Op-emph140021 122..133

Background and objectives: Low social status increases risk of disease due, in part, to the psychosocial stress that accompanies feeling subordinate or poor. Previous studies report that chronic stress and chronically elevated cortisol can impair cardiovascular and immune function. We test whether lower status is more benign in small-scale, relatively egalitarian societies, where leaders lack coercive authority and there is minimal material wealth to contest. Methodology: Among Tsimane’ forager-horticulturalists of lowland Bolivia, we compare informal political influence among men with urinary cortisol, immune activation (innate and acquired), and morbidity as assessed during routine medical exams. Results: After controlling for potential confounds, we find that politically influential men have lower cortisol, and that this association is partly attributable to access to social support. Cortisol is positively associated with men’s income, which may reflect chronic psychosocial stress from market involvement. Greater influence is also associated with lower probability of respiratory infection, which is a frequent source of morbidity among Tsimane’. Among men who lost influence over a 4-year period, cortisol and probability of respiratory infection were higher the greater the decline in influence. Conclusions and implications: Deleterious effects of low status on health are not merely ‘diseases of civilization’ but may result from how (even subtle) status differences structure human behavior. K E Y W O R D S : hierarchy; status; cooperation; stress; cortisol original research article 122 The Author(s) 2014. Published by Oxford University Press on behalf of the Foundation for Evolution, Medicine, and Public Health. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. by gest on O cber 2, 2014 ht://em ph.oxfournals.org/ D ow nladed from BACKGROUND AND OBJECTIVES Within diverse human societies, health improves with every step up the socioeconomic ladder [1–3]. The sources of this gradient in health are multiple, and inter-individual differences in healthcare and lifestyle behaviors (e.g. physical activity level and diet) do not fully explain it. Non-human primates demonstrate a similar relationship between status and health that is influenced but not fully explained by activity level or diet [4–8]. Many of the effects that status has on health have been attributed to chronic psychosocial stress that accompanies social subordination and reduced access to resources [2–12]. Among humans, it remains an open question whether links between status, psychosocial stress and health are unique features of institutionalized or dominance-based hierarchies, given the paucity of studies in relatively egalitarian, small-scale societies. The effects of status variation in smallscale societies have significant evolutionary implications since large-scale societies with heritable, material wealth represent only the past 10 millennia of human history. Egalitarian, small-scale societies are characterized by extensive resource pooling across households and minimal disparity in wealth [13, 14]. Adults may differ in their informal political influence, which is based less on dominance than on prestige due to generosity or skill [15, 16]. Modest status differences can affect access to mates and social support [16–18]. Similarly, modest differences in socioeconomic status (SES) relative to neighbors or social contacts influence well-being in large-scale societies [19–21]. The most salient status comparisons are not typically with individuals at the opposite end of the SES spectrum, but with individuals with whom we are in frequent face-to-face contact and in direct competition for resources or respect [22–24]. Here we examine links between informal political influence and biomarkers of stress and disease among semi-sedentary Tsimane’ foragerhorticulturalists of Amazonian Bolivia. We measured the influence of 199 men (aged 18–83 years) from four villages using a ranking strategy. Villages are often subdivided into clusters of extended families which may congregate to work or socialize (e.g. resolve disputes and discuss community affairs). While no man wields coercive authority over another, the opinions and desires of more influential men carry more weight during village gatherings. Because influential men have more social support from kin and non-kin [16], they can steer the consensus-based decision-making of community meetings in their favor. These men may also receive deference in other contexts, including mate competition and conflict resolution. Disputes over access to arable land and accusations of extramarital sex, theft or free-riding on community projects are common conflicts among men [25]. First, we test whether Tsimane’ men with less informal political influence have higher urinary cortisol (prediction 1). Basal cortisol levels and the cortisol response to waking are positively associated with psychosocial stress among Westerners [9, 26–28], non-Westerners [29] and non-human primates [4–7]. Cortisol is an important metabolic hormone with many physiological functions in the body; acute and long-term stressors can induce cortisol responses by the adrenal cortex, which prepares the body for action by increasing blood glucose. Chronic psychosocial stress can not only produce relatively high levels of cortisol but in severe cases is associated with ‘burnout’ of the hypothalamic– pituitary–adrenal axis and low levels of cortisol, or reduced circadian variation in cortisol [28]. We also consider alternative explanations to psychosocial stress for an influence–cortisol relationship, including age, body size and lifestyle differences associated with income from sporadic wage labor or horticultural sales. High status individuals may be less prone to psychosocial stress due to a greater sense of control [30, 31] and to greater recourse to social support to buffer stressful events [26, 32, 33]. For example, a study of government and military leaders finds they have lower cortisol than non-leaders, and this effect is mediated by sense of control [9]. Among nonhuman primates, subordinates who have less social support and who are subject to frequent harassment exhibit higher levels of cortisol than dominants [4–7]. However, dominants may experience more psychosocial stress and produce higher cortisol levels than subordinates when the hierarchy is unstable, or when dominants have neurotic, anti-social personalities [5, 6]. Under these conditions, highranking individuals may adopt greater vigilance to monitor threats to their status and have less recourse to social support. Second, we test whether the effect of influence on cortisol is mediated by social support and by conflict with other men (predictions 2a,b), as both reduced support and greater conflict can increase psychosocial stress. We also test whether the influence– cortisol relationship is moderated by men’s Hierarchy and health among forager-farmer men von Rueden et al. | 123 by gest on O cber 2, 2014 ht://em ph.oxfournals.org/ D ow nladed from personality as assessed by scores on the Big Five Inventory (BFI) (prediction 3) or moderated by hierarchy stability (prediction 4). We measure hierarchy stability using longitudinal influence data within one village and comparisons of conflict frequency across four villages. Tsimane’ conflicts are often mediated by third parties, and therefore higher conflict frequency can reduce men’s sense of control or predictability. Even if men do not directly experience conflict, more intra-village conflict may place men at greater risk of gaining or losing influence if conflict resolution does not always favor the status quo. In non-human primates, hierarchy instability is concomitant with increases in dominance interactions [5]. Status-related stress can increase risk of communicable and non-communicable disease, in part through the effects of cortisol and the sympathetic nervous system on energy mobilization, inflammation and acquired immunity [34]. In Western societies, chronic stress has previously been associated with hypertension [35] and biomarkers of inflammation that indicate risk of cardiovascular disease (CVD), including an elevated erythrocyte sedimentation rate and higher levels of C-reactive protein (CRP) [36, 37]. Risk of infectious disease is also increased with chronic stress, due to neuroendocrine suppression of lymphocyte and antibody production [38, 39]. We therefore test whether more influential Tsimane’ men are healthier (prediction 5), based on their blood pressure, sedimentation rate, CRP, lymphocyte counts and clinical diagnoses of cardiovascular abnormalities (e.g. cardiac-type chest pain and arrhythmia), intestinal parasites, respiratory infections and skin infections. Tsimane’ experience frequent infection-related inflammation but minimal hypertension and CVD [40]. Acute infections may contribute most to status-related health outcomes, unlike Western populations where chronic diseases are a principal source of status-related morbidity. Nevertheless, we may still find variation in blood pressure or CVD that is associated with men’s influence.