Early maternal loss affects diurnal cortisol slopes in immature but not mature wild chimpanzees

Abstract

In mammals, early life adversity negatively affects survival and reproductive success. A key causal mechanism is proposed by the biological embedding model which posits that adversity experienced early in life has deleterious consequences on individual physiology across the lifespan. In particular, early life adversity is expected to be a severe stressor leading to long-term alteration of the hypothalamic pituitary adrenal (HPA) axis activity. Here we tested this idea by assessing whether, as in humans, maternal loss had short and long-term impacts on orphan chimpanzee urinary cortisol levels and diurnal urinary cortisol slopes, as an indicator of the HPA axis functioning. We used 18 years of data on 50 immature and 28 mature male wild chimpanzees belonging to four communities in Tai National Park, Ivory Coast. Immature orphans who experienced early maternal loss had diurnal cortisol slopes characterised by higher early morning and late afternoon cortisol levels indicative of high activation of the HPA axis. Recently orphaned immatures had higher cortisol levels than other immatures, possibly reflecting social and nutritional stress. However, unlike in humans, we did not find significantly different cortisol profiles in orphan and non-orphan adult male chimpanzees. Our study highlights that long-term alteration of stress physiology related to early life adversity may not be viable in some wild animal populations and/or that chimpanzees, as humans, may have access to mechanisms that buffer this physiological stress, such as adoption. Our results suggest that biological embedding of altered HPA axis function is unlikely to be a mechanism contributing to the demonstrated long-term fitness consequences of maternal loss, such as reduced reproductive success, in wild long-lived mammals.

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

“…Rodent studies also suggest that maternal effects may occur via epigenetic processes, such as DNA methylation of GC receptor promotor regions, leading to altered responsivity to stressors (Champagne, 2008; Champagne and Curley, 2009; Zhang et al, 2013). Non-human primate (hereafter primate) studies of the role of maternal effects on cortisol secretion and reactivity have typically employed maternal deprivation paradigms, either via experimental separations or due to naturally occurring maternal loss (Champagne and Curley, 2009; Girard-Buttoz et al, 2020; Rosenbaum et al, 2020). Here, maternal loss is linked to elevations in cortisol levels or alterations to diurnal rhythm (Girard-Buttoz et al, 2020; Shannon et al, 1998), however, these effects do not necessarily last into adulthood (Girard-Buttoz et al, 2020; Rosenbaum et al, 2020).…”

“…Non-human primate (hereafter primate) studies of the role of maternal effects on cortisol secretion and reactivity have typically employed maternal deprivation paradigms, either via experimental separations or due to naturally occurring maternal loss (Champagne and Curley, 2009; Girard-Buttoz et al, 2020; Rosenbaum et al, 2020). Here, maternal loss is linked to elevations in cortisol levels or alterations to diurnal rhythm (Girard-Buttoz et al, 2020; Shannon et al, 1998), however, these effects do not necessarily last into adulthood (Girard-Buttoz et al, 2020; Rosenbaum et al, 2020). Similarly, in human studies, tests of maternal effects on cortisol regulation classically examine the consequences of negative maternal or early life circumstances (e.g.…”