How social experience shapes song representation in the brain of starlings

Birdsong, like speech, is a learned behaviour whose critical function is to communicate with others and whose development critically depends on social influences. Song learning is a complex phenomenon that involves not only the development of species-specific vocalisations, but also the development of the ability to organise these vocalisations and to use them in an appropriate context. Although the fact that interactions with adult experienced models are essential for song production to develop properly has been well established, far less is known about song perception and processing. The fact that songbirds learn to vocalise and to use their vocalisations selectively through interactions with adults questions whether such interactions are also required for songbirds to perceive and process their vocalisations selectively and whether social interactions may shape song perception and processing as they shape song production. In order to address these questions, our team uses an original neuroethological approach to study the neural bases of song behaviour in a highly social songbird species: the European starlings. We provide here a synthesis of the results we have obtained using this approach over the last decade. Our results show that direct social experience with adult experienced models not only shapes song behaviour but also shapes these songbirds’ brains and their ability to perceive and to process acoustic signals whose communicative value, as well as their acoustic structure, have to be learned.     

Social ageing: exploring the drivers of late-life changes in social behaviour in mammals

Social interactions help group-living organisms cope with socio-environmental challenges and are central to survival and reproductive success. Recent research has shown that social behaviour and relationships can change across the lifespan, a phenomenon referred to as ‘social ageing’. Given the importance of social integration for health and well-being, age-dependent changes in social behaviour can modulate how fitness changes with age and may be an important source of unexplained variation in individual patterns of senescence. However, integrating social behaviour into ageing research requires a deeper understanding of the causes and consequences of age-based changes in social behaviour. Here, we provide an overview of the drivers of late-life changes in sociality. We suggest that explanations for social ageing can be categorized into three groups: changes in sociality that (a) occur as a result of senescence; (b) result from adaptations to ameliorate the negative effects of senescence; and/or (c) result from positive effects of age and demographic changes. Quantifying the relative contribution of these processes to late-life changes in sociality will allow us to move towards a more holistic understanding of how and why these patterns emerge and will provide important insights into the potential for social ageing to delay or accelerate other patterns of senescence.     

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’.     

Effects of provisioning on the social behaviour of Japanese and rhesus macaques: Implications for socioecology

Long-term studies have shown remarkable similarity in the social behaviour and relationships of Japanese and rhesus macaques living in free-ranging groups. The vast majority of these studies have been of provisioned groups and many key principles have been derived from them. Provisioning is known to influence various aspects of life history and demography, as well as quantitative aspects of social behaviour, such as the frequencies of grooming and aggression. It has been widely assumed, however, that the fundamental characteristics of social behaviour and relationships observed in provisioned populations are representative of those that would occur under natural conditions. This paper reviews findings from fieldwork on Japanese macaques living under natural conditions, and compares them with patterns of social behaviour reported by multiple studies of provisioned groups of both species. Differences are apparent in the nature of social relationships between adult females, between adult males, and between adult males and females. Some of these differences can be attributed to the increased levels of aggression associated with provisioning. Others appear to be related to demographic peculiarities of provisioned groups, such as large size and skewed sex ratio. These differences can be used to generate predictions concerning the influence of ecological variables on the dynamics of social relationships and social structure. Ways in which these predictions could be tested by further fieldwork on provisioned and natural populations are discussed.     

Longevity and ageing: appraising the evolutionary consequences of growing old

Senescence or ageing is an increase in mortality and/or decline in fertility with increasing age. Evolutionary theories predict that ageing or longevity evolves in response to patterns of extrinsic mortality or intrinsic damage. If ageing is viewed as the outcome of the processes of behaviour, growth and reproduction then it should be possible to predict mortality rate. Recent developments have shown that it is now possible to integrate these ecological and physiological processes and predict the shape of mortality trajectories. By drawing on the key exciting developments in the cellular, physiological and ecological process of longevity the evolutionary consequences of ageing are reviewed. In presenting these ideas an evolutionary demographic framework is used to argue how trade-offs in life-history strategies are important in the maintenance of variation in longevity within and between species. Evolutionary processes associated with longevity have an important role in explaining levels of biological diversity and speciation. In particular, the effects of life-history trait trade-offs in maintaining and promoting species diversity are explored. Such trade-offs can alleviate the effects of intense competition between species and promote species coexistence and diversification. These results have important implications for understanding a number of core ecological processes such as how species are divided among niches, how closely related species co-occur and the rules by which species assemble into food-webs. Theoretical work reveals that the proximate physiological processes are as important as the ecological factors in explaining the variation in the evolution of longevity. Possible future research challenges integrating work on the evolution and mechanisms of growing old are briefly discussed.     

Social Dominance in a Gregarious Bird is Related to Body Size But not to Standard Personality Assays

The recent growth of research on animal personality could provide new insights into our understanding of sociality and the structure of animal groups. Although simple assays of the type commonly used to study animal personality have been shown to correlate with social aggressiveness in some bird species, conflicting empirical results do not yet make it clear when such assays, typically using isolated individuals, predict behaviour within social groups. We measured aggressiveness in groups of a very gregarious species, the common waxbill (Estrilda astrild), and performed five commonly used behavioural assays on the same individuals: tonic immobility, mirror test, novel object test, open‐field test and a variant of the latter in an enriched environment. We found that larger individuals were more dominant and that differences in aggressiveness were repeatable. None of the traditional behavioural assays were related to aggressiveness or dominance. Standard personality assays may fail to capture individual differences relevant to predict social behaviour, and we discuss biological and methodological explanations for these results, such as social behaviour being in part an emergent property of groups rather than an intrinsic property of individuals, or gregarious species being particularly sensitive to the conditions of standard personality assays that test individuals alone.     

The evolution of social behaviour in Blaberid cockroaches with diverse habitats and social systems: phylogenetic analysis of behavioural sequences

The adequacy and utility of behavioural characters in phylogenetics is widely acknowledged, especially for stereotyped behaviours. However, the most common behaviours are not stereotyped, and these are usually seen as inappropriate or more difficult to analyze in a phylogenetic context. A few methods have been proposed to deal with such data, although they have never been tested on samples larger than six species, which limits their evolutionary interest. In the present study, we perform behavioural observations on 13 cockroach species and derive behavioural phylogenetic characters with the successive event‐pairing method. We combine these characters with morphological and molecular data (approximately 6800 bp) in a phylogenetic study of 41 species. We then reconstruct ancestral states of the behavioural data to study evolution of social behaviour in these insects with regard to their social systems (i.e. solitary, gregarious, and subsocial) and diversity of habitat choice. We report for the first time that nonstereotyped behavioural data are adequate for phylogenetic analyses: they are no more homoplastic than traditional data, and support several phylogenetic relationships that we discuss. From an evolutionary perspective, we show that the solitary species Thanatophyllum akinetum does not display original behavioural interactions, suggesting phylogenetic inertia of interactive behaviours despite a radical change in social structure. Conversely, the subsocial species Parasphaeria boleiriana shows original behavioural interactions, which could result from its peculiar social system or habitat. We conclude that phylogenetic approaches in studies of behaviour are useful for deciphering evolution of behaviour and discriminating between its different modalities, even for nonstereotyped characters. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 58–77.     

Experimental Manipulation of Food Accessibility Affects Conflict Management Behaviour in Ravens

Conflict management strategies such as reconciliation and bystander affiliation have been described for a variety of species. A common determinant seems to be a ‘complex’ social life, with individuals relying on affiliate relationships or social bonds. Little is known, however, about the strategic and flexible use of conflict management skills in experimental settings in species other than primates. We here investigated conflict and post‐conflict behaviour of ravens by manipulating the accessibility of food and, thus, the likelihood of aggressive interactions while foraging. Specifically, we presented birds with a certain amount of highly preferred food that varied in the number of pieces (one piece, two pieces or, as a control, small pieces matching the number of participating birds) and observed their agonistic behaviour during feeding and their affiliative behaviour afterwards. The results showed that high levels of conflicts during feeding in the 1‐piece and 2‐piece conditions led to high levels of affiliation after feeding. Depending on the experimental condition, this effect is best explained (a) by the affiliative behaviour of former aggressors (1‐piece condition) and (b) by the affiliation directed to the receivers of aggression after feeding (2‐piece condition). Those dyads that engaged in allo‐preening after feeding also engaged in allo‐preening outside the experimental setting, suggesting that socially bonded individuals provided third‐party affiliation to victims of aggression. Moreover, socially bonded ravens fed close to each other in the experiment when food was clumped, indicating that they actively coordinated their behaviour when there was a high conflict potential. Taken together, these findings support the assumption that ravens use their social bonds to avoid conflicts by choosing with whom to feed, and to buffer effects of conflicts by engaging in third‐party affiliation as post‐conflict behaviour.     

A comparison of pectoral fin contact between two different wild dolphin populations

Contact behaviour involving the pectoral fin has been documented in a number of dolphin species, and various explanations about its function have been offered. Pectoral fin contact can take a variety of forms, and involves a number of body parts and movements, likely differing depending upon social or ecological context. For this study, we compare the pectoral fin contact behaviour of two species of wild dolphins: Indo-Pacific bottlenose dolphins (Tursiops aduncus) from around Mikura Island, Japan, and Atlantic spotted dolphins (Stenella frontalis) from The Bahamas. The two study populations exhibit surprising similarity in the ways in which pectoral fin contacts are used, despite differences in species and environmental conditions at the two sites. Differences in contact rates for calves between the two sites suggest that calf-focused aggression from adult dolphins is more prevalent at Mikura than in The Bahamas. Our results suggest that pectoral fin contact behaviour seems to be driven primarily by social pressures, and may be similar in function to allogrooming described in primates.     

Social structure and indirect genetic effects: genetics of social behaviour

The social environment modulates gene expression, physiology, behaviour and patterns of inheritance. For more than 50 years, this concept has been investigated using approaches that include partitioning the social component out of behavioural heritability estimates, studying maternal effects on offspring, and analysing dominance hierarchies. Recent advances have formalized this ‘social environment effect’ by providing a more nuanced approach to the study of social influences on behaviour while recognizing evolutionary implications. Yet, in most of these formulations, the dynamics of social interactions are not accounted for. Also, the reciprocity between individual behaviour and group‐level interactions has been largely ignored. Consistent with evolutionary theory, the principles of social interaction are conserved across a broad range of taxa. While noting parallels in diverse organisms, this review uses Drosophila melanogaster as a case study to revisit what is known about social interaction paradigms. We highlight the benefits of integrating the history and pattern of interactions among individuals for dissecting molecular mechanisms that underlie social modulation of behaviour.     

Social molecular pathways and the evolution of bee societies

Bees provide an excellent model with which to study the neuronal and molecular modifications associated with the evolution of sociality because relatively closely related species differ profoundly in social behaviour, from solitary to highly social. The recent development of powerful genomic tools and resources has set the stage for studying the social behaviour of bees in molecular terms. We review 'ground plan' and 'genetic toolkit' models which hypothesize that discrete pathways or sets of genes that regulate fundamental behavioural and physiological processes in solitary species have been co-opted to regulate complex social behaviours in social species. We further develop these models and propose that these conserved pathways and genes may be incorporated into 'social pathways', which consist of relatively independent modules involved in social signal detection, integration and processing within the nervous and endocrine systems, and subsequent behavioural outputs. Modifications within modules or in their connections result in the evolution of novel behavioural patterns. We describe how the evolution of pheromonal regulation of social pathways may lead to the expression of behaviour under new social contexts, and review plasticity in circadian rhythms as an example for a social pathway with a modular structure.     

Social flexibility in a primitively social allodapine bee (Hymenoptera: Apidae): results of a translocation experiment

Many species of social animals are known to exhibit intraspecific variation in social traits between different populations. In the social insects, geographically separate populations may show wide-ranging forms of social behaviour, presumably because of variation in environmental parameters such as climate. For example, several bee species are known to exhibit eusocial or solitary behaviour depending on the latitude or altitude of the population. However, there is little or no empirical evidence to determine if this variation is a result of behavioural plasticity or long-term adaptation to local conditions, both of which have implications for the evolution of sociality. In this study, colonies of the allodapine bees Exoneura robusta and E. nigrescens were translocated between a montane and heathland habitat in southern Australia to assess the effect of habitat change on social behaviour. Results indicate that brood development in translocated colonies of both species differed from control colonies, leading to opportunities for different forms of social behaviour. However, there was also a high degree of variation within each habitat, suggesting an influence of both within and between habitat factors.     

Ultrasound and mating behaviour in rodents with some observations on other behavioural situations

Ultrasounds have been detected during mating behaviour in all 11 species of myomorph rodents in which this behaviour has been observed. The signals produced by each of the species studied are described. In all species except hamsters, these signals appear to be produced by the male. Ultrasounds have also been detected from rodents in other situations such as during and after disturbance and when placed in new surroundings. The possible significance of these ultrasonic signals in the lives of rodents is discussed.     

Ultrasound and aggressive behaviour in rats and other small mammals

Aggressive behaviour has been observed in rats, Rattus norvegicus, and fourteen other species of small mammals. Ultrasounds were detected during aggressive behaviour in at least seven of these species, and in rats two distinct types of signal were recorded. Short ultrasounds of 3 to 65 ms duration and at frequencies of about 50 kHz were produced in aggressive situations, while long pulses up to 3400 ms duration and at about 25 kHz appeared to be synchronous with the long exhalations of submissive rats. Aggressive behaviour was reduced in encounters where long pulses were emitted. The physical characteristics of the ultrasounds produced by the different species are described and the importance of these signals in the establishment and maintenance of social relationships in small mammals is discussed.     

Information transfer about food locations is not a benefit of group living in the solitary foraging striped mouse (Rhabdomys pumilio)

The benefits of group living have primarily been investigated in species which form permanent groups. There are, however, several species that forage alone but still form groups that share the same territory and nest. One of these group-living solitary foragers is the striped mouse (Rhabdomys pumilio) from the Succulent Karoo in South Africa. I performed field experiments on this species to investigate the hypothesis that mice benefit from group living by exchanging information in social groups about the location and availability of food sources. Presenting additional food sources in the field altered individual foraging decisions. A mouse that found food at one location visited it again the next day; other mice of the same group did not arrive, however. Establishment of permanent feeding stations for 1 week affected individual foraging even 1 week after termination of feeding, a result demonstrating the strong effect trapping can have on the behaviour of study species. Results from this study suggest that information transfer about good food sources was of little importance in the evolution of group living in the striped mouse.     

Heaven it's my wife! Male canaries conceal extra-pair courtships but increase aggressions when their mate watches

Many animals live in a communication network, an environment where individuals can obtain information about competitors or potential mates by observing interactions between conspecifics. In such an environment, interactants might benefit by changing their signalling behaviour in the presence of an audience. This audience effect seems widespread among species, has been observed during various types of interaction (e.g. intra-sexual vs. inter-sexual interaction) and varies according to the social context (e.g. gender, hierarchical or mating status of the audience). However, the way individuals might adapt their signalling behaviour to a combination of these factors remains poorly understood. To address this question, we studied how the presence of an audience affects the behaviour of male domestic canaries Serinus canaria during two types of interactions: (i) an extra-pair interaction and (ii) a male-male competition for food. Males were observed under three conditions: (a) in the absence of audience, (b) in the presence of their mate or (c) of a familiar female. Our results show that male domestic canaries minutely adapt their courting and agonistic behaviours to a combination of: (i) the type of interaction (extra-pair interaction/male-male competition), (ii) the social context (mate, familiar female or nobody in audience) and (iii) the behaviours of both the audience and the interactant. These results highlight the ability of animals to subtly adapt their behaviour to the social environment. This also raises questions about the cognitive foundations and evolution of these processes especially considering that canaries are known neither for having high cognitive abilities nor for being a typical example for the social intelligence hypothesis.     

Conflicting social norms and community conservation compliance

Though the success of conservation initiatives relies on changing behaviour, little social psychological research has examined factors such as attitudes and social norms in the context of actual conservation campaigns. In the context of reducing light pollution around sea turtle nesting habitats, researching technological solutions has clear merit. Problems such as light glow are, however, fundamentally about human behaviour, and so finding ways to effect behavioural change is critical. Social norms, or perceptions about what other people think and do, have been widely used in behaviour change campaigns across various domains, including campaigns to promote conservation behaviour. Here, we investigate how the norms of different groups may influence our behaviour in the context of a campaign to alter behavioural norms about light glow pollution in a community. We examine attitudes, social norms, and the degree of conflict (versus congruence) between the behaviours of different groups, and their relationship with intentions to engage in conservation behaviours relevant to sea turtle conservation. We show that attitudes and norms are related to behavioural intentions, and conflicts between social norms influence intentions, over and above the norms themselves. This highlights an important consideration for conservation campaigns utilising social norms-based behaviour change appeals.     

Oxytocin, vasopressin and pair bonding: implications for autism

Understanding the neurobiological substrates regulating normal social behaviours may provide valuable insights in human behaviour, including developmental disorders such as autism that are characterized by pervasive deficits in social behaviour. Here, we review the literature which suggests that the neuropeptides oxytocin and vasopressin play critical roles in modulating social behaviours, with a focus on their role in the regulation of social bonding in monogamous rodents. Oxytocin and vasopressin contribute to a wide variety of social behaviours, including social recognition, communication, parental care, territorial aggression and social bonding. The effects of these two neuropeptides are species-specific and depend on species-specific receptor distributions in the brain. Comparative studies in voles with divergent social structures have revealed some of the neural and genetic mechanisms of social-bonding behaviour. Prairie voles are socially monogamous; males and females form long-term pair bonds, establish a nest site and rear their offspring together. In contrast, montane and meadow voles do not form a bond with a mate and only the females take part in rearing the young. Species differences in the density of receptors for oxytocin and vasopressin in ventral forebrain reward circuitry differentially reinforce social-bonding behaviour in the two species. High levels of oxytocin receptor (OTR) in the nucleus accumbens and high levels of vasopressin 1a receptor (V1aR) in the ventral pallidum contribute to monogamous social structure in the prairie vole. While little is known about the genetic factors contributing to species-differences in OTR distribution, the species-specific distribution pattern of the V1aR is determined in part by a species-specific repetitive element, or 'microsatellite', in the 5' regulatory region of the gene encoding V1aR (avpr1a). This microsatellite is highly expanded in the prairie vole (as well as the monogamous pine vole) compared to a very short version in the promiscuous montane and meadow voles. These species differences in microsatellite sequence are sufficient to change gene expression in cell culture. Within the prairie vole species, intraspecific variation in the microsatellite also modulates gene expression in vitro as well as receptor distribution patterns in vivo and influences the probability of social approach and bonding behaviour. Similar genetic variation in the human AVPR1A may contribute to variations in human social behaviour, including extremes outside the normal range of behaviour and those found in autism spectrum disorders. In sum, comparative studies in pair-bonding rodents have revealed neural and genetic mechanisms contributing to social-bonding behaviour. These studies have generated testable hypotheses regarding the motivational systems and underlying molecular neurobiology involved in social engagement and social bond formation that may have important implications for the core social deficits characterizing autism spectrum disorders.     

The social brain: allowing humans to boldly go where no other species has been

The biological basis of complex human social interaction and communication has been illuminated through a coming together of various methods and disciplines. Among these are comparative studies of other species, studies of disorders of social cognition and developmental psychology. The use of neuroimaging and computational models has given weight to speculations about the evolution of social behaviour and culture in human societies. We highlight some networks of the social brain relevant to two-person interactions and consider the social signals between interacting partners that activate these networks. We make a case for distinguishing between signals that automatically trigger interaction and cooperation and ostensive signals that are used deliberately. We suggest that this ostensive signalling is needed for ‘closing the loop’ in two-person interactions, where the partners each know that they have the intention to communicate. The use of deliberate social signals can serve to increase reputation and trust and facilitates teaching. This is likely to be a critical factor in the steep cultural ascent of mankind.     

Social behaviour in a web-building lynx spider, Tapinillus sp. (Araneae: Oxyopidae)

Social behaviour involving cooperative prey capture and communal feeding is reported for the first time in the spider family Oxyopidae (lynx spiders), in a web-building species of the genus Tapinillus. This social spider inhabits communal webs that may contain several dozen individuals, including adults of both sexes and juveniles of different cohorts. Its colonies occur in clusters and appear to be long-lived, much like those of non-territorial permanently social species such as Anelosimus eximius (Theridiidae) or Agelena consociata (Agelenidae). However, unlike colonies of these other cooperative spiders, the colonies of the social Tapinillus do not have highly female-biased sex ratios. The possible explanations for this difference are discussed.