Honey bee larval and adult microbiome life stages are effectively decoupled with vertical transmission overcoming early life perturbations

Microbiomes provide a range of benefits to their hosts which can lead to the coevolution of a joint ecological niche. However, holometabolous insects, some of the most successful organisms on Earth, occupy different niches throughout development, with larva and adults being physiologically and morphologically highly distinct. Furthermore, transition between the stages usually involves the loss of the gut microbiome since the gut is remodeled during pupation. We here tested whether vertical microbiome transmission can overcome perturbations of the larval microbiome in honey bees (Apis mellifera). We manipulated the gut microbiome of in vitro reared larvae and after pupation inoculated the emerged bees with adult microbiome to test whether adult and larval microbiome stages may be coupled (e.g., through immune priming). We performed 16S ampliconsequencing to describe the bacterial community and mRNA sequencing to check for gene expression differences in larval as well as adult treatments. Larval treatments differed in bacterial composition and abundance, depending on diet, which also drove larval gene expression. Nonetheless, adults converged on the typical core taxa and showed limited gene expression variation. This work demonstrates that honey bee adult and larval stages are effectively microbiologically decoupled, and the core adult microbiome is remarkably stable to early developmental perturbations. Combined with the transmission of the microbiome in early adulthood, this allows the formation of long-term host-microbiome associations.