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.

Keywords: Cortisol; Early social environment; HPA programming; Parental care.

Figure 1

Urinary cortisol levels during social separation challenges at 6, 12, and 18 months of age for offspring receiving high (●) and low (○) rates of carrying (a-c), licking and grooming (LG; d-f), and infant rejections (IR; g-i) from the entire family group. Offspring from high-IR families had higher urinary cortisol levels across the duration of social separation compared to offspring from low-IR families. ¹Significant main effect of group; ²Significant group by time interaction. *p<.05; + p<.10.

Figure 2

Urinary cortisol levels during social separation challenges at 6, 12, and 18 months of age for offspring receiving high (●) and low (○) rates of infant rejections (IR) from their mothers. Offspring from high-IR mothers had higher urinary cortisol levels across the duration o social separation compared to offspring from low-IR mothers. ¹Significant main effect of group; ²Significant group by time interaction. *p<.05; + p<.10.

Figure 3

Urinary cortisol levels during social separation challenges at 6, 12, and 18 months of age for offspring receiving high (●) and low (○) rates of infant rejections (IR) from fathers. Offspring from high-IR fathers had higher urinary cortisol levels across the duration of social separation compared to offspring from low-IR families at 12 and 18 months, but not 6 months. ¹Significant main effect of group; ²Significant group by time interaction. *p<.05; + p<.10.

Figure 4

Urinary cortisol levels during social separation challenges at 6, 12, and 18 months of age for offspring receiving high (●) and low (○) rates of infant rejections (IR) from siblings. Offspring from high-IR siblings had higher urinary cortisol levels across the duration of social separation compared to offspring from low-IR families at 18 months, but not at 6 or 12 months; ¹Significant main effect of group; ²Significant group by time interaction. *p<.05; + p<.10.