Early life gut microbiome dynamics mediate maternal effects on infant growth in vervet monkeys

ABSTRACT Background Maternal parity is associated with variation in infant growth across mammals, but the mechanisms underlying this relationship are unclear. Given emerging links between growth and the microbiome, and the importance of maternal microbiota in establishing this community, the assembly of the infant gut microbiome may be a mediator of parity effects on infant growth. Results Here, we analyzed 118 fecal and milk samples from mother-infant vervet monkey dyads across the first 6 months postpartum in a population with high growth-associated infant mortality. Despite poorer milk production, infants born to low parity females were larger at 6 months of age than their counterparts and exhibited divergent patterns in gut microbiome assembly. Gut microbiome alpha diversity increased rapidly from the first days of life to 4 months old in all infants, but infants born to low parity females exhibited reduced gut microbiome alpha diversity during early life. At the taxonomic level, infants broadly exhibited a shift from Bacteroides fragilis to Prevotella dominance. Infants of low parity females housed more B. fragilis in their guts, and B. fragilis dominance drove reduced alpha diversity. Maternal vertical transmission to the infant gut was greater from milk than from the maternal gut, and was greatest among infants born to low parity females. B. fragilis was 15-fold more abundant in milk than in the maternal gut and was greater in the milk of low parity females, suggesting that milk may be the primary maternal reservoir of B. fragilis . Path analyses demonstrated that both infant gut alpha diversity and B. fragilis mediated parity effects on postnatal growth: infants were larger at 6 months old if they exhibited reduced alpha diversity and a greater relative abundance of B. fragilis during early life. Conclusion The first days of life are a critical period of infant gut microbiome organization during which the establishment of a less diverse, milk-oriented microbial community abundant in B. fragilis promotes growth among infants born to reproductively inexperienced females.