Maternal effects on early-life gut microbiome maturation in a wild nonhuman primate

Abstract

Early-life gut microbial colonization is an important process shaping host physiology, immunity and long-term health outcomes in humans and other animals. However, our understanding of this dynamic process remains poorly investigated in wild animals, where developmental mechanisms can be better understood within ecological and evolutionary relevant contexts. Using 16s rRNA amplicon sequencing on 525 fecal samples from a large cohort of infant and juvenile geladas (Theropithecus gelada), we characterized gut microbiome maturation during the first three years of life and assessed the role of maternal effects in shaping offspring microbiome assembly. Microbial diversity increased rapidly in the first months of life, followed by more gradual changes until weaning. As expected, changes in gut microbiome composition and function with increasing age reflected progressive dietary transitions: in early infancy when infants rely heavily on their mother’s milk, microbes that facilitate milk glycans and lactose utilization dominated, while later in development as graminoids are progressively introduced into the diet, microbes that metabolize plant complex polysaccharides became dominant. Furthermore, the microbial community of nursing infants born to first-time (primiparous) mothers was more “milk-oriented” compared to similarly-aged infants born to experienced (multiparous) mothers. Comparisons of matched mother-offspring fecal samples to random dyads did not support vertical transmission as a conduit for these maternal effects, which instead could be explained by slower phenotypic development (and associated slower gut microbiome maturation) in infants born to first-time mothers. Together, our findings highlight the dynamic nature of gut colonization in early life and the role of maternal effects in modulating this trajectory in a wild primate.

Social and environmental predictors of gut microbiome age in wild baboons

“…We report three main findings. First, similar to humans and other animals (11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24) prediction may be more successful in baboons than humans for at least three reasons. First, signs of age in the baboon gut microbiome may be more consistent across hosts, perhaps because of the relatively homogeneity in host environments and lifestyles in baboons compared to humans (51).…”

“…One valuable marker of biological aging may lie in the composition and dynamics of the mammalian gut microbiome (7)(8)(9)(10). Age-related changes in gut microbiota are well documented in humans and other animals, and the gut microbiome has the potential to reflect a wide variety of aging processes for individual hosts (11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24). Mammalian gut microbiota interact with the immune, endocrine, nervous, and digestive systems, all of which change with age (25)(26)(27)(28).…”

Maternal transmission gives way to social transmission during gut microbiota assembly in wild mice

“…Although bifidobacteria were not identified as important for maternal transmission in this study, they were detected in the wood mouse gut microbiota. Other candidate maternally-transmitted taxa include Lactobacillus [48] and Bacteroides [11,27]. All these taxa are implicated in the degradation of milk oligosaccharides.…”

“…Studies attempting to isolate the impact of maternal transmission in wild systems, where environmental and social influences can freely operate, are rare (but see [26][27][28]), and among existing studies, the maternal transmission signal is often not robustly isolated from other confounding variables. A second challenge is that the influence of maternal transmission may vary with offspring age.…”