Stronger social bonds do not always predict greater longevity in a gregarious primate

Abstract In group‐living species, individuals often have preferred affiliative social partners, with whom ties or bonds can confer advantages that correspond with greater fitness. For example, in adult female baboons and juvenile horses, individuals with stronger or more social ties experience greater survival. We used detailed behavioral and life history records to explore the relationship between tie quality and survival in a gregarious monkey (Cercopithecus mitis stuhlmanni), while controlling for dominance rank, group size, and life history strategy. We used Cox proportional hazards regressions to model the cumulative (multi‐year) and current (single‐year) relationships of social ties and the hazard of mortality in 83 wild adult females of known age, observed 2–8 years each (437 subject‐years) in eight social groups. The strength of bonds with close partners was associated with increased mortality risk under certain conditions: Females that had strong bonds with close partners that were inconsistent over multiple years had a higher risk of mortality than females adopting any other social strategy. Within a given year, females had a higher risk of death if they were strongly bonded with partners that changed from the previous year versus with partners that remained consistent. Dominance rank, number of adult female groupmates, and age at first reproduction did not predict the risk of death. This study demonstrates that costs and benefits of strong social bonds can be context‐dependent, relating to the consistency of social partners over time.

Affiliative relationships can influence fitness in several ways (Cords & Thompson, 2017). The general benefits of group living may be amplified by living with especially tolerant and familiar partners. Such partners may work together more efficiently in cooperative hunting (Ruch, Herberstein, & Schneider, 2014), communal care of offspring (Weidt, Lindholm, & Koenig, 2014), or attending to predators (Micheletta et al., 2012). In several species, affiliative partners, often kin, compete more effectively as allies, and alliances help to maintain dominance rank (Chapais, 1995;Mitani, Merriwether, & Zhang, 2000;Schülke et al., 2010) or increase access to mates (Connor, Read, & Wrangham, 2000;Feh, 1999). Affiliative partners may also provide psychosocial support that attenuates prolonged stress responses to events such as infanticide or the loss of close social partners (Engh et al., 2006;Wittig et al., 2008), although links between chronically elevated glucocorticoids and fitness may not be as direct or as prevalent in wild animals as in humans (Beehner & Bergman, 2017). More general integration in social groups, for example, having more affiliative partners, may also provide such a buffering effect and protect individuals from environmental risks such as cold temperatures (Lehmann et al., 2016;McFarland & Majolo, 2013;McFarland et al., 2015), enhance access to relevant social and environmental information (Archie, Moss, & Alberts, 2006;Templeton, Reed, Campbell, & Beecher, 2012), and help individuals survive traumatic population-wide events (Nuñez et al., 2015).
Although most studies emphasize the effects of affiliative and cooperative relations on fitness outcomes, agonistic interactions may also be important. In Barbary macaques, individuals that either received or directed aggression to more partners, and whose aggressive partners were not aggressive toward one another, were more likely to survive a hard winter (Lehmann et al., 2016). Similarly, yellow-bellied marmots (Marmota flaviventris) lived longer if they initiated aggression toward more recipients, although the benefits of aggression here likely derived from its association with social dominance (Lea, Blumstein, Wey, & Martin, 2010). Indeed, dominance status or rank, derived from agonistic interactions, has a pervasive influence on fitness-related variables in female mammals, as rank frequently corresponds with priority of access to food (Clutton-Brock & Huchard, 2013). Dominance rank can predict survival (Pusey, Williams, & Goodall, 1997;Silk et al., 2010b), possibly because high-ranking individuals are able to access safer microhabitats and avoid predation (van Schaik & Van Noordwijk, 1986), better access nutrients (Foerster, Cords, & Monfort, 2011), and avoid harassment during development (Silk, Samuels, & Rodman, 1981). In our study species, the blue monkey, rank has no effect on conception probability (Roberts & Cords, 2013), but higher-ranking females had lower baseline glucocorticoid levels during an energetically challenging period when lactation overlapped with low food availability (Foerster et al., 2011).
Variables other than the quality of social ties and rank can also influence survival in group-living animals. Large group size may enhance survival by providing benefits similar to those of maintaining particularly affiliative relationships, such as more effective vigilance for predators (Elgar, 1989;Lehtonen & Jaatinen, 2016;Roberts, 1996;van Schaik & Van Noordwijk, 1986), defense of young offspring (Grinnell & McComb, 1996;Wolff & Peterson, 1998), or defense of feeding territories (Radford & du Plessis, 2004;Roth & Cords, 2016). Nevertheless, living in larger groups may also exact costs by increasing within-group competition for food (Roberts & Cords, 2013;VanderWaal, Mosser, & Packer, 2009), or by increasing the risk of male takeovers and subsequent infanticide (Steenbeek & van Schaik, 2001). In some cases, the way the cost-benefit balance changes in larger social groups means that intermediate group sizes are optimal for individual fitness (Markham, Gesquiere, Alberts, & Altmann, 2015;Roberts & Cords, 2013). Finally, at a basic life history level, individuals may trade off energetic investment in somatic growth and maintenance (survival) for reproduction (Descamps, Boutin, Berteaux, & Gaillard, 2006;Hamel et al., 2010).
In this study, we used survival analyses to examine the link between affiliative social ties and lifespan of wild adult female blue monkeys, while also controlling for the influence of other sociodemographic factors and a potential life history trade-off. We examined both the cumulative (multi-year) and current (annual) effect of social experience on survival, using fixed-effect and time-dependent Cox models to test for each, respectively. We focused mainly on affiliative relations because agonistic interactions occur at low rates in this species (Klass & Cords, 2015).
Although blue monkeys differ from other cercopithecines in multiple ways, we expected to confirm patterns documented in certain macaques (Lehmann et al., 2016) and baboons (Archie et al., 2014;Silk et al., 2010b), namely, that more or higher-quality social ties, either cumulatively over multiple years or in one's current environment, correspond with higher survival. Unlike these other species, blue monkeys are highly arboreal, live in a less seasonal (rainforest) environment, seem to experience relatively strong feeding competition between groups but relatively weak competition within groups (Cords, 2007;Klass & Cords, 2015), and live in groups with a single male. Despite these differences, we hypothesized that strong and stable female-female affiliative ties would enhance longevity in female blue monkeys because, like other cercopithecines, they have a female-philopatric and matrilineally structured society in which grooming is the most obvious form of affiliation. We combine long-term life history data with detailed behavioral observations from an 8-year period on a wild population. We predicted specifically that females that maintained consistent and strong bonds with their closest partners would have a survival advantage relative to females with weak and inconsistent bonds, and that the benefits of strong and consistent bonds would be more pronounced over the long term.
The ca. 2 km 2 study area supports a high density of blue monkeys, with approximately 192 individuals/km 2 in old secondary forest and fewer in mixed indigenous plantations (Fashing et al., 2012). Betweengroup territorial disputes are common, occurring about every other day (Cords, 2007). Blue monkey groups usually comprise a single adult male, multiple adult philopatric females, and their young. This population has been monitored since 1979, and all study group members were identifiable based on natural physical variation (Cords, 2012).
During the period of data collection for this study (2006)(2007)(2008)(2009)(2010)(2011)(2012)(2013)(2014), we observed 83 adult (parous) female subjects in eight study groups, four of which resulted from two fission events that occurred in 2008 and 2009 (Figure 1 in Klass & Cords, 2015). In addition, in one group, three juveniles of unknown provenance joined the group in 2010 and became adult subjects in our analysis.
Long-term monitoring of demographic events (Cords, 2012) allowed us to specify birth and death dates; females alive at the end of the study (N = 63) were right-censored. For 12 of the oldest adult females and three who had immigrated as juveniles, we estimated birthdates based on changes in juvenile body size (average precision ± 0.75 years, range: 0.08-2). We inferred most deaths based on permanent disappearances as observers rarely found carcasses of missing animals. Female dispersal from the natal group is extremely rare in this species (two possible events in 111 group-years of monitoring, although these may have been small group fusions, author MC pers.
obs.), and several females that disappeared either left behind young offspring (<2 years) or were in poor physical condition prior to disappearance. Cause of death was seldom known, but most deaths probably resulted from intrinsic factors or predation. We considered a subject to be present in a given observation year if she was a subject for >10% of the year (69 of 467 subject-years < full

| Behavioral data collection
year, mean days observed if < full year = 310).
During focal samples, observers made instantaneous records at 1min intervals of subject activity (including grooming, resting, feeding, and moving) and the identity of all "neighbors" within 1 m whenever the subject was grooming or resting, or within 7 m if she was feeding. Because of the dense vegetation, subjects sometimes went out of sight. If observers relocated the subject within 15 min, they continued the sample until they achieved 30 min of observation; otherwise, the sample was terminated. Samples lasting <20 min were discarded.
Data on agonism, used to calculate dominance rank, came from focal and ad libitum observations (Klass & Cords, 2015). Observers recorded winners and losers in all decided agonistic interactions (in which one and only one opponent showed submission).

| Social predictors of survival
In many primates, mothers of young infants attract extra social attention. To measure social interaction that was not driven by short-term attraction to infants (Henzi & Barrett, 2002), we removed observation records when a subject or her partner had an infant <100 days old.
Infant blue monkeys begin to spend a substantial time away from their mothers at this age (Förster & Cords, 2005).
To see how the quality of social bonds affected survival, we first calculated bond strength for a given subject and all her adult female social partners in a given year. For this, we used an annual dyadic sociality index (DSI, Silk, Cheney, & Seyfarth, 2013) based on grooming and time spent resting in proximity (1 m), each expressed as a proportion of total dyad observation time (which was the sum of time observed for each dyad member as a subject). Grooming and resting within 1 m are two measures of affiliation known to be strongly biased toward maternal kin (Cords & Nikitopoulos, 2015). Matrices of dyadic proportions of time spent grooming or resting in proximity were correlated in 28 of 43 group-years, so their combination in a composite F I G U R E 1 Two adult female blue monkeys grooming index seemed justified (electronic supplementary material, Table S1).
We calculated the index as follows: where G ij represents the proportion of time that the dyad members spent grooming, R ij and R ji represent the proportion of time each dyad member i and j, as focal subjects, spent resting within 1 m of the other (without grooming or feeding), and G med and R med are the median values of all within-group dyads across social groups in the same year.
We divided the resting association data for a given dyad into two equal components based on focal subject identity to account for the fact that resting proximity was not symmetrical within the dyad (i.e., a resting focal subject might have a neighbor who was feeding, when observers scored proximity partners within a larger 7-m distance). A DSI of 1 would represent a typical dyad, while values >1 represent a dyad with stronger than median social ties.
To characterize each subject's bondedness over multiple years, we first averaged DSIs with her top three partners in a given year and then averaged over her annual values. We chose to average the DSIs of a female's top three partners for two reasons. First, across several species of social mammals, individuals tend to associate with decreasing intensity across social partners in tiers that scale by a multiple 3-3.15 (e.g., tier 1 = individual, tier 2 = grooming clique, Zhou, Sornette, Hill, & Dunbar, 2005;Hill, Bentley, & Dunbar, 2008). Second, averaging over top three partners allowed us to compare results with previous landmark studies on closely related primates (Silk et al., 2003(Silk et al., , 2009). Nevertheless, to assess whether ties with top three partners specifically were meaningful, we also explored the influence of DSIs averaged over the top six closest partners.
To measure partner consistency over multiple years, we first identified those individuals among the top three partners that were "consistent," and then asked what proportion of a female's top three partner "slots," across the years in which she was observed, were occupied by such consistent partners. We considered a top partner in a given year to be consistent if her DSI continued to place her in the top three positions at least once in the next two years (Silk et al., 2009). In a subject's second to last year of observation, we counted a top partner as consistent if she was among the top three in the next year only. We then determined what fraction of a female's top three "slots," summed across years, were occupied by a consistent partner. The number of "slots" was 3Y-3, where Y is the total number of observation years; we subtracted 3 because we could not assess consistency status of partners in the last year. This fraction varied from 0 (low consistency) to 1 (high consistency). Partner consistency was not related to number of years observed. To correspond with our alternative measure of bond strength with top six partners, we also calculated consistency in top six partners over time. During a few years, some subjects lived in groups with fewer than six or even three adult female groupmates.
To measure current partner consistency (i.e., within a given year), we counted the proportion of a female's top three or six partners that were present among her top partners at least once in the previous 2 years. For a female's second year of observation, we counted the proportion of top partners present from the previous year of observation alone. As the consistency of partners in a female's first year of observation could not be measured, annual partner consistencies were calculated for 354 of 437 subject-years. We calculated annual partner consistency retrospectively because we considered current (not future) partner stability relative to previous years to be most relevant to survival in the same year. Although prospective and retrospective measures of multi-year partner consistency do not differ greatly, measuring multi-year consistency prospectively assesses whether a female invested in partners that then remained consistent, and perhaps whether current partner choices would pay off over time.
Similar to a previous study (Silk et al., 2010b), we wished to condense bond strength and partner consistency into a single measure of relationship quality. Multi-year bond strength and partner consistency were correlated (N = 83, r = .23, p = .03); however, they were not correlated so closely as to load on a single principal component (Table S2). The relative independence of these variables led us to categorize females in one of the four classes of above (+) and We calculated dominance ranks from records of decided agonistic interactions among adult females using the I&SI method as implemented in DomiCalc (Schmid & de Vries, 2013). We expressed ranks as the proportion of adult female groupmates a female outranked in each year. For multi-year analyses, we averaged subjects' annual ranks over all years in which she was observed.

| Demographic and environmental predictors of survival
Long-term records allowed us to specify females' age at first birth and the number of adult female groupmates (Cords, 2012

| Survival analysis
We or at the subject's age at first birth (if she became an adult later). In all models, we used standardized covariates (Schielzeth, 2010).
We considered a predictor to influence the hazard if the 95% confidence interval of its parameter estimate did not include zero (Nakagawa & Cuthill, 2007

| RESULTS
Averaging annual measures of social predictor variables appeared to be a valid approach, as each predictor showed repeatable interindividual differences (electronic supplementary material, Table S3).
Nevertheless, as the lower confidence limit of bond strength's repeatability statistic was close to zero, a female's bond strength did appear to vary from year to year. Such intraindividual variation supported our analysis of time-dependent predictors.
Across 83 females, the average female's bond strength with her top three partners was 7.6 ± 2.5, that is, 7.6 times greater than the median bond strength between any two adult coresident females, and 51 ± 18% of the top three partner identities remained consistent (as per definition) during her observation period (electronic supplementary material, Table S4). Females lived with an average of 13.6 ± 4.2 adult female groupmates (range 3-21).
Measures of bond strength and partner consistency with top three partners were each highly correlated with their corresponding measure including top six partners (Table S4). Each multi-year measure decreased as group size increased, such that females had weaker and less consistent close partners in larger social groups (Table S4). Indeed, average number of adult female groupmates varied by strength-consistency class with top three partners, such that females that had strong and consistent partners (class 4, +/+) lived on average in smaller groups than females that had weak and inconsistent bond partners   Figure 3). The difference in the hazards of classes 1 (−/−), 2 (−/+), and 4 (+/+) did not reach significance according to 95% CIs (Tables S5   and S6). Yet according to permutation tests, the hazard ratio of females with weak and inconsistent bonds (class 1, −/−) versus females with strong and consistent bonds (class 4, +/+) was significantly higher than expected by chance. There were no differences in risk between intermediate-risk classes 1 and 2 according to either 95% CIs or permutation tests.

| Influences on risk of death
When we considered a females' multi-year relationship quality with top six partners, there were no significant contrasts in the hazards among strength-consistency classes according to 95% CIs.
The significant effects according to permutation tests are potentially false positives, which may arise as a result of breaking ancillarity (Anderson & Legendre, 1999;Dekker et al., 2007). Permuting values of a predictor variable in a multiple regression breaks ancillarity if there is any collinearity among predictor variables, as it removes any relationships between them. Indeed, there were several unavoidable correlations among bond strength, partner consistency, rank, and group size (Table S4), although collinearity among them in linear regression Cox models was not problematically high (max VIF all models, excluding model with quadratic term = 1.23). These contrasts in results according to parametric versus permutation-based null hypotheses may contribute further to discussion in the ecological literature about the suitability of permuting an independent social variable when estimating its partial regression coefficient.
Neither multi-year dominance rank's nor group size's influence on survival reached significance (Table 1, fixed-time models). Group size also did not demonstrate a quadratic relationship with survival (Tables S10 and S11). Age at first reproduction did approach significance in the expected direction, such that later ages at maturity would increase longevity (Table 1). All models including either dominance rank or number of adult female groupmates as a competition variable did not depart from proportional hazards (all global p > .10).
Time-dependent covariate models revealed patterns similar to those of fixed-time models. Strong bonds with few top three partners from the previous two years (class 3: + strength/-consistency) were associated with a higher risk of death than having strong bonds with consistent partners from previous years (class 4 +/+, Cox proportional hazards, N = 354, ß class 3 vs. 4 = −1.52, hazard ratio = 0.22, 95% CI = −3.03 to −0.01; electronic supplementary material, Tables S12 and S13, Figures S2 and S3). However, no other comparison between annual strength-consistency classes was more or less hazardous than the other. Fewer between-class comparisons reached significance in time-dependent models and the lower 95% confidence limit of the coefficient of class 3 versus 4 was very near zero, suggesting that an- strength-consistency class with top six partners also did not significantly influence survival in a time-dependent way. Similarly in bighorn ewes, social ties had a stronger effect than body mass on survival (Vander Wal et al., 2014). We also found no evidence of an effect of dominance rank and group size on survival, either over multiple years or in a particular year.

| Influences on the risk of death
Maintaining strong bonds when partners are inconsistent from year to year (highest risk multi-year strategy, Table 1 Figure 3) may represent an investment that outweighs the return, that is, females invest in partners that are too inconsistent to reciprocate or cooperate as allies.
In general, consistent partners help to create a stable social environment, and the loss of important partners can elicit a stress response (Engh et al., 2006). Affiliative partners that persist over time may also promote reciprocal grooming (Taborsky, 2013) or provide coalitionary or affiliative support on a subject's behalf during or after an aggressive encounter (Silk et al., 2010a). More passively, consistent partners may tolerate a subject's presence during feeding (Marshall, Carter, Coulson, Rowcliffe, & Cowlishaw, 2012). The benefits of consistent partners are presumably amplified when partners affiliate more intensely (Silk et al., 2010b). The fact that strong bonds over multiple years actually decreased survival when partners were inconsistent, rather than having a neutral influence, suggests that maintaining strong bonds may be costly to blue monkey females.
T A B L E 1 Influence of (standardized) fixed-time predictors on risk of death. N = 83 females, 20 deaths The effects of current relationship quality on immediate survival (in a time-dependent model) also suggested that strong bonds were costly.
Maintaining currently strong bonds with few close partners from previous years was riskier than being strongly bonded with many previously close partners. This finding emphasizes that if a female maintains strong bonds, she should do so with partners that are relatively consistent. It also suggests that females may not only lose the return on investment in strong bonds with future inconsistent partners, but they may also pay a cost when associating most frequently with "new" partners.

| Comparison with other social species
This study is the first survival analysis to examine how social connections influence longevity in an arboreal primate (Archie et al., 2014;Brent et al., 2017;Foster et al., 2012;McFarland et al., 2017;Nuñez et al., 2015;Silk et al., 2009Silk et al., , 2010bStanton & Mann, 2012;Yee et al., 2008) and to compare the cumulative versus current effects of relationship quality. Results both concur with and differ from these and other previous studies of how social relations influence other direct fitness measures Cameron et al., 2009;Gilby et al., 2013;Kalbitzer et al., 2017;McDonald, 2007;Schülke et al., 2010;Silk et al., 2003;Vander Wal et al., 2014).
Similar to all the above studies, we found that greater sociality in the form of stronger top bonds can indeed correspond with higher survival in blue monkey females. However, in contrast to several previous studies, strong bonds actually correspond with lower survival in certain situations (i.e., when bond partners change from year to year), suggesting that maintaining bonds is costly. Indeed, over multiple years, females that were weakly bonded had a lower risk of death than females that were strongly bonded to partners that were inconsistent over time.
Blue monkey females seem to receive a return on their social investment only if bond partners are relatively consistent. Somewhat similarly, affiliation appears to be costly to female marmots because strongly affiliating females produced fewer offspring (although the causal relationship between affiliation and reproduction was not clear, Wey & Blumstein, 2012) and are more likely to die during hibernation (Yang, Maldonado-Chaparro, & Blumstein, 2016). Also similarly, in white-faced capuchin, the costs and benefits of females' strong bonds depend on male behavior (Kalbitzer et al., 2017). The offspring of strongly bonded females was more likely to fall victim to infanticide during alpha male replacements, but during periods of alpha male stability, they were more likely to survive. As the strongest bonds of blue monkey females are not necessarily with a consistent set of partners (unlike in baboons, Silk et al., 2010b), females may actually benefit by saving the time and energy spent on cultivating strong bonds. Those savings and their benefits remain to be quantified on a mechanistic level.
Because within-group agonism and alliances are rare in blue monkeys (Klass & Cords, 2015), the function of their social bonds in general may be to maintain group cohesiveness rather than orchestrate competitive power relations within groups. Group-wide cohesion may not require particularly strong bonds.

| CONCLUSIONS
We found that stronger bonds do not necessarily increase survival in females in a matrilocal, gregarious species. In adult female blue monkeys, stronger bonds with close social partners decreased survival when close partners were inconsistent over time. When strong bonds were consistent over multiple years, survival was high relative to all other strategies. It appears, then, that strong bonds may be costly to adult females and are a productive "investment" only in situations where their benefit outweighs their cost. Other longitudinal, individual-based studies that examine the influence of social ties on fitness may find it useful to incorporate variables that capture variation in the potential costs and benefits of social ties.
In general, studies such as ours that find a correlation between the quality of social ties and survival in animals are only a first step in understanding the actual mechanisms by which social ties influence fitness. Although it is a regular challenge of long-term field studies to obtain high-resolution data on individuals' physiological status and social interactions simultaneously, future studies should aim to resolve the three-part connection between social ties, physiological status, and fitness outcomes whenever possible. Consideration of social measures and timescales relevant to study species will help us to understand how social ties influence fitness.