Social learning of fear and safety is determined by the demonstrator's racial group

Social learning offers an efficient route through which humans and other animals learn about potential dangers in the environment. Such learning inherently relies on the transmission of social information and should imply selectivity in what to learn from whom. Here, we conducted two observational learning experiments to assess how humans learn about danger and safety from members (‘demonstrators'') of an other social group than their own. We show that both fear and safety learning from a racial in-group demonstrator was more potent than learning from a racial out-group demonstrator.     

Ecological validity of social interaction tests in rats and mice

Different rat and mouse models are used in studies of social interactions. Simple behavioral measures, which are commonly used in the laboratory, allow to perform relatively short experiments and to use multiple brain manipulation techniques. However, too much focus on the simplest behavioral models generates a serious risk of reducing ecological validity or even studying phenomena which would never happen outside of the laboratory. In this review, we discuss the suitability of mice and rats as model organisms for studying social behaviors, with focus on social transmission of fear paradigms. First, we briefly introduce the concept of domestication and what impact it had on laboratory rodents. Then, we present two aspects of social behaviors, sociability and dominance, which are crucial for social organization in these species. Finally, we present experimental models used for studying how animals transmit information about danger between each other, and how these models may reflect what happens in the natural environment. We discuss the difficulties that arise from our limited knowledge of rat and mouse ecology, especially their social life. We also explore the subject of balancing ecological validity and controllability in rodent models of social behaviors, the latter being particularly important for studying brain activity. Although it is very challenging, an efficient program for social neuroscience research should, in our opinion, aim at bridging the gap between laboratory and field studies.     

Reproductive state affects reliance on public information in sticklebacks

The degree to which animals use public and private sources of information has important implications for research in both evolutionary ecology and cultural evolution. While researchers are increasingly interested in the factors that lead individuals to vary in the manner in which they use different sources of information, to date little is known about how an animal''s reproductive state might affect its reliance on social learning. Here, we provide experimental evidence that in foraging ninespine sticklebacks (Pungitius pungitius), gravid females increase their reliance on public information generated by feeding demonstrators in choosing the richer of two prey patches than non-reproductive fish, while, in contrast, reproductive males stop using public information. Subsequent experiments revealed reproductive males to be more efficient asocial foragers, less risk-averse and generally less social than both reproductive females and non-reproductives. These findings are suggestive of adaptive switches in reliance on social and asocial sources of information with reproductive condition, and we discuss the differing costs of reproduction and the proximate mechanisms that may underlie these differences in information use. Our findings have important implications for our understanding of adaptive foraging strategies in animals and for understanding the way information diffuses through populations.     

Not just passengers: pigeons,Columba livia,can learn homing routes while flying with a more experienced conspecific

For animals that travel in groups, the directional choices of conspecifics are potentially a rich source of information for spatial learning. In this study, we investigate how the opportunity to follow a locally experienced demonstrator affects route learning by pigeons over repeated homing flights. This test of social influences on navigation takes advantage of the individually distinctive routes that pigeons establish when trained alone. We found that pigeons learn routes just as effectively while flying with a partner as control pigeons do while flying alone. However, rather than learning the exact route of the demonstrator, the paired routes shifted over repeated flights, which suggests that the birds with less local experience also took an active role in the navigational task. The efficiency of the original routes was a key factor in how far they shifted, with less efficient routes undergoing the greatest changes. In this context, inefficient routes are unlikely to be maintained through repeated rounds of social transmission, and instead more efficient routes are achieved because of the interaction between social learning and information pooling.     

Acquisition of flavour preferences in pigs through interactions with conspecifics that had previously consumed flavoured protein solutions

It is known that pigs can acquire flavour preferences by brief social interactions with conspecifics that previously consumed a flavoured solid feed. However, there is no information about whether a flavoured solution could support flavour preferences through social transmission. Ninety-six pigs (49 days old) were housed in 12 pens (8 pigs/pen). Four animals per pen were randomly selected to act as observers and four as demonstrators. Demonstrator animals were temporarily moved to an empty pen where a protein solution was offered (porcine digestive peptides (PDPs), 4% weight/volume) with the addition of 0.075% aniseed (six pens) or garlic (six pens) powdered artificial flavours for 30 min. Afterwards, demonstrators were returned to interact with observer animals for 30 min. A choice test (30 min) between aniseed and garlic PDP was performed for each observer group after the interaction. Observers showed a higher intake of solutions previously consumed by their demonstrator conspecifics (648 v. 468 ml; SEM 61.36, P < 0.05). As with flavoured solid feeds, protein solutions containing artificial flavours can create preferences in pigs for those flavours through social transmission from conspecifics.     

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.     

Review. The multiple roles of cultural transmission experiments in understanding human cultural evolution

In this paper, we explore how experimental studies of cultural transmission in adult humans can address general questions regarding the 'who, what, when and how' of human cultural transmission, and consequently inform a theory of human cultural evolution. Three methods are discussed. The transmission chain method, in which information is passed along linear chains of participants, has been used to identify content biases in cultural transmission. These concern the kind of information that is transmitted. Several such candidate content biases have now emerged from the experimental literature. The replacement method, in which participants in groups are gradually replaced or moved across groups, has been used to study phenomena such as cumulative cultural evolution, cultural group selection and cultural innovation. The closed-group method, in which participants learn in groups with no replacement, has been used to explore issues such as who people choose to learn from and when they learn culturally as opposed to individually. A number of the studies reviewed here have received relatively little attention within their own disciplines, but we suggest that these, and future experimental studies of cultural transmission that build on them, can play an important role in a broader science of cultural evolution.     

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.     

How social network structure affects decision-making in Drosophila melanogaster

Animals use a number of different mechanisms to acquire crucial information. During social encounters, animals can pass information from one to another but, ideally, they would only use information that benefits survival and reproduction. Therefore, individuals need to be able to determine the value of the information they receive. One cue can come from the behaviour of other individuals that are already using the information. Using a previous extended dataset, we studied how individual decision-making is influenced by the behaviour of conspecifics in Drosophila melanogaster. We analysed how uninformed flies acquire and later use information about oviposition site choice they learn from informed flies. Our results suggest that uninformed flies adjust their future choices based on how coordinated the behaviours of the informed individuals they encounter are. Following social interaction, uninformed flies tended either to collectively follow the choice of the informed flies or to avoid it. Using social network analysis, we show that this selective information use seems to be based on the level of homogeneity of the social network. In particular, we found that the variance of individual centrality parameters among informed flies was lower in the case of a ‘follow’ outcome compared with the case of an ‘avoid’ outcome.     

Simulated Trust: A cheap social learning strategy

Animals use heuristic strategies to determine from which conspecifics to learn socially. This leads to directed social learning. Directed social learning protects them from copying non-adaptive information. So far, the strategies of animals, leading to directed social learning, are assumed to rely on (possibly indirect) inferences about the demonstrator’s success. As an alternative to this assumption, we propose a strategy that only uses self-established estimates of the pay-offs of behavior. We evaluate the strategy in a number of agent-based simulations. Critically, the strategy’s success is warranted by the inclusion of an incremental learning mechanism. Our findings point out new theoretical opportunities to regulate social learning for animals. More broadly, our simulations emphasize the need to include a realistic learning mechanism in game-theoretic studies of social learning strategies, and call for re-evaluation of previous findings.     

Social learning of a brood parasite by its host

Arms races between brood parasites and their hosts provide model systems for studying the evolutionary repercussions of species interactions. However, how naive hosts identify brood parasites as enemies remains poorly understood, despite its ecological and evolutionary significance. Here, we investigate whether young, cuckoo-naive superb fairy-wrens, Malurus cyaneus, can learn to recognize cuckoos as a threat through social transmission of information. Naive individuals were initially unresponsive to a cuckoo specimen, but after observing conspecifics mob a cuckoo, they made more whining and mobbing alarm calls, and spent more time physically mobbing the cuckoo. This is the first direct evidence that naive hosts can learn to identify brood parasites as enemies via social learning.     

Natural pedagogy as evolutionary adaptation

We propose that the cognitive mechanisms that enable the transmission of cultural knowledge by communication between individuals constitute a system of 'natural pedagogy' in humans, and represent an evolutionary adaptation along the hominin lineage. We discuss three kinds of arguments that support this hypothesis. First, natural pedagogy is likely to be human-specific: while social learning and communication are both widespread in non-human animals, we know of no example of social learning by communication in any other species apart from humans. Second, natural pedagogy is universal: despite the huge variability in child-rearing practices, all human cultures rely on communication to transmit to novices a variety of different types of cultural knowledge, including information about artefact kinds, conventional behaviours, arbitrary referential symbols, cognitively opaque skills and know-how embedded in means-end actions. Third, the data available on early hominin technological culture are more compatible with the assumption that natural pedagogy was an independently selected adaptive cognitive system than considering it as a by-product of some other human-specific adaptation, such as language. By providing a qualitatively new type of social learning mechanism, natural pedagogy is not only the product but also one of the sources of the rich cultural heritage of our species.     

When to approach novel prey cues? Social learning strategies in frog-eating bats

Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.     

Avoidance of potentially harmful food cannot be socially transmitted between rats

The social transmission of food preferences(STFP) is a behavioural task of olfactory memory, in which an observer rat learns safe food odours from a demonstrator rat, and shows preference for this odour in a subsequent choice test. However, previous studies have failed to detect the transmission of information about food of potential danger and food aversion using STFP test. In this study, we tested how demonstrators' health affects the exchange of odour information and whether observers can learn danger information from an unhealthy demonstrator. As expected, the observer rat formed an odour preference after interacting with a demonstrator rat that had just eaten food containing a new odour, however, odour preference rather than aversion was also formed after interacting with a demonstrator rat injected with LiCl(used to induce gastric malaise). Furthermore, anaesthetized demonstrator rats and half-anaesthetized demonstrator rats, which showed obvious motor deficits suggesting an unhealthy state, also socially transmitted food preferences to observers. These results suggest that the social transmission of food preferences task is independent of a demonstrators' health, and that information about dangerous foods cannot be transmitted using this behavioural task.     

Social transmission of maladaptive information in the guppy

Many animals are capable of learning from others, a processreferred to as social learning. There is little doubt that acapacity for social learning is an adaptation and that it typicallyresults in adaptive behavior. What is less clear is whetherthere are circumstances under which social learning can resultin the transmission of outdated, inappropriate, or maladaptiveinformation. Here we report an experimental study that investigatedthe social learning and transmission of maladaptive foraginginformation through small social groups of guppies, Poeciliareticulata. This experiment used a transmission chain designin which fish in small founder groups were trained to take eitheran energetically costly circuitous route to a feeder or a lesscostly short route, with trained founder members gradually replacedby untrained conspecifics. Three days after all the foundershad been removed, the behavioral traditions of groups of untrainedfish were still strongly influenced by their founder's behavior.Moreover, the rate at which untrained subjects that shoaledwith founder conspecifics trained to take the long route learnedto take the short route was significantly slower than for fishforaging alone. The results provide unequivocal evidence thatmaladaptive information can be socially transmitted throughanimal populations and imply that socially learned informationcan inhibit learning of the optimal behavior pattern.     

Beyond existence and aiming outside the laboratory: estimating frequency-dependent and pay-off-biased social learning strategies

The existence of social learning has been confirmed in diverse taxa, from apes to guppies. In order to advance our understanding of the consequences of social transmission and evolution of behaviour, however, we require statistical tools that can distinguish among diverse social learning strategies. In this paper, we advance two main ideas. First, social learning is diverse, in the sense that individuals can take advantage of different kinds of information and combine them in different ways. Examining learning strategies for different information conditions illuminates the more detailed design of social learning. We construct and analyse an evolutionary model of diverse social learning heuristics, in order to generate predictions and illustrate the impact of design differences on an organism's fitness. Second, in order to eventually escape the laboratory and apply social learning models to natural behaviour, we require statistical methods that do not depend upon tight experimental control. Therefore, we examine strategic social learning in an experimental setting in which the social information itself is endogenous to the experimental group, as it is in natural settings. We develop statistical models for distinguishing among different strategic uses of social information. The experimental data strongly suggest that most participants employ a hierarchical strategy that uses both average observed pay-offs of options as well as frequency information, the same model predicted by our evolutionary analysis to dominate a wide range of conditions.     

Network-based diffusion analysis: a new method for detecting social learning

Social learning has been documented in a wide diversity of animals. In free-living animals, however, it has been difficult to discern whether animals learn socially by observing other group members or asocially by acquiring a new behaviour independently. We addressed this challenge by developing network-based diffusion analysis (NBDA), which analyses the spread of traits through animal groups and takes into account that social network structure directs social learning opportunities. NBDA fits agent-based models of social and asocial learning to the observed data using maximum-likelihood estimation. The underlying learning mechanism can then be identified using model selection based on the Akaike information criterion. We tested our method with artificially created learning data that are based on a real-world co-feeding network of macaques. NBDA is better able to discriminate between social and asocial learning in comparison with diffusion curve analysis, the main method that was previously applied in this context. NBDA thus offers a new, more reliable statistical test of learning mechanisms. In addition, it can be used to address a wide range of questions related to social learning, such as identifying behavioural strategies used by animals when deciding whom to copy.     

Social foraging: individual learning and cultural transmission of innovations

We present two stochastic models of individual and social learningthat count the number of individuals exhibiting a learned, resource-producingtrait in a group of social foragers. The novelty of our modelingresults from incorporating the empirically based assumptionthat rates of both individual and social learning should dependon the frequency of the learned trait within the group. Whenresources occur as clumps shared by group members, a naive individual'sacquisition of the skill required for clump discovery/productionshould involve opposing processes of frequency dependence. Theopportunity to learn via cultural transmission should increasewith the trait's frequency, but the opportunity for learningindividually should decrease as the trait's frequency increases.The results of the model suggest that the evolution of the capacityfor cultural transmission may be promoted in environments wherescrounging at resource clumps inhibits rates of individual learning.     

Shoal and prey patch choice by co-occurring fishes and prawns: inter-taxa use of socially transmitted cues

Animals can use socially transmitted information to learn about the distribution and quality of resources without incurring the costs associated with having to search for and sample them first hand. Recently, it has been shown that the use of chemical social information specific to patterns of diet and habitat use is an important mechanism underpinning recognition and social organization in shoaling fishes. In this study we revealed that the use of resource-specific chemical information is not limited to conspecifics, or even members of the same taxon. In a series of laboratory experiments, we showed that threespine sticklebacks (Gasterosteus aculeatus) could recognize similar patterns of habitat use in common prawns (Leander serratus), preferentially orientating towards groups of prawns exposed to the same habitats as themselves, and even selecting foraging patches located close to them. Prawns were seen to use habitat-specific cues generated by conspecifics, but not by sticklebacks, suggesting that the benefits of forming these heterospecific social association patterns may be unequal for prawns and fishes. Our findings suggest that some species might use co-occurring, unrelated species as information centres in order to orient and locate resources within their surroundings.     

The Effect of Familiarity with Demonstrators on Social Learning in Three‐Spined Sticklebacks (Gasterosteus aculeatus)

Social learning is an important process in the spread of information, especially in changing environments where inherited behaviors may not remain relevant. In many species, the decision of whom to trust to have reliable information depends on the relationship between individuals. Many fish species, including three‐spined sticklebacks, preferentially associate with familiar individuals. Previous studies in three‐spined sticklebacks have provided mixed evidence about the effect of familiarity on social learning in this species. Therefore, this study further explores familiarity and social learning in sticklebacks, specifically from a demonstrator‐focused perspective. We found that in a food patch discrimination task, individuals with unfamiliar demonstrators performed significantly better than those with familiar demonstrators. In a problem‐solving task, we found that focal fish attended to the behavior of demonstrators, but we did not detect an effect of familiarity on performance, and indeed the proportion of individuals to solve the task after observing demonstrators was low. These results suggest that sticklebacks have a preference for unfamiliar demonstrators, but that the use of social information varies depending on context.