Transgenerational Effects of Variable Foraging Demand Stress in Female Bonnet Macaques

Abstract

Stress coping is an important part of mammalian life, influencing somatic and mental health, social integration, and reproductive success. The experience of early psychological stress helps shape lifelong stress coping strategies. Recent studies have shown that the effects of early stress may not be restricted to the affected generation, but may also be transmitted to offspring. Understanding whether early stress influences development in subsequent generations may help us understand somewhat why many stress-related traits and diseases, for which little genetic basis has been discovered, run in families. Experimental early life “variable foraging demand” (VFD) stress has been associated with behavioral hypo-responsiveness to stress in infant and adolescent bonnet macaques. The present study examined the behavioral effects of experimental early VFD stress in adult bonnet macaques, and further investigated whether non-exposed adolescent offspring of VFD macaques were also affected. Thirty female bonnet macaques from four rearing histories were observed for behavioral response during stress: adults which had been VFD reared as infants (n = 11), adults which had been Control reared as infants (n = 9), and foraging demand naïve adolescents whose mothers were VFD (n = 4) or Control reared (n = 6). Subjects were observed for behavioral response during two experimental stressor conditions, including: (1) relocation to a novel environment; and (2) relocation with exposure to a “human intruder” making eye contact. Factor analysis yielded five factors that described categories of behavior across stress conditions. While adult VFD and Control reared females unexpectedly did not differ significantly, non-exposed adolescent offspring of VFD reared mothers displayed significant hypo-responsiveness in all behavioral categories compared with non-exposed adolescent offspring of Control females. We suggest that stress hypo-responsiveness previously observed in adolescent VFD reared animals may abate with age, but is nonetheless observed in the next generation. We conclude that VFD stress affects behavioral development of subsequent generations in non-human primates.

The lasting impact of early‐life adversity on individuals and their descendants: potential mechanisms and hope for intervention

“…All in all, this study provides an amazing illustration of intergenerational transmission of learned behavior and neuroanatomical structure. Multigenerational transmission of stress phenotypes has also been reported for the behavior and cortisol levels of non‐human primates exposed to higher stress environments (Fairbanks et al ; Kinnally et al ) and for the behavior and metabolic responses of rodents exposed to maternal separation and unpredictable maternal stress (in a complex, sex‐specific manner; Franklin et al ; Gapp et al ). It will be interesting to determine whether the early emergence of long‐term, and relapse prone, fear memory in infants exposed to early‐life stress (as described earlier) is also transmitted across generations.…”

Paternal line effects of early experiences persist across three generations in rhesus macaques

“…Standardized procedures were designed to ensure that each subject had comparable experiences to all other subjects who underwent assessment. These F I G U R E 1 Schematic of sample size in each paternal line NR and CONTROL ancestral line procedures have been described in detail elsewhere (Golub et al, 2009;Kinnally et al, 2013), and not all measures collected were considered in present study; rather we chose to test specific hypotheses based on our previous work (Kinnally & Capitanio, 2015). with 2.5IU Adrenocorticotopic hormone and blood was sampled 30 min later (ACTH sample).…”

“…It has long been known that the effects of early stress are not limited to the exposed generation, but may impact subsequent generations as well (Dodge, Bates, & Pettit, 1990;Francis, Diorio, Liu, & Meaney, 1999;Spinetta & Rigler, 1972). Transgenerational influences may occur through the maternal and/or paternal line in mammals (Fairbanks, 1989;Maestripieri, 2005;McCormack, Sanchez, Bardi, & Maestripieri, 2006;Kinnally & Capitanio, 2015;Kinnally et al, 2013), although potentially through distinct mechanisms. For example, there is ample comparative evidence to suggest that maternal early stress affects anxiety-related traits in the next generation in rodents (poor maternal care: Francis et al, 1999), non-human primates (poor maternal care: Fairbanks, 1989; variable foraging demand stress: Kinnally et al, 2013) and humans (trauma: Yehuda & Bierer, 2008;Yehuda et al, 2014).…”

Epigenetic Risk Factors for Diseases: A Transgenerational Perspective

“…Serotonergic signaling and Rcan1 expression are functionally linked (Hoeffer et al 2013 ), suggesting that the similarities between social alterations in both studies may share overlapping molecular signaling mechanisms. Other studies using various chronic stress models in rats and monkeys have noted effects of social-and stress-related responses in the offspring (Kinnally et al 2013 ;Babb et al 2014 ). However, as the matriline was studied without controlling for maternal care, the results may be confounded by maternal effects and are therefore not informative with regard to germline non-genetic inheritance (see Appendix 1 ).…”