Individual variation in social aggression and the probability of inheritance: theory and a field test

Recent theory suggests that much of the wide variation in individual behavior that exists within cooperative animal societies can be explained by variation in the future direct component of fitness, or the probability of inheritance. Here we develop two models to explore the effect of variation in future fitness on social aggression. The models predict that rates of aggression will be highest toward the front of the queue to inherit and will be higher in larger, more productive groups. A third prediction is that, in seasonal animals, aggression will increase as the time available to inherit the breeding position runs out. We tested these predictions using a model social species, the paper wasp Polistes dominulus. We found that rates of both aggressive "displays" (aimed at individuals of lower rank) and aggressive "tests" (aimed at individuals of higher rank) decreased down the hierarchy, as predicted by our models. The only other significant factor affecting aggression rates was date, with more aggression observed later in the season, also as predicted. Variation in future fitness due to inheritance rank is the hidden factor accounting for much of the variation in aggressiveness among apparently equivalent individuals in this species.     

Social correlates of variation in urinary cortisol in wild male bonobos (Pan paniscus)

Cortisol excretion in males of group living species is often associated with social rank and competition for oestrous females. Rank-related patterns of cortisol levels can be used to study mechanisms of rank maintenance and costs associated with mate competition. Bonobos (Pan paniscus) are interesting because males form a linear dominance hierarchy but are not dominant over females and therefore aggressive male-male competition over access to females alone is not considered to be a successful reproductive strategy. In this study on social correlates of urinary cortisol in wild male bonobos, we investigated the relationship between cortisol levels and several aspects of mate competition, including male rank, aggression rates, and association time with oestrous females. We found that cortisol levels correlated positively with dominance rank when oestrous females were present, but not when they were absent. This result is consistent with the idea that aggressive behaviour plays a minor role in maintenance of high rank. While aggression received from males and females explained within-individual variation in cortisol levels, it was the time spent in association with oestrous females that best explained between-individual variation in male cortisol levels. The observed increase in male cortisol may be associated with spatial proximity to oestrous females and could result from anticipated aggression from other group members, reduced feeding time in the males, or a combination of both.     

The ghost of social environments past: dominance relationships include current interactions and experience carried over from previous groups

Dominance hierarchies pervade animal societies. Within a static social environment, in which group size and composition are unchanged, an individual's hierarchy rank results from intrinsic (e.g. body size) and extrinsic (e.g. previous experiences) factors. Little is known, however, about how dominance relationships are formed and maintained when group size and composition are dynamic. Using a fusion-fission protocol, we fused groups of previously isolated shore crabs (Carcinus maenas) into larger groups, and then restored groups to their original size and composition. Pre-fusion hierarchies formed independently of individuals' sizes, and were maintained within a static group via winner/loser effects. Post-fusion hierarchies differed from pre-fusion ones; losing fights during fusion led to a decline in an individual's rank between pre- and post-fusion conditions, while spending time being aggressive during fusion led to an improvement in rank. In post-fusion tanks, larger individuals achieved better ranks than smaller individuals. In conclusion, dominance hierarchies in crabs represent a complex combination of intrinsic and extrinsic factors, in which experiences from previous groups can carry over to affect current competitive interactions.     

Affiliative relationships among Sorraia mares: influence of age, dominance, kinship and reproductive state

The influence of individual factors on dominance rank and the relationship between rank distance and patterns of aggression predicted by models of evolutionarily stable strategies (ESS) of animal conflict were investigated in a managed bachelor group of Sorraia horses, Equus caballus. The group was composed of four to six stallions 3- to 12-years-old during the study period. The dominance hierarchy was significantly linear and rank was not related to age, weight, height or aggressiveness. Frequency and intensity of agonistic interactions were low, but higher-ranking stallions did not receive lower aggressiveness than lower-ranking stallions. There was some evidence that dominance relationships were more contested among close-ranking stallions, as predicted. Agonistic-related interactions among close-ranking stallions served similar functions to those among distant-ranking stallions, but the latter interacted more frequently than expected for access to resting sites and/or resting partners. Therefore, we found some evidence that agonistic-related interactions among distant-ranking stallions play a larger role in providing access to valuable and defendable resources than those among close-ranking stallions. Nevertheless, the fact that space to escape from aggression was limited and breeding access was independent from dominance rank may have reduced the benefits relative to costs of aggression and therefore limited the occurrence of contests over dominance and resources.     

Correlates and Consequences of Dominance in a Social Rodent

In harem‐polygynous societies, body condition is often correlated with dominance rank. However, the consequences of dominance are less clear. High‐ranking males do not inevitably have the highest reproductive success, especially in systems where females mate with multiple males. In such societies, we expect male reproductive success to be more highly skewed than female reproductive success, but reproductive skew in females can still arise from rankings established within matrilineal societies. Dominance can also impact life‐history decisions by influencing dispersal patterns in yearlings. To better understand the function of dominance in harem‐polygynous societies, we studied the causes and consequences of dominance in yellow‐bellied marmots (Marmota flaviventris), a social rodent with skewed male reproductive success and female reproductive suppression. Specifically, we examined body condition as a predictor and the probability of breeding, number of offspring, and dispersal as outcomes of dominance. Additionally, we looked at variation in dominance between males and females and adults and yearlings, because marmots can engage in distinct interactions depending on the type of individuals involved. We found that marmots in better body condition have higher dominance rank than those in poorer condition. In addition, adults are dominant over yearlings. Within yearlings, dominance does not influence dispersal, but those in better body condition are less likely to disperse. Within all adults, individuals in better condition produce more offspring per year. Within adult males, more dominant males have greater reproductive success. Despite previous evidence of reproductive suppression in females, we found no effects of dominance rank on female reproductive success in the current study. The function of dominance in female marmots remains enigmatic.     

Social stability and helping in small animal societies

In primitively eusocial societies, all individuals can potentially reproduce independently. The key fact that we focus on in this paper is that individuals in such societies instead often queue to inherit breeding positions. Queuing leads to systematic differences in expected future fitness. We first discuss the implications this has for variation in behaviour. For example, because helpers nearer to the front of the queue have more to lose, they should work less hard to rear the dominant''s offspring. However, higher rankers may be more aggressive than low rankers, even if they risk injury in the process, if aggression functions to maintain or enhance queue position. Second, we discuss how queuing rules may be enforced through hidden threats that rarely have to be carried out. In fishes, rule breakers face the threat of eviction from the group. In contrast, subordinate paper wasps are not injured or evicted during escalated challenges against the dominant, perhaps because they are more valuable to the dominant. We discuss evidence that paper-wasp dominants avoid escalated conflicts by ceding reproduction to subordinates. Queuing rules appear usually to be enforced by individuals adjacent in the queue rather than by dominants. Further manipulative studies are required to reveal mechanisms underlying queue stability and to elucidate what determines queue position in the first place.     

A theory of leadership in human cooperative groups

Two types of models aim to account the origins of rank differentiation and social hierarchy in human societies. Conflict models suggest that the formation of social hierarchies is synonymous with the establishment of relationships of coercive social dominance and exploitation. Voluntary or 'integrative' models, on the other hand, suggest that rank differentiation - the differentiation of leader from follower, ruler from ruled, or state from subject - may sometimes be preferred over more egalitarian social arrangements as a solution to the challenges of life in social groups, such as conflict over resources, coordination failures, and free-riding in cooperative relationships. Little formal theoretical work, however, has established whether and under what conditions individuals would indeed prefer the establishment of more hierarchical relationships over more egalitarian alternatives. This paper provides an evolutionary game theoretical model for the acceptance of leadership in cooperative groups. We propose that the effort of a leader can reduce the likelihood that cooperation fails due to free-riding or coordination errors, and that under some circumstances, individuals would prefer to cooperate in a group under the supervision of a leader who receives a share of the group's productivity than to work in an unsupervised group. We suggest, in particular, that this becomes an optimal solution for individual decision makers when the number of group members required for collective action exceeds the maximum group size at which leaderless cooperation is viable.     

Effect of testosterone and melatonin on social dominance and agonistic behavior in male Tscheskia triton

Social dominance and agonistic behavior play important roles in animal societies. Melatonin and testosterone are closely related to social dominance and agonistic behavior in rodents, but interactions between both of them remain unknown. In this study we investigated the effects of testosterone and melatonin by manipulating photoperiod and castration on social dominance and agonistic behavior in male Tscheskia triton. Castration significantly decreases social dominance of both short- and long-day males, suggesting that testosterone benefits social dominance of males in both breeding and non-breeding seasons. In intact conditions, long-day males tended to dominate short-day males, suggesting that the effect of testosterone on social dominance was a little stronger than melatonin. However, castrated short-day males became dominant over their castrated long-day opponents meaning that high melatonin levels obviously benefit social dominance in males. Hormone implantation indicated that testosterone had no effect on non-breeding condition, but that melatonin was important during the breeding season. Our results indicate that both testosterone and melatonin are important in determining social dominance in male hamsters, and the effect of testosterone appears to be stronger than melatonin. Testosterone is responsible for aggression and social dominance in male hamsters during the breeding season, while melatonin regulates behavior during non-breeding, probably due to the different seasonal secretory patterns of the hormones.     

Age and sex affect quantitative genetic parameters for dominance rank and aggression in free‐living greylag geese

Knowledge of the genetic and environmental influences on a character is pivotal for understanding evolutionary changes in quantitative traits in natural populations. Dominance and aggression are ubiquitous traits that are selectively advantageous in many animal societies and have the potential to impact the evolutionary trajectory of animal populations. Here we provide age‐ and sex‐specific estimates of additive genetic and environmental components of variance for dominance rank and aggression rate in a free‐living, human‐habituated bird population subject to natural selection. We use a long‐term data set on individually marked greylag geese (Anser anser) and show that phenotypic variation in dominance‐related behaviours contains significant additive genetic variance, parental effects and permanent environment effects. The relative importance of these variance components varied between age and sex classes, whereby the most pronounced differences concerned nongenetic components. In particular, parental effects were larger in juveniles of both sexes than in adults. In paired adults, the partner's identity had a larger influence on male dominance rank and aggression rate than in females. In sex‐ and age‐specific estimates, heritabilities did not differ significantly between age and sex classes. Adult dominance rank was only weakly genetically correlated between the sexes, leading to considerably higher heritabilities in sex‐specific estimates than across sexes. We discuss these patterns in relation to selection acting on dominance rank and aggression in different life history stages and sexes and suggest that different adaptive optima could be a mechanism for maintaining genetic variation in dominance‐related traits in free‐living animal populations.     

Social relationships in a herd of Sorraia horses Part I. Correlates of social dominance and contexts of aggression

Factors related to dominance rank and the functions of aggression were studied in a herd of Sorraia horses, Equus caballus, under extensive management. Subjects were 10 adult mares 5-18 years old and a stallion introduced into the group for breeding. Dominance relationships among mares were clear, irrespective of rank difference, and remained stable after introduction of the stallion. The dominance hierarchy was significantly linear and rank was positively correlated with age and total aggressiveness. Higher-ranking mares received lower frequency and intensity of agonistic interactions. Nevertheless, higher-ranking dominants were not more likely to elicit submission from their subordinates than lower-ranking dominants. Neither close-ranking mares nor mares with less clear dominance relationships were more aggressive towards each other. Agonistic interactions seemed to be used more importantly in regulation of space than to obtain access to food or to reassert dominance relationships. Contexts of aggression were related to mare rank. The results suggest that dominance relationships based on age as a conventional criterion were established to reduce aggressiveness in a herd where the costs of aggression are likely to outweigh the benefits.     

Dominance, reproduction and survival in banded mongooses: towards an egalitarian social system?

The banded mongoose, Mungos mungo, is a social species that forms multimale and multifemale family groups. Earlier studies suggest these family groups are relatively egalitarian with small differences in reproductive opportunities among individuals of different rank. In contrast, previous studies of other social mongooses have focused on species with more despotic control of reproduction (meerkats, Suricata suricatta, dwarf mongooses, Helogale parvula). In these species, the distribution of reproductive opportunities amongst individuals of different rank has met the predictions of reproductive skew theory: dominant individuals accrue greater reproductive benefits than subordinates, with subordinates breeding less often than dominants. In this paper we test how well two predictions of reproductive skew theory explain variance in measures of reproductive effort, and its correlates, in a wild population of banded mongooses in Queen Elizabeth National Park, Uganda. We measure dominance rank in males and females, and we investigate whether individuals of higher social rank accrue greater benefits than subordinates in terms of survival and reproduction. Banded mongoose dominance hierarchies showed linearity, but low reproductive skew. Rank was not significantly correlated with age. Furthermore, there were only small effects of dominance rank on nutritional levels, and no effects on reproduction and survival, suggesting that banded mongoose societies are indeed relatively egalitarian. No evidence of reproductive suppression was found and other forms of reproductive control were not observed. However, we do not exclude the possibility of increased reproductive competition in circumstances of higher ecological constraints. These findings show that reproductive skew theory is equally useful in explaining variation in reproduction in societies with low reproductive skew, as it is in explaining the allocation of reproductive effort in despotic social systems. Copyright 2001 The Association for the Study of Animal Behaviour.     

Dominance and queen succession in captive colonies of the eusocial naked mole-rat,Heterocephalus glaber.

Naked mole-rat colonies exhibit a high reproductive skew, breeding being typically restricted to one female (the ''queen'') and one to three males. Other colony members are reproductively suppressed, although this suppression can be reversed following the removal or death of the queen. We examined dominance and queen succession within captive colonies to investigate the relationship between urinary testosterone and cortisol, dominance rank and reproductive status; and to determine if behavioural and/or physiological parameters can be used as predictors of queen succession. Social structure was characterized by a linear dominance hierarchy before and after queen removal. Prior to queen removal, dominance rank was negatively correlated with body weight and urinary testosterone and cortisol titres in males and females. Queen removal results in social instability and aggression between high ranking individuals. Dominance rank appears to be a good predictor of reproductive status: queens are the highest ranking colony females and are succeeded by the next highest ranking females. The intense dominance-related aggression that accompanies reproductive succession in naked mole-rats provides empirical support for optimal skew theory.     

The dining etiquette of desert baboons: the roles of social bonds, kinship, and dominance in co-feeding networks

To better understand how individual relationships influence patterns of social foraging in primate groups, we explored networks of co-feeding in wild desert baboons (Papio ursinus). To minimize the risk of aggression and injury associated with contest competition, we expected that individual group members would choose to co-feed with those group-mates that are most likely to show tolerance and a willingness to share food patches. We tested two alternative hypotheses about who those group-mates might be: the "social bonds hypothesis" predicts that preferred foraging partners will be those with whom individuals share strong social bonds, indexed by grooming, whereas the "kinship hypothesis" predicts that preferred foraging partners will be relatives. We also investigated and controlled for the effects of dominance rank, given that competitive ability is known to shape foraging patterns. Social network analyses of over 5,000 foraging events for 14 adults in a single troop revealed that baboon co-feeding was significantly correlated with grooming relationships but not genetic relatedness, and this finding was also true of the female-only co-feeding network. Dominant individuals were also found to be central to the co-feeding network, frequently sharing food patches with multiple group-mates. This polyadic analysis of foraging associations between individuals underlines the importance of dominance and affiliation to patterns of primate social foraging.     

Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis)

In group-living animals relative rank positions are often associated with differences in glucocorticoid output. During phases of social stability, when dominance positions are clear and unchallenged, subordinates often face higher costs in terms of social stress than dominant individuals. In this study we test this prediction and examine additional potential correlates of stress, such as reproductive season, age and amount of aggression received in wild, seasonally breeding Assamese macaques (Macaca assamensis). During a mating and a non-mating season we collected 394 h of focal observational data and 440 fecal samples of six adult and six large subadult males living in a multimale–multifemale group in their natural habitat in northeastern Thailand. The mating season was characterized by a general increase in aggressive behavior and glucocorticoid excretion across all males compared to the non-mating season. Among adult males, mating season glucocorticoid levels were significantly negatively related with dominance rank and positively with the amount of aggression received. Both relationships were non-significant among large subadult males. Thus, our results suggest that in adult Assamese macaques a high dominance position is not associated with high costs. Low costs of dominance might be induced by strong social bonds among top-ranking males, which exchange frequent affiliative interactions and serve as allies in coalitionary aggression against potentially rank-challenging subordinate males.     

Dominance,aggression and physiological stress in wild male Assamese macaques (Macaca assamensis)

In group-living animals relative rank positions are often associated with differences in glucocorticoid output. During phases of social stability, when dominance positions are clear and unchallenged, subordinates often face higher costs in terms of social stress than dominant individuals. In this study we test this prediction and examine additional potential correlates of stress, such as reproductive season, age and amount of aggression received in wild, seasonally breeding Assamese macaques (Macaca assamensis). During a mating and a non-mating season we collected 394 h of focal observational data and 440 fecal samples of six adult and six large subadult males living in a multimale–multifemale group in their natural habitat in northeastern Thailand. The mating season was characterized by a general increase in aggressive behavior and glucocorticoid excretion across all males compared to the non-mating season. Among adult males, mating season glucocorticoid levels were significantly negatively related with dominance rank and positively with the amount of aggression received. Both relationships were non-significant among large subadult males. Thus, our results suggest that in adult Assamese macaques a high dominance position is not associated with high costs. Low costs of dominance might be induced by strong social bonds among top-ranking males, which exchange frequent affiliative interactions and serve as allies in coalitionary aggression against potentially rank-challenging subordinate males.     

Variation in social rank acquisition influences lifetime reproductive success in black-capped chickadees

Dominance relationships structure many animal societies, yet the process of rank attainment is poorly understood. We investigated acquisition of social dominance in winter flocks and its fitness consequences in male black-capped chickadees (Poecile atricapillus) over a 10-year period. Age was the best predictor of rank, and paired comparisons showed high-ranked males to be older than their low-ranked flock-mates. When controlling for age, morphological variables did not predict male social rank, but high-ranked males were heavier, had lower fat scores and were in leaner condition than low-ranked males. Males that survived between years tended to increase in rank over time; however, the rate of rank advancement varied individually. Rank reversals between familiar contestants were rare, and changes in male social rank were associated with changes in flock membership. Average lifetime reproductive success (LRS) of males and females was variable and best predicted by lifespan. Male rank history also influenced realized reproductive success. Birds with higher average rank over their lifespan were more likely to reproduce successfully. However, among successful birds, average rank did not significantly predict LRS. Thus, birds that lived longer and attained high social rank earlier had higher fitness, but this effect was not manifested as fine-scale differences among successful individuals. Taken together, these findings demonstrate the importance of social factors influencing individual fitness.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 85–95.     

Dyadic and triadic reconciliation in pigtail macaques (Macaca nemestrina)

The tendency in primates for former antagonists to approach and affiliate following aggression has been termed reconciliation because the response is thought to resolve social conflicts produced by aggression. In primate societies, however, an aggressive interaction between two individuals often spreads to include other group members, especially the kin of the combatants. If post conflict affiliation resolves aggressive conflicts in a group, then affiliative increases might occur between combatants and the kin of their opponents following aggression as well as between former opponents. This hypothesis was tested in a captive group of 39 pigtail macaques (Macaca nemestrina) by comparing affiliative response frequencies of combatants during the 5 minute period following aggression to affiliative response frequencies during 5 minute baseline periods not preceded by aggressive activity. Following aggression, affiliation rates increased between combatants and their opponents, aggressors and the kin of their opponents, and aggressors and their own kin. Additional analyses showed that aggression among kin was reconciled more often than aggression among nonkin. Recipients of aggression reconciled with their attackers more often than aggressors reconciled with their victims. Animals with similar dominance ranks reconciled proportionately more often than those with large rank disparities and aggressive infractions of a calculated dominance hierarchy were reconciled more often than attacks consistent with the hierarchy. Results suggest that both dyadic and triadic reconciliations occur in M. nemestrina and that compared to other primate species M. nemestrina exhibit a moderate-to-high conciliatory tendency.     

Exploring the components, asymmetry and distribution of relationship quality in wild Barbary macaques (Macaca sylvanus)

Social relationships between group members are a key feature of many animal societies. The quality of social relationships has been described by three main components: value, compatibility and security, based on the benefits, tenure and stability of social exchanges. We aimed to analyse whether this three component structure could be used to describe the quality of social relationships in wild Barbary macaques (Macaca sylvanus). Moreover, we examined whether relationship quality was affected by the sex, age and rank differences between social partners, and investigated the asymmetric nature of social relationships. We collected over 1,900 hours of focal data on seven behavioural variables measuring relationship quality, and used principal component analysis to investigate how these variables clustered together. We found that relationship quality in wild Barbary macaques can be described by a three component structure that represents the value, compatibility and security of a relationship. Female-female dyads had more valuable relationships and same-age dyads more compatible relationships than any other dyad. Rank difference had no effect on the quality of a social relationship. Finally, we found a high degree of asymmetry in how members of a dyad exchange social behaviour. We argue that the asymmetry of social relationships should be taken into account when exploring the pattern and function of social behaviour in animal societies.     

Social parameters and urinary testosterone level in male chimpanzees (Pan troglodytes)

Studies investigating relationships between social parameters (such as dominance rank, rates of aggressive and sexual behaviors) and androgen (particularly, testosterone) levels in male primates have yielded inconsistent results. In the present study, we address the relationship between androgens, male dominance rank and rank-associated behaviors in two groups of captive chimpanzees, a species characterized by a pronounced dominance hierarchy between adult males. By combining behavioral observations with urinary testosterone (T) measurements, we found that the differences in T concentrations between males were small and not obviously related to their dominance rank. T levels were not related to the rates of initiated aggression and copulatory behavior, but a significant negative relationship between male T level and the rates of strong aggression received was apparent. Our findings, combined with those of others, suggest that any relationship between dominance rank and T depends upon the extent to which individual rank-associated behaviors (e.g. aggressive/sexual) are themselves related to T.     

Costs and benefits of maternal aggression in lactating female rhesus macaques

Data from over 400 hr of observation of mother-infant rhesus macaques indicate that during the first 12 weeks of lactation infants are at risk from other group members and that mothers use aggression as well as restraining to protect them. Maternal aggression was negatively correlated with infant restraining. High-ranking mothers reacted aggressively to individuals handling their infants more than did middle- and low-ranking mothers. Conversely, middle- and low-ranking mothers restrained their infants more than did high-ranking mothers. Maternal aggression did not vary with infant age. Maternal aggression was directed toward a higher proportion of higher-ranking adult females and their immature offspring and was more likely to be followed by counter-aggression than nonmaternal aggression, i.e. aggression not related to interactions involving the infant. Middle-and low-ranking mothers suffered higher costs in terms of retaliation than high-ranking mothers. It is argued that the occurrence and distribution of maternal aggression among species and individuals should depend on the risk posed to infants by conspecifics as well as on the characteristics of the social structure (e.g. degree of asymmetry of agonistic contests) and of the mother (e.g. her dominance rank) which may affect the probability of retaliation.