Offspring Hormones Reflect the Maternal Prenatal Social Environment: Potential for Foetal Programming?

Abstract

Females of many species adaptively program their offspring to predictable environmental conditions, a process that is often mediated by hormones. Laboratory studies have shown, for instance, that social density affects levels of maternal cortisol and testosterone, leading to fitness-relevant changes in offspring physiology and behaviour. However, the effects of social density remain poorly understood in natural populations due to the difficulty of disentangling confounding influences such as climatic variation and food availability. Colonially breeding marine mammals offer a unique opportunity to study maternal effects in response to variable colony densities under similar ecological conditions. We therefore quantified maternal and offspring hormone levels in 84 Antarctic fur seals (Arctocephalus gazella) from two closely neighbouring colonies of contrasting density. Hair samples were used as they integrate hormone levels over several weeks or months and therefore represent in utero conditions during foetal development. We found significantly higher levels of cortisol and testosterone (both P < 0.001) in mothers from the high density colony, reflecting a more stressful and competitive environment. In addition, offspring testosterone showed a significant positive correlation with maternal cortisol (P < 0.05). Although further work is needed to elucidate the potential consequences for offspring fitness, these findings raise the intriguing possibility that adaptive foetal programming might occur in fur seals in response to the maternal social environment. They also lend support to the idea that hormonally mediated maternal effects may depend more strongly on the maternal regulation of androgen rather than cortisol levels.

Chemical patterns of colony membership and mother-offspring similarity in Antarctic fur seals are reproducible over time

“…For example, stressful conditions such as high densities of conspecifics can suppress microbial diversity (Bailey et al, 2011; Stothart et al, 2016; Noguera et al, 2018; Partrick et al, 2018; Zha et al, 2018). This is consistent with our data, as breeding females on SSB are present at higher density and have chronically elevated levels of the stress hormone cortisol (Meise et al, 2016), while skin microbial diversity is also lower in this colony (Grosser et al 2019). Investigating the potential linkages between social stress, cortisol, microbial community structure and chemical phenotypes therefore represents a promising avenue for future research.…”

Chronic stress in the mother-infant dyad: Maternal hair cortisol, infant salivary cortisol and interactional synchrony

“…Maternal HCC and child HCC have been concurrently related in older children (Ouellette et al, 2015). In Antarctic seals, fur cortisol concentrations were correlated in mothers and their newborn pups, and were higher in mothers breeding in high density colonies, suggesting possible fetal programming (Meise et al, 2016). In light of the long-term health implications of infant HPA dysregulation, it is critical to examine the role of maternal chronic physiological stress in infants' cortisol exposure.…”

Fur seal microbiota are shaped by the social and physical environment, show mother–offspring similarities and are associated with host genetic quality

“…Antarctic fur seals breed in colonies that vary in social density by an order of magnitude and rookeries of contrasting density can be found in close geographical proximity, providing a “natural experiment” that controls (as far as possible in a natural setting) for potentially confounding environmental effects (Meise, von Engelhardt, Forcada, & Hoffman, ). On Bird Island, breeding females from two colonies situated just 200 m apart (Figure )—special study beach (SSB) and freshwater beach (FWB)—are genetically undifferentiated and exposed to the same prevailing climatic conditions (Stoffel et al, ).…”