Phylosymbiosis in the making: Host-associated microbiota and host gene expression profiles exhibit discordant timing of phylogenetic congruence over early mammalian development

Most animal species harbor distinct microbiomes that exhibit eco-evolutionary patterns termed phylosymbiosis, by which the composition of these communities reflect host evolutionary history. However, most studies documenting these patterns, especially in mammals, have been conducted at single time points in adult animals. Thus, the processes by which phylosymbiotic signals emerge during early mammalian life stages are unclear. Here, we compared gut microbial communities from pups of four species of Peromyscus mice (P. californicus, P. leucopus, P. polionotus, and P. maniculatus) bred in captivity, collecting samples from three developmental timepoints (birth, mid-weaning, and weaning). Further, we evaluated host gene expression in large intestine tissue and used a novel application of congruence to compare host gene expression profiles across developmental stages as a means to investigate potential mechanisms by which hosts select their microbiome. We find that Peromyscus pups are not born with phylosymbiotic large intestinal microbial communities, but that these signatures emerge halfway through the weaning period. Strikingly, the host gene expression profiles exhibit different trajectories, such that host transcriptomic profiles closely reflect host phylogeny at birth, but this pattern weakens over development. Finally, Peromyscus spp. exhibit a significant number of differentially expressed genes across all developmental stages, including some clusters of genes implicated in host-microbe interactions. Collectively, these data demonstrate complex community assembly processes in early mammalian development and establish Peromyscus spp. as a powerful model to explore how transcriptomic variation influences host selection and microbiota filtering.