Tina W. Wey

Social cohesion in yellow-bellied marmots is established through age and kin structuring

Individual characteristics and choices can influence social structure in animal groups. Social behaviour is likely to change throughout an individual’s life, resulting in different social roles at different ages. Individuals may also choose to interact differently with others based on their age, sex or kinship. We used social network analysis to examine biological correlates of individual social variation in free-living groups of yellow-bellied marmots, Marmota flaviventris. To measure social variation, we chose network measures that reflect an individual’s tendency to initiate or receive both direct and indirect interactions. We asked how age, sex and kinship influenced patterns of affiliative (socially cohesive) and agonistic (socially competitive) interactions. Specifically, we predicted that individuals would vary in their tendency to initiate and receive interactions according to these characteristics, and that they would be more likely to interact affiliatively with more similar individuals and to interact agonistically with more dissimilar individuals. We found that patterns of direct and indirect interactions changed significantly with age, with younger animals being more involved in affiliative interactions and older animals initiating more agonistic ones. Furthermore, affiliative networks tended to be structured by age and kinship. Our results suggest that yearling yellow-bellied marmots are more important for maintaining social cohesion than has previously been recognized, and that marmot colonies are largely organized based on age group and kinship. 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

A test of the social cohesion hypothesis: interactive female marmots remain at home

Individuals frequently leave home before reaching reproductive age, but the proximate causes of natal dispersal remain relatively unknown. The social cohesion hypothesis predicts that individuals who engage in more (affiliative) interactions are less likely to disperse. Despite the intuitive nature of this hypothesis, support is both limited and equivocal. We used formal social network analyses to quantify precisely both direct and indirect measures of social cohesion in yellow-bellied marmots. Because approximately 50 per cent of female yearlings disperse, we expected that social relationships and network measures of cohesion would predict dispersal. By contrast, because most male yearlings disperse, we expected that social relationships and cohesion would play a less important role. We found that female yearlings that interacted with more individuals, and those that were more socially embedded in their groups, were less likely to disperse. For males, social interactions were relatively unimportant determinants of dispersal. This is the first strong support for the social cohesion hypothesis and suggests that the specific nature of social relationships, not simply the number of affiliative relationships, may influence the propensity to disperse.

Heritable victimization and the benefits of agonistic relationships

Here, we present estimates of heritability and selection on network traits in a single population, allowing us to address the evolutionary potential of social behavior and the poorly understood link between sociality and fitness. To evolve, sociality must have some heritable basis, yet the heritability of social relationships is largely unknown. Recent advances in both social network analyses and quantitative genetics allow us to quantify attributes of social relationships and estimate their heritability in free-living populations. Our analyses addressed a variety of measures (in-degree, out-degree, attractiveness, expansiveness, embeddedness, and betweenness), and we hypothesized that traits reflecting relationships controlled by an individual (i.e., those that the individual initiated or were directly involved in) would be more heritable than those based largely on the behavior of conspecifics. Identifying patterns of heritability and selection among related traits may provide insight into which types of relationships are important in animal societies. As expected, we found that variation in indirect measures was largely explained by nongenetic variation. Yet, surprisingly, traits capturing initiated interactions do not possess significant additive genetic variation, whereas measures of received interactions are heritable. Measures describing initiated aggression and position in an agonistic network are under selection (0.3 < |S| < 0.4), although advantageous trait values are not inherited by offspring. It appears that agonistic relationships positively influence fitness and seemingly costly or harmful ties may, in fact, be beneficial. Our study highlights the importance of studying agonistic as well as affiliative relationships to understand fully the connections between sociality and fitness.

Toward an integrative understanding of social behavior: New models and new opportunities

Social interactions among conspecifics are a fundamental and adaptively significant component of the biology of numerous species. Such interactions give rise to group living as well as many of the complex forms of cooperation and conflict that occur within animal groups. Although previous conceptual models have focused on the ecological causes and fitness consequences of variation in social interactions, recent developments in endocrinology, neuroscience, and molecular genetics offer exciting opportunities to develop more integrated research programs that will facilitate new insights into the physiological causes and consequences of social variation. Here, we propose an integrative framework of social behavior that emphasizes relationships between ultimate-level function and proximate-level mechanism, thereby providing a foundation for exploring the full diversity of factors that underlie variation in social interactions, and ultimately sociality. In addition to identifying new model systems for the study of human psychopathologies, this framework provides a mechanistic basis for predicting how social behavior will change in response to environmental variation. We argue that the study of non-model organisms is essential for implementing this integrative model of social behavior because such species can be studied simultaneously in the lab and field, thereby allowing integration of rigorously controlled experimental manipulations with detailed observations of the ecological contexts in which interactions among conspecifics occur.

Social attributes and associated performance measures in marmots: bigger male bullies and weakly affiliating females have higher annual reproductive success

Studying the structure of social interactions is fundamental in behavioral ecology as social behavior often influences fitness and thus natural selection. However, social structure is often complex, and determining the most appropriate measures of variation in social behavior among individuals can be difficult. Social network analysis generates numerous, but often correlated, measures of individual connectedness derived from a network of interactions. We used measures of individual connectedness in networks of affiliative and agonistic interactions in yellow-bellied marmots, Marmota flaviventris, to first determine how variance was structured among network measures. Principal component analysis reduced our set of network measures to four “social attributes” (unweighted connectedness, affiliation strength, victimization, and bullying), which revealed differences between patterns of affiliative and agonistic interactions. We then used these extracted social attributes to examine the relationship between an individual’s social attributes and several performance measures: annual reproductive success, parasite infection, and basal stress. In male marmots, bullying was positively associated with annual reproductive success, while in females, affiliation strength was negatively associated with annual reproductive success. No other social attributes were significantly associated with any performance measures. Our study highlights the utility of considering multiple dimensions when measuring the structure and functional consequences of social behavior.

Reproductive correlates of social network variation in plurally breeding degus (Octodon degus)

Studying the causes and reproductive consequences of social variation can provide insight into the evolutionary basis of sociality. Individuals are expected to behave adaptively to maximize reproductive success, but reproductive outcomes can also depend on group structure. Degus (Octodon degus) are plurally breeding rodents, in which females allonurse indiscriminately. However, communal rearing does not appear to enhance female reproductive success, and larger group sizes are correlated with decreasing per capita pup production. To further investigate mechanisms underlying these patterns, we asked how differences in sex, season and average group reproductive success are related to degu association networks. We hypothesized that if reproductive differences mirror social relationships, then females (core group members) should show stronger and more stable associations than males, and female association strength should be strongest during lactation. We also hypothesized that, at the group level, social cohesion would increase reproductive output, while social conflict would decrease it. Females did have higher association strength and more preferred partners than males, but only during lactation, when overall female associations increased. Females also had more stable preferred social partnerships between seasons. A measure of social cohesion (average association strength) was not related to per capita pup production of female group members, but potential social conflict (heterogeneity of association strengths) was negatively related to per capita pup production of female group members. Our results highlight temporal and multilevel patterns of social structure that may reflect reproductive costs and benefits to females.

Effects of behavioural type, social skill and the social environment on male mating success in water striders

We examined the relative importance of individual differences in personality (activity and aggressiveness), social skill and the social environment (average activity and aggressiveness of the group, presence of hyperaggressive males) in determining the behaviour and mating success of males of the stream water strider, Aquarius remigis. Males that had a consistently more active–aggressive behavioural type had, on average, higher mating success largely because they spent more time active in microhabitats associated with acquiring mates. Some active–aggressive males, however, showed hyperaggressive behaviour, apparently attempting to mate forcibly with other males, or forcibly separate pairs, which was rarely successful. A higher tendency to be hyperaggressive was associated with reduced mating success (i.e. being hyperaggressive represents low social skill). The overall effect was thus stabilizing sexual selection on male activity and aggression. The social environment also had large effects on male behaviour and mating success. In particular, the presence of a keystone hyperaggressive male had strong negative effects on the mating success and general activity of other males in the pool. Notably, males with a more active–aggressive behavioural type maintained higher mating success than less active–aggressive males in the presence of a hyperaggressive male. Social plasticity (change in behaviour in response to changing social conditions) also depended on the males behavioural type; males with a more active–aggressive behavioural type were more plastic.

Environment modulates population social structure: Experimental evidence from replicated social networks of wild lizards

Social structure is a fundamental component of a population that drives ecological and evolutionary processes ranging from parasite transmission to sexual selection. Nevertheless, we have much to learn about factors that explain variation in social structure. We used advances in biologging and social network analysis to experimentally test how the local habitat, and specifically habitat complexity, modulates social structure at different levels in wild populations. Sleepy lizards, Tiliqua rugosa, establish nonrandom social networks that are characterized by avoidance of some neighbours and frequent interactions with one opposite-sex individual. Using synchronous GPS locations of all adult lizards, we constructed social networks based on spatial proximity of individuals. We increased habitat structural complexity in two study populations by adding 100 short fences across the landscape. We then compared the resulting movement behaviour and social structure between these populations and two unmanipulated populations. Social connectivity (network density) and social stability, measured at weekly intervals, were greater in populations with increased habitat structural complexity. The level of agonistic interaction (quantified as scale damage) was also higher, indicating a fitness cost of greater social connectivity. However, some network parameters were unaffected by increased complexity, including disassortative mixing by sex, and at the individual level, social differentiation among associates (coefficient of variation of edge weights) and maximal interaction frequencies (maximal edge weight). This suggests divergent effects of changed ecological conditions on individual association behaviour compared to the resulting social structure of the population. Our results contrast with those from studies of more gregarious species, in which higher structural complexity in the environment relaxed the social connectivity. This shows that the response to altered ecological conditions can differ fundamentally between species or between populations, and we suggest that it depends on their tendency for gregarious behaviour.

Personalities and presence of hyperaggressive males influence male mating exclusivity and effective mating in stream water striders

Male expected reproductive success can be enhanced by increased mating success (mate number) or, when females can mate multiply, by increased mating exclusivity (i.e., reduced partner promiscuity). A positive or negative covariance between these two mating outcomes could substantially increase or decrease overall variation in male expected reproductive success, yet the relationship between these mating outcomes is relatively understudied. We examined this relationship and the influence of male personality traits, female personality traits, and the social environment on mating outcomes in stream water striders, Aquarius remigis, at two experimental sex ratios: equal and 2:1 male-biased. To our knowledge, this study is the first to quantify this full set of effects. We found that mating frequency (mating success) and mating exclusivity were positively correlated in the male-biased treatment, but were not related at equal sex ratios. At both sex ratios, males that were more active and aggressive had both higher mating frequency and higher mating exclusivity. A male’s effective mating (the product of mating frequency and mating exclusivity) was also higher if on average he mated with females that tended to hide in refuges (and were presumably less available for future matings). Finally, males that were more often in pools with extremely aggressive (“hyperaggressive”) males actually had increased mating exclusivity, potentially because hyperaggression reduced average female promiscuity. This study highlights the importance of considering mating outcomes beyond mating success and examining the simultaneous contribution of male behaviours, female behaviours and social factors to mating dynamics.

Current directions in animal social networks

A social network approach provides a framework to study the link between individual behaviour and population-level patterns and processes. Studies have demonstrated how animal social network structure can be influenced by factors ranging from characteristics of the environment to characteristics of the individual, such as developmental experience and personality. At the level of the individual, the patterning of social connections can be an important determinant of fitness, predicting both survival and reproductive success. At the population level, network structure can influence the patterning of ecological and evolutionary processes, such as frequency-dependant selection and disease and information transmission.