Honey Bee Larval and Adult Microbiome Life Stages Are Effectively Decoupled with Vertical Transmission Overcoming Early Life Perturbations

Abstract

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 larvae 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. Most eusocial organisms appear to have evolved a workaround to this problem by sharing their communal microbiome across generations. However, whether this vertical microbiome transmission can overcome perturbations of the larval microbiome remains untested. Honey bees have a relatively simple, conserved, coevolved adult microbiome which is socially transmitted and affects many aspects of their biology. In contrast, larval microbiomes are more variable, with less clear roles. Here, we manipulated the gut microbiome of in vitro-reared larvae, and after pupation of the larvae, we inoculated the emerged bees with adult microbiome to test whether adult and larval microbiome stages may be coupled (e.g., through immune priming). 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. IMPORTANCE This work investigated host-microbiome interactions during a crucial developmental stage—the transition from larvae to adults, which is a challenge to both, the insect host and its microbiome. Using the honey bee as a tractable model system, we showed that microbiome transfer after emergence overrides any variation in the larvae, indicating that larval and adult microbiome stages are effectively decoupled. Together with the reliable vertical transfer in the eusocial system, this decoupling ensures that the adults are colonized with a consistent and derived microbiome after eclosion. Taken all together, our data provide additional support that the evolution of sociality, at least in the honey bee system tested here, is linked with host-microbiome relationships.