Weaning age in primates has been challenging to measure and new methods, involving molecular biomarkers in feces, tissue, or teeth have contributed to a solution. Here, we used a direct approach by briefly anesthetizing 442 female toque macaques (
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.
more » « less- PAR ID:
- 10463120
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative And Comparative Biology
- Volume:
- 63
- Issue:
- 3
- ISSN:
- 1540-7063
- Format(s):
- Medium: X Size: p. 569-584
- Size(s):
- p. 569-584
- Sponsoring Org:
- National Science Foundation
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Abstract Macaca sinica ) of Sri Lanka (over a 17‐year period) and manually testing their mammary tissue for the presence or absence of milk. Milk tests were related to known offspring ages and maternal care behaviors and indicated that older infants suckled milk well past the weaning age of 7 months that is often reported for food‐provisioned primates. Mothers strongly rejected their infants' nursing attempts in two phases, the first at 7 months as an honest signal “giving notice” promoting a shift to greater independence from milk to solid food, and when “shutting down” at final weaning after 12–18 months. The shift to supplementary lactation coincided also with the cessation of mothers carrying their infants and a resumption of cycling. All infants up to 7.2 months suckled milk, 91% of them did up to 18 months, this continued for 42% of infants beyond 18 months, and normally none received milk after 22 months. Lactation extended into 2.2% of cycling and 10.7% of pregnant females (up to 50% of gestation). The interbirth interval was prolonged by factors predicted to draw on female metabolic energy reserves and included the duration of lactation, growth among primiparas, and dietary limitations. The last also increased menarche. Females offset the metabolic costs of lactation with increased foraging and catabolism, but infants died when lactation costs seemingly compromised maternal condition. The prolonged lactation and slowed reproduction are considered adaptations to promote infant survival and growth in an environment where the natural food supply limits population growth and competition for food and water impacts the mortality of the youngest the most. -
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Abstract Objectives 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.
Methods 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.
Results 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.
Conclusions 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.
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Among mammals, numerous bioactive factors in milk vary across mothers and influence offspring outcomes. This emerging area of research has primarily investigated such dynamics within rodent biomedical models, domesticated dairy breeds, and among humans in clinical contexts. Less understood are signaling factors in the milk of non‐human primates. Here, we report on multiple bioactive components in rhesus macaque (
Macaca mulatta ) milk and their associations with maternal and infant characteristics. Milk samples were collected from 59 macaques at multiple time points across lactation in conjunction with maternal and infant morphometrics and life‐history animal records. Milk was assayed for adiponectin (APN), epidermal growth factor (EGF) and its receptor (EGF‐R), and transforming growth factor beta 2 (TGF‐β2). Regression models were constructed to assess the contributions of maternal factors on variation in milk bioactives, and on the relationship of this variation to infant body mass and growth. Maternal body mass, parity, social rank, and infant sex were all predictive of concentrations of milk bioactives. Primiparous mothers produced milk with higher adiponectin, but lower EGF, than multiparous mothers. Heavier mothers produced milk with lower EGF and EGF‐R, but higher TGF‐β2. Mothers of daughters produced milk with higher TGF‐β2. Mid‐ranking mothers produced milk with higher mean EGF and adiponectin concentrations than low‐ranking mothers. Milk EGF and EGF‐R were positively associated with infant body mass and growth rate. Importantly, these signaling bioactives (APN, EGF, EGF‐R, and TGF‐β2) were significantly correlated with nutritional values of milk. The effects of milk signals remained after controlling for the available energy in milk revealing the added physiological role of non‐nutritive milk bioactives in the developing infant. Integrating analyses of energetic and other bioactive components of milk yields an important perspective for interpreting the magnitude, sources, and consequences of inter‐individual variation in milk synthesis. Am. J. Primatol. 78:838–850, 2016. © 2016 Wiley Periodicals, Inc. -
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Abstract Traits that reflect the amount of energy allocated to offspring by mothers, such as infant body mass, are predicted to have long‐lasting effects on offspring fitness. In very long‐lived species, such as anthropoid primates, where long‐lasting and obligate parental care is required for successful recruitment of offspring, there are few studies on the fitness implications of low body mass among infants.
Using body mass data collected from 253 free‐ranging rhesus macaque
Macaca mulatta infants on Cayo Santiago, Puerto Rico, we examined if lower infant body mass predicts lower chance of survival through to reproductive maturation (4th year of life). We also used data on inter‐birth intervals and suckling behaviours to determine whether the duration of maternal care was adjusted to infant body mass.Rhesus macaque infants experienced on average 5% reduced hazard of death for an increase in body mass of 0.1
SD (~100 g) above the mean within their age–sex class. The positive association between body mass and early life survival was most pronounced in the 1st year of life.Infant body mass tended to be lower if mothers were young or old, but the link between infant body mass and early life survival remained after controlling for maternal age. This finding suggests that maternal effects on early life survival such as maternal age may act through their influence on infant body mass.
Mothers of heavier infants were less likely to be delayed in subsequent reproduction, but the estimated association slightly overlapped with zero. The timing of the last week of suckling did not differ by infant body mass.
Using infant body mass data that has been rarely available from free‐ranging primates, our study provides comparative evidence to strengthen the existing body of literature on the fitness implications of variation in infant body mass.
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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.
