Multiple stressors affect developing and adult organisms, thereby partly structuring their phenotypes. Determining how stressors influence health, well-being, and longevity in human and nonhuman primate populations are major foci within biological anthropology. Although much effort has been devoted to examining responses to multiple environmental and sociocultural stressors, no holistic metric to measure stress-related physiological dysfunction has been widely applied within biological anthropology. Researchers from disciplines outside anthropology are using allostatic load indices (ALIs) to estimate such dysregulation and examine life-long outcomes of stressor exposures, including morbidity and mortality. Following allostasis theory, allostatic load represents accumulated physiological and somatic damage secondary to stressors and senescent processes experienced over the lifespan. ALIs estimate this wear-and-tear using a composite of biomarkers representing neuroendocrine, cardiovascular, metabolic, and immune systems. Across samples, ALIs are associated significantly with multiple individual characteristics (e.g., age, sex, education, DNA variation) of interest within biological anthropology. They also predict future outcomes, including aspects of life history variation (e.g., survival, lifespan), mental and physical health, morbidity and mortality, and likely health disparities between groups, by stressor exposures, ethnicity, occupations, and degree of departure from local indigenous life ways and integration into external and commodified ones. ALIs also may be applied to similar stress-related research areas among nonhuman primates. Given the reports from multiple research endeavors, here we propose ALIs may be useful for assessing stressors, stress responses, and stress-related dysfunction, current and long-term cognitive function, health and well-being, and risk of early mortality across many research programs within biological anthropology. K E Y W O R D Saging, allostasis, frailty, growth and development, nonhuman primates, senescence, stress | I N T R O D U C T I O NTraditional research foci within biological anthropology include variations in stress, morbidity, and mortality (for reviews, see Ice & James, 2007;Little, 2010). Despite this long-term focus, the field continues to pursue a reliable, relatively easy to apply metric for assessing lifetime stress and stress-related outcomes. We suggest incorporating the theory of allostasis and methods for assessing allostatic load within anthropological theory and methodology to aid in closing this gap. As a theory, allostasis was developed to explain how mammalian physiological responses to stressors in their environments evolved to maximize the probability of survival while limiting somatic damage (Korte, Koolhaas, Wingfield, & McEwen, 2005;McEwen & Stellar, 1993;McEwen & Wingfield, 2003;Sterling, 2004Sterling, , 2012Sterling & Eyer, 1988). Unfortunately, such beneficial defensive responses come at a cost and, over time, repeated allostatic activi...
Animal welfare, conservation, and stress assessment are all critical components of species survival. As organisms experience stressors, they accumulate physiologic dysregulation, leading to multiple negative health outcomes. This brief review suggests measuring the degree of stress-induced damage, known as allostatic load, and then using allostatic load to evaluate changes implemented to improve animal welfare and conservation efforts. Over the past two decades, human clinical research has developed multiple allostatic load indices constructed from composites of neuroendocrine, cardiovascular, metabolic, and immune biomarkers. These indices are designed to estimate allostatic load in hopes of ameliorating or even negating damaging effects of stress. Among humans, allostatic load is associated with a variety of factors such as age, sex, stressful experiences, personality, social position, and early life history. Despite conservation of stress responses throughout mammalian species, reported allostatic load indices for animals are rare. Because many zoo researchers and field scientists already collect data on multiple biomarkers, constructing allostatic load indices may be a relatively affordable, easily implemented, and powerful tool for assessing relative risks of morbidity and mortality within wildlife. As an example, in a study among zoo-housed gorillas, an allostatic load index constructed using seven biomarkers was associated significantly with age, sex, stressful experiences, rearing history, markers of poor health, and mortality risk. Such results evidence that allostatic load is as applicable to animal populations as it is to humans. By using allostatic load as a predictive tool, human caretakers will be better informed of individuals at greatest risk for health declines. Most importantly, allostatic load may provide earlier opportunity for preemptive care while contributing a transformational tool to animal welfare research. Additionally, allostatic load may be compared between individuals and groups within the same population and allow comparisons of health between and across populations, consequently informing habitat and population protection efforts.
Disrupted rearing history is a psychological and physical stressor for nonhuman primates, potentially resulting in multiple behavioral and physiological changes. As a chronic, soma-wide stressor, altered rearing may be best assessed using a holistic tool such as allostatic load (AL). In humans, AL estimates outcomes of lifetime stress-induced damage. We predicted mother-reared gorillas would have lower AL than nursery-reared and wild-caught conspecifics. We estimated AL for 27 gorillas housed at the Columbus Zoo and Aquarium between 1956 and 2014. AL estimates were calculated using biomarkers obtained during previous anesthetic events. Biomarkers in the high-risk quartile were counted toward a gorilla's AL. Rearing history was categorized as mother-reared, nursery-reared, and wild-caught. Using ANCOVA, rearing history and AL are significantly associated when age and sex are entered as covariates. Wild-caught gorillas have significantly higher AL than mother-reared gorillas. Neither wild-caught nor mother-reared gorillas are significantly different from nursery-reared gorillas. When examined by sex, males of all rearing histories have significantly lower AL than females. We suggest males face few stressors in human care and ill effects of rearing history do not follow. Wild-caught females have significantly higher AL than mother-reared females, but neither is significantly different from nursery-reared females. Combined with our previous work on AL in this group, wherein females had twofold higher AL than males, we suggest females in human care face more stressors than males. Disrupted rearing history may exacerbate effects of these stressors. Providing opportunities for females to choose their distance from males may help reduce their AL.
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