Get 20M+ Full-Text Papers For Less Than $1.50/day. Subscribe now for You or Your Team.

Learn More →

Social support reduces stress hormone levels in wild chimpanzees across stressful events and everyday affiliations

Social support reduces stress hormone levels in wild chimpanzees across stressful events and... ARTICLE Received 4 Dec 2015 | Accepted 27 Sep 2016 | Published 1 Nov 2016 DOI: 10.1038/ncomms13361 OPEN Social support reduces stress hormone levels in wild chimpanzees across stressful events and everyday affiliations 1,2,3, 1,2,3, 1 4 1, Roman M. Wittig *, Catherine Crockford *, Anja Weltring , Kevin E. Langergraber , Tobias Deschner ** 2,3,5, & Klaus Zuberbu¨hler ** Stress is a major cause of poor health and mortality in humans and other social mammals. Close social bonds buffer stress, however much of the underlying physiological mechanism remains unknown. Here, we test two key hypotheses: bond partner effects occur only during stress (social buffering) or generally throughout daily life (main effects). We assess urinary glucocorticoids (uGC) in wild chimpanzees, with or without their bond partners, after a natural stressor, resting or everyday affiliation. Chimpanzees in the presence of, or interacting with, bond partners rather than others have lowered uGC levels across all three contexts. These results support the main effects hypothesis and indicate that hypothalamic-pituitary- adrenocortical (HPA) axis regulation is mediated by daily engagement with bond partners both within and out of stressful contexts. Regular social support with bond partners could lead to better health through daily ‘micro-management’ of the HPA axis, a finding with potential medical implications for humans. 1 2 Max Planck Institute for Evolutionary Anthropology, Department of Primatology, 04103 Leipzig, Germany. University of St Andrews, School of Psychology 3 4 & Neuroscience, St Andrews, KY16 9JP, UK. Budongo Conservation Field Station, PO Box 362, Masindi, Uganda. Arizona State University, School of Human Evolution & Social Change and Institute of Human Origins, Tempe, Arizona 85281, USA. University of Neuchatel, Department of Comparative Cognition, 2000 Neuchatel, Switzerland. * These authors contributed equally to this work. ** These authors jointly supervised this work. Correspondence and requests for materials should be addressed to R.M.W. (email: wittig@eva.mpg.de) or to C.C. (email: crockfor@eva.mpg.de). NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 24,25 or animals, including humans, there is much evidence that provide predictable social support . Here, we compared individuals who maintain stable, close social bonds have the effects of partners with predictable support patterns (bond Fgreater reproductive success, increased longevity and better partners) with those of unpredictable support patterns (non-bond 1–5 health compared with those who do not . A key mechanism partners) on uGC levels. through which these benefits could operate is through social In contrast to previous correlational studies, where GC measures buffering, in which social support provided by bond partners were typically averaged over extended time periods, which 9–11,23 cushions the aversive effects of stressful events through mediation included a multitude of stressful events ,we used an event 6–9 of the hypothalamic-pituitary-adrenocortical (HPA) axis . sampling approach measuring uGC levels that corresponded to a In particular, the presence of bond partners during a stressful single event . Applying a fixed latency for clearance of GCs into 7–10 26,27 event can result in lower glucocorticoid (GC) levels or urine , we created relative uGC levels by dividing uGC levels help to reduce them sooner after the event, compared with when relating to the event by uGC levels relating to before the event. 11–13 bond partners are not available . Events were stressors (intergroup encounters), everyday affiliations Alternatively, bond partners may have a more generalized (grooming) or control periods (resting without social interaction). positive effect, insofar as subjects can rely on general social Intergroup encounters are highly stressful events, associated support beyond periods of acute stress. General social support with high GC levels , in which chimpanzees face potentially 29–31 may create more predictability within social interactions and lethal aggression when they encounter rival groups ,but 6,14 more stability in the social environment . This main effects they can also involve social support. A key factor in winning inter- 6 31,32 hypothesis is less examined in non-human animals, despite its group encounters is to out-number rivals through coordinated 6,14,15 33,34 potential implications for promoting health and longevity . attacks involving coalitionary support against rivals . Although there is some empirical support for this hypothesis in Coalitionary and social support rather than retreat (defection) 15–17 humans , the underlying mechanism that enables such a from group members is crucial to rout rivals in direct 29,32 main effect is unknown. Some studies suggest main effects may confrontations . Thus, we noted the occurrence of social 6 14,17 also be mediated by the HPA axis , or by other mechanisms . support during intergroup encounters, only when individuals Physically and psychologically-induced stress can cause joined in vocal or physical aggression against rivals. 6–8 dysregulation of the HPA axis, provided the stress is repeatedly To test the social buffering hypothesis in wild chimpanzees 18 19 acute or chronic . This dysregulation can lead to severe health using a within-subjects design, we predict the following: if social 8,20 problems , suggesting that any mechanisms that moderate such support in chimpanzees is effective during stressors, we expected aversive effects will be under positive selection. Social buffering the Relationship Quality of the participants to impact on urinary during stress exposure shows regulatory, stabilizing effects on glucocorticoid (uGC) levels only when experiencing a stressor. 7,8 HPA activity , but it is equally possible that the same effect is Specifically, we predicted an interaction between Event (intergroup also caused by everyday affiliations between individuals that encounter, resting, grooming) and Relationship Quality (bond, predictably offer social support to one another. non-bond) such that uGC levels would be reduced during stressors While the main effects hypothesis predicts HPA regulatory (intergroup encounters) but not during resting or everyday effects of social partners in both stressful and non-stressful affiliations (grooming), when bond partners rather than other situations, the social buffering hypothesis excludes HPA axis individuals participated. 6,14 regulation outside of stressful events. To test between these two To test the main effects hypothesis , we predicted the hypotheses and to investigate their predicted impact on HPA axis following: if social support impacts on uGC levels during activity, we monitored subjects’ urinary glucocorticoid (uGC) everyday affiliation (grooming), resting and during a stressor levels in reaction to acute stressors, everyday affiliations and (intergroup encounters), we expected the Relationship Quality of resting. Since general social support is usually measured as social participants to impact on uGC levels irrespective of context, such 6,14 integration in the community or as the presence of reliable that GC levels would be reduced by bond partners rather than 7,11–13 supporters , we contrasted subjects’ uGC levels in the three other individuals across contexts. In addition, we predicted no contexts depending on the participation or presence of a bond interaction effects between Event and Relationship Quality. partner, who by definition provides predictable support. We tested the social buffering and main effects hypotheses by The impact of social support on stress and health is often comparing uGC levels in wild chimpanzees associated with posited as a causative relationship; however, whether social three events: potentially life-threatening stressors (intergroup 29,31 11,23 relationships promote lower stress and better health or rather encounters ), everyday affiliations (social grooming ) and whether healthier and less stressed individuals are better able to control periods (resting). We show that chimpanzees have maintain relationships is not well established, given that most reduced uGC levels when they are together with bond partners studies are correlational . To address this issue, we used a within- rather than other chimpanzees, irrespective of context. Further subjects design, so that the same individuals were tested in each analyses revealed that the ameliorative effects of bond partners condition and we compared changes in uGC levels due to events. were most pronounced during contexts requiring active support Another unresolved issue is whether only active support rather than the passive presence of bond partners, with the largest 6,17 (instrumental help) mediates HPA axis activity, or whether effects during stressors then grooming contexts, and least so 6,17 the mere presence of a bond partner (social companionship) is during resting contexts. Our results indicate that the predictable enough to do so. Also, it remains unclear whether perceived or social support of bond partners may help to micro-manage HPA 14,17,22 actual support is more beneficial , or whether predictability axis activity, during both stressful and everyday events, 15,23 of support is a key component for stress regulation . supporting the main effects hypothesis. Chimpanzees are a good model species for exploring these issues. They have highly differentiated relationships with group members, with individuals maintaining close social bonds with Results one or several other group members . Close social bonds are Stressful events and everyday affiliation predict uGC levels.We defined as high rates of consistent mutual cooperative and first tested if relative uGC levels were influenced by Event affiliative behaviours (grooming, coalitionary support and (intergroup encounters, resting, grooming). To control for food sharing) between two individuals, which are maintained physical exertion, security in numbers and sex effects, we added over several months or years. Bond partners, thus by definition Event Duration, Number of Chimpanzees Present and Subject’s 2 NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 ARTICLE Sex as control predictors. Given that subjects were sampled more we tested whether chimpanzees’ relative uGC levels within each than once and sometimes from the same Event, we added Subject context were significantly higher or lower than expected ID and Event ID as random effects (Table 1: General Model). levels. We calculated the expected relative uGC level by Both Event and Event Duration significantly affected uGC levels estimating the diurnal decline in uGC levels (Supplementary (likelihood ratio test: df ¼ 2, w2 ¼ 7.98 and P ¼ 0.019), but the Note 1, Supplementary Fig. 2). The results of the bootsrap interaction of Event and Event Duration was not significant, and procedure showed that grooming with a bond partner decreased ± ± therefore removed (Wald test: df ¼ 2, w2 ¼ 5.21, P ¼ 0.074, uGC levels (bootstrap: mean deviation SE¼ 13.3 6.5, Supplementary Table 1). Intergroup encounters resulted in CI ¼ (  25.9;  0.8), N ¼ 10, Po0.05) and engaging in higher relative uGC levels than grooming or resting events intergroup encounters without a bond partner increased ± ± (Fig. 1; Table 1: General Model) and longer events resulted in uGC levels (bootstrap: mean deviation SE ¼ 31.9 12.9, higher relative uGC levels (Supplementary Fig. 1), while Number CI ¼ (7.9; 64.9), N ¼ 7, Po0.05). In contrast, when grooming a of Chimpanzees Present and Subject’s Sex did not significantly non-bond partner (bootstrap: mean deviation±SE ¼ 2.7±4.1, influence uGC levels. The effect size of the fixed effects in model 1 CI ¼ (  6.4, 9.5), N ¼ 11) and engaging in intergroup encounters was R ¼ 0.170. with a bond partner (bootstrap: mean deviation SE ¼ 0.5 9.0, CI ¼ (  17.8; 16.5), N ¼ 8), confidence intervals included 0 and therefore were not different from expected relative Social buffering and main effects hypotheses. In the second uGC levels. Finally, relative uGC levels after resting with a bond model we investigated whether the social buffering or main effects partner did not differ from expected values (bootstrap: mean hypotheses were best supported by the data. We tested if relative ± ± deviation SE¼ 2.5 5.5, CI ¼ (  13.3; 7.0), N ¼ 13), but uGC levels were affected by the interaction of predictors resting without bond partners had an insufficient sample size to Event and Relationship Quality (bond versus non-bond partners), be tested (N ¼ 5). while controlling for the Sex and Kin (close maternal kin) relationships of the two participants, and including Subject ID and Event ID as random factors. Although the full model was Discussion significantly different from the null model (likelihood ratio test: Within each event, subjects’ relative urinary glucocorticoid levels df ¼ 5, w2 ¼ 13.93,P ¼ 0.016), we neither found a significant were lower when engaging with bond partners rather than other interaction between Event and Relationship Quality on uGC individuals, whether during a stressor (intergroup encounters), levels, nor between Subject’s Sex and Partner’s Sex (Table 2a: everyday affiliation (grooming) or resting. Bond partner effects, Social Buffering Model, Fig. 2). After removing both non-significant interactions from the model, both test predictors (Event and Relationship Quality) significantly influenced relative uGC levels (Table 2b: Main Effects Model, Fig. 2). Specifically, relative uGC levels were on average almost 22% higher after intergroup encounters than after 110 grooming events and on average 48% higher after resting than grooming events. In addition, subjects participating in events with 100 bond partners rather than other individuals had on average 23% lower relative uGC levels, across events (Table 2b: Main Effects Model). Neither Kin nor Sex of subject showed a significant influence on relative uGC levels, while the relative uGC levels varied depending on the Sex of Partner, with subjects of male partners having higher relative uGC levels. The effect size of the Grooming Resting Intergroup encounter fixed effects in model 2 was R ¼ 0.196. Figure 1 | Individual relative urinary glucocorticoid (uGC) levels change Extent of bond partner impact on uGC levels. Engaging with with Event. Mean relative uGC levels (%) 95% confidence interval bond partners lowered relative uGC levels across all events, depend on the event sampled (grooming N ¼ 31, resting N ¼ 18, intergroup encounter N ¼ 21), such that Event predicted the relative uGC level of Sonso although to determine the extent of bond partner impact within contexts requires further testing. Therefore, using bootstrapping, chimpanzees (Wald test: df ¼ 2, w2 ¼ 7.98, P ¼ 0.018). Table 1 | The impact of Event on urinary glucocorticoid (uGC) levels. Response variable: relative uGC P value Parameter Estimate SE t Predictor variable df v2 General model Intercept 65.8 11.7 Event* 2 7.98 0.018 Intergroup 25.55 9.36 2.73 Rest  4.50 9.35  0.48 Groom 0 Subject’s Sex 1 0.51 0.474 Male  6.17 8.33  0.74 Number of Chimpanzees Present 1 0.05 0.828 0.15 0.67 0.23 Event Duration 1 7.60 0.006 Minutes 0.45 0.15 2.86 Random factors: Identity of Subject, Event. Bold: Po0.05. Intergroup: Intergroup encounter, Rest: resting event, Groom: grooming event. Likelihood ratio test (full versus null model comparison): df ¼ 2, w2 ¼ 7.98, P ¼ 0.019. Effect Size of fixed effects: marginal R ¼ 0.170. This model with the non-significant interaction of duration and event is presented in Supplementary Table 1. LMM: *test predictor, wcontrol variable. NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications 3 Relative uGC levels ± 95% CI ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 Table 2 | The impact of Event and Relationship Quality on urinary glucocorticoid (uGC) levels. Response variable: relative uGC P value Parameter Estimate SE t Predictor variable df v2 (a) Social Buffering Model Intercept 68.01 16.13 Event  Relationship Quality* 2 1.66 0.437 Intergroup  Bond  13.71 16.64  0.82 Rest  Bond 13.80 19.55 0.71 Groom  Bond 0 Kin 1 2.29 0.130 Kin 20.32 13.15 1.55 Subject’s Sex  Partner’s Sex 1 0.16 0.686 Male  Male  8.01 19.77  0.41 (b) Main Effects Model Intercept 71.43 14.78 Event* 2 6.14 0.047 Intergroup 21.78 8.60 2.53 Rest 8.35 9.37 0.89 Groom 0 Relationship Quality* 1 6.77 0.009 Bond  23.13 8.65  2.67 Kin 1 2.78 0.096 Kin 20.99 12.27 1.71 Subject’s Sex 1 0.01 0.979 Male  0.25 9.66  0.03 Partner’s Sex 1 4.46 0.035 Male 21.77 10.13 2.15 Random factors: Identity of Subject, Event. Bold: Po0.05. Intergroup: Intergroup encounter, Rest: resting event, Groom: grooming event. (a) Social Buffering Model testing social buffering hypothesis. Likelihood ratio test (full versus null model comparison): df ¼ 5, w2 ¼ 13.93, P ¼ 0.016. (b) Main Effects Model testing the main effects hypothesis. Likelihood ratio test (full versus null model comparison): df ¼ 3, w2 ¼ 12.94, P ¼ 0.005. Effect Size of fixed effects: marginal R ¼ 0.196. LMM: *test predictor, wcontrol variable. partners did not participate in the encounter. The same chimpanzees facing potentially life-threatening intergroup encounters together with a bond partner did not have elevated uGC levels. This result demonstrates that the participation of a bond partner, who by definition provides predictable social support, regulates HPA activity and buffers the stress reaction 110 even in potentially lethal situations. Less predictable supporters were less effective in buffering uGC levels. Our results showing buffering effects of bond partners on HPA axis activity concur 12,13 with experimental studies in humans , where bond partners buffer psychologically-induced stress, and studies examining 9–11 naturally occurring social stressors in non-human primates . In the non-human primate studies, correlations show that bond 60 partners seem to buffer baseline GC levels following severe social stressors, such as, the threat of infanticide , sudden social isolation and during milder social stressors, such as conspecific aggression . Grooming Resting Intergroup encounter bond non-bond bond non-bond bond non-bond Chimpanzees showed lower relative uGC levels during every- day affiliative interactions (grooming events) compared with Figure 2 | Event and Relationship Quality change individual relative resting events. However, uGC levels decreased only when urinary glucocorticoid (uGC) levels. Mean relative uGC levels (%) 95% chimpanzees groomed with a bond partner. In contrast, subjects confidence interval depend on the Event sampled: occurring with either a grooming with a non-bond partner showed uGC levels similar to bond or a non-bond partner (grooming with bond partner N ¼ 14 and non- resting control samples. This shows that bond partners have bond partner N ¼ 17, resting with bond partner N ¼ 13 and with non-bond moderating effects on HPA activity during everyday grooming partner N ¼ 5, intergroup encounter with bond partner N ¼ 11 and non-bond events, outside of stressor contexts. A correlational study on wild partner N ¼ 10). Both Event (Wald test: df ¼ 2, w2 ¼ 6.14, P ¼ 0.047) and baboons is also suggestive of this pattern, where female baboons Relationship Quality (Wald test: df ¼ 1, w2 ¼ 6.77, P ¼ 0.009) predicted the during periods of social stability had lower baseline GC levels relative uGC level of Sonso chimpanzees. when they were able to focus their grooming on a few preferred individuals rather than showing more distributed grooming however, were strongest during intergroup encounters, then patterns . In both stressful and grooming contexts, our results during grooming and least during resting. The social buffering indicate a positive relationship between predictable social support hypothesis predicts bond partner effects during stressors only, objectively measured from social interaction histories and the whilst the main effects hypothesis expects bond partner effects stress buffering potential of supporters. during both stressors and everyday events. Thus, our results show Model 2 suggests that bond partner effects on uGC levels were support for the main effects rather than the social buffering also evident during resting events. This result, however, has to be hypothesis (see Fig. 2 in ref. 6). treated with caution, since sample size for resting without Chimpanzees showed significantly higher relative uGC levels bond-partners is low which leads to instability problems. after stressful events (intergroup encounters) compared with after Nevertheless, the result is interesting since experimental studies resting. However, uGC elevation was evident only when bond with humans usually do not distinguish between social support 4 NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications Relative uGC levels ± 95% CI NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 ARTICLE due to the mere presence of bond partners , and active support oxytocin may be key to the underlying mechanism precipitating 13 7–9 offered by bond partners . In our study, although the effect is the the social regulation of the HPA axis . same, the estimates due to bond partners are different (Fig. 2), Crucially, engaging an oxytocin—HPA axis interaction by increasing from resting to grooming to intergroup contexts. This participating with predictable supporters during ordinary everyday finding indicates that active support from bond partners is more affiliative contexts may help maintain a healthy homoeostasis. We effective in lowering uGC levels than is their mere presence. propose that a possible underlying process could be that daily Everyday affiliative interactions with bond partners have been affiliative social interactions help regulate—or micromanage—the predicted to improve physical and mental health, although the HPA axis. This in turn may help to maintain stable immune- mechanism through which the benefits might be accrued has function, cardio-function, fertility, cognition and mood, key 14,16 6 8,14,15,39 remained evasive . Cohen and Wills suggested that benefits aspects known to be affected by a dysregulated HPA axis . might be mediated through similar mechanisms as social The close phylogenetic relationship between humans and buffering effects, specifically involving the HPA axis. Our chimpanzees suggests that HPA axis micro-management through results suggest that this is indeed the case: engaging in three daily affiliative social interactions could also occur in humans. types of activity with predictable bond partners lowered subjects’ Bond partner effects were strong such that even during a uGC levels, whether during highly stressful interactions, resting potentially life-threatening inter-group encounter, bond partners or everyday affiliative interactions. buffered the stress response. It could be argued that since the Given that both male and female subjects participate in triggering of the stress response is vital for maximizing the 34 40 grooming and intergroup encounters (and this study), we physical response in a fight situation , it is not necessarily contrasted the relative uGC levels of both female and male adaptive for bond partners to buffer the stress response in fight subjects, as well as the sex combination of the dyad. Neither contexts. However, bond partners by definition in this study have subjects’ sex nor the sex combination of the dyad influenced a predictable history of providing social and agonistic support to relative uGC levels in any model. Thus, for both male and female one another . Thus, it may be that subjects are indeed safer when chimpanzees, the impact of participating in stressors or everyday engaging in inter-group encounters when bond partners are also affiliations with a predictable partner of either sex, compared with participating and subjects thus ‘require’ less or shorter HPA axis another individual, similarly regulates the HPA axis. This result is activity to ensure survival. This interpretation might offer one not unexpected, even in intergroup encounters, where both males explanation as to why chimpanzees and humans seek bond 34 30,33,36 and females participate. Females engage often in vocal aggression partners when initiating conflict with rival groups . Another (Supplementary Movie 1), which is highly effective in deterring possible explanation for these results is that our method can only 24 34,35 within-group , as well as out-group members . Both sexes can measure strong changes in relative uGC levels and do not detect incur high costs from attacking or being attacked (injury or short or minor increases in stress response activity. 31,36,37 death) . However, it is likely that males do not gain In this study, chimpanzees supported by bond partners showed comparable vocal or physical support from females as they do no significant up-regulation of their HPA axis when participating in from males, and we cannot rule out that a larger sample may show an intense stressor (inter-group encounters), and showed signifi- some sex effects. It should be noted that in this data set, all mixed- cant down-regulation of their HPA axis in everyday affiliations sex bond partner dyads consisted of mothers and their sons. (grooming) compared with support from other individuals. These For grooming events, the uGC patterns mirror urinary results suggest that bond partners can influence HPA axis activity oxytocin levels found after grooming in the same chimpanzee both during highly stressful situations, as well as during everyday population . In this previous study, grooming with a bond activities, such as grooming. The HPA axis is vulnerable to partner was associated with higher urinary oxytocin levels dysregulation, particularly when exposed to intense or repeated 8,18–20 compared with grooming with a non-bond partner or periods stressors . Such HPA axis dysregulation can have negative and 8,18–20,39,41 of resting, independent of whether subjects were giving or long-term effects on physical and mental health . Social receiving grooming. These contrasting GC and oxytocin results buffering may have an immediate effect during a stressor of 6–8,12,13 are similar to those of two social buffering experiments exposing reducing HPA axis activity . However, daily management of humans to a psychological stressor. In trials in which social the HPA axis through repeated affiliations from predictable social support was offered from a bond partner, subjects had earlier supporters may protect against dysregulation of the HPA axis over decreasing GC levels. One study showed lower GC levels and the longer term . The mechanism that might account for returned faster to baseline in conditions in which urinary reported effects of better health when engaging in everyday 13 6,14,16,17,21 oxytocin levels increased . The other study showed greatest affiliations with bond partners, has remained elusive . GC decreases in trials with both social support by bond partners Here, we demonstrate that, as for stressors, bond partners also and intranasal application of oxytocin before the stressor . Thus downregulate HPA axis activity even during an everyday affiliation, our observations are in line with the idea that oxytocin has a grooming and with a weaker effect, by their mere presence when 7–9 6 dampening role in cortisol secretion . In chimpanzees, active resting, as proposed by Cohen and Wills’ main effects hypothesis . social support from bond partners seems to have more From these results, we hypothesize for future testing that regular pronounced effects on urinary oxytocin levels , as well as on and repeated, everyday affiliations have the potential to regularly uGC levels, than the mere presence of bond partners . Likewise, and repeatedly re-align the HPA axis throughout the day. This it is possible that participating in activities with predictable bond could amount to ‘micro-managing’ effects on the regulation of the partners in humans may be more effective in HPA axis HPA axis, resulting in stable HPA activity over time, and providing management than either merely associating with bond partners long-term benefits to physical and mental health. without active participation, or participation with less predictable supporters. To date, these conditions have rarely been contrasted Methods 12,13 in the human literature . Given that we examined the same Subjects. We observed chimpanzees (Pan troglodytes schweinfurthii, 0 0 Supplementary Data 1) of the Sonso community, Budongo Forest (135 —155 N, chimpanzees in the same contexts with and without bond partner 0 0 3108 —3142 E), Uganda, from February 2008 to July 2010. The Sonso participation, and that we measured relative change in uGC levels community has been continuously observed since 1990 (ref. 42), and was after, compared with before, the events, supports a causative effect comprised of 15 males (adults: Z15 years: 10; subadult: 10–14 years: 5), 35 females between bond partner support and lower HPA axis activity, in (adult: Z14 years: 27; subadult: 10–13 years: 8) and 28 juvenile and infants during everyday affiliations as well as during stressors. The neuropeptide the study period. We sampled urine from nine adult male and eight adult female NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications 5 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 urine samples in 4 events, N ¼ 6 subjects). Chimpanzees show intimate reassurance chimpanzees—those that were regularly observed to improve the likelihood of behaviour after detecting rival groups, including embracing, placing their finger in within-subject sampling across behavioural conditions. Permissions to conduct this others’ mouth, holding others’ testes or grooming (Supplementary Movie 1). research was granted by Uganda Wildlife Authority (TDO/33/02) and Uganda Urinary GC levels were measured at the Behavioural Endocrinology Lab at the National Council for Science and Technology (NS 181) and overseen by Budongo Max Planck Institute for Evolutionary Anthropology using high-performance Conservation Field Station and the University Teaching and Research Ethics liquid chromatography-tandem mass spectrometry (LC-MS/MS) . Samples with a Committee of St Andrews University. recovery of the internal standard deviating by o 50% from the expected value were included in the analysis. In cases of large deviation we re-measured the Observation methods. A team of up to six observers followed up to three parties samples. If a large deviation persisted, we re-extracted and re-measured the of chimpanzees (independently moving subgroups of flexible composition) from samples. We excluded samples where the large deviation still persisted. B7 a.m. to 5 p.m. through the forest, recording behaviours using ‘all occurrence’ Examination of LC-MS/MS data was carried out with MassLynx (version 4.1; sampling for aggressive (agonistic support, contact and non-contact aggression) QuanLynx-Software). Only a fraction of plasma cortisol can be found in 27 44 and affiliative social interactions (grooming, food sharing, sitting in close proximity chimpanzee urine , while metabolites of cortisol are found in higher quantities . (within 1 m)), and 15 min scan sampling for party composition, where ‘party’ is a To quantify the urinary glucocorticoid excretion (uGC), we used the sum of subgroup of individuals in view. In addition, we recorded intergroup encounters urinary cortisol plus four of its metabolites (tetrahydrocortisol, whenever they were observed. We focused on three event types: (1) intergroup tetrahydrocortisone, 5b-androstane and 11-oxoetiocholanolon). The sum of uGC encounters: subjects had auditory or visual contact with a rival community. comprised on average 9% cortisol, 37% tetrahydrocortisol, 35% tetrahydrocortison, Subjects were sampled if classified as engaging in social support of group members, 5% 5b-androstane and 14% 11- oxoetiocholanolon. We corrected the uGC levels which required approaching in the direction of the rivals and responding with with the creatinine levels of each sample to control for differences in water content chorused (coalitionary) vocal aggressive behaviour (barks, pant roars, buttress of urine samples . We excluded samples with a creatinine level of o0.05 mg drumming and pant hoots) and/or coalitionary physically aggressive behaviour creatinine ml urine from the analysis. 26,38,46 (charging, chasing, hitting and biting) towards out-group members. Support was Using an event-sampling approach , we then calculated the relative uGC coded as ‘mutual’ in all cases, given that all receive a benefit from another’s levels for each Event, using a method that took the clearance window of cortisol participation, whether it occurs before or after their own. These intergroup events into urine into account (see Fig. 1 in ref. 26). We defined a pre-period (representing were also not characterized by grooming bouts either before, during or after the the uGC levels from before the event) and a peak-period (representing the uGC intergroup encounters. Since the natural frequency of encounters with the rival levels related to the event), taking into account the delayed GC clearance in 26,27 47 communities was low (nine encounters were sampled during the observation time), chimpanzee urine and the diurnal decrease of uGC levels in chimpanzees we also conducted four drumming experiments to simulate the presence of a rival (Supplementary Fig. 2, Supplementary Note 1). We calculated the mean uGC levels community (see experimental procedure); (2) resting events, in which one for the pre-period (from samples taken between the start of the event until 135 min individual had no social interaction for a minimum of one hour and was sitting or after the start of the event) and the mean uGC levels for the peak-period (from lying for at least the first 30 min; and (3) grooming events, in which two individuals samples taken between 135 min until 270 min after the event þ event duration) for groomed each other for at least 20 min without a break and had no additional each event. Samples taken within 30 min after the pre or the peak-period were still social interaction for at least 1 h after the beginning of the grooming event. assigned to the preceding period, if the focal individual had not urinated within the Grooming duration as well as minutes spent giving, receiving or engaging in both last 30 min of the preceding period . Finally we calculated the relative uGC levels simultaneously (mutual) were recorded. as a percentage of how high the uGC levels were during the peak-period compared with the pre-period: uGC peak  period Experimental procedure. We waited for a subgroup—or party—of chimpanzees relative uGC ¼ 100 ð1Þ to rest in the periphery of their territory in an area where we had observed uGC pre  period intergroup encounters during the last year. After resting without vocalising for at We calculated an average decrease of 5.55% of the uGC level per hour of the day. least 10 min, an experienced field assistant mimicked a typical mid-length chim- Taking an average time difference of 135 min between peak and pre-period panzee buttress tree drum, striking 7 beats with his fists on the buttress roots of a samples, peak-period samples should be 12.49% lower than pre-period samples. A tree about 100 m away from the resting party in the direction of the rival com- relative uGC level of about 87.5% therefore reflected a neutral effect of the event munity’s territory. Importantly, before and during the drumming simulation, we behaviour on the uGC level only including the estimated diurnal decline of uGC. took extreme care that Sonso chimpanzees could not see or hear any person Levels above the expected relative uGC level of 87.5% would represent an increase moving in the direction where the drumming experiment would or just had and below the 87.5% would represent a decrease in uGC levels due to the event. occurred. In all four trials, the chimpanzees showed behaviour indistinguishable from natural intergroup encounters (pilo-erection, reassurance behaviours, cautious and silent approach to the drumming tree followed by aggressive displays, Definition of social bonds. The Relationship Quality of chimpanzees can be aggressive vocalizations, like pant-roars and pant-barks and drumming). Eight of 48 defined by three components such that those that share close social bonds engage 21 intergroup encounter data points were experimentally simulated encounters in: (1) high rates of socio-positive and cooperative behaviours and low rates of (Supplementary Data 1). We found that experimentally simulated intergroup socio-negative behaviours, (2) balanced or symmetrical offering of high rates of encounters produced no different reaction in uGC levels than natural encounters socio-positive and cooperative behaviours over time, (3) sustained patterns of (1) (likelihood ratio test: w ¼ 0.869, df ¼ 2, P ¼ 0.648; Supplementary Table 2). and (2) over at least a six month period. We described the quality of social Therefore we merged natural observations and experimental simulations of 24,38,46 relationships by calculating the composite relationship index (CRI) over intergroup encounters. quarter-year periods for all possible dyads. The CRI contrasts socio-positive and negative behaviours in relation to average behaviour rates per sex combination across dyads. Urine collection and hormone data analysis. After observing one of our target SP1ij SP2ij chimpanzees engaging in one of the three events (grooming, resting, intergroup NPij 43 SP1 SP2 encounters), we switched to ‘focal animal’ sampling of that individual for the next CRI ¼  ð2Þ 2 NP 6 h, collecting every possible urine sample and recording each behaviour and change in activity (see ref. 26). Urine was either pipetted from plastic bags, after the where SP1 ¼ rate of grooming bouts plus rate of resting in 1m proximity; bags were tied over a forked stick and held in the urine stream when subjects were SP2 ¼ rate of food sharing plus rate of coalitionary support; NP ¼ rate of aggression sitting in a tree, or from leaf matter when urination occurred on the ground after and contra-intervention, i ¼ individual (receiver of service) and j ¼ dyad partner subjects had moved away. After collection, urine samples were stored in a thermos (offering of service). A positive CRI indicated a more socio-positive relationship flask containing ice and were frozen in liquid nitrogen upon arrival in camp, which and a negative CRI showed a socio-negative relationship. A good indication that was within 10 h after collection. Urine collection did not commence if subjects had grooming and food-sharing are important bonding behaviours is that both have 38,46 engaged in aggression or grooming within the hour before the activities, and was been linked with elevated urinary oxytocin levels in chimpanzees . Dyads were aborted if subjects engaged in additional aggression or grooming within two hours only defined as bond partners when socio-positive relationships were symmetrical after the activity. We collected a total of N ¼ 574 urine samples from adult (reflecting similar rates of offered affiliations from both dyad partners) and long chimpanzees where we were able to determine uGC levels. lasting (Z 6 months: at least two consecutive blocks of quarter-year periods). We were able to assign N ¼ 394 of these urine samples (nine male and eight Balance and duration of relationships: scored through either a mutual socio- female chimpanzees, Supplementary Data 1) to a single event, either: (1) social positive relationship (CRI40) during the annual quarter of the sampled event and grooming (social support in an everyday context), sustained for 420 min (N ¼ 31 the preceding quarter, or a large mutual socio-positive relationship (CRI410) data point including 172 urine samples in 28 events, N ¼ 14 subjects); (2) resting during one of the quarters and a socio-neutral or positive relationship (CRIZ0) 24,38,46 (no support control), sustained for 430 min (N ¼ 18 data points including 108 during the other quarter . urine samples in 18 events, N ¼ 16 subjects); and (3) intergroup encounters (social Bond partners were defined as those with whom subjects engaged in high rates support in a stressful context), when chimpanzees saw out-group chimpanzees or of affiliative and cooperative behaviours (grooming, food sharing, coalitionary reacted vocally to calls of chimpanzees from real or simulated intergroup support) and low rates of aggression in both directions over at least two consecutive encounters (N ¼ 21 data points from natural encounters including 73 urine three month time periods providing an objective measure of historical samples in 9 events, N ¼ 7 subjects; and from simulated encounters including 41 predictability of social support . A histogram of mean CRI scores per dyad shows 6 NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 ARTICLE a bimodal distribution, with bonded relationships clustering in the higher scores model 2a (Social Buffering Model) where the interactions of Event and and non-bonded relationships clustering around zero (Supplementary Fig. 3). For Relationship Quality, as well as the interaction of Subject’s and Partner’s Sex this reason, we use Relationship Quality as a binomial variable. showed some instability and thus requires careful interpretation. To investigate whether or not the skewed distribution in the resting event has caused the insignificant effect for the test predictors’ interaction term, we run a full versus null Definition of kin relationships. We used genetic analysis to classify dydas as close model comparison, testing the interaction of Event and Relationship Quality only maternal kin (that is, mothers with offspring and maternal siblings) or not. for resting events and intergroup encounters (Supplementary Table 3). This Previous research suggests that as in most other group-living primates , comparison showed no significant effect of the interaction term (Wald test: df ¼ 1, chimpanzees can recognize and discriminate their mothers and maternal siblings . w2 ¼ 1.01, P ¼ 0.315), confirming the result of model 2a. Variables did not exhibit However, the ability of chimpanzees to recognize more distant maternal kin, who problems of collinearity (Variance Inflation Factor o4 in all cases, derived using anyways would be rare when all males stay in their natal group and the vast R-package car , and were tested using a standard linear model excluding the majority of female disperse, as occurs in Sonso, has not been demonstrated. Nor do random effect), suggesting that each predictor variable accounted for a portion of chimpanzees seem to recognize and discriminate their paternal kin . We collected the variance. We established the significance of the full model as compared with the fresh faecal samples after individually identified chimpanzees were observed null model (comprised of control predictors and random factors) using a likelihood defecating. Samples were either collected in plastic tubes and frozen within a 12 h ratio test . Since interactions between predictors do not allow interpretation of the period, collected in plastic tubes containing dessicating silica beads or collected in effect of the respective fixed factors in the model, we removed non-significant tubes filled with 95–99% ethanol and then transferred to tubes containing interactions to investigate the effects of the predictors. We calculated the marginal dessicating silica beads after 12–24 h (ref. 50). DNA was extracted from faeces 2 R (relative variance explained by fixed factors in relation to total variance) as the using the Qiagen DNA stool kit. We genotyped 92 chimpanzees at up to 19 effect size for the model. autosomal microsatellite loci. To guard against allelic dropout at the autosomal 61,62 Finally, we used bootstrap sampling methods with 1,000 permutations to loci, we first estimated the amount of amplifiable DNA in each extract through test whether relative uGC levels were significantly smaller or larger than the quantitative PCR, and then followed previously established guidelines showing that expected relative value, which was calculated to include estimated diurnal 26,47 depending on the amount of amplifiable DNA present in an extract, up to four decline (Supplementary Note 1). We calculated the mean for each individual independent PCR replications are required to be 99% confident that a putatively for each event with or without bond partner engagement and calculated the homozygous genotype is indeed homozygous . For heterozygous genotypes, each deviation from the expected value (expected relative uGC ¼ 87.5%). Values above 0 allele was observed in at least two independent PCRs (ref. 51). To guard against indicated an increase of uGC levels due to the event, values below 0 indicated a misidentification of individuals during sample collection or sample mix-up, in decrease of uGC levels due to the event. Since we had directed predictions (increase dyads that we strongly suspected from behavioural observations to be of uGC when interacting with a non-bond partner, decrease of uGC levels when mother-offspring pairs we checked that individuals shared at least one allele at interacting with a bond partner), we calculated the 5% interval on the predicted every autosomal locus. For individuals without suspected first-order maternal side of deviation from the expected value. relatives, we used a second, independently collected faecal sample to repeat the genotyping at six or more loci and required a perfect match with the original genotype. Using these methods, we were able to determine that o1% of samples Data availability. The authors declare that the data supporting the findings of this came from an incorrectly identified individual. In these cases, we genotyped study are available within the paper and its Supplementary Information files. additional extracts from independently collected faecal sample until the conflict was resolved. Microsatellite genotypes were produced through a two-step PCR multiplex procedure, using unlabelled primers for all 19 primers in the first References amplification, and fluorescently labelled forward primers and nested primers in the 1. House, J. S., Landis, K. R. & Umberson, D. Social relationships and health. subsequent single locus PCR reaction . PCR products were electrophoresed on an Science 241, 540–545 (1988). ABI PRISM 3100 Genetic Analyzer. Allele sizes determined using an internal size 2. Holt-Lunstad, J., Smith, T. B. & Layton, J. B. Social relationships and mortality standard (ROX labelled HD400) and Genemapper software version 3.7 (ref. 51). risk: a meta-analytic review. PLoS Med. 7, e1000316 (2010). We used the autosomal genotypes in likelihood based maternity analyses .All 3. Silk, J. B., Alberts, S. C. & Altmann, J. Social bonds of female baboons enhance eight dydas suspected of being mother-offspring from behavioural observations infant survival. Science 302, 1231–1234 (2003). shared an allele at each autosomal microsatellite locus and had maternity 4. Schu¨lke, O., Bhagavatula, J., Vigilant, L. & Ostner, J. Social bonds enhance assignments at the 95% confidence level using the CERVUS likelihood based reproductive success in male macaques. Curr. Biol. 20, 2207–2210 (2010). parentage program (Supplementary Data 2). There were two dyads (Harriette— 5. Silk, J. B. et al. Strong and consistent social bonds enhance the longevity of Gladis and Kalema—Kutu), where both members of a pair had unassigned female baboons. Curr. Biol. 20, 1359–1361 (2010). mothers, because the mothers’ samples were unavailable for genotyping; for these 6. Cohen, S. & Wills, T. A. Stress, social support, and the buffering hypothesis. two dyads the maternity assignments precluded a mother-offspring but not a Psychol. Bull. 98, 310–357 (1985). maternal sibling relationship. However, for one dyad (Kalema—Kutu) we were able 7. Hennessy, M. B., Kaiser, S. & Sachser, N. Social buffering of the stress response: to exclude the possibility that they were maternal siblings because they had different 473 base pair haplotypes at the hypervariable region-1 of the maternally diversity, mechanisms, and functions. Front. Neuroendocrinol. 30, 470–482 (2009). inherited mitochondrial DNA (ref. 53). While we could not use genetic data to exclude the possibility that the other dyad (Harriette—Gladis) were maternal 8. Kikusui, T., Winslow, J. T. & Mori, Y. Social buffering: relief from stress and siblings, we consider this unlikely given the low incidence of female philopatry at anxiety. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 361, 2215–2228 (2006). Sonso and in chimpanzees more generally (suggesting that Harriette and Gladis are 9. Young, C., Majolo, B., Heistermann, M., Schu¨lke, O. & Ostner, J. Responses to immigrants rather than natal to Sonso), as well as research in another community social and environmental stress are attenuated by strong male bonds in wild showing that it is extremely rare for maternal sisters to transfer from their natal macaques. Proc. Natl Acad. Sci. 111, 18195–18200 (2014). community to the same new community . We thus classified Harriette—Gladis as 10. Engh, A. L. et al. Behavioural and hormonal responses to predation in female unrelated in all analyses. chacma baboons. Proc. R. Soc. B 273, 707–712 (2006). 11. Wittig, R. M. et al. Focused grooming networks and stress alleviation in wild female baboons. Horm. Behav. 54, 170–177 (2008). Statistics. We employed linear mixed models to test the effects of the test 12. Heinrichs, M., Baumgartner, T., Kirschbaum, C. & Ehlert, U. Social support predictors Event (Model 1) and Event together with Relationship Quality and oxytocin interact to suppress cortisol and subjective responses to (Model 2) on relative uGC levels. We included Subject Identity and unique Event psychosocial stress. Biol. Psychiatry 54(12): 1389–1398 (2003). Identity as random factors and included several control predictors as additional 13. Seltzer, L. J., Ziegler, T. E. & Pollak, S. D. Social vocalizations can release fixed effects. To control for ‘safety in numbers’ we included the Number of oxytocin in humans. Proc. R. Soc. B 277, 2661–2666 (2010). Chimpanzees Present during each event. To control for expected glucocorticoid 14. Lakey, B. & Orehek, E. Relational regulation theory: a new approach to explain release due to energetic costs during intergroup encounters , we included the the link between perceived social support and mental health. Psychol. Rev. 118, event duration, predicting an interaction with event and event duration such that 482–495 (2011). longer intergroup encounters should result in higher energetic output and thus 15. Sapolsky, R. M. The influence of social hierarchy on primate health. Science higher uGC levels than shorter ones. This is in contrast to grooming and resting 308, 648–652 (2005). contexts in which no increase in energetic output was expected with event 16. Lakey, B. & Cronin, A. in Risk factors for depression (eds Dobson, K. S. & duration. To control for effects related to either subject’s sex, or partner’s sex or the Dozois, D.) 385–408 (Academic Press, 2008). combination of both, we included an interaction of these terms. Finally, when 17. Thoits, P. A. Mechanisms linking social ties and support to physical and mental testing the Relationship Quality we controlled for kin, since we expected close health. J. Health Soc. Behav. 52, 145–161 (2011). social bonds would provide uGC level effects regardless of kinship. 18. Radley, J. J. et al. Repeated stress induces dendritic spine loss in the rat medial The models were fitted in R 3.1.3 (ref. 57) using the function ‘lmer’ of the prefrontal cortex. Cerebr. Cortex 16, 313–320 (2006). R-package lme4 (ref. 58) with Maximum Likelihood. Residuals were normally distributed and homogenous, as shown by visual inspection of qq plots and 19. Juster, R. P., McEwen, S. B. & Lupien, S. J. Allostatic load biomarkers of chronic residual plots against fitted values. We checked for model stability by excluding stress and impact on health and cognition. Neurosci. Biobehav. Rev. 35, 2–16 subjects one at a time from the data and found models were stable, apart from (2010). NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications 7 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 20. McEwen, B. S. Central effects of stress hormones in health and disease: 49. Langergraber, K. E. in The Evolution of Primate Societies (eds Mitani, J. C., Understanding the protective and damaging effects of stress and stress Call, J, Kappeler, P. M., Palombit, R. A. & Silk, J.B.) 491–513 (Chicago mediators. Euro. J. Pharmacol. 583, 174–185 (2008). University Press, 2012). 21. Cohen, S. & Janicki-Deverts, D. Can we improve our physical health by altering 50. Nsubuga, A. M. et al. Factors affecting the amount of genomic DNA extracted our social networks? Perspec. Psychol. Sci. 4, 375–378 (2008). from ape faeces and the identification of an improved sample storage method. 22. Hostinar, C. E., Sullivan, R. M. & Gunnar, M. R. Psychobiological mechanisms Mol. Ecol. 13, 2089–2094 (2004). underlying the social buffering of the hypothalamic–pituitary–adrenocortical 51. Arandjelovic, M. et al. Two-step multiplex polymerase chain reaction improves axis: a review of animal models and human studies across development. the speed and accuracy of genotyping using DNA from noninvasive and Psychol. Bull. 140, 256–282 (2014). museum samples. Mol. Ecol. Res. 9, 28–36 (2009). 23. Crockford, C., Wittig, R. M., Whiten, P., Seyfarth, R. M. & Cheney, D. L. Social 52. Kalinowski, S. T., Taper, M. L. & Marshall, T. C. Revising how the computer stressors and coping mechanisms in wild female baboons (Papio hamadryas program CERVUS accommodates genotyping error increases success in ursinus). Horm. Behav. 53, 254–265 (2008). paternity assignments. Mol. Ecol. 16, 1099–1106 (2007). 24. Wittig, R. M., Crockford, C., Langergraber, K. E. & Zuberbu¨hler, K. Triadic 53. Langergraber, K. E. et al. The genetic signature of sex-biased migration in social interactions operate across time: a field experiment with wild patrilocal chimpanzees and humans. PLoS ONE 2, e973 (2007). chimpanzees. Proc. R. Soc. B 281, 20133155 (2014). 54. Langergraber, K. E., Mitani, J. & Vigilant, L. Kinship and social bonds in female 25. Langergraber, K. E., Mitani, J. C. & Vigilant, L. The limited impact of kinship chimpanzees (Pan troglodytes). Am. J. Primatol. 71, 840–851 (2009). on cooperation in wild chimpanzees. Proc. Natl Acad. Sci. 104, 7786–7790 55. Baayen, R. H. Analyzing Linguistic Data: a Practical Introduction to Statistics (2007). Using R (Cambridge University Press, 2008). 26. Wittig, R. M., Crockford, C., Weltring, A., Deschner, T. & Zuberbu¨hler, K. 56. Muller, M. N. & Wrangham, R. M. Dominance, cortisol and stress in wild Single aggressive interactions increase urinary glucocorticoid levels in wild male chimpanzees (Pan troglodytes schweinfurthii). Behav. Ecol. Sociobiol. 55, chimpanzees. PLoS ONE 10, e0118695 (2015). 332–340 (2004). 27. Bahr, N. I., Palme, R., Mo¨hle, U., Hodges, J. K. & Heistermann, M. Comparative 57. R Core Team. R: A language and environment for statistical computing aspects of the metabolism and excretion of cortisol in three individual (R Foundation for Statistical Computing, 2015). nonhuman primates. Gen. Comp. Endocrinol. 117, 427–438 (2000). 58. Bates, D., Ma¨chler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects 28. Sobolewski, M. E. The Hormonal Correlates of Male Chimpanzee Social models using lme4. J. Stat. Softw. 67, 1–48 (2015). Behavior (Doctoral dissertation, Smithsonian Institution, 2012). 59. Fox, J. & Weisberg, S. An R companion to applied regression (Sage, 2011). 29. Mitani, J. C., Watts, D. P. & Amsler, S. J. Lethal intergroup aggression leads to 60. Forstmeier, W. & Schielzeth, H. Cryptic multiple hypotheses testing in linear territorial expansion in wild chimpanzees. Curr. Biol. 20, R507–R508 (2010). models: overestimated effect sizes and the winner’s curse. Behav. Ecol. Sociobiol. 30. Watts, D. P. & Mitani, J. C. Boundary patrols and intergroup encounters in wild 65, 47–55 (2011). chimpanzees. Behaviour 138, 299–327 (2001). 61. DiCiccio, T. J. & Efron, B. Bootstrap confidence intervals. Stat. Sci. 11, 189–212 31. Wilson, M. L. et al. Lethal aggression in Pan is better explained by adaptive (1996). strategies than human impacts. Nature 513, 414–417 (2014). 62. Wittig, R. M. & Boesch, C. Receiving post-conflict affiliation from the enemy’s 32. Wrangham, R. W. & Glowacki, L. Intergroup aggression in chimpanzees and friend reconciles former opponents. PLoS ONE 5, e13995 (2010). war in nomadic hunter-gatherers. Hum. Nat. 23, 5–29 (2012). 33. Macfarlan, S. J., Walker, R. S., Flinn, M. V. & Chagnon, N. A. Lethal Acknowledgements coalitionary aggression and long-term alliance formation among Yanomamo¨ We thank Fred Babweteera, director of Budongo Conservation Field Station, and field men. Proc. Natl Acad. Sci. 111, 16662–16669 (2014). staff Monday Gideon, Jackson Okuti, Sam Adue and Jacob Aoli for their support during 34. Boesch, C. et al. Intergroup conflicts among chimpanzees in Tai National data collection. We acknowledge Royal Zoological Society of Scotland for providing core Park: lethal violence and the female perspective. Am. J. Primatol. 70, 519–532 funding to BCFS and Leakey Foundation (R.M.W., C.C., T.D., K.Z.), British Academy (2008). (C.C.), Leverhulme Trust (K.Z.) and Max Planck Society (R.M.W., C.C. and T.D.) for 35. Herbinger, I., Papworth, S., Boesch, C. & Zuberbu¨hler, K. Vocal, gestural and funding the research. locomotor responses of wild chimpanzees to familiar and unfamiliar intruders: a playback study. Anim. Behav. 78, 1389–1396 (2009). 36. Goodall, J. The Chimpanzees of Gombe: Patterns of Behavior (Belknap Press of Author contributions Harvard University Press, 1986). R.M.W. and C.C.: conception, implementation, statistical analyses, paper writing; T.D.: 37. Townsend, S. W., Slocombe, K. E., Thompson, M. E. & Zuberbu¨hler, K. conception, endocrinological field and lab advisor, paper writing; A.W.: glucorticoid Female-led infanticide in wild chimpanzees. Curr. Biol. 17, R355–R356 (2007). analyses; K.E.L.: genetic analyses, paper writing; K.Z.: conception, field support, paper 38. Crockford, C. et al. Urinary oxytocin and social bonding in related and writing. unrelated wild chimpanzees. Proc. R. Soc. B 280, 20122765 (2013). 39. Slavich, G. M. & Cole, S. W. The emerging field of human social genomics. Clin. Psychol. Sci. 1, 331–348 (2013). Additional information 40. Sapolsky, R. M., Romero, L. M. & Munck, A. U. How do glucocorticoids Supplementary Information accompanies this paper at http://www.nature.com/ influence stress responses? Integrating permissive, suppressive, stimulatory, and naturecommunications preparative actions. Endocr. Rev. 21, 55–89 (2000). 41. Holt-Lunstad, J. & Uchino, B. in Health Behavior: Theory, research and Competing financial interests: The authors declare no competing financial interests. practice (eds Hlanz, K., Riemer, B. K. & Viswanath, K.) 183–204 (Jossey-Bass, Reprints and permission information is available online at http://npg.nature.com/ San Francisco, CA, 2015). reprintsandpermissions/ 42. Reynolds, V. The Chimpanzees of the Budongo Forest: ecology, behaviour, and conservation (Oxford University Press, 2005). How to cite this article: Wittig, R. M. et al. Social support reduces stress hormone levels 43. Altmann, J. Observational study of behavior: sampling methods. Behaviour 49, in wild chimpanzees across stressful events and everyday affiliations. Nat. Commun. 7, 227–266 (1974). 13361 doi: 10.1038/ncomms13361 (2016). 44. Hauser, B., Deschner, T. & Boesch, C. Development of a liquid chromatography–tandem mass spectrometry method for the determination of Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in 23 endogenous steroids in small quantities of primate urine. J. Chromatogr. published maps and institutional affiliations. 862, 100–112 (2008). 45. Erb, R. E., Tillson, S. A., Hodgen, G. D. & Plotka, E. D. Urinary creatinine as an This work is licensed under a Creative Commons Attribution 4.0 index compound for estimating rate of excretion of steroids in the domestic International License. The images or other third party material in this sow. J. Anim. Sci. 30, 79–85 (1970). article are included in the article’s Creative Commons license, unless indicated otherwise 46. Wittig, R. M. et al. Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees. Proc. R. Soc. B 281, in the credit line; if the material is not included under the Creative Commons license, 20133096 (2014). users will need to obtain permission from the license holder to reproduce the material. 47. Muller, M. N. & Lipson, S. F. Diurnal patterns of urinary steroid excretion in To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ wild chimpanzees. Am. J. Primatol. 60, 161–166 (2003). 48. Fraser, O. N., Schino, G. & Aureli, F. Components of relationship quality in r The Author(s) 2016 chimpanzees. Ethology 114, 834–843 (2008). 8 NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Nature Communications Springer Journals

Social support reduces stress hormone levels in wild chimpanzees across stressful events and everyday affiliations

Loading next page...
 
/lp/springer-journals/social-support-reduces-stress-hormone-levels-in-wild-chimpanzees-2pyl2MnBNO

References (133)

Publisher
Springer Journals
Copyright
Copyright © 2016 by The Author(s)
Subject
Science, Humanities and Social Sciences, multidisciplinary; Science, Humanities and Social Sciences, multidisciplinary; Science, multidisciplinary
eISSN
2041-1723
DOI
10.1038/ncomms13361
Publisher site
See Article on Publisher Site

Abstract

ARTICLE Received 4 Dec 2015 | Accepted 27 Sep 2016 | Published 1 Nov 2016 DOI: 10.1038/ncomms13361 OPEN Social support reduces stress hormone levels in wild chimpanzees across stressful events and everyday affiliations 1,2,3, 1,2,3, 1 4 1, Roman M. Wittig *, Catherine Crockford *, Anja Weltring , Kevin E. Langergraber , Tobias Deschner ** 2,3,5, & Klaus Zuberbu¨hler ** Stress is a major cause of poor health and mortality in humans and other social mammals. Close social bonds buffer stress, however much of the underlying physiological mechanism remains unknown. Here, we test two key hypotheses: bond partner effects occur only during stress (social buffering) or generally throughout daily life (main effects). We assess urinary glucocorticoids (uGC) in wild chimpanzees, with or without their bond partners, after a natural stressor, resting or everyday affiliation. Chimpanzees in the presence of, or interacting with, bond partners rather than others have lowered uGC levels across all three contexts. These results support the main effects hypothesis and indicate that hypothalamic-pituitary- adrenocortical (HPA) axis regulation is mediated by daily engagement with bond partners both within and out of stressful contexts. Regular social support with bond partners could lead to better health through daily ‘micro-management’ of the HPA axis, a finding with potential medical implications for humans. 1 2 Max Planck Institute for Evolutionary Anthropology, Department of Primatology, 04103 Leipzig, Germany. University of St Andrews, School of Psychology 3 4 & Neuroscience, St Andrews, KY16 9JP, UK. Budongo Conservation Field Station, PO Box 362, Masindi, Uganda. Arizona State University, School of Human Evolution & Social Change and Institute of Human Origins, Tempe, Arizona 85281, USA. University of Neuchatel, Department of Comparative Cognition, 2000 Neuchatel, Switzerland. * These authors contributed equally to this work. ** These authors jointly supervised this work. Correspondence and requests for materials should be addressed to R.M.W. (email: wittig@eva.mpg.de) or to C.C. (email: crockfor@eva.mpg.de). NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 24,25 or animals, including humans, there is much evidence that provide predictable social support . Here, we compared individuals who maintain stable, close social bonds have the effects of partners with predictable support patterns (bond Fgreater reproductive success, increased longevity and better partners) with those of unpredictable support patterns (non-bond 1–5 health compared with those who do not . A key mechanism partners) on uGC levels. through which these benefits could operate is through social In contrast to previous correlational studies, where GC measures buffering, in which social support provided by bond partners were typically averaged over extended time periods, which 9–11,23 cushions the aversive effects of stressful events through mediation included a multitude of stressful events ,we used an event 6–9 of the hypothalamic-pituitary-adrenocortical (HPA) axis . sampling approach measuring uGC levels that corresponded to a In particular, the presence of bond partners during a stressful single event . Applying a fixed latency for clearance of GCs into 7–10 26,27 event can result in lower glucocorticoid (GC) levels or urine , we created relative uGC levels by dividing uGC levels help to reduce them sooner after the event, compared with when relating to the event by uGC levels relating to before the event. 11–13 bond partners are not available . Events were stressors (intergroup encounters), everyday affiliations Alternatively, bond partners may have a more generalized (grooming) or control periods (resting without social interaction). positive effect, insofar as subjects can rely on general social Intergroup encounters are highly stressful events, associated support beyond periods of acute stress. General social support with high GC levels , in which chimpanzees face potentially 29–31 may create more predictability within social interactions and lethal aggression when they encounter rival groups ,but 6,14 more stability in the social environment . This main effects they can also involve social support. A key factor in winning inter- 6 31,32 hypothesis is less examined in non-human animals, despite its group encounters is to out-number rivals through coordinated 6,14,15 33,34 potential implications for promoting health and longevity . attacks involving coalitionary support against rivals . Although there is some empirical support for this hypothesis in Coalitionary and social support rather than retreat (defection) 15–17 humans , the underlying mechanism that enables such a from group members is crucial to rout rivals in direct 29,32 main effect is unknown. Some studies suggest main effects may confrontations . Thus, we noted the occurrence of social 6 14,17 also be mediated by the HPA axis , or by other mechanisms . support during intergroup encounters, only when individuals Physically and psychologically-induced stress can cause joined in vocal or physical aggression against rivals. 6–8 dysregulation of the HPA axis, provided the stress is repeatedly To test the social buffering hypothesis in wild chimpanzees 18 19 acute or chronic . This dysregulation can lead to severe health using a within-subjects design, we predict the following: if social 8,20 problems , suggesting that any mechanisms that moderate such support in chimpanzees is effective during stressors, we expected aversive effects will be under positive selection. Social buffering the Relationship Quality of the participants to impact on urinary during stress exposure shows regulatory, stabilizing effects on glucocorticoid (uGC) levels only when experiencing a stressor. 7,8 HPA activity , but it is equally possible that the same effect is Specifically, we predicted an interaction between Event (intergroup also caused by everyday affiliations between individuals that encounter, resting, grooming) and Relationship Quality (bond, predictably offer social support to one another. non-bond) such that uGC levels would be reduced during stressors While the main effects hypothesis predicts HPA regulatory (intergroup encounters) but not during resting or everyday effects of social partners in both stressful and non-stressful affiliations (grooming), when bond partners rather than other situations, the social buffering hypothesis excludes HPA axis individuals participated. 6,14 regulation outside of stressful events. To test between these two To test the main effects hypothesis , we predicted the hypotheses and to investigate their predicted impact on HPA axis following: if social support impacts on uGC levels during activity, we monitored subjects’ urinary glucocorticoid (uGC) everyday affiliation (grooming), resting and during a stressor levels in reaction to acute stressors, everyday affiliations and (intergroup encounters), we expected the Relationship Quality of resting. Since general social support is usually measured as social participants to impact on uGC levels irrespective of context, such 6,14 integration in the community or as the presence of reliable that GC levels would be reduced by bond partners rather than 7,11–13 supporters , we contrasted subjects’ uGC levels in the three other individuals across contexts. In addition, we predicted no contexts depending on the participation or presence of a bond interaction effects between Event and Relationship Quality. partner, who by definition provides predictable support. We tested the social buffering and main effects hypotheses by The impact of social support on stress and health is often comparing uGC levels in wild chimpanzees associated with posited as a causative relationship; however, whether social three events: potentially life-threatening stressors (intergroup 29,31 11,23 relationships promote lower stress and better health or rather encounters ), everyday affiliations (social grooming ) and whether healthier and less stressed individuals are better able to control periods (resting). We show that chimpanzees have maintain relationships is not well established, given that most reduced uGC levels when they are together with bond partners studies are correlational . To address this issue, we used a within- rather than other chimpanzees, irrespective of context. Further subjects design, so that the same individuals were tested in each analyses revealed that the ameliorative effects of bond partners condition and we compared changes in uGC levels due to events. were most pronounced during contexts requiring active support Another unresolved issue is whether only active support rather than the passive presence of bond partners, with the largest 6,17 (instrumental help) mediates HPA axis activity, or whether effects during stressors then grooming contexts, and least so 6,17 the mere presence of a bond partner (social companionship) is during resting contexts. Our results indicate that the predictable enough to do so. Also, it remains unclear whether perceived or social support of bond partners may help to micro-manage HPA 14,17,22 actual support is more beneficial , or whether predictability axis activity, during both stressful and everyday events, 15,23 of support is a key component for stress regulation . supporting the main effects hypothesis. Chimpanzees are a good model species for exploring these issues. They have highly differentiated relationships with group members, with individuals maintaining close social bonds with Results one or several other group members . Close social bonds are Stressful events and everyday affiliation predict uGC levels.We defined as high rates of consistent mutual cooperative and first tested if relative uGC levels were influenced by Event affiliative behaviours (grooming, coalitionary support and (intergroup encounters, resting, grooming). To control for food sharing) between two individuals, which are maintained physical exertion, security in numbers and sex effects, we added over several months or years. Bond partners, thus by definition Event Duration, Number of Chimpanzees Present and Subject’s 2 NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 ARTICLE Sex as control predictors. Given that subjects were sampled more we tested whether chimpanzees’ relative uGC levels within each than once and sometimes from the same Event, we added Subject context were significantly higher or lower than expected ID and Event ID as random effects (Table 1: General Model). levels. We calculated the expected relative uGC level by Both Event and Event Duration significantly affected uGC levels estimating the diurnal decline in uGC levels (Supplementary (likelihood ratio test: df ¼ 2, w2 ¼ 7.98 and P ¼ 0.019), but the Note 1, Supplementary Fig. 2). The results of the bootsrap interaction of Event and Event Duration was not significant, and procedure showed that grooming with a bond partner decreased ± ± therefore removed (Wald test: df ¼ 2, w2 ¼ 5.21, P ¼ 0.074, uGC levels (bootstrap: mean deviation SE¼ 13.3 6.5, Supplementary Table 1). Intergroup encounters resulted in CI ¼ (  25.9;  0.8), N ¼ 10, Po0.05) and engaging in higher relative uGC levels than grooming or resting events intergroup encounters without a bond partner increased ± ± (Fig. 1; Table 1: General Model) and longer events resulted in uGC levels (bootstrap: mean deviation SE ¼ 31.9 12.9, higher relative uGC levels (Supplementary Fig. 1), while Number CI ¼ (7.9; 64.9), N ¼ 7, Po0.05). In contrast, when grooming a of Chimpanzees Present and Subject’s Sex did not significantly non-bond partner (bootstrap: mean deviation±SE ¼ 2.7±4.1, influence uGC levels. The effect size of the fixed effects in model 1 CI ¼ (  6.4, 9.5), N ¼ 11) and engaging in intergroup encounters was R ¼ 0.170. with a bond partner (bootstrap: mean deviation SE ¼ 0.5 9.0, CI ¼ (  17.8; 16.5), N ¼ 8), confidence intervals included 0 and therefore were not different from expected relative Social buffering and main effects hypotheses. In the second uGC levels. Finally, relative uGC levels after resting with a bond model we investigated whether the social buffering or main effects partner did not differ from expected values (bootstrap: mean hypotheses were best supported by the data. We tested if relative ± ± deviation SE¼ 2.5 5.5, CI ¼ (  13.3; 7.0), N ¼ 13), but uGC levels were affected by the interaction of predictors resting without bond partners had an insufficient sample size to Event and Relationship Quality (bond versus non-bond partners), be tested (N ¼ 5). while controlling for the Sex and Kin (close maternal kin) relationships of the two participants, and including Subject ID and Event ID as random factors. Although the full model was Discussion significantly different from the null model (likelihood ratio test: Within each event, subjects’ relative urinary glucocorticoid levels df ¼ 5, w2 ¼ 13.93,P ¼ 0.016), we neither found a significant were lower when engaging with bond partners rather than other interaction between Event and Relationship Quality on uGC individuals, whether during a stressor (intergroup encounters), levels, nor between Subject’s Sex and Partner’s Sex (Table 2a: everyday affiliation (grooming) or resting. Bond partner effects, Social Buffering Model, Fig. 2). After removing both non-significant interactions from the model, both test predictors (Event and Relationship Quality) significantly influenced relative uGC levels (Table 2b: Main Effects Model, Fig. 2). Specifically, relative uGC levels were on average almost 22% higher after intergroup encounters than after 110 grooming events and on average 48% higher after resting than grooming events. In addition, subjects participating in events with 100 bond partners rather than other individuals had on average 23% lower relative uGC levels, across events (Table 2b: Main Effects Model). Neither Kin nor Sex of subject showed a significant influence on relative uGC levels, while the relative uGC levels varied depending on the Sex of Partner, with subjects of male partners having higher relative uGC levels. The effect size of the Grooming Resting Intergroup encounter fixed effects in model 2 was R ¼ 0.196. Figure 1 | Individual relative urinary glucocorticoid (uGC) levels change Extent of bond partner impact on uGC levels. Engaging with with Event. Mean relative uGC levels (%) 95% confidence interval bond partners lowered relative uGC levels across all events, depend on the event sampled (grooming N ¼ 31, resting N ¼ 18, intergroup encounter N ¼ 21), such that Event predicted the relative uGC level of Sonso although to determine the extent of bond partner impact within contexts requires further testing. Therefore, using bootstrapping, chimpanzees (Wald test: df ¼ 2, w2 ¼ 7.98, P ¼ 0.018). Table 1 | The impact of Event on urinary glucocorticoid (uGC) levels. Response variable: relative uGC P value Parameter Estimate SE t Predictor variable df v2 General model Intercept 65.8 11.7 Event* 2 7.98 0.018 Intergroup 25.55 9.36 2.73 Rest  4.50 9.35  0.48 Groom 0 Subject’s Sex 1 0.51 0.474 Male  6.17 8.33  0.74 Number of Chimpanzees Present 1 0.05 0.828 0.15 0.67 0.23 Event Duration 1 7.60 0.006 Minutes 0.45 0.15 2.86 Random factors: Identity of Subject, Event. Bold: Po0.05. Intergroup: Intergroup encounter, Rest: resting event, Groom: grooming event. Likelihood ratio test (full versus null model comparison): df ¼ 2, w2 ¼ 7.98, P ¼ 0.019. Effect Size of fixed effects: marginal R ¼ 0.170. This model with the non-significant interaction of duration and event is presented in Supplementary Table 1. LMM: *test predictor, wcontrol variable. NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications 3 Relative uGC levels ± 95% CI ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 Table 2 | The impact of Event and Relationship Quality on urinary glucocorticoid (uGC) levels. Response variable: relative uGC P value Parameter Estimate SE t Predictor variable df v2 (a) Social Buffering Model Intercept 68.01 16.13 Event  Relationship Quality* 2 1.66 0.437 Intergroup  Bond  13.71 16.64  0.82 Rest  Bond 13.80 19.55 0.71 Groom  Bond 0 Kin 1 2.29 0.130 Kin 20.32 13.15 1.55 Subject’s Sex  Partner’s Sex 1 0.16 0.686 Male  Male  8.01 19.77  0.41 (b) Main Effects Model Intercept 71.43 14.78 Event* 2 6.14 0.047 Intergroup 21.78 8.60 2.53 Rest 8.35 9.37 0.89 Groom 0 Relationship Quality* 1 6.77 0.009 Bond  23.13 8.65  2.67 Kin 1 2.78 0.096 Kin 20.99 12.27 1.71 Subject’s Sex 1 0.01 0.979 Male  0.25 9.66  0.03 Partner’s Sex 1 4.46 0.035 Male 21.77 10.13 2.15 Random factors: Identity of Subject, Event. Bold: Po0.05. Intergroup: Intergroup encounter, Rest: resting event, Groom: grooming event. (a) Social Buffering Model testing social buffering hypothesis. Likelihood ratio test (full versus null model comparison): df ¼ 5, w2 ¼ 13.93, P ¼ 0.016. (b) Main Effects Model testing the main effects hypothesis. Likelihood ratio test (full versus null model comparison): df ¼ 3, w2 ¼ 12.94, P ¼ 0.005. Effect Size of fixed effects: marginal R ¼ 0.196. LMM: *test predictor, wcontrol variable. partners did not participate in the encounter. The same chimpanzees facing potentially life-threatening intergroup encounters together with a bond partner did not have elevated uGC levels. This result demonstrates that the participation of a bond partner, who by definition provides predictable social support, regulates HPA activity and buffers the stress reaction 110 even in potentially lethal situations. Less predictable supporters were less effective in buffering uGC levels. Our results showing buffering effects of bond partners on HPA axis activity concur 12,13 with experimental studies in humans , where bond partners buffer psychologically-induced stress, and studies examining 9–11 naturally occurring social stressors in non-human primates . In the non-human primate studies, correlations show that bond 60 partners seem to buffer baseline GC levels following severe social stressors, such as, the threat of infanticide , sudden social isolation and during milder social stressors, such as conspecific aggression . Grooming Resting Intergroup encounter bond non-bond bond non-bond bond non-bond Chimpanzees showed lower relative uGC levels during every- day affiliative interactions (grooming events) compared with Figure 2 | Event and Relationship Quality change individual relative resting events. However, uGC levels decreased only when urinary glucocorticoid (uGC) levels. Mean relative uGC levels (%) 95% chimpanzees groomed with a bond partner. In contrast, subjects confidence interval depend on the Event sampled: occurring with either a grooming with a non-bond partner showed uGC levels similar to bond or a non-bond partner (grooming with bond partner N ¼ 14 and non- resting control samples. This shows that bond partners have bond partner N ¼ 17, resting with bond partner N ¼ 13 and with non-bond moderating effects on HPA activity during everyday grooming partner N ¼ 5, intergroup encounter with bond partner N ¼ 11 and non-bond events, outside of stressor contexts. A correlational study on wild partner N ¼ 10). Both Event (Wald test: df ¼ 2, w2 ¼ 6.14, P ¼ 0.047) and baboons is also suggestive of this pattern, where female baboons Relationship Quality (Wald test: df ¼ 1, w2 ¼ 6.77, P ¼ 0.009) predicted the during periods of social stability had lower baseline GC levels relative uGC level of Sonso chimpanzees. when they were able to focus their grooming on a few preferred individuals rather than showing more distributed grooming however, were strongest during intergroup encounters, then patterns . In both stressful and grooming contexts, our results during grooming and least during resting. The social buffering indicate a positive relationship between predictable social support hypothesis predicts bond partner effects during stressors only, objectively measured from social interaction histories and the whilst the main effects hypothesis expects bond partner effects stress buffering potential of supporters. during both stressors and everyday events. Thus, our results show Model 2 suggests that bond partner effects on uGC levels were support for the main effects rather than the social buffering also evident during resting events. This result, however, has to be hypothesis (see Fig. 2 in ref. 6). treated with caution, since sample size for resting without Chimpanzees showed significantly higher relative uGC levels bond-partners is low which leads to instability problems. after stressful events (intergroup encounters) compared with after Nevertheless, the result is interesting since experimental studies resting. However, uGC elevation was evident only when bond with humans usually do not distinguish between social support 4 NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications Relative uGC levels ± 95% CI NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 ARTICLE due to the mere presence of bond partners , and active support oxytocin may be key to the underlying mechanism precipitating 13 7–9 offered by bond partners . In our study, although the effect is the the social regulation of the HPA axis . same, the estimates due to bond partners are different (Fig. 2), Crucially, engaging an oxytocin—HPA axis interaction by increasing from resting to grooming to intergroup contexts. This participating with predictable supporters during ordinary everyday finding indicates that active support from bond partners is more affiliative contexts may help maintain a healthy homoeostasis. We effective in lowering uGC levels than is their mere presence. propose that a possible underlying process could be that daily Everyday affiliative interactions with bond partners have been affiliative social interactions help regulate—or micromanage—the predicted to improve physical and mental health, although the HPA axis. This in turn may help to maintain stable immune- mechanism through which the benefits might be accrued has function, cardio-function, fertility, cognition and mood, key 14,16 6 8,14,15,39 remained evasive . Cohen and Wills suggested that benefits aspects known to be affected by a dysregulated HPA axis . might be mediated through similar mechanisms as social The close phylogenetic relationship between humans and buffering effects, specifically involving the HPA axis. Our chimpanzees suggests that HPA axis micro-management through results suggest that this is indeed the case: engaging in three daily affiliative social interactions could also occur in humans. types of activity with predictable bond partners lowered subjects’ Bond partner effects were strong such that even during a uGC levels, whether during highly stressful interactions, resting potentially life-threatening inter-group encounter, bond partners or everyday affiliative interactions. buffered the stress response. It could be argued that since the Given that both male and female subjects participate in triggering of the stress response is vital for maximizing the 34 40 grooming and intergroup encounters (and this study), we physical response in a fight situation , it is not necessarily contrasted the relative uGC levels of both female and male adaptive for bond partners to buffer the stress response in fight subjects, as well as the sex combination of the dyad. Neither contexts. However, bond partners by definition in this study have subjects’ sex nor the sex combination of the dyad influenced a predictable history of providing social and agonistic support to relative uGC levels in any model. Thus, for both male and female one another . Thus, it may be that subjects are indeed safer when chimpanzees, the impact of participating in stressors or everyday engaging in inter-group encounters when bond partners are also affiliations with a predictable partner of either sex, compared with participating and subjects thus ‘require’ less or shorter HPA axis another individual, similarly regulates the HPA axis. This result is activity to ensure survival. This interpretation might offer one not unexpected, even in intergroup encounters, where both males explanation as to why chimpanzees and humans seek bond 34 30,33,36 and females participate. Females engage often in vocal aggression partners when initiating conflict with rival groups . Another (Supplementary Movie 1), which is highly effective in deterring possible explanation for these results is that our method can only 24 34,35 within-group , as well as out-group members . Both sexes can measure strong changes in relative uGC levels and do not detect incur high costs from attacking or being attacked (injury or short or minor increases in stress response activity. 31,36,37 death) . However, it is likely that males do not gain In this study, chimpanzees supported by bond partners showed comparable vocal or physical support from females as they do no significant up-regulation of their HPA axis when participating in from males, and we cannot rule out that a larger sample may show an intense stressor (inter-group encounters), and showed signifi- some sex effects. It should be noted that in this data set, all mixed- cant down-regulation of their HPA axis in everyday affiliations sex bond partner dyads consisted of mothers and their sons. (grooming) compared with support from other individuals. These For grooming events, the uGC patterns mirror urinary results suggest that bond partners can influence HPA axis activity oxytocin levels found after grooming in the same chimpanzee both during highly stressful situations, as well as during everyday population . In this previous study, grooming with a bond activities, such as grooming. The HPA axis is vulnerable to partner was associated with higher urinary oxytocin levels dysregulation, particularly when exposed to intense or repeated 8,18–20 compared with grooming with a non-bond partner or periods stressors . Such HPA axis dysregulation can have negative and 8,18–20,39,41 of resting, independent of whether subjects were giving or long-term effects on physical and mental health . Social receiving grooming. These contrasting GC and oxytocin results buffering may have an immediate effect during a stressor of 6–8,12,13 are similar to those of two social buffering experiments exposing reducing HPA axis activity . However, daily management of humans to a psychological stressor. In trials in which social the HPA axis through repeated affiliations from predictable social support was offered from a bond partner, subjects had earlier supporters may protect against dysregulation of the HPA axis over decreasing GC levels. One study showed lower GC levels and the longer term . The mechanism that might account for returned faster to baseline in conditions in which urinary reported effects of better health when engaging in everyday 13 6,14,16,17,21 oxytocin levels increased . The other study showed greatest affiliations with bond partners, has remained elusive . GC decreases in trials with both social support by bond partners Here, we demonstrate that, as for stressors, bond partners also and intranasal application of oxytocin before the stressor . Thus downregulate HPA axis activity even during an everyday affiliation, our observations are in line with the idea that oxytocin has a grooming and with a weaker effect, by their mere presence when 7–9 6 dampening role in cortisol secretion . In chimpanzees, active resting, as proposed by Cohen and Wills’ main effects hypothesis . social support from bond partners seems to have more From these results, we hypothesize for future testing that regular pronounced effects on urinary oxytocin levels , as well as on and repeated, everyday affiliations have the potential to regularly uGC levels, than the mere presence of bond partners . Likewise, and repeatedly re-align the HPA axis throughout the day. This it is possible that participating in activities with predictable bond could amount to ‘micro-managing’ effects on the regulation of the partners in humans may be more effective in HPA axis HPA axis, resulting in stable HPA activity over time, and providing management than either merely associating with bond partners long-term benefits to physical and mental health. without active participation, or participation with less predictable supporters. To date, these conditions have rarely been contrasted Methods 12,13 in the human literature . Given that we examined the same Subjects. We observed chimpanzees (Pan troglodytes schweinfurthii, 0 0 Supplementary Data 1) of the Sonso community, Budongo Forest (135 —155 N, chimpanzees in the same contexts with and without bond partner 0 0 3108 —3142 E), Uganda, from February 2008 to July 2010. The Sonso participation, and that we measured relative change in uGC levels community has been continuously observed since 1990 (ref. 42), and was after, compared with before, the events, supports a causative effect comprised of 15 males (adults: Z15 years: 10; subadult: 10–14 years: 5), 35 females between bond partner support and lower HPA axis activity, in (adult: Z14 years: 27; subadult: 10–13 years: 8) and 28 juvenile and infants during everyday affiliations as well as during stressors. The neuropeptide the study period. We sampled urine from nine adult male and eight adult female NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications 5 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 urine samples in 4 events, N ¼ 6 subjects). Chimpanzees show intimate reassurance chimpanzees—those that were regularly observed to improve the likelihood of behaviour after detecting rival groups, including embracing, placing their finger in within-subject sampling across behavioural conditions. Permissions to conduct this others’ mouth, holding others’ testes or grooming (Supplementary Movie 1). research was granted by Uganda Wildlife Authority (TDO/33/02) and Uganda Urinary GC levels were measured at the Behavioural Endocrinology Lab at the National Council for Science and Technology (NS 181) and overseen by Budongo Max Planck Institute for Evolutionary Anthropology using high-performance Conservation Field Station and the University Teaching and Research Ethics liquid chromatography-tandem mass spectrometry (LC-MS/MS) . Samples with a Committee of St Andrews University. recovery of the internal standard deviating by o 50% from the expected value were included in the analysis. In cases of large deviation we re-measured the Observation methods. A team of up to six observers followed up to three parties samples. If a large deviation persisted, we re-extracted and re-measured the of chimpanzees (independently moving subgroups of flexible composition) from samples. We excluded samples where the large deviation still persisted. B7 a.m. to 5 p.m. through the forest, recording behaviours using ‘all occurrence’ Examination of LC-MS/MS data was carried out with MassLynx (version 4.1; sampling for aggressive (agonistic support, contact and non-contact aggression) QuanLynx-Software). Only a fraction of plasma cortisol can be found in 27 44 and affiliative social interactions (grooming, food sharing, sitting in close proximity chimpanzee urine , while metabolites of cortisol are found in higher quantities . (within 1 m)), and 15 min scan sampling for party composition, where ‘party’ is a To quantify the urinary glucocorticoid excretion (uGC), we used the sum of subgroup of individuals in view. In addition, we recorded intergroup encounters urinary cortisol plus four of its metabolites (tetrahydrocortisol, whenever they were observed. We focused on three event types: (1) intergroup tetrahydrocortisone, 5b-androstane and 11-oxoetiocholanolon). The sum of uGC encounters: subjects had auditory or visual contact with a rival community. comprised on average 9% cortisol, 37% tetrahydrocortisol, 35% tetrahydrocortison, Subjects were sampled if classified as engaging in social support of group members, 5% 5b-androstane and 14% 11- oxoetiocholanolon. We corrected the uGC levels which required approaching in the direction of the rivals and responding with with the creatinine levels of each sample to control for differences in water content chorused (coalitionary) vocal aggressive behaviour (barks, pant roars, buttress of urine samples . We excluded samples with a creatinine level of o0.05 mg drumming and pant hoots) and/or coalitionary physically aggressive behaviour creatinine ml urine from the analysis. 26,38,46 (charging, chasing, hitting and biting) towards out-group members. Support was Using an event-sampling approach , we then calculated the relative uGC coded as ‘mutual’ in all cases, given that all receive a benefit from another’s levels for each Event, using a method that took the clearance window of cortisol participation, whether it occurs before or after their own. These intergroup events into urine into account (see Fig. 1 in ref. 26). We defined a pre-period (representing were also not characterized by grooming bouts either before, during or after the the uGC levels from before the event) and a peak-period (representing the uGC intergroup encounters. Since the natural frequency of encounters with the rival levels related to the event), taking into account the delayed GC clearance in 26,27 47 communities was low (nine encounters were sampled during the observation time), chimpanzee urine and the diurnal decrease of uGC levels in chimpanzees we also conducted four drumming experiments to simulate the presence of a rival (Supplementary Fig. 2, Supplementary Note 1). We calculated the mean uGC levels community (see experimental procedure); (2) resting events, in which one for the pre-period (from samples taken between the start of the event until 135 min individual had no social interaction for a minimum of one hour and was sitting or after the start of the event) and the mean uGC levels for the peak-period (from lying for at least the first 30 min; and (3) grooming events, in which two individuals samples taken between 135 min until 270 min after the event þ event duration) for groomed each other for at least 20 min without a break and had no additional each event. Samples taken within 30 min after the pre or the peak-period were still social interaction for at least 1 h after the beginning of the grooming event. assigned to the preceding period, if the focal individual had not urinated within the Grooming duration as well as minutes spent giving, receiving or engaging in both last 30 min of the preceding period . Finally we calculated the relative uGC levels simultaneously (mutual) were recorded. as a percentage of how high the uGC levels were during the peak-period compared with the pre-period: uGC peak  period Experimental procedure. We waited for a subgroup—or party—of chimpanzees relative uGC ¼ 100 ð1Þ to rest in the periphery of their territory in an area where we had observed uGC pre  period intergroup encounters during the last year. After resting without vocalising for at We calculated an average decrease of 5.55% of the uGC level per hour of the day. least 10 min, an experienced field assistant mimicked a typical mid-length chim- Taking an average time difference of 135 min between peak and pre-period panzee buttress tree drum, striking 7 beats with his fists on the buttress roots of a samples, peak-period samples should be 12.49% lower than pre-period samples. A tree about 100 m away from the resting party in the direction of the rival com- relative uGC level of about 87.5% therefore reflected a neutral effect of the event munity’s territory. Importantly, before and during the drumming simulation, we behaviour on the uGC level only including the estimated diurnal decline of uGC. took extreme care that Sonso chimpanzees could not see or hear any person Levels above the expected relative uGC level of 87.5% would represent an increase moving in the direction where the drumming experiment would or just had and below the 87.5% would represent a decrease in uGC levels due to the event. occurred. In all four trials, the chimpanzees showed behaviour indistinguishable from natural intergroup encounters (pilo-erection, reassurance behaviours, cautious and silent approach to the drumming tree followed by aggressive displays, Definition of social bonds. The Relationship Quality of chimpanzees can be aggressive vocalizations, like pant-roars and pant-barks and drumming). Eight of 48 defined by three components such that those that share close social bonds engage 21 intergroup encounter data points were experimentally simulated encounters in: (1) high rates of socio-positive and cooperative behaviours and low rates of (Supplementary Data 1). We found that experimentally simulated intergroup socio-negative behaviours, (2) balanced or symmetrical offering of high rates of encounters produced no different reaction in uGC levels than natural encounters socio-positive and cooperative behaviours over time, (3) sustained patterns of (1) (likelihood ratio test: w ¼ 0.869, df ¼ 2, P ¼ 0.648; Supplementary Table 2). and (2) over at least a six month period. We described the quality of social Therefore we merged natural observations and experimental simulations of 24,38,46 relationships by calculating the composite relationship index (CRI) over intergroup encounters. quarter-year periods for all possible dyads. The CRI contrasts socio-positive and negative behaviours in relation to average behaviour rates per sex combination across dyads. Urine collection and hormone data analysis. After observing one of our target SP1ij SP2ij chimpanzees engaging in one of the three events (grooming, resting, intergroup NPij 43 SP1 SP2 encounters), we switched to ‘focal animal’ sampling of that individual for the next CRI ¼  ð2Þ 2 NP 6 h, collecting every possible urine sample and recording each behaviour and change in activity (see ref. 26). Urine was either pipetted from plastic bags, after the where SP1 ¼ rate of grooming bouts plus rate of resting in 1m proximity; bags were tied over a forked stick and held in the urine stream when subjects were SP2 ¼ rate of food sharing plus rate of coalitionary support; NP ¼ rate of aggression sitting in a tree, or from leaf matter when urination occurred on the ground after and contra-intervention, i ¼ individual (receiver of service) and j ¼ dyad partner subjects had moved away. After collection, urine samples were stored in a thermos (offering of service). A positive CRI indicated a more socio-positive relationship flask containing ice and were frozen in liquid nitrogen upon arrival in camp, which and a negative CRI showed a socio-negative relationship. A good indication that was within 10 h after collection. Urine collection did not commence if subjects had grooming and food-sharing are important bonding behaviours is that both have 38,46 engaged in aggression or grooming within the hour before the activities, and was been linked with elevated urinary oxytocin levels in chimpanzees . Dyads were aborted if subjects engaged in additional aggression or grooming within two hours only defined as bond partners when socio-positive relationships were symmetrical after the activity. We collected a total of N ¼ 574 urine samples from adult (reflecting similar rates of offered affiliations from both dyad partners) and long chimpanzees where we were able to determine uGC levels. lasting (Z 6 months: at least two consecutive blocks of quarter-year periods). We were able to assign N ¼ 394 of these urine samples (nine male and eight Balance and duration of relationships: scored through either a mutual socio- female chimpanzees, Supplementary Data 1) to a single event, either: (1) social positive relationship (CRI40) during the annual quarter of the sampled event and grooming (social support in an everyday context), sustained for 420 min (N ¼ 31 the preceding quarter, or a large mutual socio-positive relationship (CRI410) data point including 172 urine samples in 28 events, N ¼ 14 subjects); (2) resting during one of the quarters and a socio-neutral or positive relationship (CRIZ0) 24,38,46 (no support control), sustained for 430 min (N ¼ 18 data points including 108 during the other quarter . urine samples in 18 events, N ¼ 16 subjects); and (3) intergroup encounters (social Bond partners were defined as those with whom subjects engaged in high rates support in a stressful context), when chimpanzees saw out-group chimpanzees or of affiliative and cooperative behaviours (grooming, food sharing, coalitionary reacted vocally to calls of chimpanzees from real or simulated intergroup support) and low rates of aggression in both directions over at least two consecutive encounters (N ¼ 21 data points from natural encounters including 73 urine three month time periods providing an objective measure of historical samples in 9 events, N ¼ 7 subjects; and from simulated encounters including 41 predictability of social support . A histogram of mean CRI scores per dyad shows 6 NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 ARTICLE a bimodal distribution, with bonded relationships clustering in the higher scores model 2a (Social Buffering Model) where the interactions of Event and and non-bonded relationships clustering around zero (Supplementary Fig. 3). For Relationship Quality, as well as the interaction of Subject’s and Partner’s Sex this reason, we use Relationship Quality as a binomial variable. showed some instability and thus requires careful interpretation. To investigate whether or not the skewed distribution in the resting event has caused the insignificant effect for the test predictors’ interaction term, we run a full versus null Definition of kin relationships. We used genetic analysis to classify dydas as close model comparison, testing the interaction of Event and Relationship Quality only maternal kin (that is, mothers with offspring and maternal siblings) or not. for resting events and intergroup encounters (Supplementary Table 3). This Previous research suggests that as in most other group-living primates , comparison showed no significant effect of the interaction term (Wald test: df ¼ 1, chimpanzees can recognize and discriminate their mothers and maternal siblings . w2 ¼ 1.01, P ¼ 0.315), confirming the result of model 2a. Variables did not exhibit However, the ability of chimpanzees to recognize more distant maternal kin, who problems of collinearity (Variance Inflation Factor o4 in all cases, derived using anyways would be rare when all males stay in their natal group and the vast R-package car , and were tested using a standard linear model excluding the majority of female disperse, as occurs in Sonso, has not been demonstrated. Nor do random effect), suggesting that each predictor variable accounted for a portion of chimpanzees seem to recognize and discriminate their paternal kin . We collected the variance. We established the significance of the full model as compared with the fresh faecal samples after individually identified chimpanzees were observed null model (comprised of control predictors and random factors) using a likelihood defecating. Samples were either collected in plastic tubes and frozen within a 12 h ratio test . Since interactions between predictors do not allow interpretation of the period, collected in plastic tubes containing dessicating silica beads or collected in effect of the respective fixed factors in the model, we removed non-significant tubes filled with 95–99% ethanol and then transferred to tubes containing interactions to investigate the effects of the predictors. We calculated the marginal dessicating silica beads after 12–24 h (ref. 50). DNA was extracted from faeces 2 R (relative variance explained by fixed factors in relation to total variance) as the using the Qiagen DNA stool kit. We genotyped 92 chimpanzees at up to 19 effect size for the model. autosomal microsatellite loci. To guard against allelic dropout at the autosomal 61,62 Finally, we used bootstrap sampling methods with 1,000 permutations to loci, we first estimated the amount of amplifiable DNA in each extract through test whether relative uGC levels were significantly smaller or larger than the quantitative PCR, and then followed previously established guidelines showing that expected relative value, which was calculated to include estimated diurnal 26,47 depending on the amount of amplifiable DNA present in an extract, up to four decline (Supplementary Note 1). We calculated the mean for each individual independent PCR replications are required to be 99% confident that a putatively for each event with or without bond partner engagement and calculated the homozygous genotype is indeed homozygous . For heterozygous genotypes, each deviation from the expected value (expected relative uGC ¼ 87.5%). Values above 0 allele was observed in at least two independent PCRs (ref. 51). To guard against indicated an increase of uGC levels due to the event, values below 0 indicated a misidentification of individuals during sample collection or sample mix-up, in decrease of uGC levels due to the event. Since we had directed predictions (increase dyads that we strongly suspected from behavioural observations to be of uGC when interacting with a non-bond partner, decrease of uGC levels when mother-offspring pairs we checked that individuals shared at least one allele at interacting with a bond partner), we calculated the 5% interval on the predicted every autosomal locus. For individuals without suspected first-order maternal side of deviation from the expected value. relatives, we used a second, independently collected faecal sample to repeat the genotyping at six or more loci and required a perfect match with the original genotype. Using these methods, we were able to determine that o1% of samples Data availability. The authors declare that the data supporting the findings of this came from an incorrectly identified individual. In these cases, we genotyped study are available within the paper and its Supplementary Information files. additional extracts from independently collected faecal sample until the conflict was resolved. Microsatellite genotypes were produced through a two-step PCR multiplex procedure, using unlabelled primers for all 19 primers in the first References amplification, and fluorescently labelled forward primers and nested primers in the 1. House, J. S., Landis, K. R. & Umberson, D. Social relationships and health. subsequent single locus PCR reaction . PCR products were electrophoresed on an Science 241, 540–545 (1988). ABI PRISM 3100 Genetic Analyzer. Allele sizes determined using an internal size 2. Holt-Lunstad, J., Smith, T. B. & Layton, J. B. Social relationships and mortality standard (ROX labelled HD400) and Genemapper software version 3.7 (ref. 51). risk: a meta-analytic review. PLoS Med. 7, e1000316 (2010). We used the autosomal genotypes in likelihood based maternity analyses .All 3. Silk, J. B., Alberts, S. C. & Altmann, J. Social bonds of female baboons enhance eight dydas suspected of being mother-offspring from behavioural observations infant survival. Science 302, 1231–1234 (2003). shared an allele at each autosomal microsatellite locus and had maternity 4. Schu¨lke, O., Bhagavatula, J., Vigilant, L. & Ostner, J. Social bonds enhance assignments at the 95% confidence level using the CERVUS likelihood based reproductive success in male macaques. Curr. Biol. 20, 2207–2210 (2010). parentage program (Supplementary Data 2). There were two dyads (Harriette— 5. Silk, J. B. et al. Strong and consistent social bonds enhance the longevity of Gladis and Kalema—Kutu), where both members of a pair had unassigned female baboons. Curr. Biol. 20, 1359–1361 (2010). mothers, because the mothers’ samples were unavailable for genotyping; for these 6. Cohen, S. & Wills, T. A. Stress, social support, and the buffering hypothesis. two dyads the maternity assignments precluded a mother-offspring but not a Psychol. Bull. 98, 310–357 (1985). maternal sibling relationship. However, for one dyad (Kalema—Kutu) we were able 7. Hennessy, M. B., Kaiser, S. & Sachser, N. Social buffering of the stress response: to exclude the possibility that they were maternal siblings because they had different 473 base pair haplotypes at the hypervariable region-1 of the maternally diversity, mechanisms, and functions. Front. Neuroendocrinol. 30, 470–482 (2009). inherited mitochondrial DNA (ref. 53). While we could not use genetic data to exclude the possibility that the other dyad (Harriette—Gladis) were maternal 8. Kikusui, T., Winslow, J. T. & Mori, Y. Social buffering: relief from stress and siblings, we consider this unlikely given the low incidence of female philopatry at anxiety. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 361, 2215–2228 (2006). Sonso and in chimpanzees more generally (suggesting that Harriette and Gladis are 9. Young, C., Majolo, B., Heistermann, M., Schu¨lke, O. & Ostner, J. Responses to immigrants rather than natal to Sonso), as well as research in another community social and environmental stress are attenuated by strong male bonds in wild showing that it is extremely rare for maternal sisters to transfer from their natal macaques. Proc. Natl Acad. Sci. 111, 18195–18200 (2014). community to the same new community . We thus classified Harriette—Gladis as 10. Engh, A. L. et al. Behavioural and hormonal responses to predation in female unrelated in all analyses. chacma baboons. Proc. R. Soc. B 273, 707–712 (2006). 11. Wittig, R. M. et al. Focused grooming networks and stress alleviation in wild female baboons. Horm. Behav. 54, 170–177 (2008). Statistics. We employed linear mixed models to test the effects of the test 12. Heinrichs, M., Baumgartner, T., Kirschbaum, C. & Ehlert, U. Social support predictors Event (Model 1) and Event together with Relationship Quality and oxytocin interact to suppress cortisol and subjective responses to (Model 2) on relative uGC levels. We included Subject Identity and unique Event psychosocial stress. Biol. Psychiatry 54(12): 1389–1398 (2003). Identity as random factors and included several control predictors as additional 13. Seltzer, L. J., Ziegler, T. E. & Pollak, S. D. Social vocalizations can release fixed effects. To control for ‘safety in numbers’ we included the Number of oxytocin in humans. Proc. R. Soc. B 277, 2661–2666 (2010). Chimpanzees Present during each event. To control for expected glucocorticoid 14. Lakey, B. & Orehek, E. Relational regulation theory: a new approach to explain release due to energetic costs during intergroup encounters , we included the the link between perceived social support and mental health. Psychol. Rev. 118, event duration, predicting an interaction with event and event duration such that 482–495 (2011). longer intergroup encounters should result in higher energetic output and thus 15. Sapolsky, R. M. The influence of social hierarchy on primate health. Science higher uGC levels than shorter ones. This is in contrast to grooming and resting 308, 648–652 (2005). contexts in which no increase in energetic output was expected with event 16. Lakey, B. & Cronin, A. in Risk factors for depression (eds Dobson, K. S. & duration. To control for effects related to either subject’s sex, or partner’s sex or the Dozois, D.) 385–408 (Academic Press, 2008). combination of both, we included an interaction of these terms. Finally, when 17. Thoits, P. A. Mechanisms linking social ties and support to physical and mental testing the Relationship Quality we controlled for kin, since we expected close health. J. Health Soc. Behav. 52, 145–161 (2011). social bonds would provide uGC level effects regardless of kinship. 18. Radley, J. J. et al. Repeated stress induces dendritic spine loss in the rat medial The models were fitted in R 3.1.3 (ref. 57) using the function ‘lmer’ of the prefrontal cortex. Cerebr. Cortex 16, 313–320 (2006). R-package lme4 (ref. 58) with Maximum Likelihood. Residuals were normally distributed and homogenous, as shown by visual inspection of qq plots and 19. Juster, R. P., McEwen, S. B. & Lupien, S. J. Allostatic load biomarkers of chronic residual plots against fitted values. We checked for model stability by excluding stress and impact on health and cognition. Neurosci. Biobehav. Rev. 35, 2–16 subjects one at a time from the data and found models were stable, apart from (2010). NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications 7 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13361 20. McEwen, B. S. Central effects of stress hormones in health and disease: 49. Langergraber, K. E. in The Evolution of Primate Societies (eds Mitani, J. C., Understanding the protective and damaging effects of stress and stress Call, J, Kappeler, P. M., Palombit, R. A. & Silk, J.B.) 491–513 (Chicago mediators. Euro. J. Pharmacol. 583, 174–185 (2008). University Press, 2012). 21. Cohen, S. & Janicki-Deverts, D. Can we improve our physical health by altering 50. Nsubuga, A. M. et al. Factors affecting the amount of genomic DNA extracted our social networks? Perspec. Psychol. Sci. 4, 375–378 (2008). from ape faeces and the identification of an improved sample storage method. 22. Hostinar, C. E., Sullivan, R. M. & Gunnar, M. R. Psychobiological mechanisms Mol. Ecol. 13, 2089–2094 (2004). underlying the social buffering of the hypothalamic–pituitary–adrenocortical 51. Arandjelovic, M. et al. Two-step multiplex polymerase chain reaction improves axis: a review of animal models and human studies across development. the speed and accuracy of genotyping using DNA from noninvasive and Psychol. Bull. 140, 256–282 (2014). museum samples. Mol. Ecol. Res. 9, 28–36 (2009). 23. Crockford, C., Wittig, R. M., Whiten, P., Seyfarth, R. M. & Cheney, D. L. Social 52. Kalinowski, S. T., Taper, M. L. & Marshall, T. C. Revising how the computer stressors and coping mechanisms in wild female baboons (Papio hamadryas program CERVUS accommodates genotyping error increases success in ursinus). Horm. Behav. 53, 254–265 (2008). paternity assignments. Mol. Ecol. 16, 1099–1106 (2007). 24. Wittig, R. M., Crockford, C., Langergraber, K. E. & Zuberbu¨hler, K. Triadic 53. Langergraber, K. E. et al. The genetic signature of sex-biased migration in social interactions operate across time: a field experiment with wild patrilocal chimpanzees and humans. PLoS ONE 2, e973 (2007). chimpanzees. Proc. R. Soc. B 281, 20133155 (2014). 54. Langergraber, K. E., Mitani, J. & Vigilant, L. Kinship and social bonds in female 25. Langergraber, K. E., Mitani, J. C. & Vigilant, L. The limited impact of kinship chimpanzees (Pan troglodytes). Am. J. Primatol. 71, 840–851 (2009). on cooperation in wild chimpanzees. Proc. Natl Acad. Sci. 104, 7786–7790 55. Baayen, R. H. Analyzing Linguistic Data: a Practical Introduction to Statistics (2007). Using R (Cambridge University Press, 2008). 26. Wittig, R. M., Crockford, C., Weltring, A., Deschner, T. & Zuberbu¨hler, K. 56. Muller, M. N. & Wrangham, R. M. Dominance, cortisol and stress in wild Single aggressive interactions increase urinary glucocorticoid levels in wild male chimpanzees (Pan troglodytes schweinfurthii). Behav. Ecol. Sociobiol. 55, chimpanzees. PLoS ONE 10, e0118695 (2015). 332–340 (2004). 27. Bahr, N. I., Palme, R., Mo¨hle, U., Hodges, J. K. & Heistermann, M. Comparative 57. R Core Team. R: A language and environment for statistical computing aspects of the metabolism and excretion of cortisol in three individual (R Foundation for Statistical Computing, 2015). nonhuman primates. Gen. Comp. Endocrinol. 117, 427–438 (2000). 58. Bates, D., Ma¨chler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects 28. Sobolewski, M. E. The Hormonal Correlates of Male Chimpanzee Social models using lme4. J. Stat. Softw. 67, 1–48 (2015). Behavior (Doctoral dissertation, Smithsonian Institution, 2012). 59. Fox, J. & Weisberg, S. An R companion to applied regression (Sage, 2011). 29. Mitani, J. C., Watts, D. P. & Amsler, S. J. Lethal intergroup aggression leads to 60. Forstmeier, W. & Schielzeth, H. Cryptic multiple hypotheses testing in linear territorial expansion in wild chimpanzees. Curr. Biol. 20, R507–R508 (2010). models: overestimated effect sizes and the winner’s curse. Behav. Ecol. Sociobiol. 30. Watts, D. P. & Mitani, J. C. Boundary patrols and intergroup encounters in wild 65, 47–55 (2011). chimpanzees. Behaviour 138, 299–327 (2001). 61. DiCiccio, T. J. & Efron, B. Bootstrap confidence intervals. Stat. Sci. 11, 189–212 31. Wilson, M. L. et al. Lethal aggression in Pan is better explained by adaptive (1996). strategies than human impacts. Nature 513, 414–417 (2014). 62. Wittig, R. M. & Boesch, C. Receiving post-conflict affiliation from the enemy’s 32. Wrangham, R. W. & Glowacki, L. Intergroup aggression in chimpanzees and friend reconciles former opponents. PLoS ONE 5, e13995 (2010). war in nomadic hunter-gatherers. Hum. Nat. 23, 5–29 (2012). 33. Macfarlan, S. J., Walker, R. S., Flinn, M. V. & Chagnon, N. A. Lethal Acknowledgements coalitionary aggression and long-term alliance formation among Yanomamo¨ We thank Fred Babweteera, director of Budongo Conservation Field Station, and field men. Proc. Natl Acad. Sci. 111, 16662–16669 (2014). staff Monday Gideon, Jackson Okuti, Sam Adue and Jacob Aoli for their support during 34. Boesch, C. et al. Intergroup conflicts among chimpanzees in Tai National data collection. We acknowledge Royal Zoological Society of Scotland for providing core Park: lethal violence and the female perspective. Am. J. Primatol. 70, 519–532 funding to BCFS and Leakey Foundation (R.M.W., C.C., T.D., K.Z.), British Academy (2008). (C.C.), Leverhulme Trust (K.Z.) and Max Planck Society (R.M.W., C.C. and T.D.) for 35. Herbinger, I., Papworth, S., Boesch, C. & Zuberbu¨hler, K. Vocal, gestural and funding the research. locomotor responses of wild chimpanzees to familiar and unfamiliar intruders: a playback study. Anim. Behav. 78, 1389–1396 (2009). 36. Goodall, J. The Chimpanzees of Gombe: Patterns of Behavior (Belknap Press of Author contributions Harvard University Press, 1986). R.M.W. and C.C.: conception, implementation, statistical analyses, paper writing; T.D.: 37. Townsend, S. W., Slocombe, K. E., Thompson, M. E. & Zuberbu¨hler, K. conception, endocrinological field and lab advisor, paper writing; A.W.: glucorticoid Female-led infanticide in wild chimpanzees. Curr. Biol. 17, R355–R356 (2007). analyses; K.E.L.: genetic analyses, paper writing; K.Z.: conception, field support, paper 38. Crockford, C. et al. Urinary oxytocin and social bonding in related and writing. unrelated wild chimpanzees. Proc. R. Soc. B 280, 20122765 (2013). 39. Slavich, G. M. & Cole, S. W. The emerging field of human social genomics. Clin. Psychol. Sci. 1, 331–348 (2013). Additional information 40. Sapolsky, R. M., Romero, L. M. & Munck, A. U. How do glucocorticoids Supplementary Information accompanies this paper at http://www.nature.com/ influence stress responses? Integrating permissive, suppressive, stimulatory, and naturecommunications preparative actions. Endocr. Rev. 21, 55–89 (2000). 41. Holt-Lunstad, J. & Uchino, B. in Health Behavior: Theory, research and Competing financial interests: The authors declare no competing financial interests. practice (eds Hlanz, K., Riemer, B. K. & Viswanath, K.) 183–204 (Jossey-Bass, Reprints and permission information is available online at http://npg.nature.com/ San Francisco, CA, 2015). reprintsandpermissions/ 42. Reynolds, V. The Chimpanzees of the Budongo Forest: ecology, behaviour, and conservation (Oxford University Press, 2005). How to cite this article: Wittig, R. M. et al. Social support reduces stress hormone levels 43. Altmann, J. Observational study of behavior: sampling methods. Behaviour 49, in wild chimpanzees across stressful events and everyday affiliations. Nat. Commun. 7, 227–266 (1974). 13361 doi: 10.1038/ncomms13361 (2016). 44. Hauser, B., Deschner, T. & Boesch, C. Development of a liquid chromatography–tandem mass spectrometry method for the determination of Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in 23 endogenous steroids in small quantities of primate urine. J. Chromatogr. published maps and institutional affiliations. 862, 100–112 (2008). 45. Erb, R. E., Tillson, S. A., Hodgen, G. D. & Plotka, E. D. Urinary creatinine as an This work is licensed under a Creative Commons Attribution 4.0 index compound for estimating rate of excretion of steroids in the domestic International License. The images or other third party material in this sow. J. Anim. Sci. 30, 79–85 (1970). article are included in the article’s Creative Commons license, unless indicated otherwise 46. Wittig, R. M. et al. Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees. Proc. R. Soc. B 281, in the credit line; if the material is not included under the Creative Commons license, 20133096 (2014). users will need to obtain permission from the license holder to reproduce the material. 47. Muller, M. N. & Lipson, S. F. Diurnal patterns of urinary steroid excretion in To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ wild chimpanzees. Am. J. Primatol. 60, 161–166 (2003). 48. Fraser, O. N., Schino, G. & Aureli, F. Components of relationship quality in r The Author(s) 2016 chimpanzees. Ethology 114, 834–843 (2008). 8 NATURE COMMUNICATIONS | 7:13361 | DOI: 10.1038/ncomms13361 | www.nature.com/naturecommunications

Journal

Nature CommunicationsSpringer Journals

Published: Nov 1, 2016

There are no references for this article.