Gut microbiome disturbances of altricial Blue and Great tit nestlings are countered by continuous microbial inoculations from parental microbiomes

Abstract

Gut microbial communities are complex and heterogeneous and play critical roles for animal hosts. Early-life disruptions to microbiome establishment can negatively impact host fitness and development. However, the consequences of such early-life disruptions are unknown in wild birds. To help fill this gap, after validating the disruptive influence of antibiotic and probiotic treatments on the gut microbiome in adult Great tits (Parus major) (efficacy experiment), we investigated the effect of continuous early-life gut microbiome disruptions on the establishment and development of gut communities in wild Great and Blue tit (Cyanistes caeruleus) nestlings (field experiment). Despite negative impacts of treatments on microbial alpha and beta diversities in the efficacy experiment, treatment did not affect the composition of nestling microbiomes in the field experiment. Independent of treatment, nestling gut microbiomes of both species grouped by brood, sharing high numbers of bacterial taxa with both the nest environment and their mother. The distance between nests increased inter-brood microbiome dissimilarity, but only in Great tits, indicating species-specific influence of environment on microbiomes. The strong maternal effect, driven by continuous recolonization from the nest environment and vertical transfer of microbes during feeding thus appear to provide resilience towards early-life disruptions in nestling gut microbiomes.

Individual variation in the avian gut microbiota: The influence of host state and environmental heterogeneity

“…If the nestling's gut microbiota were directly determined by their parents' microbiota, then we should have seen a positive correlation between parent and offspring gut microbiota. Similarly, mothers and offspring are expected to share more similar ASV's than nonoffspring, as has been found in other studies (Diez‐Méndez et al, 2022, preprint; Grosser et al, 2019). However we did not see this in our data, lending support to the dominant influence of local environmental factors in nestlings (Teyssier, Lens, et al, 2018), which we suggest is most probably linked to local food availability.…”

“…However we did not see this in our data, lending support to the dominant influence of local environmental factors in nestlings (Teyssier, Lens, et al, 2018), which we suggest is most probably linked to local food availability. In line with this interpretation, experimental disruption of the microbiota in nestling great tits and blue tits did not have any lasting effect (Diez‐Méndez et al, 2022, preprint); the authors provide indirect evidence to suggest that this was most probably due to the parents replenishing the microbiota through feeding and continuous recolonisation from the nest environment. We note that our results do not preclude microbial transfer between parents and nestlings, just that the community and diversity metrics measured here are not comparable between parents and offspring.…”

Disentangling relationships between physiology, morphology, diet, and gut microbial diversity in American kestrel nestlings

“…Birds hatch with little to no gut microbial diversity (Grond et al 2017, Trevelline et al 2018) and then slowly inoculate their gut microbial communities via horizontal transmission with the nest environment and prey items (Ballou et al 2016, van Veelan et al 2020). Even when nestling gut microbial communities are disrupted with antibiotics or probiotics, continuous recolonization from the nest environment and vertical transfer of microbes during feeding washes out any sign of disturbance to the nestling microbial communities (Diez‐Méndez et al 2022).…”

Microbiome assembly and maintenance across the lifespan of bumble bee workers

“…There are many potential proximate causes of microbiome stability in old age. Communal living may buffer microbiome disturbances by providing a continuous source of microbes that can be transmitted between individuals or via a shared social environment, such as a nest (Diez‐Méndez et al, 2022 ; Moeller et al, 2018 ; Tung et al, 2015 ; Yarlagadda et al, 2021 ). In our experiment, diet was kept constant, and bees appear to consume pollen even in old age based on the presence of plant DNA in metagenomes (Figure S7 ) and observations of gut colour.…”