Evolution and Functional Potential of Gut Microbiota in Honeybees: A Comparative Metagenomic Approach

Studying gut microbiota evolution across animals is crucial for understanding microbiome ecology and evolution. However, this is hampered by the lack of high-resolution genomic data, especially from natural systems. Honeybees, with their specialized gut microbiota and well-known host ecology and evolutionary history, offer an ideal system for studying this evolution. Using shotgun metagenomics on 200 honeybee workers from five species, we recovered thousands of metagenome-assembled genomes, identifying several novel bacterial species.

Our analysis revealed that microbial communities were mainly host-specific. Yet, we found specialist and generalist bacteria, even among bacterial species within the same genera, with notable variation between host species. Intriguingly, some generalists exhibited host-specificity only at the strain level, suggesting recent host-switch events. Contrary to expectations, we found no evidence of co-diversification between honeybee species and their gut microbiota. Instead, the gut microbiota displayed dynamic patterns of gains, losses, and replacements that could influence key functional traits, such as the degradation of pollen-derived pectin—an important process for honeybee nutrition and health.

These findings advance our understanding of host specificity in gut microbiota-host associations and show that ancient interactions can be maintained in the absence of co-diversification. We also highlight the importance of other factors, such as host distribution and ecology, in driving microbiome diversity. Beyond offering new insights into gut microbiota evolution, our study uncovers the functional potential of the gut microbiota of Asian honeybees, which remained underexplored despite the crucial role of these pollinators in their native ecosystem.