Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the life span. Here, we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.
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Higher early life mortality with lower infant body mass in a free‐ranging primate
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 Rhesus macaque infants experienced on average 5% reduced hazard of death for an increase in body mass of 0.1 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.
- PAR ID:
- 10456949
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Journal of Animal Ecology
- Volume:
- 89
- Issue:
- 10
- ISSN:
- 0021-8790
- Page Range / eLocation ID:
- p. 2300-2310
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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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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.
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Animals, and mammals in particular, vary widely in their “pace of life,” with some species living long lives and reproducing infrequently (slow life histories) and others living short lives and reproducing often (fast life histories). These species also vary in the importance of maternal care in offspring fitness: In some species, offspring are fully independent of their mothers following a brief period of nutritional input, while others display a long period of continued dependence on mothers well after nutritional dependence. Here, we hypothesize that these two axes of variation are causally related to each other, such that extended dependence of offspring on maternal presence leads to the evolution of longer lives at the expense of reproduction. We use a combination of deterministic modeling and stochastic agent-based modeling to explore how empirically observed links between maternal survival and offspring fitness are likely to shape the evolution of mortality and fertility. Each of our modeling approaches leads to the same conclusion: When maternal survival has a strong impact on the survival of offspring and grandoffspring, populations evolve longer lives with less frequent reproduction. Our results suggest that the slow life histories of humans and other primates as well as other long-lived, highly social animals such as hyenas, whales, and elephants are partially the result of the strong maternal care that these animals display. We have designed our models to be readily parameterized with demographic data that are routinely collected by long-term researchers, which will facilitate more thorough testing of our hypothesis.
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Abstract Objectives A key feature of human life history evolution is that modern humans wean their infants 2–4 years earlier on average than African apes. However, our understanding of weaning variation in apes remains limited. Here we provide the first such report in chimpanzees by examining weaned age variation using long‐term data from Gombe National Park, Tanzania.
Material and Methods We analyzed 41 years of observational behavioral data from 65 offspring of 29 mothers to examine the relationships between weaned age (defined as cessation of suckling) in wild chimpanzees and maternal age, dominance rank and parity, and offspring sex. We used Cox proportional hazards regression with mixed effects to model time to weaning and to examine potential sources of variation in offspring weaned age.
Results We found that male offspring were less likely than female offspring to wean by a given age and that weaned age of males varied more than weaned age of females. In addition, maternal dominance rank interacted with offspring age, such that low‐ranking mothers were less likely to wean offspring early, but this effect decreased with offspring age.
Discussion We found that male offspring and offspring of low‐ranking females were less likely to wean early, but did not find evidence for variable weaning according to maternal age or parity. As more data accumulate, we will be better able to disentangle the effects of maternal dominance rank, age and parity. Such studies will not only provide a richer understanding of living ape life history characteristics, but will also provide an important framework for understanding the evolution of early weaning in humans.
