Abstract: Many species use social interactions to cope with challenges in their environment and a growing number of studies show that individuals which are well-connected to their group have higher fitness than socially isolated individuals. However, there are many ways to be ‘well-connected’ and it is unclear which aspects of sociality drive fitness benefits. Being well-connected can be conceptualized in four main ways: individuals can be socially integrated by engaging in a high rate of social behaviour or having many partners; they can have strong and stable connections to favoured partners; they can indirectly connect to the broader group structure; or directly engage in a high rate of beneficial behaviours, such as grooming. In this study, we use survival models and long-term data in adult female rhesus macaques (Macaca mulatta) to compare the fitness outcomes of multiple measures of social connectedness. Females that maintained strong connections to favoured partners had the highest relative survival probability, as did females well-integrated owing to forming many weak connections. We found no survival benefits to being structurally well-connected or engaging in high rates of grooming. Being well-connected to favoured partners could provide fitness benefits by, for example, increasing the efficacy of coordinated or mutualistic behaviours.
4. Discussion
By quantifying the relationship between survival and four of the most common operational definitions of social connectedness in a single system, this study highlights the fact that being ‘well-connected’ is multi-faceted in nature and provides evidence that some aspects of sociality represent more straightforward routes to biological success than others. In particular, we found support for a relationship between survival and dyadic connectedness: adult female rhesus macaques that frequently interacted with their top partners and that had partners that were stable over time were more likely to survive than females which interacted less often with their preferred and stable partners. However, we found no relationship between a female's number of strong connections and her probability of survival. For dyadic connections, at least, it appeared as though quality was more important than quantity. We also found some support for a relationship between social integration and survival: females that had a large number of weak connections experienced a lower mortality hazard. Other predictions of the social integration hypothesis were not supported, and there was little evidence that being structurally or directly well-connected resulted in survival benefits.
Our results add to previous studies linking the quality of dyadic relationships with positive fitness outcomes in social animals (table 1). In this study, rhesus macaque females with the strongest connections to their top partner had an 11% higher probability of survival than females that were less well-connected to their top partner. Repeatedly interacting with the same small number of individuals may facilitate the emergence and maintenance of cooperative relationships, whereby partners exchange behavioural services, such as grooming and coalitionary support, and where the consistency of partner identity may improve coordination of those behaviours and deter cheating [60,61].
Consistent and frequent partners may also result in benefits related to mutual social tolerance. In despotic, hierarchical, societies, like those of many female Old World primates, tolerated access to necessary resources, including food and space, may be beneficial to individuals [62–64]. Repeated and stable partnerships may initially arise because of shared needs or preferences amongst pairs of individuals. For example, individuals with similar metabolisms, thermoregulatory needs, or preferences for certain foods, may repeatedly find themselves attempting to access the same resource [65,66]. If alliances between pairs of individuals result in tolerance of that pair when accessing a resource, combined with mutualistic joint defence of that resource against competing groupmates, repeated and stable relationships may emerge. This scenario relies on relative stability in resource availability and in individual differences in needs and preferences. Individuals living outside of those conditions may have little need for stable partners, and may therefore exhibit a divergent relationship between dyadic connectedness and fitness [22,23,30]. In these species, a more flexible and generalized strategy of connectedness—via, for example, social integration—may be a better strategy for coping with the challenges of group-living.
In addition to dyadic connectedness, we found that some aspects of social integration predicted survival in this study; the number of weak connections a female maintained was linked to her mortality hazard. Wide social tolerance derived from these connections may allow a female to feed without disturbance or avoid harassment in a greater number of settings than females with fewer weak connections. Similar to the results presented here, blue monkeys (Cercopithecus mitis) survival has been shown to be positively associated with both strong-consistent connections and weak-inconsistent connections [51]. In the current population of rhesus macaques, measures of social integration have been positively linked to reproductive output [12] and proxies of social integration (family size) have been linked to survival [6]. Interestingly, correlations (electronic supplementary material, figure S1) and principal component analysis (electronic supplementary material, figure S6) suggest that dyadic connectedness measures and social integration measures are negatively associated in this population. That is, females with strong dyadic connectedness tend to have weak social integration. Taken together, these results may suggest that both dyadic connectedness and social integration can provide fitness benefits (albeit perhaps of different types) within the same system.
There was quantitative and qualitative variation in the relationship between survival and a female's number of strong connections, and between survival and number of weak connections depending on the threshold used to define connections as strong or weak. Choice of the threshold can, therefore, have important implications for the conclusions reached by a study, and we suggest that thresholds either be based on features of the data or behaviour of study species. More generally, connectedness is an individual effect. Defining connections as strong or weak at the population level and then calculating connectedness at the individual level may not best represent the salient features of the social environment experienced by individuals. This is highlighted by our contrasting results for number of strong connections and strength of connection to top associates (which is a measure defined at the individual level).
We found no evidence of a relationship between an individual's position in the broader social network and their probability of surviving. Individuals that are well-connected to their broader social worlds have been suggested to benefit from being among the first to receive useful information when it enters the system. For example, in resident-ecotype killer whales, indirect network position predicts male survival, potentially because well-positioned males are more likely to receive information about the presence and location of resources [13]. The rhesus macaques in our study were provisioned at regular intervals and predictable locations and have no predators. The opportunities for individuals to gain survival benefits from social information in this population may, therefore, be limited. Although information about the social environment such as mating opportunities, changes in group membership or dominance rank, are probably important for the success of these animals, the benefits of this information might be more tightly born out in terms of reproductive success [12] and less so in terms of survival.
Measures of direct connectedness were also not important predictors of survival in female rhesus macaques: neither a greater amount of time spent in proximity to others, engaged in grooming, nor the relative amount of grooming received were associated with increased probability of survival. In some primate species, grooming rates have been linked to lower parasite loads (e.g. [35]). Our findings suggest that the benefits of sociality are not directly derived from the behaviours involved in sociality, at least in this population. This interpretation aligns with suggestions that relationships are a commodity or resource that are promoted and maintained in some social animals.
Other social factors not considered in detail here are also likely to influence mortality. Dominance rank has been shown to be an important predictor of fitness and health (e.g. [10]) and a source of variation in social behaviour [67]) in primates, including in rhesus macaques [6,42,68]. Dominance rank did not significantly predict survival when evaluated as a term on its own and it was therefore not included as a main effect in subsequent models. Dominance rank was also not included as an interaction term with social connectedness because of concerns of overfitting. The analyses—in essence—represent the fitness consequences of sociality in females of ‘average’ rank. Including the interaction between connectedness and rank in future analyses may reveal important subtleties in the relationship between sociality and fitness. It is conceivable, for example, that the importance of social connectedness differs for females of high and low rank, though it should be noted that including rank has increased the observed benefits of sociality in this study system [6]. Further analyses based on longer observations and increased sample sizes would be needed to reveal how rank, and other behavioural and ecological constraints, influence the relationship between connectedness and longevity.
Overall, the results presented here demonstrate the value of understanding what exactly is meant by being ‘socially well-connected’. Although ‘sociality’ and ‘connectedness’ are useful catch-all terms, the methods used to measure them can influence results revealed and the conclusions reached. We have highlighted how different aspects of sociality can result in different biological conclusions. Future work in other species is needed to understand the generality of the conclusions reached here. Testing whether different conceptualizations of being well-connected are related to proxies of fitness other than survival, such as reproductive success, are also required, as are studies investigating how different aspects of connectedness interact in other systems.
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