Role of priority effects in the early-life assembly of the gut microbiota

Abstract

Understanding how microbial communities develop is essential for predicting and directing their future states. Ecological theory suggests that community development is often influenced by priority effects, in which the order and timing of species arrival determine how species affect one another. Priority effects can have long-lasting consequences, particularly if species arrival history varies during the early stage of community development, but their importance to the human gut microbiota and host health remains largely unknown. Here, we explore how priority effects might influence microbial communities in the gastrointestinal tract during early childhood and how the strength of priority effects can be estimated from the composition of the microbial species pool. We also discuss factors that alter microbial transmission, such as delivery mode, diet and parenting behaviours such as breastfeeding, which can influence the likelihood of priority effects. An improved knowledge of priority effects has the potential to inform microorganism-based therapies, such as prebiotics and probiotics, which are aimed at guiding the microbiota towards a healthy state.

The impact of colonization history on the composition of ecological systems

“…That is, colonization history can introduce priority effects, where the persistence of species depends on the order at which they join a given community. However, it remains unclear under which conditions can colonization history have the strongest impact on the assembly of ecological communities [12][13][14][15]. For example, are there any conditions under which colonization history will completely dominate community composition?…”

Vertical transmission of sponge microbiota is inconsistent and unfaithful

“…While this mixture of mechanisms likely reduces the strength and consistency of vertical transmission, it may have other benefits that increase the chances of dispersing larvae to settle and reach adulthood in diverse and varying environments. For example, which microbes first colonize the host strongly influence subsequent community succession and stability [80, 81, 82, 83].…”

Can the microbiome influence host evolutionary trajectories?

“…Environmental factors, like diet or climate, also substantially influence the reservoir of possible microbial partners, leading to changes in the microbiome independent of any host evolution [38][39][40] . Host phenotypes also may be more strongly shaped by distinct microbial variation early in life, but because microbial dynamics operate at shorter timescales than host generations, those relevant microbes may not be faithfully transmitted across host generations 8,41,42 . Such complexities muddle the inheritance of the microbiome, challenging how frequently the microbiome could influence host evolution [6][7][8][9]25 .…”

“…1). However, in other cases, stochastic variation and priority effects during microbial community assembly may create microbial variation between hosts 8,42,98 . Such an increase in microbial variation may increase phenotypic variation in host population, enabling more individuals to explore broader phenotypic spaces 99,100 (Fig.…”