The Influence of Social Hierarchy on Primate Health

“An important mechanism linking social status and health is the glucocorticoid stress response (Sapolsky 2004, 2005).”

“Many researchers examine correlations between dominance and fitness-related measures, like reproductive success (e.g., Ang and Manica, 2010; Muniz et al., 2010; Vervaecke et al., 2007) and susceptibility to disease (Sapolsky, 2005).”

“Dominant individuals are the most physiologically stressed in species in which dominance is maintained by frequent overt aggressive acts towards subordinates, while lower-ranking individuals tend to be more stressed in species in which dominance is maintained primarily by signaling [72].”

“The use of socially housed non-human primates provides an opportunity to assess the socially-induced consequences on a number of health-related phenotypes (Abbott et al., 2003a; McKenzie-Quirk and Miczek, 2008; Sapolsky, 2005).”

“The importance of an individual’s social associates can also be context dependent and can shift with changes in developmental, environmental or social conditions (Hinde 1976a; Sapolsky 2005).”

“hand, are defined as the anticipation of such homeostatic challenges whether warranted or not (Sapolsky 2005).”

“In primates, including humans, contests are more often ritualized and often no serious harm comes to defeated individuals (Sapolsky, 2005).”

“Given wellknown links between social status and stress (Sapolsky, 2005; Williams & Jackson, 2005), participants belonging to oppressed groups (i.e., women and ethnic/racial minorities) may experience exacerbated psychological and physiological responses during election week due to heighted stress.”

“Sapolsky (2005) has argued that low status is associated with high stress in despotic primate species, in which high-ranking individuals maintain dominance through threats and other forms of psychological intimidation (e.g., macaques, baboons, chimpanzees).”

“4% of the behavioural scans, dominance relationships may still have an effect on health and stress levels [53,54].”

“Instead, the socioeconomic status is used in psychoneuroimmunological studies as a variable (Sapolsky, 2005).”

“It has been demonstrated that social stress due to hierarchy activates the adrenal-cortical axis, increases cortisol and catecholamine production and, in the long term, can affect the cardiovascular function, fertility, immunosuppression and neurologic dysfunction [12].”

“Short-term increases in the secretion of GC are adaptive and enable an individual to overcome stressful stimuli and meet acute challenges (Abbott et al., 2003; Romero, 2002, 2004; Sapolsky, 2005; Sapolsky et al., 2000).”

“Observational and experimental studies of dominance hierarchies among nonhuman animals in captivity and in the wild have shown that subordinate animals experience higher levels of stress than other animals (Sapolsky, 2005; Shively, Laber-Laird, & Anton, 1997).”

“Stressed individuals react with a fight-or-flight response: energy is mobilized via putting out glucocorticoides to exercise muscles, and other nonessential processes for fighting or fleeing are deferred, such as digestion, growth, inflammation, and tissue repair, and immune function is inhibited (Sapolsky, 2005).”

“ORIGINAL RESEARCH ARTICLE published: 05 December 2014 doi: 10.3389/fpsyg.2014.01404 The undervalued self: social class and self-evaluation”

“…competitive regimes, combined with the frequent disappearance of individuals (through human persecution) may create unstable dominance structures, possibly leading to elevated stress levels linked to rearrangements of hierarchical relationships (see Sapolsky 2005 for an example on social primates).”

“A position at the bottom of the status hierarchy may be experienced as such, but this is considerably less likely in adolescents who are highly regarded in other respects, since people tend to value most the hierarchy in which they rank highest (Sapolsky, 2005).”

“Physical size and dominance predicts leadership hierarchies in several primate species (de Waal, 2005, 2007; Mason and Mendoza, 1993; Sapolsky, 2005) and the associations among physical stature, dominance and leadership ability in humans may reflect the use of size and strength in determining social status throughout…”

“Endocrinology, January 2011, 152(1):291–302 endo.”

“Studies on subordinate social rank support this theory, both in primate and human experiments (Mendelson et al., 2008; Sapolsky, 2005).”

“In many species, a single defeat results in lasting autonomic, reproductive, and behavioral changes (Tornatzky and Miczek, 1993; Koolhaas et al., 1997; Blanchard et al., 2001; Korte and De Boer, 2003; Sapolsky, 2005).”

“Under certain circumstances, high-ranking individuals are healthier than subordinates, while under other conditions the opposite is true (Sapolsky, 2005).”

“Along with future work, the research reviewed here may inform efforts to mitigate negative outcomes of constant social comparisons.”

“It appears to be inherited from our ancestors’ general primate tendency to use physical intimidation and threat to gain social supremacy, which we still share with many of our primate “cousins” (Sapolsky, 2005).”

“Similarly, a need to advance in the social hierarchy and to be sensitive to threats to one’s status within a group appears to be inherited from our primate ancestors (Sapolsky, 2005).”

“…de Waal, & Krakauer, 2005; Flack, Girvan, de Waal, & Krakauer, 2006), the anxiety associated with potentially losing their high-ranking position (Sapolsky, 2005) can cause them to undermine the positive relationships among their subordinates (e.g., via separating interventions; de Waal, 1982;…”

“Evidence supports this possibility in some species of primates (Sapolsky 2005).”

“In this scenario, dominance or high socioeconomic status are often associated with priority of access to resources and are considered protective for the development of a number of pathologies (Tamashiro et al., 2007; Shively et al., 2009; Sapolsky, 2005; Bartolomucci et al., 2005; Gesquiere et al., 2012).”

“Social stress is also an important part of the lives of animals in the wild (Sapolsky 2005).”

“(a) 2(high VAT:SAT, low VAT:SAT) × 16(hours) analysis of variance, main effect of VAT:SAT: F(1, 39) = 1.”

“For example, subordinates may have access to fewer resources (Sapolsky, 2005) or experience decreased opportunities for social support (Abbott et al.”

“Low dominant individuals show the reverse pattern—blunted responding during group formation and higher cortisol in the familiar group (Hellhammer et al., 1997; Saltzman, Hogan, & Abbott, 2006; Sapolsky, 2005).”

“…effects of stress, thereby socially buffering an individual to decrease their susceptibility to infection (Hennessy, Kaiser & Sachser, 2009; Kikusui, Winslow & Mori, 2006;McCowan et al., 2016; Sapolsky, 2005; Sapolsky, Romero & Munck, 2000; Segerstrom &Miller, 2004; Young et al., 2014).”

“Our results combine with those of previous studies to suggest that its omission ignores a major source of variance, one that is perhaps unsurprising in retrospect, given the centrality of social relationships to fitness outcomes in social species (2, 4).”

“as food, sexual partners, and territory, which helps them to stay healthy (Sapolsky, 2005).”

“While physical stressors are, thereby, defined as external challenges to homeostasis, psychological stressors are stated as the anticipation, justified or not, of a challenge to homeostasis (9).”

“The impacts of social status on physiological, cellular, and molecular processes have been widely documented across species from rodents to nonhuman primates (McClintock et al. 2005; Sapolsky 2005; Tung et al. 2012).”

“Subsequent studies provided supporting evidence through an association between subordinate social rank, stress, and mortality in primates (Sapolsky, 2005) as well as in humans (Mendelson et al., 2008).”

“…as maladaptive, as they can damage their own negative feedback mechanism, individuals’ long-term memory and fertility (Sapolsky et al., 2000; Sapolsky, 2005), and increase inflammatory immune profiles (Snyder-Mackler et al., 2016), it is still unclear how relevant consistently elevated GC…”

“Many studies have focused on the 33 connection between a single characteristic, such as dominance status (Sapolsky, 2005), 34 and health.”

“…with crysl violet for histological confirmation of the injection area Episodic stress-induced behavioral plasticity Evidence supports the hypothesis that environmental stressors enhance the incidence of psychiatric illnesses (for reviews see Yui et al. 1999; Sinha 2001; McEwen 2004; Sapolsky 2005).”

“Animal research suggests that the psychological and physiological advantages associated with social status can be influenced by personality characteristics of status holders, by how the status hierarchy is maintained, and by the stability of the hierarchy (Sapolsky, 2005).”

“…rank is likely to be stressful because such individuals can reliably expect to receive aggression, harassment, and/or intimidation from dominants, have little control over the occurrence of such interactions, and have fewer social outlets to cope with this harassment (Schino, 2001; Sapolsky, 2005).”

“Indeed, group-living does not make interpersonal dominance obsolete, but potentiates the long-term fitness impli-cationsof rank-based,recurrent outcomes withinthegroup, as they are remembered by individuals who know one another [43,53–55].”

“Shortterm increases in glucocorticoid secretion enable to overcome stressful stimuli andmeet acute challenges, and are therefore adaptive [19–22].”

“…literature on the relationship between circulating testosterone and aggression and social dominancewith higher circulating testosterone levels being commonly observed in the dominants of many species (Gesquiere et al., 2011; Higham et al., 2012; Mendonça-Furtado et al., 2014; Sapolsky, 2005).”

“Studies have highlighted the role of social hierarchy in individual well-being, leading to better availability of resources essential to survival, such as food, space, and mating partners (48, 49).”

“This support can result in numerous fitness benefits, such as increased food intake rates, longevity and reproductive success (Janson 1985; van Noordwijk & van Schaik 1999; Sapolsky 2005; Silk et al. 2010).”

“…species socially subordinate individuals are more at risk for stress-related diseases (with, for example, lower levels of hormones involved to wound healing, impaired testicular physiology, immune suppression, less “good” cholesterol, and increased incidences of atherosclerosis) (Sapolsky 2005).”

“, 1974; Shively and Kaplan, 1984) and have less control over their social and physical environments (Bernstein, 1976; Sapolsky, 2005), mimicking the matrilineal hierarchy in free-ranging groups (Altmann, 1962; Sade, 1967).”

“A direct consequence of low social status in female rhesus monkeys is reduced control over both social and physical environments (Sapolsky, 2005) that result in disruption of LHPA function including diminished glucocorticoid negative feedback (Jarrell et al., 2008; Shively, 1998; Wilson et al.,…”

“These two hypotheses suggest that social stress may be experienced by both high- and low-ranking individuals and varies as a function of social organisation and behavioural traits associated with high and low rank as well as with the stability of the social hierarchy (Creel, 2001; Sapolsky, 2005).”

“Although this interpretation is impossible to rule out, prior work in humans and other social primates has shown that exposure to chronic social stressors can lead to HPA axis dysfunction and stress-associated disease (42).”

“It is also possible that lower-ranking individuals may experience more rapid senescence due to greater adversity (6, 51), which might accelerate declines in sociality with age.”

“With regard to ultimate causes, the behavior of contemporary male chacma baboons has been interpreted as adapted to their historical ecology, which only allowed for small groups (Henzi and Barrett, 2003, 2005).”

“As a result, a strong association between social status and health is generally accepted (Sapolsky, 2005; von Holst, 1998).”

“As a highly pervasive principle of social organization across almost all species (Chiao, 2010), social hierarchy affects the way we see ourselves and others (Zink et al., 2008) and influences both physical health (Sapolsky, 2005) and intellectual development (Bates et al., 2013).”

“Moreover, the extent to which individuals can effectively trade-off the allocation of resources (such as energy) towards either reproductive behaviour or self-maintenance is suggested to be closely linked to individual quality or condition [66], which can vary with social status [67,68].”

“Under the condition of depression, the over secretion of GC after HPA being stimulated [14,15] can indirectly induce cell survival and reproduction by impairing the immune systems [26,27].”