Host-associated beneficial gut microbiota boosts induced immunity and limits immune deployment costs in bumblebees

Ecological immunology posits that variation in host resistance to infection may be attributed partly to the ecological and evolutionary costs of immunity. While the deployment of immune defence is necessary to combat pathogenic infection, hosts pay energetic and other costs for activation. Host-associated beneficial microbiota have been shown to affect multiple host traits, including immunity, but how interactions with these microbial communities may mitigate the costs of immune activation remains an open question. For apid bees, including eusocial bumblebees, core members of the adult gut microbiota contribute to a variety of fitness-relevant traits and provide a key ecological and evolutionary relationship contributing to ecological success. Here we test the hypothesis that the host-associated microbiota provides benefits to bumblebee immunity, including the mitigation of the costs associated with inducible immune responses. Freshly emerged germ-free adult workers were supplemented with their native microbiota via experimental faecal transplants from nestmates or kept deprived of their native microbiota inoculum. We assessed functional measures of induced immunity and assessed the costs of non-pathogenic immune activation for survival. In support of our hypothesis, we find that microbiota supplementation strengthened functional antibacterial immunity. Moreover, although we observed a cost of immune activation for survival, the cost was much greater for bees deprived of their native gut microbiota compared to those supplemented. Thus, we provide evidence that in addition to other roles, the microbiota mitigates costs of immune deployment. This demonstrates a key role for host-associated microbiota in the realization of induced immune defence, and contributes more broadly to our understanding of microbiota-immune interactions in the context of ecological immunology.