Maternal effects on offspring stress physiology in wild chimpanzees

Abstract

Early life experiences are known to influence hypothalamic-pituitary-adrenal (HPA) axis development, which can impact health outcomes through the individual's ability to mount appropriate physiological reactions to stressors. In primates, these early experiences are most often mediated through the mother and can include the physiological environment experienced during gestation. Here, we investigate stress physiology of dependent offspring in wild chimpanzees for the first time and examine whether differences in maternal stress physiology are related to differences in offspring stress physiology. Specifically, we explore the relationship between maternal rank and maternal fecal glucocorticoid metabolite (FGM) concentration during pregnancy and early lactation (first 6 months post-partum) and examine whether differences based on maternal rank are associated with dependent offspring FGM concentrations. We found that low-ranking females exhibited significantly higher FGM concentrations during pregnancy than during the first 6 months of lactation. Furthermore, during pregnancy, low-ranking females experienced significantly higher FGM concentrations than high-ranking females. As for dependent offspring, we found that male offspring of low-ranking mothers experienced stronger decreases in FGM concentrations as they aged compared to males with high-ranking mothers or their dependent female counterparts. Together, these results suggest that maternal rank and FGM concentrations experienced during gestation are related to offspring stress physiology and that this relationship is particularly pronounced in males compared to females. Importantly, this study provides the first evidence for maternal effects on the development of offspring HPA function in wild chimpanzees, which likely relates to subsequent health and fitness outcomes. Am. J. Primatol. 80:e22525, 2018. © 2016 Wiley Periodicals, Inc.

Prenatal programming of stress responsiveness and behaviours: Progress and perspectives

“…The effects appear to depend on the severity and duration of prenatal stress, as well as the timing of HPA and behavioural assessment. 19 Similar results have been reported in a model of repeated stress during pregnancy in guinea pigs where juvenile male offspring exhibited lower concentration of basal cortisol both in plasma and FGM. 14 Infants whose mothers experienced high anxiety in late gestation exhibited an increased cortisol response at 5 weeks but reduced responses at 2 months and 1 year.…”

“…sGC is a substrate for placental P-gp that decreases the transfer of sGC across the placenta. 80 In another study, restraint stress (gestational days [14][15][16][17][18][19][20][21] F I G U R E 1 Effects of maternal and paternal stress or glucocorticoid exposure. 73 Interestingly, previous rodent studies have shown that chronic prenatal stress results in increased DNA methylation at multiple CpG sites within the placental Hsd11b2 gene promoter, resulting in a down-regulation of placental transcription.…”

Circadian Rhythms of Urinary Cortisol Levels Vary Between Individuals in Wild Male Chimpanzees: A Reaction Norm Approach

“…There is however evidence for some genetic predisposition of glucocorticoid excretion mechanisms (Linkowski et al, 1993;Oswald et al, 2004;Pflüger et al, 2016). Furthermore, a multitude of species has prolonged phases of intensive maternal care (e.g., Purvis and Harvey, 1995), rendering priming of glucocorticoid excretion patterns possible (e.g., Plotsky and Meaney, 1993, but see Aizer et al, 2015;Berghänel et al, 2016;Murray et al, 2016;McCormick et al, 2017). Therefore, exposure to differential levels of parental care and differences in genetic makeup could generate glucocorticoid trait repeatability among adult individuals in mammals.…”

“…Chimpanzees are an interesting species to study repeatability of urinary cortisol excretion and urinary cortisol reaction norms as infants are nursed by their mothers for around 4 years and carried and cared for even longer (Boesch and BoeschAchermann, 2000), rendering maternal priming of the HPA axis possible. Factors affecting glucocorticoid levels, such as circadian rhythms (Muller and Lipson, 2003), dominance rank (e.g., Muller and Wrangham, 2004;Anestis, 2005;Anestis et al, 2006;Muehlenbein and Watts, 2010), social dynamics (e.g., Fraser et al, 2008;Emery Thompson et al, 2010;Wittig et al, 2016), and maternal care (Murray et al, 2016) are well-studied in this species. This allows for an informed decision on potential control factors in statistical models and a sound biological interpretation of different patterns.…”

“…The circadian rhythm qualifies for the investigation of between individual variability in cortisol excretion for several reasons: (i) it represents a predictable internal gradient; (ii) due to ever changing social and environmental conditions within individual variation in cortisol levels along the gradient can be expected; (iii) lastly, the circadian rhythm in cortisol levels monitored over many years allows for detailed examination of repeatability estimates over shorter and longer periods. We predicted to find trait repeatability of cortisol phenotypes, which could either be due to differences in genetic makeup or because males are likely exposed differentially to factors that have the potential to prime HPA axis functioning, such as nutritional status of the mother during pregnancy (Edwards et al, 2002;Knackstedt et al, 2005) or postnatal maternal care (Murray et al, 2016). Furthermore, given the consistent results on reaction norm repeatability of corticosterone in birds (Hau et al, 2016), we expected to find that male chimpanzees are stable and consistently different from each other in their urinary cortisol reaction norms.…”