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Social Bonds of Female Baboons Enhance Infant Survival

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Science  14 Nov 2003:
Vol. 302, Issue 5648, pp. 1231-1234
DOI: 10.1126/science.1088580

Abstract

Among nonhuman primates, females often form strong bonds with kin and other group members. These relationships are thought to have adaptive value for females, but direct effects of sociality on fitness have never been demonstrated. We present 16 years of behavioral data from a well-studied population of wild baboons, which demonstrate that sociality of adult females is positively associated with infant survival, an important component of variation in female lifetime fitness. The effects of sociality on infant survival are independent of the effects of dominance rank, group membership, and environmental conditions. Our results are consistent with the evidence that social support has beneficial effects on human health and well-being across the life span. For humans and other primates, sociality has adaptive value.

Social relationships play an important role in the daily lives of females in many species of nonhuman primates. In some species, females form close and enduring relationships with other group members, and they spend a substantial amount of time grooming and resting together (1). These social bonds have long been presumed to have adaptive consequences for females (2), but there has been no evidence directly linking the quality of social bonds to fitness outcomes. Here, we present evidence for such effects, supporting the hypothesis that social bonds have adaptive value for primates.

We draw on data from a long-term study of wild savannah baboons, Papio cynocephalus, in the Amboseli basin of Kenya to examine the relationship between social integration and female reproductive performance. Savannah baboons are an appropriate subject for this kind of analysis because they are highly gregarious and live in large mixed-sex groups. Females remain in their natal groups throughout their lives, whereas males disperse from their natal groups when they mature (3). Females form stable matrilineal dominance hierarchies in which maternal kin occupy adjacent ranks (3). Females establish strong and well-differentiated relationships with other adult females in their groups (4). Female-female relationships are typically characterized by frequent grooming, close spatial proximity, and occasional acts of coalitionary support (4, 5). Social relationships among females are hypothesized to be valuable to adult females because they enhance the prospects of obtaining coalitionary support in within-group contests (6) or increase tolerance from more powerful group members (7). Social relationships among females may also provide a benign environment for raising and socializing their offspring. Social relationships with adult males may be valuable to females because male associates shield females from harassment (8), support their offspring in agonistic interactions (9), and in some populations protect the females' infants from predators or infanticidal attacks (10).

We studied the members of several well-habituated baboon groups that occupied overlapping home ranges in the Amboseli basin at the foot of Mount Kilimanjaro (11). The study population is derived from two groups, Alto's Group and Hook's Group, which have been monitored continually since 1971 and 1980, respectively. During the study period (1984 to 1999), both of the original study groups shifted their home ranges and fissioned (11, 12).

Behavioral data were derived from 10-min focal samples of adult females (11). Data on reproductive events and infant survival were derived from demographic records that contain information about all pregnancies, births, deaths, and maturational events. Monthly dominance ranks for adult females were computed from the outcome of dyadic agonistic encounters observed during focal samples and ad libitum (11). The analyses described in this report are based on about 34,000 focal samples of 108 adult females during 633 female years.

We calculated infant survival for each female as the proportion of infants that survived to 1 year of age, the major period of infant dependency in this species. We focused on survival to 1 year because infant survival is a major component of fitness for any organism, and it has particularly large effects on long-lived animals that reproduce slowly (13). Further, both empirical and modeling results for the Amboseli baboons indicate that infant survival is an important source of variation in lifetime fitness among females, arguably the most important one (14). For each female, we computed the difference between the proportion of infants that survived to 1 year and the median proportion of all infants born in the population that survived to 1 year of age. High values of this measure, labeled relative infant survival, represent females who reproduced more successfully than the median female, and low values represent females who reproduced less successfully than the median female.

Our focal samples yielded three measures of sociality, each of which is a probability estimate based on the proportion of point samples (i) in which an adult conspecific is with 5 m, (ii) being groomed by other adults, and (iii) grooming other adults. Grooming and maintaining proximity to other group members represent the major components of female baboons' social time and are widely considered to provide meaningful measures of social relationships among nonhuman primates (15). We combined these three measures into a single composite measure of sociality, the composite sociality index (16, 17). We used this composite index, rather than investigating the three measures independently, because they were highly intercorrelated (proximity × grooming others: Spearman rank correlation test rs = 0.439, P < 0.001; proximity × being groomed: rs = 0.303, P = 0.001; grooming others × being groomed: rs = 0.404, P < 0.001; N = 108). Further, each was positively related to relative infant survival in linear regressions (18) with relative infant survival as the response variable, although not all were statistically significant predictors on their own (predictor variables were proximity: β = 0.460, t = 1.85, P = 0.068; being groomed: β = 0.175, t = 3.28, P = 0.001; and grooming others: β = 0.095, t = 1.42, P = 0.159; N = 108).

The composite sociality index provides a measure of the extent to which each female deviates from the global population on all three measures combined; high composite sociality index values represent females who were more socially integrated than the median female, and low composite sociality index values represent females who were less socially integrated than the median female.

The social integration of females was a significant predictor of infant survival (Fig. 1). Females who had high composite sociality index scores had offspring with relatively higher survival than females who had low composite sociality index scores (Table 1). High dominance rank is associated with high values of both the composite sociality index and relative infant survival (Table 1), raising the possibility that the relationship between the composite sociality index and relative infant survival is an artifact of variation in female dominance rank. However, the relationship between sociality and infant survival remains significant when the effects of dominance rank are accounted for statistically in a multiple regression (Table 1).

Fig. 1.

Effects of sociality on infant survival. For the purposes of visual representation, composite sociality index scores were ranked from low to high, and divided into four quartiles [statistical analyses were performed on composite sociality index scores as a continuous variable (Table 1)]. Quartile 1 includes the females with the lowest composite sociality index scores, and quartile 4 includes females with the highest composite sociality index scores. Means and standard errors of the mean of relative infant survival for each quartile are shown. For each quartile, N = 27.

Table 1.

Predictors of relative infant survival (RIS) and adjusted relative infant survival (adj. RIS). Regression with robust standard errors (18, 33) was used to measure the extent to which sociality and dominance rank predicted infant survival. CSI, composite sociality index; adj. CSI, adjusted values of composite sociality index. For the multivariate regressions, we report the partial-regression coefficients and parameters as well as the whole-model results. High-ranking females are assigned the lowest rank numbers, so negative coefficients indicate that higher ranking females had higher reproductive success than lower ranking females. The sample size for the regressions based on unadjusted values is 108; the sample size for the regressions based on adjusted values is 106, because two females who did not give birth during the study period were deleted from this portion of the analysis.

Model Response variable Predictor variables Partial regression parameters β R2FPt
Bivariate RIS CSI 0.270 0.078 8.15 0.005
Bivariate RIS Rank -0.011 0.040 4.62 0.034
Multivariate RIS CSI and rank 0.093 5.43 0.006
CSI 0.234 0.026 2.27
Rank -0.007 0.202 -1.28
Bivariate Adj. RIS Adj. CSI 0.332 0.081 7.20 0.009
Bivariate Adj. RIS Rank -0.007 0.011 1.21 0.275
Multivariate Adj. RIS Adj. CSI and rank 0.082 3.67 0.029
Adj. CSI 0.321 0.015 2.48
Rank -0.002 0.685 -0.41

Sociality and infant survival varied considerably over the study period, and this is likely to be linked to temporal changes in environmental conditions over the course of the study and to changes in habitat quality associated with the groups' home range shifts (12, 14, 19). Females who were observed in more favorable habitats or during more favorable time periods might have been more social and reproduced more successfully than females observed during less favorable periods, raising the possibility that the relationship between sociality and infant survival is an artifact of variation in habitat quality. To control for this possibility, we adjusted our measures of sociality and infant survival (20). We did not assess environmental conditions directly, but we controlled for the effects of ecological variation by comparing each female to other females living in the same group at the same time in the same habitat. High values of the adjusted composite sociality index represent females who were more socially integrated than other females living in the same group at the same time in the same habitat, and high values of adjusted relative infant survival represent females who reproduced more successfully than other females who were living in the same group at the same time in the same habitat.

As before, we found that females who were more fully socially integrated (defined by higher adjusted composite sociality index values) had higher adjusted relative infant survival among their offspring (Table 1). This result remains significant when the effects of dominance rank are accounted for statistically in a multiple regression (Table 1).

Our data indicate that social integration has positive effects on the reproductive performance of female baboons. Females who had more social contact with other adult group members and were more fully socially integrated into their groups were more likely than other females to rear infants successfully. These effects were independent of female dominance rank and variation in ecological conditions that affected both females' behavior and their reproductive performance. Thus, these data provide direct empirical evidence that sociality enhances the fitness of nonhuman primate females.

Our findings are consistent with data derived from epidemiological and clinical studies of humans. Social support has beneficial effects on health and well-being across the life span (2124). Social isolation increases the risk of disease, accidents, and a range of mental disorders, and the disruption of social ties, due to death, divorce, or separation, is a major source of stress. Feelings of loneliness are associated with psychological disturbances, and loneliness increases morbidity and mortality (25). Among low-income women, those with more extensive social networks give birth to heavier infants (26). Experimental studies in humans suggest that social integration is the cause not the consequence of improved health outcomes. Social support is thought to moderate the deleterious effects of chronic stress and thereby enhance well-being.

Social contact seems to have similar kinds of effects in other species (27). Human handling reduces cardiovascular responses to stressors in dogs, cats, horses, and rabbits (21). In the laboratory, group-living delays reproductive senescence in female rats (28) and enhances longevity (22). The presence of familiar conspecifics buffers experimentally induced stress in rats, mice, goats, and monkeys (21, 27). Basal cortisol levels decline when squirrel monkey females are housed with conspecific partners (29), and social isolation exacerbates coronary artery atherosclerosis among female long-tailed macaques (30). Captive long-tailed macaques tend to affiliate at higher rates when social conditions are unstable, and this is associated with enhanced immune responsiveness (31). In the Amboseli baboon population, social integration is linked to reduced levels of basal cortisol among adult males (17).

It is not yet clear whether the mechanisms that underlie the relationship between sociality and infant survival in baboons are the same as the mechanisms that link social contact and health outcomes in humans. Close association with other group members may ameliorate the deleterious effects of stress in nonhuman primates in much the same way as it does in humans. For example, grooming reduces heart rate in some monkey species, and may induce release of β-endorphins (32). Similarly, heart rate and the rate of self-directed behaviors that are correlated with physiological measures of stress decline when females reconcile with former opponents (32). Alternatively, close association with other group members may provide females and their dependent offspring with direct material benefits, such as protection from harassment or access to valuable resources. For example, in Amboseli, adult females spend much of their time near their kin, who are also their most frequent allies in agonistic disputes (5). Female baboons also spend time near adult males who sometimes protect them and their offspring from harassment (810). All of these factors, and others that we have not yet considered, may contribute to the relationship between sociality and infant survival. Whatever the mechanism, our data demonstrate that social relationships have adaptive value for primate females.

Supporting Online Material

www.sciencemag.org/cgi/content/full/302/5648/1231/DC1

Materials and Methods

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References and Notes

  1. We computed a composite index of social integration for each female as follows: Embedded Image where the values of xi are those for each of the three behavioral measures for the female, and the values of mi are the median values of the respective behavioral measure for the population. A similar index was originally used by Sapolsky, Alberts, and Altmann (17).
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