Mammal Milk Microbiome

Milk production is an ancient adaptation that unites all mammals. Milk contains a microbiome that can contribute to offspring health and development. We generated a comprehensive milk microbiome dataset (16S rRNA gene) for the class Mammalia, representing 47 species from all placental superorders, to determine how deterministic and stochastic processes structure milk microbiomes. We show that across Mammalia, milk exposes offspring to maternal bacterial and archaeal symbionts. Using a null model-based approach to examine community assembly mechanisms, we found that mammalian milk microbiomes experience high ecological stochasticity (e.g., ecological drift) accounting for 80% of all pairwise community comparisons compared to mammalian gut and mammalian skin microbiomes (69% and 45%, respectively). In contrast, deterministic processes of environmental selection accounted for 20% in milk microbiome assembly; milk microbiomes were similar from mammals with the same host superorder (Afrotheria, Laurasiathera, Euarchontoglires, Xenarthra: 6%), environment (marine captive, marine wild, terrestrial captive, terrestrial wild: 6%), diet (carnivore, omnivore, herbivore, insectivore: 5%) and milk nutrient content (sugar, fat, protein: 3%). Milk microbiomes were similar between lactation stages, suggesting similar eco-evolutionary processes act across lactation. Our results provide support for entero-mammary trafficking across mammals, representing a mechanism by which dietary-associated bacteria are transferred from the mother's gut to mammary gland and then to offspring postnatally, even amid high stochasticity. The microbial species present in milk reflect both stochastic processes and selective pressures at the host level, exemplifying various ecological and evolutionary factors acting on milk microbiomes, which, in turn, set the stage for offspring health and development.