Quality of maternal and paternal care predicts later stress reactivity in the cooperatively-breeding marmoset (Callithrix geoffroyi)

Abstract

Variation in the early postnatal social environment can have lasting effects on hypothalamic-pituitary-adrenal (HPA) axis stress responses. Both rats and macaque monkeys subjected to low quality or abusive maternal care during the early postnatal period have more pronounced HPA responses to environmental stressors throughout development and into adulthood compared to animals reared in higher quality early maternal environments. However, little is known about the relative contributions to HPA stress response styles in developing offspring in species in which offspring care is routinely provided by group members other than the mother, such as in cooperatively breeding mammals. Marmoset monkeys exhibit cooperative offspring rearing, with fathers and older siblings providing care in addition to that provided by the mother. We evaluated the effects of early maternal, paternal, and older sibling care on HPA responses to social separation across development in captive white-faced marmoset offspring (Callithrix geoffroyi). We monitored offspring care by mothers, fathers, and older siblings in marmosets for the first 60 days of life. Later in development, each marmoset experienced three standardized social separation/novelty exposure stressors at 6, 12, and 18 months of age. During separation, we collected urine samples and analyzed them via enzyme immunoassay for cortisol levels. Infants that received higher rates of rejections from the entire family group showed higher cortisol responses to social separation. This relationship was found when mothers, fathers, and older siblings, were analyzed separately as well. No differences in cortisol responses were found between offspring that received high and low rates of carrying or high and low rates of licking and grooming by any group member. In the cooperatively breeding marmoset, early social cues from multiple classes of caregivers may influence HPA stress responses throughout the lifespan.

Early-Life Experience, Epigenetics, and the Developing Brain

“…Non-human primates have also been observed to vary in their frequency of mother-infant contact (ie, an over-protective parenting style), and high levels of contact predicts decreased exploration of a novel environment (Fairbanks and McGuire, 1988). In marmosets, rearing occurs in a family context and higher rates of rejection of offspring by mothers, fathers, or siblings during the first 2 months of life results in elevated stress-induced cortisol responses (Birnie et al, 2013). Thus, the social context of rearing may induce a lasting impact on stress reactivity.…”

Early-life social adversity and developmental processes in nonhuman primates

“…Decreased baseline levels of cortisol (CORT) and/or adrenocorticotrophic hormone (ACTH) after exposure to ELSA have been observed in macaques [32,33], marmosets [3,8], and squirrel monkeys [2]. However, other studies have failed to find these differences [12,17,34,35]. Decreased baseline CORT levels may indicate a lower set point of the HPA stress axis in animals exposed to ELSA.…”

“…Lower quality parental care has been associated with increased CORT levels after a stressor in marmosets [34] and female macaques [35], suggesting increased reactivity to a stressor. In contrast, higher quality parental behavior such as grooming and carrying by caregivers does not predict CORT responses in marmosets [34]. These findings imply that exposure to poor parental care alters HPA axis dynamics, while variation in more positive parent-infant interactions have little or no effect on this system.…”

Paternal care in a fish: epigenetics and fitness enhancing effects on offspring anxiety

“…In addition to the obvious influence of parental provisioning on offspring size and morphological traits, parental care can also exert substantial influence on offspring behavioural traits [1][2][3][4]. For example in rodents and non-human primates, offspring receiving low levels of parental care, or deprived of it altogether, develop more reactive stress response systems, thereby reducing their ability to cope with stressors and leading to increased anxiety [2,3,5,6]. This suggests that receiving adequate parental care is an important part of offspring development and its removal has long-lasting consequences for how offspring react to stressors.…”