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

Abstract

The mammalian gut microbiota influences a wide array of phenotypes and is considered a key determinant of fitness, yet knowledge about the transmission routes by which gut microbes colonise hosts in natural populations remains limited. Here, we use an intensively studied wild population of wood mice (Apodemus sylvaticus) to examine how vertical (maternal) and horizontal (social) transmission routes influence gut microbiota composition throughout life. We identify independent signals of maternal transmission (sharing of taxa between a mother and her offspring) and social transmission (sharing of taxa predicted by the social network), whose relative magnitudes shift as hosts age. In early life, gut microbiota composition is predicted to a similar extent by both maternal and social relationships, but by adulthood the impact of maternal transmission becomes undetectable, leaving only a signal of social transmission. By exploring which taxa drive the maternal transmission signal, we further identify a candidate maternally-transmitted bacterial family in wood mice, the Lactobacillaceae. Overall, our findings suggest a shifting transmission landscape for wild mice, with a mother's influence on microbiota composition waning as offspring age, while the impact of social contacts remains strong and consistent.

Social and environmental transmission spread different sets of gut microbes in wild mice

“…Consistent with the idea that maternal and social transmission may spread similar bacteria, our recent study on wood mice found that as young mice age, maternal transmission processes are gradually replaced by social transmission processes (65), with maternal and social effect in these mice both driven by microbes in the same family Muribaculaceae (35,65).…”

Environmental effects rather than relatedness determine gut microbiome similarity in a social mammal

“…Cross‐fostering in this study took place at an early stage of life. For young mammals, vertical transmission of microbes is an important route of microbe colonization of the gut (Ferretti et al, 2018; Moeller et al, 2018; Wanelik et al, 2023). Potential effects of relatedness in our study could therefore be explained by both vertical transmission and host genotype.…”

Subspecies divergence, hybridisation and the spatial environment shape phylosymbiosis in the microbiome of house mice

“…To test the effects of spatial and temporal distances, species barriers, and hybridisation on the β-diversity of the intestinal community, we applied Bayesian generalised linear multilevel models using the Markov chain Monte Carlo algorithm No-U-Turn Sampler (NUTS) [54] implemented in Stan through the “brms” R package v. 2.19.0 [55]. The models had intestinal community similarity as the response, and we modelled all possible pairwise distances among mice (excluding comparisons between the same individuals) as previously described [31, 32]. We used a multimembership random effects framework that allows us to account for the individuals in each pairwise comparison (e.g., Individual A, Individual B).…”

“…Additionally, species composition as a response is a complex multivariate measure [30]. The analysis we present here is based on the realisation that effects on the community compositions can be tested elegantly using pairwise differences between samples as response (beta-diversity) and accounting for repeated comparisons using random effects in Bayesian multilevel models [31, 32]. These models require the predictor variables to be expressed in the same way as the response, as distances or other measures reflecting a compared pair.…”