How the isotopic composition of the teeth of slow-growing primates (including humans) reflects the environmental water supply is still poorly understood, despite its potential for inferring seasons of birth and death, historic and prehistoric rainfall patterns, and sustained droughts and extreme rainfall events. Here we compare secondary ion mass spectrometry (SIMS) measurements of delta O-18 values in the innermost enamel of a human child and three wild chimpanzees (Pan troglodytes verus) with concurrent local rainfall. We also compare enamel delta O-18 values from ten captive macaques (Macaca mulatta) to their drinking water delta O-18 values and/or concurrent rainfall. Synchrotron X-ray imaging shows that the innermost similar to 20 mu m of enamel is highly mineralized soon after secretion. SIMS microsampling of this zone yields a coherent record of local rainfall patterns-lower delta O-18 values during wet seasons, higher values during more arid periods, which is particularly evident in wild chimpanzees. Cross-correlation analyses reveal statistically significant relationships between enamel delta O-18 values and water inputs that are strongest in healthy individuals without physiological disruptions. Primate enamel delta O-18 values commonly vary by similar to 1-2 parts per thousand within a few weeks of birth, as well as in captive macaques during periods of dehydration due to diarrheal illnesses. Consumption of cooked foods and manipulation of municipal water supplies may also obscure rainfall trends in contemporary humans and captive primates, although several healthy macaques show parallels with delta O-18 values measured from drinking water. Predicted drinking water delta O-18 values (delta O-18(dw)) from existing water/phosphate conversion equations reveal a strong similarity with observed delta O-18(dw) values, including measured meteoric and tap water. While enamel maturation may impact primate delta O-18 values, our analysis does not detect consistent temporal offsets between physiological events or seasons and the innermost enamel. These data show that SIMS delta O-18 measurements of living and fossil primate enamel can provide a high-fidelity record for paleoseasonality reconstruction.
Since we published "Field and Laboratory Methods in Human Milk Research" in 2013, human milk research has increased dramatically in both number and diversity of studies. Anthropological human biologists and biological anthropologists have played key roles in the realization of this research, arguing that evolutionary, developmental, and biocultural perspectives as essential for understanding variation in human milk. The purpose of this review is to highlight human biologists' and biological anthropologists' contributions to our understanding of human milk, often made in broadly collaborative research, as part of the 50th anniversary of the Human Biology Association. In this review, we identify three areas where human biologists have made major contributions: (1) understanding milk as a phenotype, (2) sex-differentiated milk synthesis, and (3) the cultural ecology of milk. We end this review by discussing future research directions and the applied and translational potentials of milk research, calling on human biologists to continue our leadership in the field in the decades to come.
Mammalian mothers provide behavioral and physiological signals that offspring use to calibrate development in relation to maternal resources and environmental cues. Infants respond selectively as they prioritize certain developmental systems over others, creating developmental tradeoffs between competing biological systems. Here, we investigate the influence of maternal capital (“investment capacity”) on the growth and development of their infants in wild olive baboons ( Papio anubis ) from Laikipia, Kenya. We posit that maternal capital is influenced by a mother’s own early life experiences (e.g., drought, maternal loss) and her current life experiences (e.g., dominance rank, food availability), and is signaled to offspring via maternal effort (i.e., nursing and carrying time) and glucocorticoids. We used behavioral data on 40 infants (43% female) in the first year of life to quantify maternal effort, infant play, and infant independence (i.e., frequency of infant departures from mother). We matched these behavioral data with maternal fecal glucocorticoid measures from lactating mothers, and infant growth measures assessed via photogrammetry. Signals of low maternal capital predicted lower rates of infant play, less behavioral independence, and slower growth. There was a negative relationship between the rate of social contact play and growth rate, indicating a developmental tradeoff. Males were more sensitive than females to some of the maternal signals measured in our study. These results add to a growing body of evidence demonstrating that maternal behavioral and physiological signals shape infant development. ### Competing Interest Statement The authors have declared no competing interest. U.S. National Science Foundation, https://ror.org/021nxhr62, BCS-1732172, GRFP-1841051 Leakey Foundation, https://ror.org/018kdpd27 Arizona State University, https://ror.org/03efmqc40
Trade-offs resulting from the high demand of offspring production are a central focus of many subdisciplines within the field of biology. Yet, despite the historical and current interest on this topic, large gaps in our understanding of whole-organism trade-offs that occur in reproducing individuals remain, particularly as it relates to the nuances associated with female reproduction. This volume of Integrative and Comparative Biology (ICB) contains a series of papers that focus on reviewing trade-offs from the female-centered perspective of biology (i.e., a perspective that places female reproductive biology at the center of the topic being investigated or discussed). These papers represent some of the work showcased during our symposium held at the 2024 meeting of the Society for Integrative and Comparative Biology (SICB) in Seattle, Washington. In this roundtable discussion, we use a question-and-answer format to capture the diverse perspectives and voices involved in our symposium. We hope that the dialogue featured in this discussion will be used to motivate researchers interested in understanding trade-offs in reproducing females and provide guidance on future research endeavors.
Human milk is a highly complex liquid food tailor-made to match an infant's needs. Beyond documented positive effects of breastfeeding on infant and maternal health, there is increasing evidence that milk constituents also impact child neurodevelopment. Non-nutrient milk bioactives would contribute to the (long-term) development of child cognition and behavior, a process termed 'Lactocrine Programming'. In this review we discuss the current state of the field on human milk composition and its links with child cognitive and behavioral development. To promote state-of-the-art methodologies and designs that facilitate data pooling and meta-analytic endeavors, we present detailed recommendations and best practices for future studies. Finally, we determine important scientific gaps that need to be filled to advance the field, and discuss innovative directions for future research. Unveiling the mechanisms underlying the links between human milk and child cognition and behavior will deepen our understanding of the broad functions of this complex liquid food, as well as provide necessary information for designing future interventions.
The regular incremental secretion of enamel and dentine can be interrupted during periods of stress resulting in accentuated growth lines. These accentuated lines, visible under light microscopy, provide a chronology of an individual's stress exposure. Previously, we showed that small biochemical changes along accentuated growth lines detected by Raman spectroscopy, coincided with the timing of medical history events and disruptions of weight trajectory in teeth from captive macaques. Here, we translate those techniques to study biochemical changes related to illness and prolonged medical treatment during early infancy in humans. Chemometric analysis revealed biochemical changes related to known stress-induced changes in circulating phenylalanine as well as other biomolecules. Changes in phenylalanine are also known to affect biomineralization which is reflected in changes in the wavenumbers of hydroxyapatite phosphate bands associated with stress in the crystal lattice. Raman spectroscopy mapping of teeth is an objective, minimally-destructive technique that can aid in the reconstruction of an individual's stress response history and provide important information on the mixture of circulating biochemicals associated with medical conditions, as applied in epidemiological and clinical samples.
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.
OBJECTIVE Early life interindividual variation in hypothalamic-pituitary-adrenal (HPA) reactivity to stress is predictive of later life psychological and physical well-being, including the development of many pathological syndromes that are often sex-biased. A complex and interactive set of environmental and genetic causes for such variation has been implicated by previous studies, though little attention has been paid to nonadditive effects (e.g. dominance, X-linked) or sex-specific genetic effects. METHOD We used a large pedigreed sample of captive 3-4 months old infant rhesus macaques (N = 2,661, 54% female) to fit univariate and multivariate linear mixed quantitative genetic models for four longitudinal blood cortisol samples and three reliable ratings of infant temperament (nervousness, gentleness, confidence) during a mother-infant separation protocol. RESULTS Each trait had a moderate narrow-sense heritability (h², 0.26-0.46), but dominance effects caused the first two cortisol samples to have much larger broad-sense heritabilities (H², 0.57 and 0.77). We found no evidence for X-linked variance or common maternal environment variance. There was a sex difference in heritability of the first cortisol sample (hf² < hm²), suggesting differing genetic architecture of perception of maternal separation and relocation during infancy. Otherwise, genetic covariance matrices for the sexes were very similar. Genetic correlations between cortisol levels and temperament were weak (< |0.4|) but stronger than residual or phenotypic correlations. CONCLUSIONS HPA reactivity and temperament had a primarily additive genetic basis in infant macaques, but there were important complexities to the genetic architecture of including genetic dominance and sex differences in heritability at this early life stage. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
Rapid weight gain (RWG) by 6 months of age has been identified as one of the earliest indicators of childhood obesity. Research suggests that exclusive breastfeeding (EBF) may protect against RWG. The makeup of the infant gut microbiome (GM) may also influence RWG as differences in feeding practices may alter the bacterial makeup of the gut, potentially impacting energy metabolism. The goal of this pilot study was to evaluate differences in GM community structure over the first 6 months of life in relation to feeding practices and RWG. Pregnant mothers (n = 31) were recruited from Women, Infant, and Children's Supplemental Nutrition Program clinics and by word of mouth to participate in this study. Participants were followed over 6 months, completing home study visits postpartum, at 3 weeks and 6 months of infant age. RWG was defined as >+0.67 change in weight-for-age Z-score over the first 6 months of life. Microbial data from infant feces collected at birth, 3 weeks, and 6 months were sequenced using Illumina adapter primers for the V4 region of the 16S rRNA gene. GM diversity metrics include α-diversity, β-diversity, and differential abundance of microbes were assessed using Kruskal-Wallis and PERMANOVA comparisons, adjusted for multiple comparisons, via QIIME2. Among this cohort, 29% (n = 9) of infants experienced RWG in the first 6 months of life, and 22.6% (n = 7) were EBF for 6 months. Results suggested a significant difference in microbial community structure (weighted UniFrac) between infants who were EBF and formula-fed (FF) from birth to 3 weeks of age (p = 0.04). An exploratory analysis of longitudinal GM changes identified the family Prevotellaceae as potentially volatile over the first 6 months of life; however, this model failed to reach significance for either RWG or feeding practice. No additional differences in α- or β-diversity or differential abundance of microbes were observed among RWG or feeding practice groups. The present study suggested differences in microbial community structure between infants who were EBF versus FF from birth to 3 weeks of age. Future research is warranted to further explore potential connections between RWG, feeding practices, and the infant GM in a longitudinal study with a larger sample size and more frequent sampling. ASU-Mayo Clinic Partnership Obesity Solutions Seed Grant Program.
Bifidobacterium species are beneficial and dominant members of the breastfed infant gut microbiome; however, their health benefits are partially species-dependent. Here, we characterize the species and subspecies of Bifidobacterium in breastfed infants around the world to consider the potential impact of a historic dietary shift on the disappearance of B. longum subsp. infantis in some populations. Across populations, three distinct patterns of Bifidobacterium colonization emerged: (1) The dominance of Bifidobacterium longum subspecies infantis, (2) prevalent Bifidobacterium of multiple species, and (3) the frequent absence of any Bifidobacterium. These patterns appear related to a country’s history of breastfeeding, with infants in countries with historically high rates of long-duration breastfeeding more likely to be colonized by B. longum subspecies infantis compared with infants in countries with histories of shorter-duration breastfeeding. In addition, the timing of infant colonization with B. longum subsp. infantis is consistent with horizontal transmission of this subspecies, rather than the vertical transmission previously reported for other Bifidobacterium species. These findings highlight the need to consider historical and cultural influences on the prevalence of gut commensals and the need to understand epidemiological transmission patterns of Bifidobacterium and other major commensals.
Background Human milk oligosaccharides (HMOs) are an abundant class of compounds found in human milk and have been linked to the development of the infant, and specifically the brain, immune system, and gut microbiome. Objectives Advanced analytical methods were used to obtain relative quantitation of many structures in approximately 2000 samples from over 1000 mothers in urban, semirural, and rural sites across geographically diverse countries. Methods LC-MS-based analytical methods were used to profile the compounds with broad structural coverage and quantitative information. The profiles revealed their structural heterogeneity and their potential biological roles. Comparisons of HMO compositions were made between mothers of different age groups, lactation periods, infant sexes, and residing geographical locations. Results A common behavior found among all sites was a decrease in HMO abundances during lactation until approximately postnatal month 6, where they remained relatively constant. The greatest variations in structural abundances were associated with the presence of alpha(1,2)-fucosylated species. Genomic analyses of the mothers were not performed; instead, milk was phenotyped according to the abundances of alpha(1,2)-fucosylated structures. Mothers from the South American sites tended to have higher proportions of phenotypic secretors [mothers with relatively high concentrations of alpha(1,2)-fucosylated structures] in their populations compared to the rest of the globe, with Bolivia at similar to 100% secretors, Peru at similar to 97%, Brazil at similar to 90%, and Argentina at similar to 85%. Conversely, the cohort sampled in Africa manifested the lowest proportion of secretors (South Africa similar to 63%, the Gambia similar to 64%, and Malawi similar to 75%). Furthermore, we compared total abundances of HMOs in secretors compared with nonsecretors and found that nonsecretors have lower abundances of HMOs compared to secretors, regardless of geographical location. We also observed compositional differences of the 50+ most abundant HMOs between milk types and geographical locations. Conclusions This study represents the largest structural HMO study to date and reveals the general behavior of HMOs during lactation among different populations.
Adverse experiences during early life exert important effects on development, health, reproduction, and social bonds, with consequences often persisting across generations. A mother’s early life experiences can impact her offspring’s development through a number of pathways, such as maternal care, physiological signaling through glucocorticoids, or even intergenerational effects like epigenetic inheritance. Early life adversity in female yellow baboons (Papio cynocephalus) predicts elevated glucocorticoids, reduced sociality, shortened lifespan, and higher offspring mortality. If baboon mothers with more early life adversity, experience poorer condition and struggle to provide for their offspring, this could contribute to the persisting transgenerational effects of adversity. Here, we examined the effects of mothers’ early life adversity on their maternal effort, physiology, and offspring survivability in a population of olive baboons, Papio anubis. Mothers who experienced more adversity in their own early development exerted greater maternal effort (i.e., spent more time nursing and carrying) and had higher levels of glucocorticoid metabolites than mothers with less early life adversity. Offspring of mothers with more early life adversity had reduced survivability compared to offspring of mothers with less early life adversity. There was no evidence that high maternal social rank buffered the effects of early life adversity. Our data suggest early life experiences can have lasting consequences on maternal effort and physiology, which may function as proximate mechanisms for intergenerational effects of maternal experience. Animals exposed to early life adversity experience both immediate and lasting consequences. If early life adversity exerts developmental constraints that affect a mother’s ability to provide for her offspring, this could explain the transgenerational effects of early life adversity. In our study of wild olive baboons, we examined how a mother’s own early life adversity predicts her maternal effort (i.e., nursing and carrying time), maternal fecal glucocorticoid levels, and offspring outcomes. We found that female baboons who experienced more early life adversity had higher glucocorticoid levels during pregnancy and lactation, exerted more maternal effort, and produced offspring with higher mortality risk than females with less early life adversity. Our results suggest that female baboons with more early life adversity experience developmental constraints and struggle to invest in offspring, which likely contributes to persisting effects of early life adversity across generations.
March Mammal Madness is a science outreach project that, over the course of several weeks in March, reaches hundreds of thousands of people in the United States every year. We combine four approaches to science outreach – gamification, social media platforms, community event(s), and creative products – to run a simulated tournament in which 64 animals compete to become the tournament champion. While the encounters between the animals are hypothetical, the outcomes rely on empirical evidence from the scientific literature. Players select their favored combatants beforehand, and during the tournament scientists translate the academic literature into gripping “play-by-play” narration on social media. To date ~1100 scholarly works, covering almost 400 taxa, have been transformed into science stories. March Mammal Madness is most typically used by high-school educators teaching life sciences, and we estimate that our materials reached ~1% of high-school students in the United States in 2019. Here we document the intentional design, public engagement, and magnitude of reach of the project. We further explain how human psychological and cognitive adaptations for shared experiences, social learning, narrative, and imagery contribute to the widespread use of March Mammal Madness.
OBJECTIVES:Public engagement is increasingly viewed as an important pillar of scientific scholarship. For early career and established scholars, navigating the mosaic landscape of public education and science communication, noted for rapid "ecological" succession, can be daunting. Moreover, academics are characterized by diverse skills, motivations, values, positionalities, and temperaments that may differentially incline individuals to particular public translation activities.METHODS:Here we briefly contextualize engagement activities within a scholarly portfolio, describe the use of one public education program-March Mammal Madness (MMM)- to highlight approaches to science communication, and explore essential elements and practical considerations for creating and sustaining outreach pursuits in tandem with other scholarly activities.RESULTS:MMM, an annual simulated tournament of living and fossil animal taxa, has reached hundreds of thousands of learners since 2013. This program has provided a platform to communicate research findings from biology and anthropology and showcase numerous scholars in these fields. MMM has leveraged tournament devices to intentionally address topics of climate change, capitalist environmental degradation, academic sexism, and racist settler-colonialism. The tournament, however, has also perpetuated implicit biases that need disrupting.CONCLUSIONS:By embracing reflexive, self-interrogative, and growth attitudes, the tournament organizers iteratively refine and improve this public science education program to better align our activities with our values and goals. Our experiences with MMM suggest that dispersing science is most sustainable when we combine ancestral adaptations for cooperation, community, and storytelling with good-natured competition in the context of shared experiences and shared values.
Abstract Breastfeeding and human milk (HM) are critically important to maternal, infant and population health. This paper summarizes the proceedings of a workshop that convened a multidisciplinary panel of researchers to identify key priorities and anticipated breakthroughs in breastfeeding and HM research, discuss perceived barriers and challenges to achieving these breakthroughs and propose a constructive action plan to maximize the impact of future research in this field. Priority research areas identified were as follows: (1) addressing low breastfeeding rates and inequities using mixed methods, community partnerships and implementation science approaches; (2) improving awareness of evidence‐based benefits, challenges and complexities of breastfeeding and HM among health practitioners and the public; (3) identifying differential impacts of alternative modes of HM feeding including expressed/pumped milk, donor milk and shared milk; and (4) developing a mechanistic understanding of the health effects of breastfeeding and the contributors to HM composition and variability. Key barriers and challenges included (1) overcoming methodological limitations of epidemiological breastfeeding research and mechanistic HM research; (2) counteracting ‘breastfeeding denialism’ arising from negative personal breastfeeding experiences; (3) distinguishing and aligning research and advocacy efforts; and (4) managing real and perceived conflicts of interest. To advance research on breastfeeding and HM and maximize the reach and impact of this research, larger investments are needed, interdisciplinary collaboration is essential, and the scientific community must engage families and other stakeholders in research planning and knowledge translation.
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.