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Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers (2014)

Chapter: 6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk

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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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6


Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness

Joan B. Silk

INTRODUCTION

The goal of this paper is to assess the impact of close social bonds on the health, longevity, and reproductive success of individuals in animal groups. Much of the work I discuss has been conducted on nonhuman primates. This taxonomic bias primarily reflects the fact that primatologists have a long history of interest in the complex dynamics of social relationships and commonly collect detailed information about the form, frequency, and sequence of interactions among individually identified animals with known reproductive histories. These kinds of data are not commonly available for other taxa. However, there are indications that similar processes operate in a range of species and may be part of a broader mammalian pattern. These data suggest that there may be important parallels between humans and other species in the association between relationship quality, health, and fitness outcomes.

I approach this problem as a behavioral ecologist, which means that I am motivated to understand how evolution shapes phenotypic traits to enhance the fitness of individuals. Phenotypic traits include physical characteristics, such as body size, strength, and running speed; physiological factors, such as stress response systems and immune function; and behavioral traits, such as vigilance, foraging strategies, and parental care. Behavioral traits take on added complexity in group-living species because individuals have opportunities to interact with conspecifics on a regular basis, and social interactions create opportunities for individuals to help or harm one another.

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

Sociality evolves when the net benefits of aggregation (e.g., higher vigilance rates, pooling information, and collective resource defense) exceed the costs that come from living in close proximity to conspecifics (e.g., resource competition, disease risk, and conflicts of interest). However, for individuals that live in social groups, the costs and benefits of group life are often distributed unequally. Members of particular age-sex classes may be systematically disadvantaged in competition over resources or exposed to greater predation risks. Moreover, within age-sex classes, there may be consistent variation in benefits and costs of group life, and these disparities may generate individual variation in lifetime fitness. Natural selection is expected to favor behavioral and social strategies that enhance the benefit/cost ratio for individuals.

In some cases, the adaptive logic of these kinds of strategies is relatively straightforward. For example, animals require resources to survive and reproduce successfully, and they often compete for these resources when they are in short supply. In many group-living species, the outcomes of competitive encounters within dyads are stable from day to day, and individuals can be assigned ranks within a dominance hierarchy. If high-ranking animals have priority of access to resources, and access to resources is an important component of survival and reproductive success, then a positive correlation between dominance rank and reproductive success and for selection to favor traits that enhance success in competitive encounters would be expected. Both these predictions are widely supported, although there are some interesting exceptions to the general patterns (Ellis, 1995; Clutton-Brock, 2009; Majolo et al., 2012).

In other cases, the link between behavioral strategies and fitness outcomes is less clear. For example, animals in many taxa devote considerable amounts of time to affiliative social interactions, such as social grooming. Grooming has hygienic functions and may therefore confer direct benefits on recipients (Akinyi et al., 2013). It has also been hypothesized that animals use grooming (and other forms of affiliation) to strengthen relationships with favored partners (Dunbar, 1991) and selectively invest in social relationships that enhance their fitness (Kummer, 1978). For example, in spotted hyenas (Crocuta crocuta), bottlenosed dolphins (Tursiop aduncus), and chimpanzees (Pan trogloydytes), reproductive success depends, in part, on the ability to recruit coalitionary support. Allies may be cultivated and alliances may be reinforced by affiliative interactions, such as greetings (Smith et al, 2011), displays (Connor, 2007), or grooming (Mitani, 2006). However, until recently, there was little evidence that investments in social relationships produced fitness payoffs. This is now beginning to change as researchers explore the links between relationship quality and important components of fitness, such as infant survival and longevity.

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

This new work builds on two separate developments in primate behavioral ecology. First, there has been a shift in the unit of analysis in behavioral studies. Behavioral ecologists tend to construct analyses in which the individual is the unit of analysis, not the dyad, and to examine correlations between individual traits and fitness outcomes. However, for animals that live in social groups, the fitness of individuals depends at least in part on the outcome of their interactions with other group members. This has prompted a shift from a strict focus on individual behavior to a broader view that includes the behavior of individuals and the nature of the relationships that they form with others (Silk et al., 2013).

The second important development is that behavioral ecologists have begun to explore the physiological mechanisms that mediate the relationship between social behavior and fitness outcomes. For many years, there was a tacit division of labor among researchers working at different levels of analysis. Behavioral ecologists focused mainly on questions about how natural selection shaped behavior to enhance genetic fitness and did not evaluate the underlying mechanisms that regulate behavior. Studies of the mechanisms that influence behavior were mainly conducted by psychologists working in the laboratory where fitness effects could not be evaluated. However, the development of noninvasive methods for assessing stress physiology (Beehner and Lu, 2013) has altered the status quo. These methods allow fieldworkers to assess the impact of social factors on health and disease, a potentially important cost of living in social groups (Nunn and Altizer, 2006). They also provide insight about how animals perceive the events that they experience and how social strategies influence their ability to cope with chronic and acute sources of stress.

I begin by establishing the empirical foundation for the claim that sociality influences fitness outcomes. Much of this evidence comes from two long-term studies of baboons. I describe how social relationships in other primates are assessed, then present results drawn from this body of data. I also describe what is known about the fitness effects of sociality in other animal taxa. I then consider the mechanisms that underlie relationships between sociality and fitness outcomes, discussing both the direct benefits that animals may gain from their social partners (e.g., protection from predators) and the indirect benefits that they may derive from social ties (e.g., reduced stress levels). Finally, I consider what is known about negative impacts that sociality may have on health and fitness via its impact on the prevalence, persistence, and virulence of pathogens.

SOCIAL BONDS AND FITNESS OUTCOMES: INITIAL EVIDENCE

In the late 1990s, Susan Alberts, Jeanne Altmann, and I began a collaboration to investigate the structure and function of social bonds among

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

female baboons. Alberts and Altmann are co-directors of the Amboseli Baboon Research Project (ABRP), which has been monitoring baboons in the Amboseli basin of Kenya since the early 1970s. Systematic observations of two social groups were initiated in 1971 and 1980, respectively (Altmann and Alberts, 2003). These two study groups subsequently fissioned, and the project continues to monitor several of the daughter groups from the original study groups. The reproductive histories, dominance ranks, and maternal kinship relationships of all females in the study groups are known. Research assistants regularly conduct 10-minute focal samples on all adult females in the study groups. During these samples, the activity and nearest neighbors of focal subjects are recorded on 60-second intervals.

We developed a measure of social integration that was based on the frequency with which females groomed or were groomed by other adults and were in proximity to other adults during focal observations. We used these values to create a composite index of sociality for each female (Silk et al., 2003). Females that have high values of the index spend more time grooming and associating than the average female, and females that have low values of the index spend less time grooming and associating than the average female. To assess female reproductive success, we tabulated the proportion of infants that survived to 1 year of age. We chose this measure because infant survival is an important source of variation in lifetime fitness among females in the Amboseli population (Altmann and Alberts, 2003).

We found that females that were more socially integrated into their groups had higher reproductive success than females that were less socially integrated (Silk et al., 2003). These effects were independent of variation in female dominance rank and ecological conditions that affected both females’ activity budgets and their reproductive performance. These results attracted considerable interest because they provided the first systematic evidence that social relationships are linked to reproductive success, and they suggest that investment in close social bonds has an adaptive payoff. However, the Amboseli analyses were vulnerable to several potential questions and criticisms:

  1. The analyses included interactions and association with adult males, and it is possible that females gained fitness benefits from their associations with males, not their associations with other females. Our analyses do not tell us whether relationships among females have fitness consequences.
  2. The relationship between social integration and infant survival might reflect elevated levels of sociality for mothers of surviving infants rather than benefits derived from sociality (Henzi and Barrett, 2007) because female baboons in Amboseli are strongly attracted to other females’ infants (Altmann, 1980).
Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×
  1. The measure of social integration that we used did not fully characterize the nature of social bonds. Thus, it is not clear whether our results reflect differences in the quantity of social contacts of the quality of social bonds that females form.
  2. Our findings were based on several groups in a single population, and the results might not hold for other populations of baboons or for other taxa. Clearly, the findings warrant more attention if they turn out to be robust.

In the next section, I will discuss how my colleagues and I have addressed these problems. I begin by discussing the methods we have developed for characterizing dyadic social bonds, and then discuss the structure of social bonds among female baboons in Amboseli and in a second population of baboons.

DEFINING AND DOCUMENTING THE STRUCTURE OF SOCIAL RELATIONSHIPS

Primatologists must take a different approach to studying social relationships than psychologists or sociologists because we cannot interview our subjects about their relationships with others, and we cannot rely on introspection for an understanding of what these relationships mean to them. Instead, we have been forced to take a bottom-up approach, looking for patterns in behavior to characterize relationships.

Hinde (1983) described social relationships as abstractions that represent the history of interactions between two individuals. As empiricists, we need methods of operationalizing this concept. It may be useful to think about social relationships (or social bonds) as a multidimensional space, and the empirical task is to map the contours of that space (Silk et al., 2013). There are a number of dimensions along which relationships might vary. For example, some pairs of monkeys might interact often, while others do so rarely. Some individuals might interact in a restricted set of contexts (e.g., sexual or agonistic), while others interact in a broader range of situations. Directional interactions, like grooming or approaches, may be highly one-sided or evenly balanced. The tenor of interactions within dyads may range from mostly hostile to mainly friendly. Some pairs of individuals may interact at high rates for short periods of time, while others may consistently interact at high rates over long periods of time. Finally, some pairs may be relaxed when they are together or tense. This scheme can be expanded as other dimensions are defined.

This way of thinking about social relationships has several useful features. First, it allows for the exploration of “relationship space” in a systematic way. Second, this way of characterizing social relationships does not

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

rely on preconceived notions about how social relationships are structured. While it might be predicted that animals that frequently groom and affiliate would be very relaxed when they are together and rarely fight, it might be that these dimensions are not aligned as expected. For example, among baboons in Moremi, maternal sisters have both high rates of affiliation and high rates of aggression (Silk et al., 2010a). Third, although we initially developed this scheme to describe social relationships among baboons, it may be adapted for other taxa with different behavioral repertoires.

The Structure and Function of Social Bonds Among Female Baboons in Amboseli

We used the approach described above to assess the nature of social relationships among females. For each pair of females, we tabulated the proportion of observation time that they were nearest neighbors or grooming one another, and used these values to create a dyad-specific composite sociality index (DSI, Silk et al., 2006a). As before, high values of the dyadic index represent dyads that spent more grooming and associating than the average pair of females.

We found that most pairs of females had very low DSI values, but a small number of dyads had quite high values. As in many other primate species, females showed strong preferences for close maternal kin, particularly their mothers, daughters, and sisters. Females also distinguished between paternal half-siblings and unrelated females. In a separate analysis, we also found that females selectively supported close kin more than they supported distant kin or non-kin (Silk et al., 2004). Although the availability of close kin had strong effects on the number of close social bonds that females formed, virtually all females in the population formed at least one close social bond even if they had no close maternal relatives in the group.

There was considerable variability in the distribution of grooming within dyads. That is, in some dyads, grooming was well-balanced, but in other dyads one female groomed her partner much more than she was groomed in return. Pairs that formed strong social bonds groomed more equitably than pairs that formed weaker social bonds (Silk et al., 2006b). This result could be an artifact of maternal kinship because related partners groomed more equitably than unrelated partners and related partners also formed stronger social bonds than unrelated partners. However, the relationship between grooming balance and the strength of social bonds held when the analysis was limited to unrelated females, so the connection between the strength of social bonds and the degree of grooming balance seems to be at least partly independent of kinship.

We also examined the stability of females’ relationships with their favored partners. For each female, we identified her top three partners in

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

each year, and then we tabulated the number of consecutive years in which particular partners appeared among the focal females’ three top partners. We found that females had consistent preferences for their most favored partners (Silk et al., 2006b). For example, mothers and daughters were quite likely to remain top partners for as long as they lived together in the group. At the same time, relationships with most unrelated partners were ephemeral, with strong relationships existing in one year, but not lasting until the next. Females’ relationships with their top three partners are more likely to be sustained from year to year than would be expected by chance, while relationships with lower-ranking partners have little stability from year to year (Silk et al., 2012).

In summary, our findings indicate that female baboons in Amboseli form strong, supportive, well-balanced, and enduring relationships with selected partners. Preferred partners are typically close kin, but nearly all females seem to form a few close relationships even if no close kin are available.

Replication: The Structure and Function of Social Bonds Among Female Baboons in Moremi

After the Amboseli data were published, Dorothy Cheney and Robert Seyfarth invited me to collaborate on analyses of social relationships among female baboons in the Moremi Reserve of the Okavango Delta of Botswana. We were able to capitalize on the fact that a number of researchers who worked at the site from 2000-2007 (Jacinta Beehner, Thore Bergman, Catherine Crockford, Anne Engh, Liza Moscovice, and Roman Widdig) conducted focal observations on adult females using the same protocol that Cheney, Seyfarth, and I had used in the early 1990s.

Our analyses were designed to avoid two of the possible problems with previous analyses of the Amboseli data. That is, we limited our attention to interactions and associations among adult females and excluded observations that were conducted when females had young infants. Our goal was to draw comparisons across populations, so we mirrored the structure of the Amboseli analyses as closely as we could.

The social relationships of the Moremi females were strikingly similar to the social relationships of females in Amboseli. The Moremi females formed strong, well-balanced, supportive, and enduring relationships with selected partners (Silk, 2010a). Like the Amboseli females, the Moremi females showed strong preferences for close maternal kin and for peers. And females formed enduring relationships with preferred partners, particularly their mothers, daughters, and sisters, and only close social bonds are more likely to be sustained from year to year than would be expected by chance (Silk et al., 2012).

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

We were not able to assess the effects of paternal kinship on the strength of social bonds, but there is good reason to believe that peers will often be paternal half-sisters. Top-ranking males monopolize access to receptive females in Moremi (Bulger, 1993) and sire the majority of infants (Cheney and Seyfarth, unpublished data), but average tenure length for top-ranking males is fairly short (Palombit et al., 2000). This means that animals that are close in age are likely to have the same father.

We also evaluated the tenor of social bonds, by assessing the proportion of dyadic interactions that were friendly. Kinship did not preclude aggression, but the proportion of all interactions that were friendly was positively related to the degree of relatedness among females. Females were more tolerant of their most preferred partners than they were of others (Silk et al., 2010a).

Finally, we investigated the adaptive consequences of close social bonds among the Moremi females using survivorship analysis methods. The infants of mothers with strong social bonds lived longer than the infants of mothers with weaker social bonds (Silk et al., 2009). In contrast, female dominance rank had no consistent effect of infant survival. We also found that females that formed the strongest social bonds with their top partners lived longer than females with weaker social bonds (Silk et al., 2010b). In addition, high-ranking females lived longer than other females.

Evidence from Other Taxa

There is a gap between what is known about the form and function of social bonds in baboons and what is known about other primate taxa and in species outside the primate order. Kin are preferred partners in a wide variety of taxa, and the presence of kin has positive effects on fitness for females in a number of species (reviewed in Silk, 2007). A number of species form “fission-fusion groups,” which means that group members frequently subdivide to form temporary subgroups. Studies of a number of species that live in fission-fusion groups show that females form preferences for particular same-sex partners, and these preferences are not always based on kinship (bottle-nosed dolphins: Möller et al., 2006; giraffes, Giraffe camelopardalis: Carter et al., 2013; eastern grey kangaroos, Macropus giganteus: Best et al., 2013; Carter et al., 2009; chimpanzees, Pan troglodytes: Langergraber et al., 2009; Lehmann and Boesch, 2009). However, few details about the form or function of these relationships are available. Below I briefly describe studies in which researchers have investigated links between the some aspects of the quality of social bonds and fitness outcomes.

Schülke et al. (2010) evaluated the form and function of social bonds among male Assamese macaques, Macaca assamensis. Males in this species disperse from their natal groups at puberty and join groups in which they

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

have few close relatives. Like female baboons and male chimpanzees, the male Assamese macaques spent more time grooming and associating with some male partners than others. Schülke and his colleagues discovered that males that formed the strongest bonds were more likely to support one another in aggressive interactions. The strength of males’ social bonds was directly related to the number of infants that they sired in the subsequent breeding season.

Wild horses form stable groups that typically contain one male, a number of unrelated females, and their offspring (Linklater, 2000). Using information about time that females spent in close association with one another and their participation in grooming interactions with other females, Cameron et al. (2009) computed a composite index of social integration for each female like the one that we used for the Amboseli baboons. They found considerable variation among females in the extent of social integration, but females that were most fully integrated into their groups had higher foaling success than other females.

Bottlenosed dolphins live in fission-fusion groups, and the size and composition of parties changes frequently. Analyses of long-term party association data from Sharks Bay, Australia, indicate that females associate at higher rates with some females than others. The structure of females’ social networks are associated with the production of surviving offspring (Frére et al., 2010). Females that spend much of their time together tend to have similar reproductive success as well.

Male bottlenosed dolphins form close ties with one or two other males, often relatives, and these associations may last for many years. Close associates engage in friendly contact, and perform highly synchronized displays as they leap from the water (Connor et al., 2006). These close associations are labeled “alliances” because males team up with their associates to mate guard receptive females. In Sharks Bay, members of different alliances sometimes team up to take receptive females away from other males or to prevent disruption of their own consortships. Males with more stable alliances consort with females at higher rates (Connor et al., 2001), and the great majority of paternities are assigned to males that belong to alliances (Krützen et al., 2004). These data suggest that strong and stable bonds among male dolphins may enhance their reproductive success.

In the wild, house mice form mixed sex groups that include one adult male, several adult females, and their litters. Females that give birth about the same time usually pool their litters and nurse them communally (König et al., 1994a, 1994b; Hayes, 2000). In an experimental study of house mice, Weidt et al. (2008) evaluated the social preferences of females in groups composed of unrelated individuals and then paired females with either their most preferred partners or their least preferred partners. Females that were paired with preferred partners were significantly more

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

likely to produce litters and weaned more pups than females paired with non-preferred partners.

PROXIMATE MECHANISMS THAT MEDIATE THE RELATIONSHIP BETWEEN CLOSE SOCIAL BONDS AND FITNESS OUTCOMES

The correlation between close social bonds and fitness outcomes may arise because animals gain direct or indirect benefits from their relationships with others. Direct benefits might include things like coalitionary support, protection from harassment, greater access to resources, or reduced vulnerability to predators. Indirect benefits would include positive effects on stress response systems, immune function, and health.

Direct Benefits Derived from Close Social Bonds

There is not yet enough information to generate a comprehensive analysis of the direct benefits that animals gain from close social bonds. Instead, case studies illustrate a range of direct benefits that animals may gain that enhance their fitness.

Coalitionary Support

Male Assamese macaques that formed close social bonds also supported one another in coalitions. Males that participated in coalitions most often were most likely to rise in rank, and high-ranking males had priority of access to receptive females and achieved higher reproductive success than lower ranking males. Social bonds may enhance the likelihood of gaining coalitionary support in chimpanzees as well. In the Ngogo chimpanzee community, males spend the most time grooming the males that they most often support in agonistic coalitions (Mitani, 2006). At Gombe, chimpanzee males that participate in coalitions most often are more likely to rise in rank and sire more offspring than males that participate in coalitions less often (Gilby et al., 2013). Thus, for both male Assamese macaques and male chimpanzees, social bonds may provide a route to achieving high rank and more mating opportunities.

Predator Deterrence

Michelleta et al. (2012) examined the relationship between the strength of social bonds among females and the effectiveness of predator responses in crested macaques, Macaca nigra. Crested macaques give alarm calls when they detect the presence of pythons, and their alarm calls attract other group members who may subsequently mob the predator, often

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

leading to its retreat. Mobbing is potentially dangerous, and the success of mobbing efforts depends on the effective coordination and cooperation of participants. In experiments that simulated a python encounter, experimenters played previously tape-recorded alarm calls back to other group members. The monkeys responded more strongly to alarm calls given by close affiliates than other group members. If effective predator responses enhance survival, then the individuals that form close social bonds may gain important fitness benefits.

Eastern grey kangaroos form groups, but frequently divide up into subgroups with fluid membership. Females associate with some females more often than expected based on chance, while there are others that they spend less time with than expected by chance (Best et al., 2013; Carter et al., 2009). The strength of a female’s relationship with the female nearest to her predicted the amount of time that she spent grazing. The authors suggest that females are less vigilant when they are near preferred partners, and this enables them to devote more time to foraging.

Access to Resources

King et al. (2012) investigated the impact of close social bonds on the frequency with which female chacma baboons in semi-arid habitats in Namibia fed together in a single food patch. Their measure of relationship quality was based on the frequency of dyadic grooming. They found that females with close social bonds were more likely to feed together than females with weaker social bonds. These effects were not due to the effects of maternal kinship or dominance rank. These findings complement previous evidence that showed that females were more likely to follow preferred partners into experimental food patches (King et al., 2008) and fed at higher rates when they co-fed with preferred partners (Covas, 2005, cited in King et al., 2011).

Protection from Infanticide/Harassment

In some species, close associations among males and females may provide females and their offspring protection against harassment by conspecifics. Infanticide, in which adults direct lethal attacks on immatures, is the most severe form of harassment. As noted earlier, mothers of newborn infant baboons often form “friendships.” Male friends are often, but not always, the fathers of their friends’ infants (Nguyen et al., 2009; Moscovice et al., 2009, 2010). Mothers are primarily responsible for maintaining proximity to their male friends, and groom them more than they are groomed in return (Palombit et al., 1997). Playback experiments conducted on baboons in Moremi, where infanticide is common, show that males are

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

sensitive to their female friends’ distress (Palombit et al., 1997). And, as infants mature, males selectively support the offspring of their former associates (Moscovice et al., 2009). In Amboseli, where infanticide is not observed, male-female friendships are also common. Females’ infants receive less rough handling and exhibit less distress when their male associates are nearby (Nguyen et al., 2009).

Similarly, among wild horses, females that are more socially integrated receive less harassment from stallions (Cameron et al., 2009). This may be an important benefit because male harassment has a negative impact on female reproductive success (Linklater et al., 1999).

Indirect Benefits of Close Social Bonds

When animals experience events that threaten their well-being, such as predator attacks or aggression from conspecifics, stress response systems are activated. This enables individuals to mobilize energy reserves for critical activities, such as flight, and divert energy from other less immediately essential metabolic processes, such as growth and maintenance (Sapolsky, 2005). Stress responses are also activated in anticipation of danger, and animals react most strongly to events that they cannot control or predict. Prolonged activation of the stress systems has deleterious long-term effects on health and reproductive function (Wingfield and Sapolsky, 2003). If social bonds enhance animals’ sense of predictability and control, or reduce the need to remain vigilant against threats from predators or conspecifics, then they may reduce stress levels and have indirect effects on health and reproductive success. In this section, I review evidence that suggests that social ties help animals cope with several major stressors, social isolation, social instability, and subordinate status. I also describe results from several studies that suggest that the structure of individuals’ social networks is linked to stress levels.

Social Isolation

If sociality is favored by natural selection because it reduces vulnerability to predation, then animals are expected to be safer and feel more secure when they are in groups than when they are alone. Social isolation may activate stress responses that enhance vigilance and responsiveness to danger. Female Norway rats, Rattus norvegicus, are gregarious, share their burrows with conspecifics, and rear offspring communally. In a series of experimental studies, McClintock and her colleagues explored the impact of social isolation on females’ ovarian function and vulnerability to mammary tumors. Isolated individuals are hypervigilant and neophobic, and they display higher cortisol levels, develop mammary tumors earlier,

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

and their tumors are more likely to be malignant (McClintock et al., 2005; Hermes et al., 2009).

Social ties can help animals cope with the stress of isolation. In mixed-sex captive groups, guinea pigs (Cavia aperea) form strong bonds with a single individual of the opposite sex. These bonds are characterized by high levels of friendly contact and sexual behavior. When males or females are removed from their social group and placed alone in an unfamiliar cage, their cortisol levels rise significantly. For both sexes, this response is reduced by the presence of their preferred partner (Sachser et al., 1998; Kaiser et al., 2003). Siberian hamster females form strong ties to their sisters, and social isolation delays wound healing (Detillion et al., 2004).

Social Instability

Social instability is a major source of stress for animals (Mendoza et al., 2000; de Vries et al., 2003). This is likely due to the fact that social relationships are altered by the presence of new group members or the absence of familiar partners. For example, when new individuals enter a group, levels of aggression often rise, new dominance relationships are formed, and the existing dominance hierarchy may be altered. And when familiar animals are removed from the group, social ties may be disrupted, important allies may be lost, and the dominance hierarchy may be disrupted.

Capitanio et al. (1998) assessed the impact of social stability on the survivorship of juvenile male rhesus macaques, Macaca mulatta, after inoculation with SIV. Monkeys that interacted regularly with the same individuals (stable associations) spent more time in proximity and more time grooming than males that regularly interacted with unfamiliar individuals (unstable associations). Levels of aggression were also higher in the unstable associations than in the stable associations. Monkeys in the stable associations survived significantly longer after exposure to SIV than monkeys in the unstable associations.

Gust et al. (1996) studied the physiological impact of group formation on juvenile rhesus macaques. They compared the cortisol levels of juveniles who were placed in a new group with a familiar peer, juveniles that were placed in a new group on their own, and juveniles that remained in their natal groups. Juveniles tended to stay close to familiar peers during their first weeks in their new groups. Those that entered new groups on their own had substantially higher cortisol levels after one week than those that were accompanied by a familiar peer.

Instability in the male dominance hierarchy has direct effects on females in some species. For example, in the Moremi baboon population, after a new male immigrates into the group and achieves top rank, he often kills unweaned infants. When mothers lose their infants, they rapidly resume

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

cycling, and the infanticidal male is then likely to be able to mate with the mother. Similar events are seen in a wide range of mammalian species, and are believed to be a product of sexual selection acting on males (Palombit, 2012). The fecal glucocorticoid (fGC) levels of females rise in the days that follow the arrival of new males, and the fGC levels of lactating females, whose infants are vulnerable to infanticide, rise more than fGC levels of females in other reproductive states (Beehner et al., 2005; Engh et al., 2006a).

Social ties can buffer the effects of social instability. Lactating females that have established friendships with adult males have significantly lower fGC levels than females without close male associates (Engh et al., 2006b). This is likely due to the fact that male friends help protect females and their infants from infanticidal aggression (Palombit et al., 1997). Moreover, during a period of instability in the male dominance hierarchy, females initially reduced the number of different females that they groomed (lower grooming diversity). Females that reduced their grooming diversity the most reduced their fGC levels the most as well (Wittig et al., 2008). Those females that had more focused grooming networks before the period of instability began experienced smaller increases in fGC than females with more diffuse grooming networks.

The disruption of close social bonds appears to be an important source of stress for female baboons. Engh et al. (2006a) monitored responses to predation events among the Moremi baboons. They found that fGC levels generally rose in the days that followed predation events. This makes sense, because the stress response system is designed to cope with imminent threats. However, females that lost a close relative experienced greater increases in fGC levels than individuals that were present in the group, but did not suffer a personal loss.

Subordinate Status

There is considerable discussion about the effects of dominance rank on stress levels, with some studies showing that high-ranking individuals have lower cortisol levels than low-ranking individuals, and others showing the opposite effect (Sapolsky, 2005). However, the effects of rank seem to be at least partially affected by the social context. Comparative analyses indicate that subordinates have high glucocorticoid (GC) levels in relation to dominants in species with high levels of harassment by dominants and low levels of social support (primates: Abbott et al., 2003; vertebrates: Goymann and Wingfield, 2004). Abbott and his colleagues also found that social support and access to kin mediate the effects of low rank on subordinates across species. Sapolsky and his colleagues showed that high-ranking male baboons in the Masai Mara of Kenya have lower GC levels than low ranking males, but high-ranking males that rarely groom females or inter-

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

act with infants have elevated GC levels (Ray and Sapolsky, 1992; Virgin and Sapolsky, 1997). In Amboseli, male baboons that are more socially integrated into their groups have significantly lower GC levels than males that are more isolated (Sapolsky et al., 1997). Ostner et al. (2008) found that high-ranking male Assamese macaques have lower cortisol levels than lower-ranking males, and they suggest that close social bonds among males (see above) may mitigate the costs of maintaining high rank.

Reciprocity

There is also some evidence that the structure of interactions may influence how individuals cope with stress. Yee et al. (2008) evaluated the behavior of young female Norway rats housed in groups of three sisters while they experienced a brief stressor. Females that had more well-balanced affiliative interactions with their sisters during these events exhibited lower corticosterone responses to an acute stress in late adulthood, developed mammary tumors later, and lived longer than females with less well-balanced relationships. It is not clear why reciprocity has this effect or whether reciprocity has similar effects in other taxa.

Social Networks

Two studies have examined the impact of an individual’s social networks on cortisol levels in primates. During a period of stability in the male dominance hierarchy, female baboons in Moremi had lower fGC months during months in which they concentrated their grooming on a small number of partners than in months in which they distributed their grooming more evenly among potential partners (Crockford et al., 2008). The structure of females’ grooming networks had a bigger impact on their fGC levels than the overall frequency that females groomed or were groomed by others.

It is not yet clear why the size of females’ social networks is linked to their cortisol levels. If grooming is exchanged for coalitionary support (Seyfarth, 1977; Schino, 2007), then females that spend more time grooming a small number of partners may be more successful in recruiting coalitionary support than females that spread their grooming over a larger number of partners. However, this hypothesis has not been tested directly

Brent et al. (2011) use social network methods to assess the impact of the distribution of grooming, affiliative vocal exchanges, and proximity on monthly fGC levels of female rhesus macaques. They evaluated a number of network metrics for each of these behaviors and found that high-ranking females had significantly lower GC levels in months in which their proximity networks were smaller and more focused. However, this was not true of

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

lower-ranking females, and the structure of grooming networks and vocal exchange networks did not have consistent effects on fGC levels of high- or low-ranking females.

Costs of Close Social Bonds

The primary costs of sociality are likely to be increased competition over access to resources, particularly food, and increased vulnerability to disease. The data reviewed above suggest that some animals use social bonds to mediate the costs of competition. Now, I turn to the relationship between sociality and disease.

There is a growing literature about the impact of sociality on the prevalence, persistence, and virulence of pathogens (Loehle, 1995; Nunn and Altizer, 2006). Much of this work has focused on the effects of group size and social structure (the patterning of social interactions within groups) on parasite loads using comparative methods (e.g., bats: Langwig et al., 2012; carnivores: Nunn et al., 2003a; rodents: Bordes et al., 2007; primates: Vitone et al., 2004; mammals: Altizer et al., 2003; mammals, birds, lizards, fish, insects, spiders: Rifkin et al., 2012.) While there is generally a positive relationship between group size and various measures of disease risk, there is considerable variation in the pattern. This variation may be related to a number of factors, including the mode of parasite transmission, the measure of pathogen risk considered, and the details of social structure. For example, there seems to be an inconsistent relationship between group size and levels of parasitism across the primate order (Nunn et al., 2003b). This may be linked to how associations are patterned in large and small groups. In a subset of 19 primate species, it was found that larger groups tend to have a more modular structure of interactions than smaller groups, and groups with more modular structure have a lower richness of socially transmitted parasites (Griffin and Nunn, 2012).

There have also been efforts to examine the effects of individual characteristics, such as age, sex, and dominance rank on disease in a broad range of species (reviewed by Benavides et al., 2012). The effects of individual characteristics such as age and dominance rank on parasitism might be due to differences in physical condition or immune function among individuals of different age or rank, but they may also be due to differences in their pathogen exposure. Griffin and Nunn’s (2012) results suggest that the structure of individuals’ social networks might matter, and several studies provide evidence that supports this idea. In free-ranging Japanese macaques, high-ranking females have higher parasite richness than lower-ranking females (Macintosh et al., 2010, 2012). High-ranking females did not have higher cortisol levels than lower-ranking females, but they did occupy more central roles in the group grooming network. Thus, the structure of females’

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

social contacts may influence their exposure to parasitic infections. Among meerkats, Suricata suricatta, those that groomed others the most were more likely to be infected with tuberculosis than those that groomed others less. At the same time, those that received the most aggression were more likely to be infected than those who received less aggression (Drewe et al., 2010). Among brush-tailed possums, Trichosurus vulpecula, the likelihood of contracting tuberculosis was higher for individuals that had frequent contacts with a small number of others than for individuals that had equal numbers of contacts spread over a larger number of partners (Porphyre et al., 2011). In a study of wild giraffes, VanderWaal et al. (2013) examined the relationship between patterns of associations, space use, and genetic similarity of a common pathogen (E. coli). They found that individuals who spent more time together shared more genetically similar subtypes of E. coli than those who spent less time together. In contrast, patterns of shared space use had little effect on parasite transmission networks.

These studies suggest that the structure of social contacts can influence pathogen transmission in group-living species. There might be tradeoffs between the stress-reducing effects of social support and close social bonds and the disease-enhancing consequences of high levels of social contact. However, the relative magnitude of these effects cannot yet be weighed because no studies have yet assessed the relationship between relationship quality, levels of parasitic infection, mortality, and fitness outcomes.

CONCLUSIONS

The data reviewed here suggest that the structure of social networks and the quality of social relationships may influence animals’ ability to enhance the benefits and reduce the costs of social life. For group-living animals, including other primates, the ability to form and maintain close social bonds may create multiple direct benefits, including reduced vulnerability to predators, greater access to food resources, and protection from harassment. Moreover, social ties seem to help animals cope with various sources of social stress, perhaps because their relationships provide a greater sense of predictability and control, and this in turn affects health outcomes.

It is not yet clear whether there are differences in the impact of well-differentiated relationships across taxa. Primatologists are typically attuned to the nuances of social relationships and record detailed information about dyadic interactions. Researchers working on other animals do not often obtain the same kind of information about their animals, and this makes it difficult to draw clear comparisons about the quality of social relationships across taxa.

Going forward, it may be useful to design studies to assess and compare the impacts of different elements of relationship quality. For example,

Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×

my colleagues and I have examined the impact of relationship strength on the fitness of female baboons, but we have not compared the effects of relationship strength and the extent of grooming balance. Similarly, Yee et al. (2008) documented the effects of reciprocity on female rats’ response to stress, but did not assess other elements of females’ relationships with one another. To conduct these kinds of analyses, there is a need to expand current methods for describing relationship quality and to learn more about the natural history of social bonds in a diverse range of species. Efforts to match detailed behavioral studies with analyses of stress, health markers, and mortality must be extended. And finally, these data must be linked to reproductive outcomes over the lifecourse.

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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
×
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Suggested Citation:"6 Evolutionary Perspectives on the Links Between Close Social Bonds, Health, and Fitness--Joan B. Silk." National Research Council. 2014. Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers. Washington, DC: The National Academies Press. doi: 10.17226/18822.
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Sociality, Hierarchy, Health: Comparative Biodemography is a collection of papers that examine cross-species comparisons of social environments with a focus on social behaviors along with social hierarchies and connections, to examine their effects on health, longevity, and life histories. This report covers a broad spectrum of nonhuman animals, exploring a variety of measures of position in social hierarchies and social networks, drawing links among these factors to health outcomes and trajectories, and comparing them to those in humans. Sociality, Hierarchy, Health revisits both the theoretical underpinnings of biodemography and the empirical findings that have emerged over the past two decades.

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