Glucocorticoid exposure predicts survival in female baboons

Abstract

Are differences in hypothalamic-pituitary-adrenal (HPA) axis activation across the adult life span linked to differences in survival? This question has been the subject of considerable debate. We analyze the link between survival and fecal glucocorticoid (GC) measures in a wild primate population, leveraging an unusually extensive longitudinal dataset of 14,173 GC measurements from 242 adult female baboons over 1634 female years. We document a powerful link between GCs and survival: Females with relatively high current GCs or high lifelong cumulative GCs face an elevated risk of death. A hypothetical female who maintained GCs in the top 90% for her age across adulthood would be expected to lose 5.4 years of life relative to a female who maintained GCs in the bottom 10% for her age. Hence, differences among individuals in HPA axis activity provide valuable prognostic information about disparities in life span.

Early maternal loss leads to short- but not long-term effects on diurnal cortisol slopes in wild chimpanzees

“…Interestingly, our study provides contrasts to studies on humans by showing that the modifications of the HPA axis activity following maternal loss are not long-lasting. Even though modifications of the HPA axis activation may have some fitness consequences in wild mammalian populations ( Campos et al, 2021 ), this mechanism is unlikely to explain the lower reproductive fitness and survival observed in adult male orphan chimpanzees ( Nakamura et al, 2014 ; Crockford et al, 2020 ). In fact, in our study male orphans who reach adulthood do not present cortisol excretion profiles that differ from those of non-orphans.…”

“…The HPA axis is considered to be at the core of the link between early-life adversity and fitness since repeated activation of the HPA axis over prolonged periods (chronic stress) and/or HPA axis malfunctioning can have detrimental effects on individual overall health ( Sapolsky, 2002 ; Slavich and Cole, 2013 ). For instance, over- and/or prolonged activation of the HPA axis is known to suppress the immune system ( Grossman, 1985 ; Setchell et al, 2010 ; Slavich and Cole, 2013 ) and reduce survival ( Campos et al, 2021 ). The HPA axis also mediates some of the observed negative effects of early-life adversity on the immune response, such as elevated levels of inflammatory markers in the blood ( Danese et al, 2011 ; Ehrlich et al, 2016 ; Rasmussen et al, 2019 , reviewed in Berens et al, 2017 ).…”

Non-genetic maternal effects shape individual differences in cortisol phenotypes in wild chimpanzees

“…Indeed, in wild baboons, early life adversity can have intergenerational effects on survival, i.e., if a mother experiences adversity, both she and her offspring can experience reduced survival outcomes (Zipple et al, 2019), which may be explained by the GC effects of adversity. Recent meta-analyses and evidence from long-term field studies now suggest that, at least for long-lived species, elevated HPA axis activity over the lifespan is a predictor of survival (Bonier et al, 2009; Campos et al, 2021; Schoenle et al, 2021). However, in wild chimpanzees, although maternal loss impacts later life reproductive success (Crockford et al, 2020), there is no evidence that this is the result of long-term HPA axis activity alteration as effects on circadian cortisol patterns following maternal loss do not endure into adulthood (Girard-Buttoz et al, 2021).…”

“…Despite the flexibility of HPA axis activity in response to external and internal stimuli, numerous studies demonstrate consistent individual differences in HPA axis activity and reactivity to environmental stimuli (Schoenemann and Bonier, 2018; Taff et al, 2018). Recent evidence suggests that inter-individual variation in HPA axis regulation can be predictive of variation in fitness outcomes (Bonier and Cox, 2020; Campos et al, 2021). For example, female baboons with consistently elevated HPA axis activity live substantially shorter lives than those with lower HPA axis activity (Campos et al, 2021).…”

“…Recent evidence suggests that inter-individual variation in HPA axis regulation can be predictive of variation in fitness outcomes (Bonier and Cox, 2020; Campos et al, 2021). For example, female baboons with consistently elevated HPA axis activity live substantially shorter lives than those with lower HPA axis activity (Campos et al, 2021). Given the profound fitness effects of individual differences in HPA axis activity and regulation, understanding the relative role of genetics, experience, and environment in shaping these GC phenotypes is key to understanding the evolution of physiological plasticity (Bonier and Martin, 2016; Guindre-Parker, 2018).…”