Cooperative breeding and monogamy in mammalian societies

Comparative studies of social insects and birds show that the evolution of cooperative and eusocial breeding systems has been confined to species where females mate completely or almost exclusively with a single male, indicating that high levels of average kinship between group members are necessary for the evolution of reproductive altruism. In this paper, we show that in mammals, the evolution of cooperative breeding has been restricted to socially monogamous species which currently represent 5 per cent of all mammalian species. Since extra-pair paternity is relatively uncommon in socially monogamous and cooperatively breeding mammals, our analyses support the suggestion that high levels of average kinship between group members have played an important role in the evolution of cooperative breeding in non-human mammals, as well as in birds and insects.     

Primate socioecology at the crossroads: Past, present, and future

Attempts to explain differences in the size and structure of primate groups have argued that they are a consequence of variation in the intensity of feeding competition caused by contrasts in food distribution. However, although feeding competition can limit the size of female groups, many other factors affect the costs and the benefits of sociality to females and contribute to differences in group size. Moreover, interspecific differences in social relationships between females, in female philopatry, and in kinship between group members appear to be more closely associated with variation in life‐history parameters, reproductive strategies, and phylogeny than with contrasts in food distribution or feeding competition. The mismatch between predictions of socioecological theory and observed variation in primate social behavior has led to protracted arguments about the future of primate socioecology. We argue that future attempts to understand the diversity of primate societies need to be based on an approach that explores separate explanations for different components of social organization, combines ecological and phylogenetic information, and integrates research on primates with similar studies of other groups of mammals. © 2012 Wiley Periodicals, Inc.     

Both social and ecological factors predict ungulate brain size

Among mammals, the members of some Orders have relatively large brains. Alternative explanations for this have emphasized either social or ecological selection pressures favouring greater information-processing capacities, including large group size, greater foraging efficiency, higher innovation rates, better invasion success and complex problem solving. However, the focal taxa for these analyses (primates, carnivores and birds) often show both varied ecological competence and social complexity. Here, we focus on the specific relationship between social complexity and brain size in ungulates, a group with relatively simple patterns of resource use, but extremely varied social behaviours. The statistical approach we used, phylogenetic generalized least squares, showed that relative brain size was independently associated with sociality and social complexity as well as with habitat use, while relative neocortex size is associated with social but not ecological factors. A simple index of sociality was a better predictor of both total brain and neocortex size than group size, which may indicate that the cognitive demands of sociality depend on the nature of social relationships as well as the total number of individuals in a group.     

Communicative roots of complex sociality and cognition

Mammals living in more complex social groups typically have large brains for their body size and many researchers have proposed that the primary driver of the increase in brain size through primate and hominin evolution was the selection pressures associated with sociality. Many mammals, and especially primates, use flexible signals that show a high degree of voluntary control and these signals may play an important role in forming and maintaining social relationships between group members. However, the specific role that cognitive skills play in this complex communication, and how in turn this relates to sociality, is still unclear. The hypothesis for the communicative roots of complex sociality and cognition posits that cognitive demands behind the communication needed to form and maintain bonded social relationships in complex social settings drives the link between brain size and sociality. We review the evidence in support of this hypothesis and why key features of cognitively complex communication such as intentionality and referentiality should be more effective in forming and maintaining bonded relationships as compared with less cognitively complex communication. Exploring the link between cognition, communication and sociality provides insights into how increasing flexibility in communication can facilitate the emergence of social systems characterised by bonded social relationships, such as those found in non‐human primates and humans. To move the field forward and carry out both within‐ and among‐species comparisons, we advocate the use of social network analysis, which provides a novel way to describe and compare social structure. Using this approach can lead to a new, systematic way of examining social and communicative complexity across species, something that is lacking in current comparative studies of social structure.     

Detecting instability in animal social networks: genetic fragmentation is associated with social instability in rhesus macaques

The persistence of biological systems requires evolved mechanisms which promote stability. Cohesive primate social groups are one example of stable biological systems, which persist in spite of regular conflict. We suggest that genetic relatedness and its associated kinship structure are a potential source of stability in primate social groups as kinship structure is an important organizing principle in many animal societies. We investigated the effect of average genetic relatedness per matrilineal family on the stability of matrilineal grooming and agonistic interactions in 48 matrilines from seven captive groups of rhesus macaques. Matrilines with low average genetic relatedness show increased family-level instability such as: more sub-grouping in their matrilineal groom network, more frequent fighting with kin, and higher rates of wounding. Family-level instability in multiple matrilines within a group is further associated with group-level instability such as increased wounding. Stability appears to arise from the presence of clear matrilineal structure in the rhesus macaque group hierarchy, which is derived from cohesion among kin in their affiliative and agonistic interactions with each other. We conclude that genetic relatedness and kinship structure are an important source of group stability in animal societies, particularly when dominance and/or affilative interactions are typically governed by kinship.     

Feedback loop between kinship and dominance: the macaque model

There is growing evidence that macaque social systems represent sets of coadapted traits in which strength of hierarchies and degree of nepotism covary. A framework is developed to explain the link between dominance and kinship phenomena, assuming that power brought by alliances among non-kin is allometrically related to those involving relatives. This can account for the type of social relationships observed in "despotic" systems vs. "egalitarian" ones. When social bonds are mostly founded on kinship, lineages are closed and social power generated by coalitions among relatives may reach high levels; social power frequently outweighs the fighting abilities of single individuals, and asymmetry of dominance between group members may be marked. When lineages are more open, social bonds and alliances are less kin-biased, social relationships are more equal, and as the influence of coalitions is less important, the individual retains a certain degree of freedom in relation to the power of kin-networks. Acknowledging that the balance between individual and social power is not set at the same level across different species can explain a number of variations in rules of rank inheritance and relative dominance of males and females among macaques. The framework illustrates how epigenetic processes may shape complex features of primate social systems, and offers opportunities for testing.     

Society, demography and genetic structure in the spotted hyena

Spotted hyenas (Crocuta crocuta) are large mammalian carnivores, but their societies, called 'clans', resemble those of such cercopithecine primates as baboons and macaques with respect to their size, hierarchical structure, and frequency of social interaction among both kin and unrelated group-mates. However, in contrast to cercopithecine primates, spotted hyenas regularly hunt antelope and compete with group-mates for access to kills, which are extremely rich food sources, but also rare and ephemeral. This unique occurrence of baboon-like sociality among top-level predators has favoured the evolution of many unusual traits in this species. We briefly review the relevant socio-ecology of spotted hyenas, document great demographic variation but little variation in social structure across the species' range, and describe the long-term fitness consequences of rank-related variation in resource access among clan-mates. We then summarize patterns of genetic relatedness within and between clans, including some from a population that had recently gone through a population bottleneck, and consider the roles of sexually dimorphic dispersal and female mate choice in the generation of these patterns. Finally, we apply social network theory under varying regimes of resource availability to analyse the effects of kinship on the stability of social relationships among members of one large hyena clan in Kenya. Although social bonds among both kin and non-kin are weakest when resource competition is most intense, hyenas sustain strong social relationships with kin year-round, despite constraints imposed by resource limitation. Our analyses suggest that selection might act on both individuals and matrilineal kin groups within clans containing multiple matrilines.     

Emergence of complex social networks from spatial structure and rules of thumb: a modelling approach

Individual-based computer models show that simple heuristic governing individuals’ behavior may suffice to generate complex patterns of social behavior at the group level such as those observed in animal societies. ‘GrooFiWorld’ is an example of such kind of computer models. In this model, self-organization and simple behavioral rules generate complex patterns of social behavior like those described in tolerant and intolerant societies of macaques. Social complexity results from the socio-spatial structure of the group, the nature of which is, in turn, a side-effect of intensity of aggression. The model suggests that a similar mechanism may give rise to complex social structures in macaques. It is, however, unknown if the spatial structure of the model and that of macaques are indeed similar. Here we used social networks analysis as a proxy for spatial structure of the group. Our findings show that the social networks of the model share similar qualitative features with those of macaques. As group size increases, the density and the average individual eigenvector centrality decrease and the modularity and centralization of the network increase. In social networks emerging from simulations resembling intolerant societies the density is lower, the modularity and centralization are higher, and the individuals ranking higher in the dominance hierarchy are more central than in the social networks emerging from simulations resembling egalitarian societies. Given the qualitative similarity between the social networks of the model and that of empirical data, our results suggest that the spatial structure of macaques is similar to that of the model. It seems thus plausible that, as in the model, the spatial structure combined with simple behavioral rules plays a role in the emergence of complex social networks and complex social behavior in macaques.     

Family feuds: social competition and sexual conflict in complex societies

Darwin was initially puzzled by the processes that led to ornamentation in males-what he termed sexual selection-and those that led to extreme cooperation and altruism in complex animal societies-what was later termed kin selection. Here, I explore the relationships between sexual and kin selection theory by examining how social competition for reproductive opportunities-particularly in females-and sexual conflict over mating partners are inherent and critical parts of complex altruistic societies. I argue that (i) patterns of reproductive sharing within complex societies can drive levels of social competition and reproductive conflict not only in males but also in females living in social groups, and ultimately the evolution of female traits such as ornaments and armaments; (ii) mating conflict over female choice of sexual partners can influence kin structure within groups and drive the evolution of complex societies; and (iii) patterns of reproductive sharing and conflict among females may also drive the evolution of complex societies by influencing kin structure within groups. Ultimately, complex societies exhibiting altruistic behaviour appear to have only arisen in taxa where social competition over reproductive opportunities and sexual conflict over mating partners were low. Once such societies evolved, there were important selective feedbacks on traits used to regulate and mediate intra-sexual competition over reproductive opportunities, particularly in females.     

Kinship shapes affiliative social networks but not aggression in ring-tailed coatis

Animal groups typically contain individuals with varying degrees of genetic relatedness, and this variation in kinship has a major influence on patterns of aggression and affiliative behaviors. This link between kinship and social behavior underlies socioecological models which have been developed to explain how and why different types of animal societies evolve. We tested if kinship and age-sex class homophily in two groups of ring-tailed coatis (Nasua nasua) predicted the network structure of three different social behaviors: 1) association, 2) grooming, and 3) aggression. Each group was studied during two consecutive years, resulting in four group-years available for analysis (total of 65 individuals). Association patterns were heavily influenced by agonistic interactions which typically occurred during feeding competition. Grooming networks were shaped by mother-offspring bonds, female-female social relationships, and a strong social attraction to adult males. Mother-offspring pairs were more likely to associate and groom each other, but relatedness had no effect on patterns of aggressive behavior. Additionally, kinship had little to no effect on coalitionary support during agonistic interactions. Adult females commonly came to the aid of juveniles during fights with other group members, but females often supported juveniles who were not their offspring (57% of coalitionary interactions). These patterns did not conform to predictions from socioecological models.     

Between-Group Variation in Female Dispersal,Kin Composition of Groups,and Proximity Patterns in a Black-and-White Colobus Monkey (Colobus vellerosus)

A growing body of evidence shows within-population variation in natal dispersal, but the effects of such variation on social relationships and the kin composition of groups remain poorly understood. We investigate the link between dispersal, the kin composition of groups, and proximity patterns in a population of black-and-white colobus (Colobus vellerosus) that shows variation in female dispersal. From 2006 to 2011, we collected behavioral data, demographic data, and fecal samples of 77 males and 92 females residing in eight groups at Boabeng-Fiema, Ghana. A combination of demographic data and a genetic network analysis showed that although philopatry was female-biased, only about half of the females resided in their natal groups. Only one group contained female-female dyads with higher average relatedness than randomly drawn animals of both sexes from the same group. Despite between-group variation in female dispersal and kin composition, female-female dyads in most of the study groups had higher proximity scores than randomly drawn dyads from the same group. We conclude that groups fall along a continuum from female dispersed, not kin-based, and not bonded to female philopatric, kin-based, and bonded. We found only partial support for the predicted link between dispersal, kin composition, and social relationships. In contrast to most mammals where the kin composition of groups is a good predictor of the quality of female-female relationships, this study provides further support for the notion that kinship is not necessary for the development and maintenance of social bonds in some gregarious species.     

Juvenile greylag geese (Anser anser) discriminate between individual siblings

Social species that maintain individualised relationships with certain others despite continuous changes in age, reproductive status and dominance rank between group members ought to be capable of individual recognition. Tests of "true" individual recognition, where an individual recognises unique features of another, are rare, however. Often kinship and/or familiarity suffice to explain dyadic interactions. The complex relationships within a greylag goose flock suggest that they should be able to recognise individuals irrespective of familiarity or kinship. We tested whether six-week-old hand-raised greylags can discriminate between two of their siblings. We developed a new experimental protocol, in which geese were trained to associate social siblings with geometrical symbols. Subsequently, focals were presented with two geometrical symbols in the presence of a sibling associated with one of the symbols. Significant choice of the geometrical symbol associated with the target present indicated that focals were able to distinguish between individual targets. Greylag goslings successfully learned this association-discrimination task, regardless of genetic relatedness or sex of the sibling targets. Social relationships within a goose flock thus may indeed be based on recognition of unique features of individual conspecifics.     

Fight for your breeding right: hierarchy re-establishment predicts aggression in a social queue

Social aggression is one of the most conspicuous features of animal societies, yet little is known about the causes of individual variation in aggression within social hierarchies. Recent theory suggests that when individuals form queues for breeding, variation in social aggression by non-breeding group members is related to their probability of inheriting breeding status. However, levels of aggression could also vary as a temporary response to changes in the hierarchy, with individuals becoming more aggressive as they ascend in rank, in order to re-establish dominance relationships. Using the group-living fish, Neolamprologus pulcher, we show that subordinates became more aggressive after they ascended in rank. Female ascenders exhibited more rapid increases in aggression than males, and the increased aggression was primarily directed towards group members of adjacent rather than non-adjacent rank, suggesting that social aggression was related to conflict over rank. Elevated aggression by ascenders was not sustained over time, there was no relationship between rank and aggression in stable groups, and aggression given by ascenders was not sex-biased. Together, these results suggest that the need to re-establish dominance relationships following rank ascension is an important determinant of variation in aggression in animal societies.     

Social network structure in wintering golden‐crowned sparrows is not correlated with kinship

Stable social organization in a wide variety of organisms has been linked to kinship, which can minimize conflict due to the indirect fitness benefits from cooperating with relatives. In birds, kin selection has been mostly studied in the context of reproduction or in species that are social year round. Many birds however are migratory, and the role of kinship in the winter societies of these species is virtually unexplored. In a previous study, we discovered striking social complexity and stability in a wintering population of migratory golden‐crowned sparrows (Zonotrichia atricapilla) – individuals repeatedly form close associations with the same social partners, including across multiple winters. Here, we test the possibility that kinship might be involved in these close and stable social affiliations. We examine the relationship between kinship and social structure for two of the consecutive wintering seasons from the previous study. We found no evidence that social structure was influenced by kinship. Relatedness between most pairs of individuals was at most that of first cousins (and mostly far lower). Genetic networks based on relatedness do not correspond to the social networks, and Mantel tests revealed no relationship between kinship and pairwise interaction frequency. Kinship also failed to predict social structure in more fine‐grained analyses, including analyses of each sex separately (in the event that sex‐biased migration might limit kin selection to one sex), and separate analyses for each social community. The complex winter societies of golden‐crowned sparrows appear to be based on cooperative benefits unrelated to kin selection.     

The evolution of group-beneficial traits in the absence of between-group selection

One specific prediction emerging from trait-group models of natural selection is that when individuals possess traits that benefit other group members, natural selection will favor "cheating" (i.e. not possessing the group-beneficial trait) within groups. Cheating is selected within groups because it allows individuals to avoid bearing the relative costs typically associated with group-beneficial traits, but to still reap the benefits associated with the acts of other group members. Selection between groups favors traits that benefit other group members. The relative strength of within- and between-group selection then determines the equilibrium frequency of those who produce group-beneficial traits and those that do not. Here we demonstrate that individual-level selection, that is selection within groups can also produce an intermediate frequency of such group-beneficial traits by frequency-dependent selection. The models we develop are general in nature, but were inspired by the evolution of antibiotic resistance in bacteria. The theory developed here is distinct from prior work that relies on reciprocity or kinship per se to achieve cooperation and altruism among group members.     

Fitness consequences of spousal relatedness in 46 small-scale societies

Social norms that regulate reproductive and marital decisions generate impressive cross-cultural variation in the prevalence of kin marriages. In some societies, marriages among kin are the norm and this inbreeding creates intensive kinship networks concentrated within communities. In others, especially forager societies, most marriages are between more genealogically and geographically distant individuals, which generates a larger number of kin and affines of lesser relatedness in more extensive kinship networks spread out over multiple communities. Here, we investigate the fitness consequence of kin marriages across a sample of 46 small-scale societies (12 439 marriages). Results show that some non-forager societies (including horticulturalists, agriculturalists and pastoralists), but not foragers, have intensive kinship societies where fitness outcomes (measured as the number of surviving children in genealogies) peak at commonly high levels of spousal relatedness. By contrast, the extensive kinship systems of foragers have worse fitness outcomes at high levels of spousal relatedness. Overall, societies with greater levels of inbreeding showed a more positive relationship between fitness and spousal relatedness.     

Bonds of bros and brothers: Kinship and social bonding in postdispersal male macaques

Group‐living animals often maintain a few very close affiliative relationships—social bonds—that can buffer them against many of the inevitable costs of gregariousness. Kinship plays a central role in the development of such social bonds. The bulk of research on kin biases in sociality has focused on philopatric females, who typically live in deeply kin‐structured systems, with matrilineal dominance rank inheritance and life‐long familiarity between kin. Closely related males, in contrast, are usually not close in rank or familiar, which offers the opportunity to test the importance of kinship per se in the formation of social bonds. So far, however, kin biases in male social bonding have only been tested in philopatric males, where familiarity remains a confounding factor. Here, we studied bonds between male Assamese macaques, a species in which males disperse from their natal groups and in which male bonds are known to affect fitness. Combining extensive behavioural data on 43 adult males over a 10‐year period with DNA microsatellite relatedness analyses, we find that postdispersal males form stronger relationships with the few close kin available in the group than with the average nonkin. However, males form the majority of their bonds with nonkin and may choose nonkin over available close kin to bond with. Our results show that kinship facilitates bond formation, but is not a prerequisite for it, which suggests that strong bonds are not restricted to kin in male mammals and that animals cooperate for both direct and indirect fitness benefits.     

A novel mammalian social structure in Indo-Pacific bottlenose dolphins (Tursiops sp.): complex male alliances in an open social network

Terrestrial mammals with differentiated social relationships live in 'semi-closed groups' that occasionally accept new members emigrating from other groups. Bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia, exhibit a fission-fusion grouping pattern with strongly differentiated relationships, including nested male alliances. Previous studies failed to detect a group membership 'boundary', suggesting that the dolphins live in an open social network. However, two alternative hypotheses have not been excluded. The community defence model posits that the dolphins live in a large semi-closed 'chimpanzee-like' community defended by males and predicts that a dominant alliance(s) will range over the entire community range. The mating season defence model predicts that alliances will defend mating-season territories or sets of females. Here, both models are tested and rejected: no alliances ranged over the entire community range and alliances showed extensive overlap in mating season ranges and consorted females. The Shark Bay dolphins, therefore, present a combination of traits that is unique among mammals: complex male alliances in an open social network. The open social network of dolphins is linked to their relatively low costs of locomotion. This reveals a surprising and previously unrecognized convergence between adaptations reducing travel costs and complex intergroup-alliance relationships in dolphins, elephants and humans.     

Individual versus social complexity, with particular reference to ant colonies

Insect societies colonies of ants, bees, wasps and termites--vary enormously in their social complexity. Social complexity is a broadly used term that encompasses many individual and colony-level traits and characteristics such as colony size, polymorphism and foraging strategy. A number of earlier studies have considered the relationships among various correlates of social complexity in insect societies; in this review, we build upon those studies by proposing additional correlates and show how all correlates can be integrated in a common explanatory framework. The various correlates are divided among four broad categories (sections). Under 'polyphenism' we consider the differences among individuals, in particular focusing upon 'caste' and specialization of individuals. This is followed by a section on 'totipotency' in which we consider the autonomy and subjugation of individuals. Under this heading we consider various aspects such as intracolony conflict, worker reproductive potential and physiological or morphological restrictions which limit individuals' capacities to perform a range of tasks or functions. A section entitled 'organization of work' considers a variety of aspects, e.g. the ability to tackle group, team or partitioned tasks, foraging strategies and colony reliability and efficiency. A final section, 'communication and functional integration', considers how individual activity is coordinated to produce an integrated and adaptive colony. Within each section we use illustrative examples drawn from the social insect literature (mostly from ants, for which there is the best data) to illustrate concepts or trends and make a number of predictions concerning how a particular trait is expected to correlate with other aspects of social complexity. Within each section we also expand the scope of the arguments to consider these relationships in a much broader sense of'sociality' by drawing parallels with other 'social' entities such as multicellular individuals, which can be understood as 'societies' of cells. The aim is to draw out any parallels and common causal relationships among the correlates. Two themes run through the study. The first is the role of colony size as an important factor affecting social complexity. The second is the complexity of individual workers in relation to the complexity of the colony. Consequently, this is an ideal opportunity to test a previously proposed hypothesis that 'individuals of highly social ant species are less complex than individuals from simple ant species' in light of numerous social correlates. Our findings support this hypothesis. In summary, we conclude that, in general, complex societies are characterized by large colony size, worker polymorphism, strong behavioural specialization and loss of totipotency in its workers, low individual complexity, decentralized colony control and high system redundancy, low individual competence, a high degree of worker cooperation wher tackling tasks, group foraging strategies, high tempo, multi-chambered tailor-made nests, high functional integration, relatively greater use of cues and modulatory signals to coordinate individuals and heterogeneous patterns of worker-worker interaction.