Among mammals, primipara who initiate reproduction before full maturity can be constrained in their maternal investment, both due to fewer somatic resources and tradeoffs between their own continued development and reproductive effort. Primipara are particularly limited in their capacity to synthesize milk during lactation, the costliest aspect of reproduction for most mammals, especially primates due to long periods of postnatal development. Due to reduced milk transfer, Firstborns may be at elevated risk for long-term consequences of deficits in early life endowment from their primiparous mothers. Here we investigated mass, growth, stature, and lactation performance among N = 273 adult daughters across N = 335 reproductions, who were their own mother’s Firstborn or Laterborn progeny, among rhesus macaques (Macaca mulatta) at the California National Primate Research Center. We further explored mass during infancy of the offspring of Firstborn and Laterborn mothers. Firstborns had accelerated growth during infancy, but had slowed growth during juvenility, compared to Laterborns. Although both Firstborns and Laterborns were the same age at reproductive debut, Firstborns had lower body mass, an effect that persisted throughout the reproductive career. Available milk energy, the product of milk energetic density and milk yield, was on average 16% lower for Firstborns compared to Laterborns, a difference that was only partially mediated by their lower mass. Despite differences in their mothers’ energy provision through milk, the mass of infants of Firstborn and Laterborn mothers did not differ at peak lactation, suggesting that infants of Firstborns devote a higher proportion of milk energy to growth than infants of Laterborns. To date few studies have explored how early life conditions shape capacities to synthesize milk and milk composition. Our findings contribute new information among primates on how early life maternal endowments are associated with persistent effects long after the period of maternal dependence well into reproductive maturity.
In humans and other mammals, maternal hormones are transferred to offspring during lactation via milk and may regulate postnatal development, including the pace of early growth. Here, we used a nonhuman primate model to test the hypotheses that milk cortisol and dehydroepiandrosterone‐sulfate (DHEAS) concentrations reflect maternal characteristics, and that changes in these hormones across lactation are associated with early postnatal growth rates.
Demographic information, morphometrics, and milk samples were collected from rhesus macaque mothers and their infants at the California National Primate Research Center in Davis, California. Using linear models, we examined the relationship between maternal traits and milk hormone concentrations (N = 104 females) and explored the effect of milk hormones on the rate of offspring growth (N = 72 mother‐infant dyads), controlling for available milk energy.
Contrary to previous studies, we found that milk cortisol concentrations were categorically higher in multiparous females than in primiparous females. However, milk DHEAS concentrations decreased with maternal parity. Neither milk cortisol nor DHEAS were related to maternal rank. Finally, changes in milk hormones predicted offspring growth in a sex‐specific and temporal manner: increases in cortisol from peak to late lactation predicted faster female growth, and increases in DHEAS concentrations from early to peak and peak to late lactation predicted faster male growth.
Our findings shed light on how hormonal components of milk have sex‐specific effects on offspring growth during early postnatal life with varying temporal windows of sensitivity.
- PAR ID:
- 10459267
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- American Journal of Human Biology
- Volume:
- 31
- Issue:
- 6
- ISSN:
- 1042-0533
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Synopsis The ability to provision offspring with milk is a significant adaptive feature of mammals that allows for considerable maternal regulation of offspring beyond gestation, as milk provides complete nutrition for developing neonates. For mothers, lactation is a period of marked increases in energetic and nutritive demands to support milk synthesis; because of this considerable increase in demand imposed on multiple physiological systems, lactation is particularly susceptible to the effects of chronic stress. Here, we present work that explores the impact of chronic stress during lactation on maternal lactation performance (i.e., milk quality and quantity) and the expression of key milk synthesis genes in mammary tissue using a Sprague–Dawley rat model. We induced chronic stress using a well-established, ethologically relevant novel male intruder paradigm for 10 consecutive days during the postpartum period. We hypothesized that the increased energetic burden of mounting a chronic stress response during lactation would decrease lactation performance. Specifically, we predicted that chronic exposure to this social stressor would decrease either milk quality (i.e., composition of proximate components and energy density) or quantity. We also predicted that changes in proximate composition (i.e., lipid, lactose, and protein concentrations) would be associated with changes in gene expression levels of milk synthesis genes. Our results supported our hypothesis that chronic stress impairs lactation performance. Relative to the controls, chronically stressed rats had lower milk yields. We also found that milk quality was decreased; milk from chronically stressed mothers had lower lipid concentration and lower energy density, though protein and lactose concentrations were not different between treatment groups. Although there was a change in proximate composition, chronic stress did not impact mammary gland expression of key milk synthesis genes. Together, this work demonstrates that exposure to a chronic stressor impacts lactation performance, which in turn has the potential to impact offspring development via maternal effects.
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Methods We analyzed concentrations of immune factors in 358 milk samples collected from women residing in 10 international sites using linear mixed‐effects models to test for an interaction between maternal condition, including population as a random effect and infant age and maternal age as fixed effects.
Results IgG concentrations were significantly lower in milk produced by women consuming diets with low diversity with male infants than those with female infants. No other significant associations were identified.
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Methods Heights and weights were collected from 206 children aged 2–18 years old. HAZ, WAZ, and BMIZ were calculated using CDC standards. DHEAS and cortisol assays were used to determine biomarker concentrations in hair. Generalized linear modeling was used to examine effects of nutritional status on DHEAS concentrations, as well as cortisol, controlling for age, sex, and population.
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