Social bonds do not mediate the relationship between early adversity and adult glucocorticoids in wild baboons

Abstract

In humans and other animals, harsh conditions in early life can have profound effects on adult physiology, including the stress response. This relationship may be mediated by a lack of supportive relationships in adulthood. That is, early life adversity may inhibit the formation of supportive social ties, and weak social support is itself often linked to dysregulated stress responses. Here, we use prospective, longitudinal data from wild baboons in Kenya to test the links between early adversity, adult social bonds, and adult fecal glucocorticoid hormone concentrations (a measure of hypothalamic–pituitary–adrenal [HPA] axis activation and the stress response). Using a causal inference framework, we found that experiencing one or more sources of early adversity led to a 9 to 14% increase in females’ glucocorticoid concentrations across adulthood. However, these effects were not mediated by weak social bonds: The direct effects of early adversity on adult glucocorticoid concentrations were 11 times stronger than the effects mediated by social bonds. This pattern occurred, in part, because the effect of social bonds on glucocorticoids was weak compared to the powerful effects of early adversity on glucocorticoid levels in adulthood. Hence, in female baboons, weak social bonds in adulthood are not enough to explain the effects of early adversity on glucocorticoid concentrations. Together, our results support the well-established notions that early adversity and weak social bonds both predict poor adult health. However, the magnitudes of these two effects differ considerably, and they may act independently of one another.

Glucocorticoid exposure predicts survival in female baboons

“…Other social gradients, including social integration and early-life adversity, are robustly linked to survival in both humans and nonhuman animals ( 50 ), including this baboon population ( 37 , 38 ). Recent work with the Amboseli baboons has shown that weak social bonds in adulthood do play a mediating role in pathways that may connect conditions experienced in early life with adult GC levels ( 51 ). A priority for future work should be to examine causal relationships between GCs and social gradients to understand the pathways through which they are linked to survival.…”

“…Because there is interannual variation in the intensity and duration of the wet and dry seasons, we also calculated a 3-month rainfall anomaly as the difference between the total rainfall in the 3 months preceding sample collection and the long-term average for the same calendar dates based on the entire 43-year rainfall record. We followed the procedure used in ( 51 ) to account for within-season rainfall variability on fGC concentrations. We calculated the mean of daily maximum temperature in the 30 days before and including the day of sample collection because previous research has shown that, within seasons, fGC concentrations are elevated during months with relatively high daily maximum temperatures ( 29 ).…”

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

“…While the effect of maternal loss on wild animal survival and reproduction has been recently established ( Foster et al, 2012 ; Andres et al, 2013 ; Tung et al, 2016 ; Walker et al, 2018 ; Surbeck et al, 2019 ; Crockford et al, 2020 ; Zipple et al, 2021 ), the mechanisms underlying these fitness costs remain understudied. Our study provides one of the rare empirical tests of the BEM (see also Rosenbaum et al, 2020 ) and ACM in wild long-lived mammals by assessing the short- and long-term physiological impacts of early maternal loss. While we found an effect of maternal loss on diurnal cortisol slopes in immature chimpanzees whose mothers died recently ( all immature and immature orphan models ), these effects were neither present in individuals who lost their mothers more than 2 years earlier ( all immature and immature orphan models ) nor in mature male chimpanzees ( adult male orphan model ).…”

“…A study on wild female baboons, using extensive long-term data, showed that simultaneous exposure to several forms of early-life adversity, and some isolated forms of adversity such as drought and low maternal rank, leads to an overall elevation in glucocorticoid levels in adulthood ( Rosenbaum et al, 2020 ), offering support for the BEM. However, maternal loss in isolation did not lead to long-term elevation of glucocorticoid levels, suggesting that baboons may have buffering mechanisms to offset the effects of biological embedding for some forms of early-life adversity.…”

How long‐term studies reveal otherwise hidden phenomena: The Long‐Term Animal Research Seminar Series

“…Furthermore, Shah demonstrated that this pattern is driven by reproductive tradeoffs between different tactics that might not have been evident from a cross‐sectional study. Finally, Elizabeth Archie and Elizabeth Lange described work in yellow baboons ( Papio cynocephalus ) that used long‐term data to link negative early life conditions to endocrine dysfunction, reduced adult social bonds, and decreased lifespan 9–11 . Their work illustrates the long‐lasting effects of early life environments and how early life and adult phenotypes drive health differences among individuals.…”