Early life determinants of the infant microbiome: social environments get “under and on the skin”

Manus, Melissa Barbara

doi:https://doi.org/10.21985/n2-63r0-av44

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Early life determinants of the infant microbiome: social environments get “under and on the skin”

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A central theme in biological anthropology is investigating how the human body responds to interactions with the surrounding environment. The microbiome—the collection of microorganisms (and their genes) that live in and on the human body— represents one such pathway that mediates the environment’s influence on human biology, physiology, and health. The fundamental connection between the microbiome and human biology lies in the microbiome’s plasticity and responsiveness to factors in the environment, as well as its impact on a range of human physiological systems. For example, diet and contact with aspects of the built and natural environment shape human-associated microbial communities, which in turn directly influence the immune system, nutrition and metabolism, and mood and behavior.In addition to factors in the physical environment, there is emerging evidence that aspects of the social environment, including interactions that occur within households and family units, also shape the human microbiome. Borrowing from metacommunity theory, the human body represents an interconnected patchwork of microbial communities, where the movement, or dispersal, of microbes occurs on two scales: (1) between individuals and (2) across the body sites of a given individual. Beginning at birth, infants acquire microbes from their mothers and other caregivers with whom they have frequent social interactions in early life. However, most research is focused on the social sharing of gut microbes and does not consider how microbial communities of other body sites are established. As the skin is a frequent point of contact between individuals during social interactions, particularly during infant caregiving, it is likely that the microbial communities on the skin are sensitive to our social behaviors. Since the skin microbiome helps to train and regulate the immune system, the acquisition of microbes during infancy may be adaptive and influence lifelong health outcomes related to immune system functioning and other aspects of physiology. Research at the intersection of early life social and microbial dynamics is salient to broader themes in biological anthropology, particularly aspects of human reproductive and life history strategies that promote social interactions between infants, mothers, and other caregivers. Unlike other great apes, humans are cooperative breeders, and human mothers rely extensively on the help of non-maternal caregivers (i.e. alloparents) for an extended period of time. Common caregiving behaviors that put alloparents and infants into contact, such as holding and feeding, likely promote microbial sharing and therefore contribute to the suite of infants’ microbial exposures. In this context, alloparental behaviors that help spread important microbes to infants may represent an additional benefit of allocare that played a role in the selection for cooperative breeding in humans. While allocare has been documented across contemporary human populations, biocultural variation can produce differences in infant-caregiver interactions within and between households, families, and populations. Therefore, the influence of infant-alloparent interactions on the developing microbiome may be an understudied dimension of the social determinants of health and disease. To this end, this dissertation takes a comparative perspective to explore the social and environmental influences on the skin and gut microbiomes of infants living in Mexico, the Philippines, and the U.S.A. By coupling microbiome samples with detailed questionnaire data, this dissertation assesses the relationship between early life environments and the infant microbiome at three spatial scales-- across populations, within households, and between infant-caregiver dyads. The data presented here suggest that population and household-level factors shape the diversity and composition of distinct microbial communities across infant body sites. In contrast to previous studies, research in Mexico probed deeper than the national, ethnic, and racial categories commonly used to explain differences in microbial communities, and instead highlighted population-level factors that likely influence early life microbial environments. These results of this dissertation also emphasize the importance of collecting microbiome samples from multiple infant body sites, particularly those that have differential patterns of contact with the surrounding environment. For example, samples collected from the armpit microbiome of infants living in different populations in Mexico and the U.S.A. consistently displayed lower microbial diversity compared to samples of microbial communities that are more “exposed” to the environment, including those on the hand and face. Similarly, research in the U.S.A. showed that certain aspects of infants’ social environments, including interactions with alloparents, are more strongly associated with the microbial diversity of the cheek and hand-- skin sites that are likely contacted during bouts of caregiving-- than the armpit. Results from this dissertation also highlight the utility of collecting longitudinal samples throughout infancy. Data from the Philippines show that the strength of the relationship between household size and infant gut microbial diversity increases as infants grow older, at the same time that the effect of specific household members weakens. Taken together, this dissertation contributes to the sparse literature on the influence of social environments on the infant gut microbiome and provides the first evidence that infant skin microbial communities are sensitive to interactions with alloparents. By connecting infants’ physical and social environments to the development of the microbiome across populations, this dissertation supports the continued use of the microbiome as a tool for measuring how variable social environments get under-- and on-- the skin to affect infant development and health. Expanding on this work, future studies should measure microbial transmission events during specific bouts of caregiving in order to pinpoint the exact routes through which infants acquire their microbes. Additionally, there is a need for research that integrates microbiome samples with other biomarkers of infant biology and physiology, such as those related to inflammation and immune function. These studies will be critical for connecting variation in infants’ social and microbial environments to differences in health outcomes, and in turn, applying microbiome science to global and public health initiatives aimed at improving infant wellbeing across different geographic and biocultural contexts.

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