Competitive advantage of rare behaviours induces adaptive diversity rather than social conformity in skill learning.

Recent studies have emphasized the role of social learning and cultural transmission in promoting conformity and uniformity in animal groups, but little attention has been given to the role of negative frequency-dependent learning in impeding conformity and promoting diversity instead. Here, we show experimentally that under competitive conditions that are common in nature, social foragers (although capable of social learning) are likely to develop diversity in foraging specialization rather than uniformity. Naive house sparrows that were introduced into groups of foraging specialists did not conform to the behaviour of the specialists, but rather learned to use the alternative food-related cues, thus forming groups of complementary specialists. We further show that individuals in such groups may forage more effectively in diverse environments. Our results suggest that when the benefit from socially acquired skills diminishes through competition in a negative frequency-dependent manner, animal societies will become behaviourally diverse rather than uniform.

Follow (or don't follow) the crowd: Young children's conformity is influenced by norm domain and age.

This study investigated whether young children's conformity to a consensus varies across the normative domain and age. A total of 168 3- and 5-year-olds participated. Each child was presented with a puzzle box that had two transparent compartments. In a reward preference condition, one of the compartments contained 1 sticker, whereas the other compartment contained 12 stickers. In perceptual judgment and arbitrary preference conditions, one compartment contained a short plank, whereas one contained a perceptually longer plank. Each child was shown a video of four female adults, each of whom was asked the same question within condition: "Which one's the biggest?" (perceptual task; each model retrieved the smaller block), "Which one do you want?" (reward preference; each model retrieved the smaller reward), and "Which one do you want?" (arbitrary preference; each model retrieved the smaller plank). Children were then asked the same question by condition and were allowed to retrieve the item. Notably, more children conformed in the arbitrary preference condition than in the reward preference and perceptual judgment conditions, with 3-year-olds conforming significantly more than 5-year-olds. The 5-year-olds were more successful and imitated with greater fidelity, including demonstrating overimitation. However, less overimitation was observed in the arbitrary preference condition. Together, these findings show that children are sensitive to the contextual cues of the domain in which they are witnessing norms and vary their own conformity based on such cues. Furthermore, children can navigate which information to copy to fulfil their own ends.

Selectivity in social and asocial learning: investigating the prevalence, effect and development of young children's learning preferences.

Culture evolution requires both modification and faithful replication of behaviour, thus it is essential to understand how individuals choose between social and asocial learning. In a quasi-experimental design, 3- and 5-year-olds (176), and adults (52) were presented individually with two novel artificial fruits, and told of the apparatus' relative difficulty (easy versus hard). Participants were asked if they wanted to attempt the task themselves or watch an experimenter attempt it first; and then had their preference either met or violated. A significant proportion of children and adults (74%) chose to learn socially. For children, this request was efficient, as observing a demonstration made them significantly quicker at the task than learning asocially. However, for 5-year-olds, children who selected asocial learning were also found to be highly efficient at the task, showing that by 5 years children are selective in choosing a learning strategy that is effective for them. Adults further evidenced this trend, and also showed selectivity based on task difficulty. This is the first study to examine the rates, performance outcomes and developmental trajectory of preferences in asocial and social learning, ultimately informing our understanding of innovation.

How the cascading effects of a single behavioral trait can generate personality.

INDIVIDUALS FROM THE SAME POPULATION GENERALLY VARY IN SUITES OF CORRELATED BEHAVIORAL TRAITS: personality. Yet, the strength of the behavioral correlations sometimes differs among populations and environmental conditions, suggesting that single underlying mechanisms, such as genetic constraints, cannot account for them. We propose, instead, that such suites of correlated traits may arise when a single key behavior has multiple cascading effects on several other behaviors through affecting the range of options available. For instance, an individual's shyness can constrain its habitat choice, which, in turn, could restrict the expression of other behavioral traits. We hypothesize that shy individuals should be especially restrained in their choice of habitat when the risk of predation is high, which then canalizes them into different behavioral options making them appear behaviorally distinct from bolder individuals. We test this idea using an individual-based simulation model. Our results show that individual differences in boldness can be sufficient, under high predation pressure, to generate behavioral correlations between boldness and both the tendency to aggregate and the propensity to use social information. Thus, our findings support the idea that some behavioral syndromes can be, at least to some extent, labile. Our model further predicts that such cascading effects should be more pronounced in populations with a long history of predation, which are expected to exhibit a low average boldness level, compared with predator-naïve populations.

The effect of exploration on the use of producer-scrounger tactics.

Individuals foraging in groups can use two different tactics for obtaining food resources. Individuals can either search for food sources themselves (producing) or they can join food discoveries of others (scrounging). In this study we use a genetic algorithm in a spatially explicit producer-scrounger game to explore how individuals compromise between exploration (an important axis of animal personality) and scrounging and how characteristics of the environment affect this compromise. Agents varied in exploration and scrounging and a genetic algorithm searched for the optimal combination of exploration and scrounging. The foraging environments featured different levels of patch richness, predation and patch density. Our simulations show that under conditions of low patch densities slow exploring scroungers were favored whereas high patch density favored fast exploring individuals that either produced (at low patch richness) or scrounged (at high patch richness). In high predation environments fast exploring individuals were selected for but only at low to intermediate patch densities. Predation did not affect scrounging behavior. We did not find a divergence of exploration 'types' within a given environment, but there was a general association between exploration and scrounging across different environments: high rates of scrounging were observed over nearly the full spectrum of exploration values, whereas high rates of producing were only observed at high exploration values, suggesting that cases in which slow explorers start producing should be rare. Our results indicate that the spatial arrangement of food resources can affect the optimal social attraction rules between agents, the optimality of foraging tactic and the interaction between both.

Frequency-dependent payoffs and sequential decision-making favour consistent tactic use.

Although natural selection should have favoured individuals capable of adjusting the weight they give to personal and social information according to circumstances, individuals generally differ consistently in their individual weighting of both types of information. Such individual differences are correlated with personality traits, suggesting that personality could directly affect individuals' ability to collect personal or social information. Alternatively, the link between personality and information use could simply emerge as a by-product of the sequential decision-making process in a frequency-dependent context. Indeed, when the gains associated with behavioural options depend on the choices of others, an individual's sequence of arrival could constrain its choice of options leading to the emergence of correlated behaviours. Any factor such as personality that affects decision order could thus be correlated with information use. To test this new explanation, we developed an individual-based model that simulates a group of animals engaged in a game of sequential frequency-dependent decision: a producer-scrounger game. Our results confirm that the sequence of decision, in this case enforced by the order in which animals enter a foraging area, consistently influences their mean tactic use and their individual plasticity, an outcome reminiscent of the correlation reported between personality and social information use.

Exploring the costs and benefits of social information use: an appraisal of current experimental evidence.

Research on social learning has focused traditionally on whether animals possess the cognitive ability to learn novel motor patterns from tutors. More recently, social learning has included the use of others as sources of inadvertent social information. This type of social learning seems more taxonomically widespread and its use can more readily be approached as an economic decision. Social sampling information, however, can be tricky to use and calls for a more lucid appraisal of its costs. In this four-part review, we address these costs. Firstly, we address the possibility that only a fraction of group members are actually providing social information at any one time. Secondly, we review experimental research which shows that animals are circumspect about social information use. Thirdly, we consider the cases where social information can lead to incorrect decisions and finally, we review studies investigating the effect of social information quality. We address the possibility that using social information or not is not a binary decision and present results of a study showing that nutmeg mannikins combine both sources of information, a condition that can lead to the establishment of informational cascades. We discuss the importance of empirically investigating the economics of social information use.

Individual differences in plasticity and sampling when playing behavioural games.

When engaged in behavioural games, animals can adjust their use of alternative tactics until groups reach stable equilibria. Recent theory on behavioural plasticity in games predicts that individuals should differ in their plasticity or responsiveness and hence in their degree of behavioural adjustment. Moreover, individuals are predicted to be consistent in their plasticity within and across biological contexts. These predictions have yet to be tested empirically and so we examine the behavioural adjustment of individual nutmeg mannikins (Lonchura punctulata), gregarious ground-feeding passerines, when playing two different social foraging games: producer-scrounger (PS) and patch-choice (PC) games. We found: (i) significant individual differences in plasticity and sampling behaviour in each of the two games, (ii) individual differences in sampling behaviour were consistent over different test conditions within a game (PC) and over a six month period (PS), (iii) but neither individual plasticity nor sampling behaviour was correlated from one social foraging game to another. The rate at which birds sampled alternative tactics was positively associated with seed intake in PS trials but negatively associated in PC trials. These results suggest that games with frequency dependence of pay-offs can maintain differences in behavioural plasticity but that an important component of this plasticity is group- and/or context-specific.

Does foraging behaviour affect female mate preferences and pair formation in captive zebra finches?

BACKGROUND: Successful foraging is essential for survival and reproductive success. In many bird species, foraging is a learned behaviour. To cope with environmental change and survive periods in which regular foods are scarce, the ability to solve novel foraging problems by learning new foraging techniques can be crucial. Although females have been shown to prefer more efficient foragers, the effect of males' foraging techniques on female mate choice has never been studied. We tested whether females would prefer males showing the same learned foraging technique as they had been exposed to as juveniles, or whether females would prefer males that showed a complementary foraging technique. METHODOLOGY/PRINCIPAL FINDINGS: We first trained juvenile male and female zebra finches (Taeniopygia guttata) to obtain a significant proportion of their food by one of two foraging techniques. We then tested whether females showed a preference for males with the same or the alternative technique. We found that neither a male's foraging technique nor his foraging performance affected the time females spent in his proximity in the mate-choice apparatus. We then released flocks of these finches into an aviary to investigate whether assortative pairing would be facilitated by birds taught the same technique exploiting the same habitat. Zebra finches trained as juveniles in a specific foraging technique maintained their foraging specialisation in the aviary as adults. However, pair formation and nest location were random with regard to foraging technique. CONCLUSIONS/SIGNIFICANCE: Our findings show that zebra finches can be successfully trained to be foraging specialists. However, the robust negative results of the conditions tested here suggest that learned foraging specializations do not affect mate choice or pair formation in our experimental context.

Learning in a game context: strategy choice by some keeps learning from evolving in others.

Behavioural decisions in a social context commonly have frequency-dependent outcomes and so require analysis using evolutionary game theory. Learning provides a mechanism for tracking changing conditions and it has frequently been predicted to supplant fixed behaviour in shifting environments; yet few studies have examined the evolution of learning specifically in a game-theoretic context. We present a model that examines the evolution of learning in a frequency-dependent context created by a producer-scrounger game, where producers search for their own resources and scroungers usurp the discoveries of producers. We ask whether a learning mutant that can optimize its use of producer and scrounger to local conditions can invade a population of non-learning individuals that play producer and scrounger with fixed probabilities. We find that learning provides an initial advantage but never evolves to fixation. Once a stable equilibrium is attained, the population is always made up of a majority of fixed players and a minority of learning individuals. This result is robust to variation in the initial proportion of fixed individuals, the rate of within- and between-generation environmental change, and population size. Such learning polymorphisms will manifest themselves in a wide range of contexts, providing an important element leading to behavioural syndromes.

Altruistic defence behaviours in aphids.

BACKGROUND: Altruistic anti-predatory behaviours pose an evolutionary problem because they are costly to the actor and beneficial to the recipients. Altruistic behaviours can evolve through indirect fitness benefits when directed toward kin. The altruistic nature of anti-predatory behaviours is often difficult to establish because the actor can obtain direct fitness benefits, or the behaviour could result from selfish coercion by others, especially in eusocial animals. Non-eusocial parthenogenetically reproducing aphids form colonies of clone-mates, which are ideal to test the altruistic nature of anti-predatory defence behaviours. Many aphids release cornicle secretions when attacked by natural enemies such as parasitoids. These secretions contain an alarm pheromone that alerts neighbours (clone-mates) of danger, thereby providing indirect fitness benefits to the actor. However, contact with cornicle secretions also hampers an attacker and could provide direct fitness to the actor. RESULTS: We tested the hypothesis that cornicle secretions are altruistic by assessing direct and indirect fitness consequences of smearing cornicle secretions onto an attacker, and by manipulating the number of clone-mates that could benefit from the behaviour. We observed parasitoids, Aphidius rhopalosiphi, foraging singly in patches of the cereal aphid Sitobion avenae of varied patch size (2, 6, and 12 aphids). Aphids that smeared parasitoids did not benefit from a reduced probability of parasitism, or increase the parasitoids' handling time. Smeared parasitoids, however, spent proportionately more time grooming and less time foraging, which resulted in a decreased host-encounter and oviposition rate within the host patch. In addition, individual smearing rate increased with the number of clone-mates in the colony. CONCLUSIONS: Cornicle secretions of aphids were altruistic against parasitoids, as they provided no direct fitness benefits to secretion-releasing individuals, only indirect fitness benefits through neighbouring clone-mates. Moreover, the use of cornicle secretions was consistent with their altruistic nature, because the occurrence of this behaviour increased with the size of indirect fitness benefits, the number of clone-mates that can benefit. This study provides evidence for a case of kin-directed altruistic defence outside eusocial animals.

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.

Testing competing measures of profitability for mobile resources.

Optimal diet theory often fails to predict a forager's diet choice when prey are mobile. Because they escape or defend themselves, mobile prey are likely to increase the forager's handling time, thereby decreasing its fitness gain rate. Many animals have been shown to select their prey so as to maximize either their fitness gain or their fitness gain rate. However, no study has yet compared directly these two measures of profitability by generating testable predictions about the choice of the forager. Under laboratory conditions, we compared these two measures of profitability, using the aphid parasitoid Aphidius colemani and its host, Myzus persicae. Fitness gain was calculated for parasitoids developing in each host instar by measuring life-history traits such as developmental time, sex ratio and fecundity. Fitness gain rate was estimated by dividing fitness gain by handling time, the time required to subdue the host. Fourth instar aphids provided the best fitness gain to parasitoids, whereas second instar aphids were the most profitable in terms of fitness gain rate. Host choice tests showed that A. colemani females preferred second instar hosts, suggesting that their decision maximizes fitness gain rate over fitness gain. Our results indicate that fitness gain rate is a reliable predictor of animal's choice for foragers exploiting resources that impose additional time cost due to their mobility.

Inadvertent social information in breeding site selection of natal dispersing birds.

Several species use the number of young produced as public information (PI) to assess breeding site quality. PI is inaccessible for synchronously breeding birds because nests are empty by the time the young can collect this information. We investigate if location cues are the next best source of inadvertent social information (ISI) used by young prospectors during breeding site choice. We experimentally deployed ISI as decoys and song playbacks of breeding males in suitable and sub-optimal habitats during pre- and post-breeding periods, and monitored territory establishment during the subsequent breeding season for a social, bobolink (Dolichonyx oryzivorus), and a more solitary species, Nelson's sharp-tailed sparrow (Ammodramus nelsoni). The sparrows did not respond to treatments, but bobolinks responded strongly to post-breeding location cues, irrespective of habitat quality. The following year, 17/20 sub-optimal plots to which bobolink males were recruited were defended for at least two weeks, indicating that song heard the previous year could exert a "carry-over attraction" effect on conspecifics the following year. Sixteen recruited males were natal dispersers, as expected when animals have little opportunity to directly sample their natal habitat quality. We suggest that differences in breeding synchronicity may induce an equivalent clinal distribution of ISI use.

Information and its use by animals in evolutionary ecology.

Information is a crucial currency for animals from both a behavioural and evolutionary perspective. Adaptive behaviour relies upon accurate estimation of relevant ecological parameters; the better informed an individual, the better it can develop and adjust its behaviour to meet the demands of a variable world. Here, we focus on the burgeoning interest in the impact of ecological uncertainty on adaptation, and the means by which it can be reduced by gathering information, from both 'passive' and 'responsive' sources. Our overview demonstrates the value of adopting an explicitly informational approach, and highlights the components that one needs to develop useful approaches to studying information use by animals. We propose a quantitative framework, based on statistical decision theory, for analysing animal information use in evolutionary ecology. Our purpose is to promote an integrative approach to studying information use by animals, which is itself integral to adaptive animal behaviour and organismal biology.

Distraction sneakers decrease the expected level of aggression within groups: a game-theoretic model.

Hawk-dove games have been extensively used to predict the conditions under which group-living animals should defend their resources against potential usurpers. Typically, game-theoretic models on aggression consider that resource defense may entail energetic and injury costs. However, intruders may also take advantage of owners who are busy fighting to sneak access to unguarded resources, imposing thereby an additional cost on the use of the escalated hawk strategy. In this article we modify the two-strategy hawk-dove game into a three-strategy hawk-dove-sneaker game that incorporates a distraction-sneaking tactic, allowing us to explore its consequences on the expected level of aggression within groups. Our model predicts a lower proportion of hawks and hence lower frequencies of aggressive interactions within groups than do previous two-strategy hawk-dove games. The extent to which distraction sneakers decrease the frequency of aggression within groups, however, depends on whether they search only for opportunities to join resources uncovered by other group members or for both unchallenged resources and opportunities to usurp.

Public information: from nosy neighbors to cultural evolution.

Psychologists, economists, and advertising moguls have long known that human decision-making is strongly influenced by the behavior of others. A rapidly accumulating body of evidence suggests that the same is true in animals. Individuals can use information arising from cues inadvertently produced by the behavior of other individuals with similar requirements. Many of these cues provide public information about the quality of alternatives. The use of public information is taxonomically widespread and can enhance fitness. Public information can lead to cultural evolution, which we suggest may then affect biological evolution.

Introduction: ecology and the central nervous system.

Behavioral ecology, the study of the survival value or function of behavior, has developed for a time by confining cognition to convenient black boxes that were assumed to be rigged by natural selection to direct an animal to the right decision for a given set of circumstances. However, the interpretation of test results concerning functional hypotheses about behavior depends crucially on assumptions made about their ability to collect and process information: cognition. Clearly, progress in behavioral ecology requires that the cognitive black boxes be opened and studied. This need coincides with an explosive growth of interest in animal cognition that has promoted and enhanced the level of interaction between behavioral ecologists and animal cognition scientists. The result promises to be profitable to the extent that it will raise interest and research in a number of new areas such as the costs in terms of survival value of evolving increased cognitive capacity or even the possibility of exploring brain morphology using a functional approach.