Abstract

The maternal environment exerts important influences on offspring mass/growth, metabolism, reproduction, neurobiology, immune function, and behavior among birds, insects, reptiles, fish, and mammals. For mammals, mother's milk is an important physiological pathway for nutrient transfer and glucocorticoid signaling that potentially influences offspring growth and behavioral phenotype. Glucocorticoids in mother's milk have been associated with offspring behavioral phenotype in several mammals, but studies have been handicapped by not simultaneously evaluating milk energy density and yield. This is problematic as milk glucocorticoids and nutrients likely have simultaneous effects on offspring phenotype. We investigated mother's milk and infant temperament and growth in a cohort of rhesus macaque (Macaca mulatta) mother-infant dyads at the California National Primate Research Center (N = 108). Glucocorticoids in mother's milk, independent of available milk energy, predicted a more Nervous, less Confident temperament in both sons and daughters. We additionally found sex differences in the windows of sensitivity and the magnitude of sensitivity to maternal-origin glucocorticoids. Lower parity mothers produced milk with higher cortisol concentrations. Lastly, higher cortisol concentrations in milk were associated with greater infant weight gain across time. Taken together, these results suggest that mothers with fewer somatic resources, even in captivity, may be "programming" through cortisol signaling, behaviorally cautious offspring that prioritize growth. Glucocorticoids ingested through milk may importantly contribute to the assimilation of available milk energy, development of temperament, and orchestrate, in part, the allocation of maternal milk energy between growth and behavioral phenotype.

Highlights

  • Since the early 20th century, scientists have revealed a multitude of maternal effects on offspring phenotype

  • Milk yield was negatively associated with cortisol in milk, as higher milk yield diluted the concentration of cortisol

  • Because cortisol in milk was associated with the caloric content in milk and the volume of milk, we used the aggregate measure of available milk energy (AME) (Hinde 2009; Hinde and Capitanio 2010) as a covariate during AICc model selection to evaluate the independent contributions of cortisol to infant outcomes

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Summary

Introduction

Since the early 20th century, scientists have revealed a multitude of maternal effects on offspring phenotype. Birds, insects, reptiles, fish, and mammals, the maternal ecology that offspring experience reflects maternal characteristics, life-history trade-offs, and ecological conditions This maternally mediated ecology of development has been demonstrated to influence offspring mass/growth, metabolism, reproduction, neurobiology, immune function, and behavior (Smith 1919; Moore et al 1927; Mousseau and Fox 1998; Räsänen and Kruuk 2007; Champagne 2008; Groothuis and Schwabl 2008; Skibiel et al 2009; Ezard et al 2014; Mateo 2014). Prenatal exposure to elevated maternal glucocorticoids, the end product of the hypothalamicpituitary-adrenal axis (corticosterone in rodents, cortisol in primates), causes low birth weight and compromised neurodevelopment and immune function (Coe and Lubach 2000; Seckl 2004; Murphy et al 2006; Singh et al 2012)

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