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

Abstract

Early-life microbial colonization is an important process shaping host physiology,^1-3 immunity,^4-6 and long-term health outcomes^7-10 in humans. However, our understanding of this dynamic process remains poorly investigated in wild animals,^11-13 where developmental mechanisms can be better understood within ecological and evolutionarily relevant contexts.^11,12 Using one of the largest developmental datasets on a wild primate-the gelada (Theropithecus gelada)-we used 16S rRNA amplicon sequencing to characterize gut microbiota maturation during the first 3 years of life and assessed the role of maternal effects in shaping offspring microbiota assembly. In contrast to recent data on chimpanzees, postnatal microbial colonization in geladas was highly similar to humans:¹⁴ microbial alpha diversity increased rapidly following birth, followed by gradual changes in composition until weaning. Dietary changes associated with weaning (from milk- to plant-based diet) were the main drivers of shifts in taxonomic composition and microbial predicted functional pathways. Maternal effects were also an important factor influencing the offspring gut microbiota. During nursing (<12 months), offspring of experienced (multi-time) mothers exhibited faster functional microbial maturation, likely reflecting the general faster developmental pace of infants born to these mothers. Following weaning (>18 months), the composition of the juvenile microbiota tended to be more similar to the maternal microbiota than to the microbiota of other adult females, highlighting that maternal effects may persist even after nursing cessation.^15,16 Together, our findings highlight the dynamic nature of early-life gut colonization and the role of maternal effects in shaping this trajectory in a wild primate.

Keywords: gelada; gut microbiome; maternal effects; maturation; primate; vertical transmission; weaning; wild microbiome.