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1. Steroid hormone concentrations in milk predict sex‐specific offspring growth in a nonhuman primate

   https://doi.org/10.1002/ajhb.23315  

   Petrullo, Lauren ; Hinde, Katie ; Lu, Amy ( August 2019 , American Journal of Human Biology)

   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.

    

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2. Bioactive factors in milk across lactation: Maternal effects and influence on infant growth in rhesus macaques ( Macaca mulatta )

   https://doi.org/10.1002/ajp.22544  

   Bernstein, Robin M. ; Hinde, Katie ( March 2016 , American Journal of Primatology)

   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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3. Gut microbiome composition of wild western lowland gorillas is associated with individual age and sex factors

   https://doi.org/10.1002/ajpa.23842  

   Pafčo, Barbora ; Sharma, Ashok K. ; Petrželková, Klára J. ; Vlčková, Klára ; Todd, Angelique ; Yeoman, Carl J. ; Wilson, Brenda A. ; Stumpf, Rebecca ; White, Bryan A. ; Nelson, Karen E. ; et al ( April 2019 , American Journal of Physical Anthropology)

   Environmental and ecological factors, such as geographic range, anthropogenic pressure, group identity, and feeding behavior are known to influence the gastrointestinal microbiomes of great apes. However, the influence of individual host traits such as age and sex, given specific dietary and social constraints, has been less studied. The objective of this investigation was to determine the associations between an individual's age and sex on the diversity and composition of the gut microbiome in wild western lowland gorillas.

   Publicly available 16S rRNA data generated from fecal samples of different groups ofGorilla gorillagorillain the Central African Republic were downloaded and bioinformatically processed. The groups analyzed included habituated, partially habituated and unhabituated gorillas, sampled during low fruit (dry,n = 28) and high fruit (wet,n = 82) seasons. Microbial community analyses (alpha and beta diversity and analyses of discriminant taxa), in tandem with network‐wide approaches, were used to (a) mine for specific age and sex based differences in gut bacterial community composition and to (b) asses for gut community modularity and bacterial taxa with potential functional roles, in the context of seasonal food variation, and social group affiliation.

   Both age and sex significantly influenced gut microbiome diversity and composition in wild western lowland gorillas. However, the largest differences were observed between infants and adults in habituated groups and between adults and immature gorillas within all groups, and across dry and wet seasons. Specifically, although adults always showed greater bacterial richness than infants and immature gorillas, network‐wide analyses showed higher microbial community complexity and modularity in the infant gorilla gut. Sex‐based microbiome differences were not evident among adults, being only detected among immature gorillas.

   The results presented point to a dynamic gut microbiome inGorillaspp., associated with ontogeny and individual development. Of note, the gut microbiomes of breastfeeding infants seemed to reflect early exposure to complex, herbaceous vegetation. Whether increased compositional complexity of the infant gorilla gut microbiome is an adaptive response to an energy‐limited diet and an underdeveloped gut needs to be further tested. Overall, age and sex based gut microbiome differences, as shown here, maybe mainly attributed to access to specific feeding sources, and social interactions between individuals within groups.

    

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4. Meager Milk: Lasting Consequences for Adult Daughters of Primiparous Mothers Among Rhesus Macaques ( Macaca mulatta )

   https://doi.org/10.1093/icb/icad022  

   Pittet, Florent ; Hinde, Katie ( May 2023 , Integrative And Comparative Biology)

   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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5. Factors influencing bacterial microbiome composition in a wild non-human primate community in Taï National Park, Côte d’Ivoire

   https://doi.org/10.1038/s41396-018-0166-1  

   Gogarten, Jan F. ; Davies, T. Jonathan ; Benjamino, Jacquelynn ; Gogarten, J. Peter ; Graf, Joerg ; Mielke, Alexander ; Mundry, Roger ; Nelson, Michael C. ; Wittig, Roman M. ; Leendertz, Fabian H. ; et al ( June 2018 , The ISME Journal)

   Microbiomes impact a variety of processes including a host’s ability to access nutrients and maintain health. While host species differences in microbiomes have been described across ecosystems, little is known about how microbiomes assemble, particularly in the ecological and social contexts in which they evolved. We examined gut microbiome composition in nine sympatric wild non-human primate (NHP) species. Despite sharing an environment and interspecific interactions, individuals harbored unique and persistent microbiomes influenced by host species, social group, and parentage, but surprisingly not by social relationships among members of a social group. We found a branching order of host-species networks constructed using the composition of their microbiomes as characters, which was incongruent with known NHP phylogenetic relationships, with chimpanzees (Pan troglodytes verus) sister to colobines, upon which they regularly prey. In contrast to phylogenetic clustering found in all monkey microbiomes, chimpanzee microbiomes were unique in that they exhibited patterns of phylogenetic overdispersion. This reflects unique ecological processes impacting microbiome composition in chimpanzees and future studies will elucidate the aspects of chimpanzee ecology, life history, and physiology that explain their unique microbiome community structure. Our study of contemporaneous microbiomes of all sympatric diurnal NHP in an ecosystem highlights the diverse dispersal routes shaping these complex communities.

    

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