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Milk is a complex biochemical fluid that includes macronutrients and microbiota, which, together, are known to facilitate infant growth, mediate the colonization of infant microbiomes, and promote immune development. Examining factors that shape milk microbiomes and milk-nutrient interplay across host taxa is critical to resolving the evolution of the milk environment. Using a comparative approach across four cercopithecine primate species housed at three facilities under similar management conditions, we test for the respective influences of the local environment (housing facility) and host species on milk (a) macronutrients (fat, sugar, and protein), (b) microbiomes (16S rRNA), and (c) predicted microbial functions. We found that milk macronutrients were structured according to host species, while milk microbiomes and predicted function were strongly shaped by the local environment and, to a lesser extent, host species. The milk microbiomes of rhesus macaques (Macaca mulatta) at two different facilities more closely resembled those of heterospecific facility-mates compared to conspecifics at a different facility. We found similar, facility-driven patterns of microbial functions linked to physiology and immune modulation, suggesting that milk microbiomes may influence infant health and development. These results provide novel insight into the complexity of milk and its potential impact on infants across species and environments., (© 2024 John Wiley & Sons Ltd. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.)

Abstract: Milk is an ancient, fundamental mammalian adaptation that provides nutrition and biochemical communication to offspring. Microbiomes have been detected in milk of all species studied to date. In this review, we discuss: (a) routes by which microbes may enter milk; (b) evidence for proposed milk microbiome adaptive functions; (c) variation in milk microbiomes across mammals; and (d) future research directions, including suggestions for how to address outstanding questions on the viability and functionality of milk microbiomes. Milk microbes may be sourced from the maternal gastrointestinal tract, oral, skin, and mammary gland microbiomes and from neonatal oral and skin microbiomes. Given the variety of microbial sources, stochastic processes strongly influence milk microbiome assembly, but milk microbiomes appear to be influenced by maternal evolutionary history, diet, environment, and milk nutrients. Milk microbes have been proposed to colonize the neonatal intestinal tract and produce gene and metabolic products that influence physiology, metabolism, and immune system development. Limited epidemiological data indicate that early-life exposure to milk microbes can result in positive, long-term health outcomes. Milk microbiomes can be modified by dietary changes including providing the mother with probiotics and prebiotics. Milk replacers (i.e. infant formula) may benefit from supplementation with probiotics and prebiotics, but data are lacking on probiotics' usefulness, and supplementation should be evidence based. Overall, milk microbiome literature outside of human and model systems is scarce. We highlight the need for mechanistic studies in model species paired with comparative studies across mammals to further our understanding of mammalian milk microbiome evolution. A broader study of milk microbiomes has the potential to inform animal care with relevance to ex situ endangered species., Lay Summary: Milk is an ancient adaptation that supports the growth and development of mammalian neonates and infants. Beyond its fundamental nutritional function, milk influences all aspects of neonatal development, especially immune function. All kinds of milks so far studied have contained a milk microbiome. In this review, we focus on what is known about the collection of bacterial members found in milk microbiomes. Milk microbiomes include members sourced from maternal and infant microbiomes and they appear to be influenced by maternal evolutionary history, diet, milk nutrients, and environment, as well as by random chance. Once a neonate begins nursing, microbes from milk colonize their gut and produce byproducts that influence their physiology, metabolism, and immune development. Empirical data on milk microbiomes outside of humans and model systems are sparse. Greater study of milk microbiomes across mammals will expand our understanding of mammalian evolution and improve the health of animals under human care.

Microbiome science has provided groundbreaking insights into human and animal health. Similarly, evolutionary medicine - the incorporation of eco-evolutionary concepts into primarily human medical theory and practice - is increasingly recognised for its novel perspectives on modern diseases. Studies of host-microbe relationships have been expanded beyond humans to include a wide range of animal taxa, adding new facets to our understanding of animal ecology, evolution, behaviour, and health. In this review, we propose that a broader application of evolutionary medicine, combined with microbiome science, can provide valuable and innovative perspectives on animal care and conservation. First, we draw on classic ecological principles, such as alternative stable states, to propose an eco-evolutionary framework for understanding variation in animal microbiomes and their role in animal health and wellbeing. With a focus on mammalian gut microbiomes, we apply this framework to populations of animals under human care, with particular relevance to the many animal species that suffer diseases linked to gut microbial dysfunction (e.g. gut distress and infection, autoimmune disorders, obesity). We discuss diet and microbial landscapes (i.e. the microbes in the animal's external environment), as two factors that are (i) proposed to represent evolutionary mismatches for captive animals, (ii) linked to gut microbiome structure and function, and (iii) potentially best understood from an evolutionary medicine perspective. Keeping within our evolutionary framework, we highlight the potential benefits - and pitfalls - of modern microbial therapies, such as pre- and probiotics, faecal microbiota transplants, and microbial rewilding. We discuss the limited, yet growing, empirical evidence for the use of microbial therapies to modulate animal gut microbiomes beneficially. Interspersed throughout, we propose 12 actionable steps, grounded in evolutionary medicine, that can be applied to practical animal care and management. We encourage that these actionable steps be paired with integration of eco-evolutionary perspectives into our definitions of appropriate animal care standards. The evolutionary perspectives proposed herein may be best appreciated when applied to the broad diversity of species under human care, rather than when solely focused on humans. We urge animal care professionals, veterinarians, nutritionists, scientists, and others to collaborate on these efforts, allowing for simultaneous care of animal patients and the generation of valuable empirical data., (© 2023 Cambridge Philosophical Society. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.)

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.

In mammalian neonates, milk consumption provides nutrients, growth factors, immune molecules, and microbes. Milk microbiomes are increasingly recognized for their roles in seeding infant gut microbiomes and priming immune development. However, milk microbiome variation within and among individuals remains under investigation. We used 16S rRNA gene sequencing to investigate factors shaping milk microbiomes in three captive great ape species: Gorilla gorilla gorilla (individuals, N = 4; samples, n = 29), Pongo abelii (N = 2; n = 16), and Pongo pygmaeus (N = 1; n = 9). We demonstrate variation among host species, over lactation, and between housing facilities. In phylogenetic community composition, milk microbiomes were distinct among the three ape species. We found only a few shared, abundant bacterial taxa and suggest that they likely serve functional roles. The diversity and community composition of milk microbiomes showed gradual changes over time in gorillas and the Bornean orangutan, which was detectable with our comprehensive sampling over lactation stages (> 300-day span). In gorillas, milk microbiomes differed between housing facilities, but were similar between dams within a facility. These results support the strong influence of evolutionary history in shaping milk microbiomes, but also indicate that more proximate cues from mother, offspring, and the environment affect the distribution of rarer microbial taxa., (© 2022. The Author(s).)

Host-associated microbiomes shape and are shaped by myriad processes that ultimately delineate their symbiotic functions. Whereas a host's stable traits, such as its lineage, relate to gross aspects of its microbiome structure, transient factors, such as its varying physiological state, relate to shorter term, structural variation. Our understanding of these relationships in primates derives principally from anthropoid studies and would benefit from a broader, comparative perspective. We thus examined the vaginal, labial and axillary microbiota of captive, female ring-tailed lemurs (Lemur catta) and Coquerel's sifakas (Propithecus coquereli), across an ovarian cycle, to better understand their relation to stable (e.g. species identity/mating system, body site) and transient (e.g. ovarian hormone concentration, forest access) host features. We used 16S amplicon sequencing to determine microbial composition and enzyme-linked immunosorbent assays to measure serum hormone concentrations. We found marked variation in microbiota diversity and community composition between lemur species and their body sites. Across both host species, microbial diversity was significantly correlated with ovarian hormone concentrations: negatively with progesterone and positively with estradiol. The hosts' differential forest access related to the diversity of environmental microbes, particularly in axillary microbiomes. Such transient endogenous and exogenous modulators have potential implications for host reproductive health and behavioral ecology., (© FEMS 2020.)

Research on animal microbiomes is increasingly aimed at determining the evolutionary and ecological factors that govern host-microbiome dynamics, which are invariably intertwined and potentially synergistic. We present three empirical studies related to this topic, each of which relies on the diversity of Malagasy lemurs (representing a total of 19 species) and the comparative approach applied across scales of analysis. In Study 1, we compare gut microbial membership across 14 species in the wild to test the relative importance of host phylogeny and feeding strategy in mediating microbiome structure. Whereas host phylogeny strongly predicted community composition, the same feeding strategies shared by distant relatives did not produce convergent microbial consortia, but rather shaped microbiomes in host lineage-specific ways, particularly in folivores. In Study 2, we compare 14 species of wild and captive folivores, frugivores, and omnivores, to highlight the importance of captive populations for advancing gut microbiome research. We show that the perturbational effect of captivity is mediated by host feeding strategy and can be mitigated, in part, by modified animal management. In Study 3, we examine various scent-gland microbiomes across three species in the wild or captivity and show them to vary by host species, sex, body site, and a proxy of social status. These rare data provide support for the bacterial fermentation hypothesis in olfactory signal production and implicate steroid hormones as mediators of microbial community structure. We conclude by discussing the role of scale in comparative microbial studies, the links between feeding strategy and host-microbiome coadaptation, the underappreciated benefits of captive populations for advancing conservation research, and the need to consider the entirety of an animal's microbiota. Ultimately, these studies will help move the field from exploratory to hypothesis-driven research., (© 2019 Wiley Periodicals, Inc.)