speaker inside the territory, accompanied by a taxidermic mount, we subsequently simulated a territorial intrusion (escalated threat level). Our two main predictions were that signalling behaviours in response to low-threat boundary playback would predict signalling responses to the escalated within-territory threat, and that these latter signalling behaviours would in turn reliably predict attack. We find clear support for both predictions: (i) specific song types (type II songs) produced early in the simulated interaction, in response to boundary playback, predicted later use of low-amplitude ‘soft’ song, in response to within-territory playback; and (ii) soft song, in turn, predicted attack of the mount. Unexpectedly, use of the early-stage signal (type II song) itself did not predict attack, despite its apparent role in aggressive escalation. This raises the intriguing question of whether type II song can actually be considered a reliable aggressive signal. Overall, our results provide new empirical insights into how songbirds may use progressive vocal signalling to convey increasing levels of threat.     

Genetic and ‘cultural’ similarity in wild chimpanzees

The question of whether animals possess ‘cultures’ or ‘traditions’ continues to generate widespread theoretical and empirical interest. Studies of wild chimpanzees have featured prominently in this discussion, as the dominant approach used to identify culture in wild animals was first applied to them. This procedure, the ‘method of exclusion,’ begins by documenting behavioural differences between groups and then infers the existence of culture by eliminating ecological explanations for their occurrence. The validity of this approach has been questioned because genetic differences between groups have not explicitly been ruled out as a factor contributing to between-group differences in behaviour. Here we investigate this issue directly by analysing genetic and behavioural data from nine groups of wild chimpanzees. We find that the overall levels of genetic and behavioural dissimilarity between groups are highly and statistically significantly correlated. Additional analyses show that only a very small number of behaviours vary between genetically similar groups, and that there is no obvious pattern as to which classes of behaviours (e.g. tool-use versus communicative) have a distribution that matches patterns of between-group genetic dissimilarity. These results indicate that genetic dissimilarity cannot be eliminated as playing a major role in generating group differences in chimpanzee behaviour.     

What behaviour in economic games tells us about the evolution of non-human species' economic decision-making behaviour

In the past decade, there has been a surge of interest in using games derived from experimental economics to test decision-making behaviour across species. In most cases, researchers are using the games as a tool, for instance, to understand what factors influence decision-making, how decision-making differs across species or contexts, or to ask broader questions about species’ propensities to cooperate or compete. These games have been quite successful in this regard. To what degree, however, do these games tap into species'' economic decision-making? For the purpose of understanding the evolution of economic systems in humans, this is the key question. To study this, we can break economic decision-making down into smaller components, each of which is a potential step in the evolution of human economic behaviour. We can then use data from economic games, which are simplified, highly structured models of decision-making and therefore ideal for the comparative approach, to directly compare these components across species and contexts, as well as in relation to more naturalistic behaviours, to better understand the evolution of economic behaviour and the social and ecological contexts that influenced it. The comparative approach has successfully informed us about the evolution of other complex traits, such as language and morality, and should help us more deeply understand why and how human economic systems evolved.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

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.     

Complex cognition and behavioural innovation in New Caledonian crows

Apes, corvids and parrots all show high rates of behavioural innovation in the wild. However, it is unclear whether this innovative behaviour is underpinned by cognition more complex than simple learning mechanisms. To investigate this question we presented New Caledonian crows with a novel three-stage metatool problem. The task involved three distinct stages: (i) obtaining a short stick by pulling up a string, (ii) using the short stick as a metatool to extract a long stick from a toolbox, and finally (iii) using the long stick to extract food from a hole. Crows with previous experience of the behaviours in stages 1–3 linked them into a novel sequence to solve the problem on the first trial. Crows with experience of only using string and tools to access food also successfully solved the problem. This innovative use of established behaviours in novel contexts was not based on resurgence, chaining and conditional reinforcement. Instead, the performance was consistent with the transfer of an abstract, causal rule: ‘out-of-reach objects can be accessed using a tool’. This suggests that high innovation rates in the wild may reflect complex cognitive abilities that supplement basic learning mechanisms.     

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.     

Non-human primate token use shows possibilities but also limitations for establishing a form of currency

Non-human primates evaluate choices based on quantitative information and subjective valuation of options. Non-human primates can learn to value tokens as placeholders for primary rewards (such as food). With those tokens established as a potential form of ‘currency’, it is then possible to examine how they respond to opportunities to earn and use tokens in ways such as accumulating tokens or exchanging tokens with each other or with human experimenters to gain primary rewards. Sometimes, individuals make efficient and beneficial choices to obtain tokens and then exchange them at the right moments to gain optimal reward. Sometimes, they even accumulate such rewards through extended delay of gratification, or through other exchange-based interactions. Thus, non-human primates are capable of associating value to arbitrary tokens that may function as currency-like stimuli, but there also are strong limitations on how non-human primates can integrate such tokens into choice situations or use such tokens to fully ‘symbolize’ economic decision-making. These limitations are important to acknowledge when considering the evolutionary emergence of currency use in our species.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Implications of the behavioural immune system for social behaviour and human health in the modern world

The ‘behavioural immune system’ is composed of mechanisms that evolved as a means of facilitating behaviours that minimized infection risk and enhanced fitness. Recent empirical research on human populations suggests that these mechanisms have unique consequences for many aspects of human sociality—including sexual attitudes, gregariousness, xenophobia, conformity to majority opinion and conservative sociopolitical attitudes. Throughout much of human evolutionary history, these consequences may have had beneficial health implications; but health implications in modern human societies remain unclear. This article summarizes pertinent ways in which modern human societies are similar to and different from the ecologies within which the behavioural immune system evolved. By attending to these similarities and differences, we identify a set of plausible implications—both positive and negative—that the behavioural immune system may have on health outcomes in contemporary human contexts. We discuss both individual-level infection risk and population-level epidemiological outcomes. We also discuss a variety of additional implications, including compliance with public health policies, the adoption of novel therapeutic interventions and actual immunological functioning. Research on the behavioural immune system, and its implications in contemporary human societies, can provide unique insights into relationships between fitness, sociality and health.     

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’.     

Does signalling mitigate the cost of agonistic interactions? A test in a cricket that has lost its song

Prevailing models of animal communication assume that signalling during aggressive conflict mitigates the costs of fighting. We tested this assumption by staging dyadic encounters between male field crickets, Teleogryllus oceanicus, under three conditions: (i) both males could sing aggressive songs, (ii) neither male could sing, and (iii) one male could sing but the other could not. We conducted experiments on males from a Hawaiian population from Kauai that has recently evolved signal loss, and males from a Hawaiian population from the Big Island that has not. Among both populations, interactions between two silent males were characterized by higher levels of aggression than interactions involving one or two singing males. Because the level of aggression is strongly related to the cost of fighting, these data demonstrate that signalling mitigates the cost of fighting. In mixed trials, we found no statistically significant differences between the behaviour of calling and non-calling males in either population. We conclude that there is no evidence that the Kauai population exhibits special adaptations to alleviate the costs of signal loss. Finally, we found that males were much more likely to signal after their opponent''s retreat than after their own retreat. Aggressive song therefore meets the definition of a ‘victory display’.     

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.     

Context-dependent ‘safekeeping’ of foraging tools in New Caledonian crows

Several animal species use tools for foraging, such as sticks to extract embedded arthropods and honey, or stones to crack open nuts and eggs. While providing access to nutritious foods, these behaviours may incur significant costs, such as the time and energy spent searching for, manufacturing and transporting tools. These costs can be reduced by re-using tools, keeping them safe when not needed. We experimentally investigated what New Caledonian crows do with their tools between successive prey extractions, and whether they express tool ‘safekeeping’ behaviours more often when the costs (foraging at height), or likelihood (handling of demanding prey), of tool loss are high. Birds generally took care of their tools (84% of 176 prey extractions, nine subjects), either trapping them underfoot (74%) or storing them in holes (26%)—behaviours we also observed in the wild (19 cases, four subjects). Moreover, tool-handling behaviour was context-dependent, with subjects: keeping their tools safe significantly more often when foraging at height; and storing tools significantly more often in holes when extracting more demanding prey (under these conditions, foot-trapping proved challenging). In arboreal environments, safekeeping can prevent costly tool losses, removing a potentially important constraint on the evolution of habitual and complex tool behaviour.