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.     

The adaptive value of sociality in mammalian groups

According to behavioural ecology theory, sociality evolves when the net benefits of close association with conspecifics exceed the costs. The nature and relative magnitude of the benefits and costs of sociality are expected to vary across species and habitats. When sociality is favoured, animals may form groups that range from small pair-bonded units to huge aggregations. The size and composition of social groups have diverse effects on morphology and behaviour, ranging from the extent of sexual dimorphism to brain size, and the structure of social relationships. This general argument implies that sociality has fitness consequences for individuals. However, for most mammalian species, especially long-lived animals like primates, there are sizable gaps in the chain of evidence that links sociality and social bonds to fitness outcomes. These gaps reflect the difficulty of quantifying the cumulative effects of behavioural interactions on fitness and the lack of information about the nature of social relationships among individuals in most taxa. Here, I review what is known about the reproductive consequences of sociality for mammals.     

A review of the evolutionary causes of rodent group-living

I analyze and summarize the empirical evidence supporting alternative hypotheses posed to explain the evolution of rodent group-living. Eight hypotheses are considered: two rely on net fitness benefits to individuals, five rely on ecological and life-history constraints, and one uses elements of both. I expose the logic behind each hypothesis, identify its key predictions, examine how the available evidence on rodent socioecology supports or rejects its predictions, and identify some priorities for future research. I show that empirical support for most hypotheses is meager due to a lack of relevant studies. Also, empirical support for a particular hypothesis, when it exists, comes from studies of the same species used to formulate the original hypothesis. Two exceptions are the hypothesis that individual rodents live in groups to reduce their predation risk and the hypothesis that group-living was adopted by individuals to reduce their cost of thermoregulation. Finally, most hypotheses have been examined without regard to competing hypotheses and often in a restricted taxonomic context. This is clearly an unfortunate situation given that most competing hypotheses are not mutually exclusive. I suggest that in the future comparative approaches should be used. These studies should examine simultaneously the relevance of different benefits and constraints hypothesized to explain the evolution of rodent sociality.     

Endocrinology of sociality: Comparisons between sociable and solitary individuals within the same population of African striped mice

The social organization of species ranges from solitary-living to complex social groups. While the evolutionary reasons of group-living are well studied, the physiological mechanisms underlying alternative social systems are poorly understood. By studying group-living and solitary individuals of the same species, we can determine hormonal correlates of sociality without the problem of confounding phylogenetic factors. The African striped mouse (Rhabdomys pumilio) is a socially flexible species, which can be solitary or alternatively form complex family groups, depending on population density and the extent of reproductive competition. We predicted group-living striped mice to show signs of reproductive suppression and social stress, resulting in higher corticosterone but lower testosterone levels when compared to solitary-living individuals. To determine whether differences in social organization correlated with hormonal differences, we collected blood samples from free-living striped mice during four breeding seasons when we experimentally induced solitary-living in philopatric individuals by locally reducing population density. Striped mice that were group-living did not change their corticosterone or estosterone levels during the study, indicating that there was no temporal effect during the breeding season. Striped mice of both sexes had significantly lower corticosterone levels after switching from group- to solitary-living. Solitary males – but not solitary females – had higher testosterone levels than group-living conspecifics. Our results suggest that group-living results in physiological stress and can induce reproductive suppression, at least in philopatric males. The switch to solitary-living may thus be a tactic to avoid reproductive competition within groups, and is associated with decreased stress hormone levels and onset of independent reproduction.     

Reconciling conflicts in a one-male society: the case of geladas (<Emphasis Type="Italic">Theropithecus gelada</Emphasis>)

Animals derive benefits from living in social groups but sociality also has its costs in that animals must compete with others for resources and mating opportunities. To cope with the conflict aftermath and social damage caused by competitive aggression, several group-living species use a variety of peace-keeping strategies. The affinitive post-conflict reunion of former opponents, defined as reconciliation, is the primary peace-keeping mechanism. In this study, we provide evidence for the occurrence of reconciliation and test some hypotheses on this post-conflict mechanism in geladas (Theropithecus gelada), a species often neglected in the study of post-conflict dynamics. The conciliatory contacts were uniformly distributed across the different sex–class combinations. Different from baboons, geladas did not show any particular kind of affinitive reconciliation behaviour. Notwithstanding the presence of a linear hierarchy, the dominance relationships did not affect the reconciliation dynamics. According to the valuable relationship hypothesis, coalitionary support seems to be a good predictor for a high level of conciliatory contacts. Finally, at an immediate level reconciliation plays a role in reducing renewed attacks by aggressors, which sought conciliatory contact more frequently than victims. In conclusion, even though the study of post-conflict behaviour in geladas needs to be continued, the patchy nature of their social network is a good model for testing some of the theoretical assumptions about primate conflict resolution.     

Sociality in the Australian Allodapine Bee Brevineura elongata: Small Colony Sizes Despite Large Benefits to Group Living

Allodapine bees (family Apidae, subfamily Xylocopinae) provide substantial material for investigating the evolution of sociality because of their wide variation in colony size, life history traits, and caste differentiation. Two recent studies have shown that the Australian allodapine genus Brevineura exhibits a strong increase in per capita brood production (PCBP) in social colonies compared to single-female nests. However both species previously examined, B. xanthoclypeata and B. froggatti, show relatively few multi-female nests, which is puzzling considering the apparently large advantages for group-living in these species. Here we show that in a third species, B. elongata, there are also substantial benefits for group living, involving increased PCBP and a greatly reduced likelihood of nests without brood. As expected from these observations, we also found strongly female biased sex allocation. Nevertheless only a small percentage of nests contained more than one adult female, similar to the other two Brevineura species, raising the question of why multifemale colonies are not more common in this genus. Solving this puzzle will throw light on conditions that constrain sociality when group living apparently provides major advantages.     

Group living in squamate reptiles: a review of evidence for stable aggregations

How sociality evolves and is maintained remains a key question in evolutionary biology. Most studies to date have focused on insects, birds, and mammals but data from a wider range of taxonomic groups are essential to identify general patterns and processes. The extent of social behaviour among squamate reptiles is under‐appreciated, yet they are a promising group for further studies. Living in aggregations is posited as an important step in the evolution of more complex sociality. We review data on aggregations among squamates and find evidence for some form of aggregations in 94 species across 22 families. Of these, 18 species across 7 families exhibited ‘stable’ aggregations that entail overlapping home ranges and stable membership in long‐term (years) or seasonal aggregations. Phylogenetic analysis suggests that stable aggregations have evolved multiple times in squamates. We: (i) identify significant gaps in our understanding; (ii) outline key traits which should be the focus of future research; and (iii) outline the potential for utilising reproductive skew theory to provide insights into squamate sociality.     

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.     

Is sociality required for the evolution of communicative complexity? Evidence weighed against alternative hypotheses in diverse taxonomic groups

Complex social communication is expected to evolve whenever animals engage in many and varied social interactions; that is, sociality should promote communicative complexity. Yet, informal comparisons among phylogenetically independent taxonomic groups seem to cast doubt on the putative role of social factors in the evolution of complex communication. Here, we provide a formal test of the sociality hypothesis alongside alternative explanations for the evolution of communicative complexity. We compiled data documenting variations in signal complexity among closely related species for several case study groups--ants, frogs, lizards and birds--and used new phylogenetic methods to investigate the factors underlying communication evolution. Social factors were only implicated in the evolution of complex visual signals in lizards. Ecology, and to some degree allometry, were most likely explanations for complexity in the vocal signals of frogs (ecology) and birds (ecology and allometry). There was some evidence for adaptive evolution in the pheromone complexity of ants, although no compelling selection pressure was identified. For most taxa, phylogenetic null models were consistently ranked above adaptive models and, for some taxa, signal complexity seems to have accumulated in species via incremental or random changes over long periods of evolutionary time. Becoming social presumably leads to the origin of social communication in animals, but its subsequent influence on the trajectory of signal evolution has been neither clear-cut nor general among taxonomic groups.     

Early Social Networks Predict Survival in Wild Bottlenose Dolphins

A fundamental question concerning group-living species is what factors influence the evolution of sociality. Although several studies link adult social bonds to fitness, social patterns and relationships are often formed early in life and are also likely to have fitness consequences, particularly in species with lengthy developmental periods, extensive social learning, and early social bond-formation. In a longitudinal study of bottlenose dolphins (Tursiops sp.), calf social network structure, specifically the metric eigenvector centrality, predicted juvenile survival in males. Additionally, male calves that died post-weaning had stronger ties to juvenile males than surviving male calves, suggesting that juvenile males impose fitness costs on their younger counterparts. Our study indicates that selection is acting on social traits early in life and highlights the need to examine the costs and benefits of social bonds during formative life history stages.     

The weight of the clan: Even in insects, social isolation can induce a behavioural syndrome

Social isolation has dramatic consequences on the development of individuals of many vertebrate species, and it induces a set of behavioural disturbances rending them unable to process environmental as well as social stimuli appropriately. We hypothesized that isolation syndrome is a ubiquitous trait of social life that can be observed in a wide array of species, including invertebrates. Here we report that gregarious cockroaches (Blattella germanica) reared in isolation showed (i) stronger exploration-avoidance, (ii) reduced foraging activity, (iii) reduced willingness to interact socially, and (iv) reduced ability to assess mating partner quality than conspecifics reared in groups. We demonstrate the occurrence of a behavioural syndrome induced by social isolation, similar to syndromes described in vertebrates, revealing the importance of social interactions and group-living in this non-eusocial insect species. We suggest that investigating social isolation effects on individual development should provide interesting results to assess social cohesion of species and thus constitute an additional tool for comparative studies focusing on the evolution of social life.     

Preparing for battle? Potential intergroup conflict promotes current intragroup affiliation

Groups of human soldiers increase their affiliative behaviour when moving into combat zones. Despite numerous other species also competing as groups, little is known about how potential intergroup conflict might influence current intragroup affiliative behaviour in non-human animals. Here, I show that allopreening (when one individual preens another) increases in groups of cooperatively breeding green woodhoopoes (Phoeniculus purpureus) when they enter areas where conflicts with neighbours are more likely. Self-preening, which is an indicator of stress in other species, did not increase in conflict areas, suggesting that the change in affiliative behaviour is not the simple consequence of greater stress. Instead, because it is the dominant breeding pair that increase their preening of subordinate helpers, it is possible that current affiliative behaviour is being exchanged for agonistic support in any intergroup conflicts that might ensue. These results are important for our understanding of group dynamics, cooperation and the evolution of sociality, but also bring to mind the intriguing possibilities of social contracts and future planning in birds.     

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.     

Dynamic interactions among badgers: implications for sociality and disease transmission

1. Direct interactions between individuals play an important part in the sociality of group-living animals, their mating system and disease transmission. Here, we devise a methodology to quantify relative rates of proximity interaction from radio-tracking data and highlight potential asymmetries within the contact network of a moderate-density badger population in the north-east of England. 2. We analysed radio-tracking data from four contiguous social groups, collected over a 3-year period. Dynamic interaction analysis of badger dyads was used to assess the movement of individuals in relation to the movement of others, both within and between social groups. Dyads were assessed with regard to season, sex, age and sett use pattern of the badgers involved. 3. Intragroup separation distances were significantly shorter than intergroup separation distances, and interactions between groups were rare. Within groups, individuals interacted with each other more often than expected, and interaction patterns varied significantly with season and sett use pattern. Non-mover dyads (using the main sett for day-resting on > 50% of occasions) interacted more frequently than mover dyads (using an outlier sett for day-resting on > 50% of occasions) or mover-non-mover dyads. Interactions between group members occurred most frequently in winter. 4. Of close intragroup interactions (< 50 m separation distance), 88.6% were associated with a main sett and only 4.4% with outlier setts. Non-mover dyads and non-mover-mover dyads interacted significantly more often at the main sett than mover-only dyads. These results highlight the importance of the main sett to badger sociality and support the suggestion that badger social groups are comprised of different subgroups, in our case based on differential sett use patterns. 5. Asymmetries in contact structure within a population will affect the way in which diseases are transmitted through a social network. Assessment of these networks is essential for understanding the persistence and spread of disease within populations which do not mix freely or which exhibit heterogeneities in their spatial or social behaviour.     

Group-living and the richness of the parasite fauna in Canadian freshwater fishes

Summary An increased transmission of ectoparasites among individual animals is considered to be an inevitable cost of living in groups, since several kinds of ectoparasites require close proximity between large numbers of hosts for successful transmission. However, we do not know whether individuals belonging to group-living species incur a greater risk of ectoparasitism than individuals of solitary species. Here, using published data from 3 families (60 species) of Canadian freshwater fishes, I test the hypothesis that group-living species are host to more species of contagious ectoparasites (copepods and monogeneans) than solitary host species. As the different fish species have been studied with varying intensity, I used the mean number of parasite species recorded per study as a standard measure of parasite numbers. Multiple regression analyses were performed separately for each family to determine the effects of group-living and of 3 other variables (host size, age, and range) on the richness of the recorded parasite fauna. Once the effects of the other variables were removed, I found no significant effect of sociality on the richness of the parasite fauna per fish species, for contagious ectoparasites and other types of parasites. Neither of the other variables had any influence on the numbers of parasite species per fish species. These results suggest that a richer ectoparasite fauna is not a cost of group-living in fishes.     

Wild justice and fair play: cooperation,forgiveness, and morality in animals

In this paper I argue that we can learn much about ‘wild justice’ and the evolutionary origins of social morality – behaving fairly – by studying social play behavior in group-living animals, and that interdisciplinary cooperation will help immensely. In our efforts to learn more about the evolution of morality we need to broaden our comparative research to include animals other than non-human primates. If one is a good Darwinian, it is premature to claim that only humans can be empathic and moral beings. By asking the question ‘What is it like to be another animal?’ we can discover rules of engagement that guide animals in their social encounters. When I study dogs, for example, I try to be a ‘dogocentrist’ and practice ‘dogomorphism.’ My major arguments center on the following ‘big’ questions: Can animals be moral beings or do they merely act as if they are? What are the evolutionary roots of cooperation, fairness, trust, forgiveness, and morality? What do animals do when they engage in social play? How do animals negotiate agreements to cooperate, to forgive, to behave fairly, to develop trust? Can animals forgive? Why cooperate and play fairly? Why did play evolve as it has? Does ‘being fair’ mean being more fit – do individual variations in play influence an individual's reproductive fitness, are more virtuous individuals more fit than less virtuous individuals? What is the taxonomic distribution of cognitive skills and emotional capacities necessary for individuals to be able to behave fairly, to empathize, to behave morally? Can we use information about moral behavior in animals to help us understand ourselves? I conclude that there is strong selection for cooperative fair play in which individuals establish and maintain a social contract to play because there are mutual benefits when individuals adopt this strategy and group stability may be also be fostered. Numerous mechanisms have evolved to facilitate the initiation and maintenance of social play to keep others engaged, so that agreeing to play fairly and the resulting benefits of doing so can be readily achieved. I also claim that the ability to make accurate predictions about what an individual is likely to do in a given social situation is a useful litmus test for explaining what might be happening in an individual's brain during social encounters, and that intentional or representational explanations are often important for making these predictions.     

Grooming in Barbary macaques: better to give than to receive?

It is well established that grooming underpins sociality in group-living primates, and a number of studies have documented the stress-reducing effects of being groomed. In this study, we quantified grooming behaviour and physiological stress (assessed by faecal glucocorticoid analysis) in free-ranging Barbary macaques, Macaca sylvanus. Our results indicate that it is the giving rather than the receiving of grooming that is associated with lower stress levels. These findings shed important new light on the benefits of this key behaviour in primate social life.     

Social trajectories and the evolution of social behavior

Current research on the evolution of sociality seeks to integrate a wealth of species-specific studies to draw more generalized conclusions. Developing a unified theory of social evolution has been a challenging process, hampered by the inherent complexity of social systems. By viewing a species' social structure as the result of a series, or "trajectory", of decisions individuals make about whether or not to disperse from their natal territory, whether to co-breed or refrain from breeding, and whether or not to provide alloparental care, we can more easily evaluate whether selective factors influencing each social decision are similar across taxa. At the same time, the social trajectory framework highlights the interrelationships among different social decisions, both throughout the life of an individual and over evolutionary time. There are likely to be multiple unifying themes within sociality research; we hope that the simple framework outlined here will promote exchange between researchers across taxonomic disciplines to begin to identify common principles.     

The functions of societies and the evolution of group living: spider societies as a test case

Many models have been advanced to suggest how different expressions of sociality have evolved and are maintained. However these models ignore the function of groups for the particular species in question. Here we present a new perspective on sociality where the function of the group takes a central role. We argue that sociality may have primarily a reproductive, protective, or foraging function, depending on whether it enhances the reproductive, protective or foraging aspect of the animal's life (sociality may serve a mixture of these functions). Different functions can potentially cause the development of the same social behaviour. By identifying which function influences a particular social behaviour we can determine how that social behaviour will change with changing conditions, and which models are most pertinent. To test our approach we examined spider sociality, which has often been seen as the poor cousin to insect sociality. By using our approach we found that the group characteristics of eusocial insects is largely governed by the reproductive function of their groups, while the group characteristics of social spiders is largely governed by the foraging function of the group. This means that models relevant to insects may not be relevant to spiders. It also explains why eusocial insects have developed a strict caste system while spider societies are more egalitarian. We also used our approach to explain the differences between different types of spider groups. For example, differences in the characteristics of colonial and kleptoparasitic groups can be explained by differences in foraging methods, while differences between colonial and cooperative spiders can be explained by the role of the reproductive function in the formation of cooperative spider groups. Although the interactions within cooperative spider colonies are largely those of a foraging society, demographic traits and colony dynamics are strongly influenced by the reproductive function. We argue that functional explanations help to understand the social structure of spider groups and therefore the evolutionary potential for speciation in social spiders.