skip to main content

Attention:

The NSF Public Access Repository (PAR) system and access will be unavailable from 11:00 PM ET on Friday, December 13 until 2:00 AM ET on Saturday, December 14 due to maintenance. We apologize for the inconvenience.


Title: Maternal care in wild toque macaques ( Macaca sinica ) involves prolonged lactation and interbirth intervals as adaptations to reduce maternal depletion and infant mortality in harsh environments
Abstract

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 (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.

 
more » « less
PAR ID:
10479783
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
American Journal of Primatology
ISSN:
0275-2565
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Synopsis

    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
  2. 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.

     
    more » « less
  3. Abstract Objectives

    Folate is an essential nutrient fundamental to human growth and development. Human milk maintains high folate content across the maternal folate status range, suggesting buffering of milk folate with prioritized delivery to milk at the expense of maternal depletion. We investigated whether and how the extent of this buffering may diminish under prolonged nutritional and/or disease stress, while taking into consideration infants' varying vulnerability to malnutrition‐related morbidity/mortality.

    Methods

    A cross‐sectional study analyzed milk specimens from northern Kenyan mothers (n = 203), surveyed during a historic drought and ensuing food shortage. Multiple regression models for folate receptor‐α (FOLR1) in milk were constructed. Predictors included maternal underweight (BMI < 18.5), iron‐deficiency anemia (hemoglobin <12 g/dl and dried‐blood‐spot transferrin receptor >5 mg/L), folate deficiency (hyperhomocysteinemia, homocysteine >12 or 14 μmol/L), inflammation (serum C‐reactive protein >5 mg/L), infant age and sex, and mother‐infant interactions.

    Results

    In adjusted models, milk FOLR1 was unassociated with maternal underweight, iron‐deficiency anemia and inflammation. FOLR1 was positively associated with maternal folate deficiency, and inversely associated with infant age. There was interaction between infant age and maternal underweight, and between infant sex and maternal folate deficiency, predicting complex changes in FOLR1.

    Conclusions

    Our results suggest that mothers buffer milk folate against their own nutritional stress even during a prolonged drought; however, the extent of this buffering may vary with infant age, and, among folate‐deficient mothers, with infant sex. Future research is needed to better understand this variability in maternal buffering of milk folate and how it relates to folate status in nursing infants.

     
    more » « less
  4.  
    more » « less
  5. Rationale

    The grey seal,Halichoerus grypus(GS), and the northern elephant seal,Mirounga angustirostris(NES), come ashore for reproduction. This period involves intense physiological processes such as lactation in females and a developmental post‐weaning fast in juveniles. Previous studies have shown thatδ13C andδ15N values are affected by starvation, but the precise effects of fasting associated with lactation and post‐weaning fast in seals remain poorly understood.

    Methods

    To examine the effect of lactation and post‐weaning fast on stable isotope ratios in GS and NES, blood and hair were sampled from 21 GS mother‐pup pairs on the Isle of May and on 22 weaned NES pups at Año Nuevo State Reserve during their respective breeding seasons. Milk samples were also collected from GS mothers. Stable isotope measurements were performed with an isotope ratio mass spectrometer coupled to an N‐C elemental analyser.

    Results

    Changes in stable isotope ratios in blood components during fasting were similar and weak between GS and NES mothers especially in blood cells (GS:Δ15N = 0.05‰,Δ13C = 0.02‰; NES:Δ15N = 0.1‰,Δ13C = 0.1‰). GS showed a15N discrimination factor between maternal and pup blood cells and milk, but not for13C. The strongest relationship between the isotopic compositions of the mother and the pup was observed in the blood cells.

    Conclusions

    Isotopic consequences of lactation, fasting, and growth seem limited in NES and GS, especially in medium‐term integrator tissues of feeding activity such as blood cells. Stable isotope ratios in the blood of pups and mothers are correlated. We observed a subtle mother‐to‐pup fractionation factor. Our results suggest that pup blood cells are mostly relevant for exploring the ecology of female seals.

     
    more » « less