Ecoevolutionary processes structure milk microbiomes across the mammalian tree of life

Abstract

Milk production is an ancient adaptation that unites all mammals. Milk contains a microbiome that can contribute to offspring health and microbial-immunological development. We generated a comprehensive milk microbiome dataset (16S rRNA gene) for the class Mammalia, representing 47 species from all placental superorders, to determine processes structuring milk microbiomes. We show that across Mammalia, milk exposes offspring to maternal bacterial and archaeal symbionts throughout lactation. Deterministic processes of environmental selection accounted for 20% of milk microbiome assembly processes; milk microbiomes were similar from mammals with the same host superorder (Afrotheria, Laurasiathera, Euarchontoglires, and Xenarthra: 6%), environment (marine captive, marine wild, terrestrial captive, and terrestrial wild: 6%), diet (carnivore, omnivore, herbivore, and insectivore: 5%), and milk nutrient content (sugar, fat, and protein: 3%). We found that diet directly and indirectly impacted milk microbiomes, with indirect effects being mediated by milk sugar content. Stochastic processes, such as ecological drift, accounted for 80% of milk microbiome assembly processes, which was high compared to mammalian gut and mammalian skin microbiomes (69% and 45%, respectively). Even amid high stochasticity and indirect effects, our results of direct dietary effects on milk microbiomes provide support for enteromammary trafficking, representing a mechanism by which bacteria are transferred from the mother’s gut to mammary gland and then to offspring postnatally. The microbial species present in milk reflect both selective pressures and stochastic processes 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.

Ontogeny drives shifts in skin bacterial communities in facultatively paedomorphic salamanders

“…Substantial immunological and structural changes occur in the skin during metamorphosis [17, 18], and thus developmental shifts in immunity or skin structure may be the mechanisms that drive the assembly of skin bacterial communities. We found that larval newts had the lowest abundances of skin microbes and lower diversity across all metrics (), which may indicate the importance of neutral processes, such as ecological drift and dispersal limitation, in driving early microbial assembly [62]. Conversely, low diversity may indicate strong host selection, though typically microbial diversity decreases with ontogeny as the role of host selection in filtering the microbial community increases [63].…”

“…We found that larval newts had the lowest abundances of skin microbes and lower diversity across all metrics ( Fig. 1 ), which may indicate the importance of neutral processes, such as ecological drift and dispersal limitation, in driving early microbial assembly [ 62 ]. Conversely, low diversity may indicate strong host selection, though typically microbial diversity decreases with ontogeny as the role of host selection in filtering the microbial community increases [ 63 ].…”

Phylosymbiosis shapes skin bacterial communities and pathogen-protective function in Appalachian salamanders

“…We used a two-step PCR library preparation and dual-index paired-end sequencing to sequence the skin microbiome of each salamander skin swab sample, as well as positive and negative controls. Briefly, we amplified the V3–V5 region of the 16S rRNA gene (~380 bp) using the universal primers 515F-Y and 939R [ 4 , 5 ], and sequenced the libraries on two MiSeq (Illumina) runs at the Center for Conservation Genomics, NZCBI ( Supplementary Methods 3 ).…”

“…Host biology is often important in predicting microbial composition and microbiomes typically differ between species [ 4 , 5 , 11 ]. These differences sometimes mirror host evolutionary history—a pattern termed phylosymbiosis—whereby microbiome dissimilarity is correlated with host phylogenetic distance [ 15 , 16 ].…”

Special series on the role of the microbiome in reproduction and fertility

“…In many animal species, the perinatal stage is known to be a key period for microbiome influences on both maternal health and appropriate colonization of the infant gut. In mammals, the milk microbiome also plays a key role during the lactation ( Keady et al 2023 ) to influence the microorganisms that take up residence in the newborn gut.…”