The gut bacterial community affects immunity but not metabolism in a specialist herbivorous butterfly

Background Many plant tissues are not resources of optimal nutritious value. They often lack essential nutritive elements and may contain a range of secondary toxic compounds. As nutritional imbalance in food intake may affect the performances of herbivores, the latter have evolved a variety of physiological mechanisms to cope with the challenges of digesting their plant-based diet. Some of these strategies involve living in association with symbiotic microbes that promote the digestion and detoxification of plant compounds, or supply their host with essential nutrients missing from the plant diet. In Lepidoptera, a growing body of evidence has, however, recently challenged the idea that herbivores are nutritionally dependent on their gut microbial community. It is suggested that many of the herbivorous species may not host a resident microbial community, but rather a transient one, acquired from their environment and diet. Results By coupling comparative meta-barcoding, immune gene expression and metabolomics analyses with experimental manipulation of the gut microbial community of pre-diapause larvae of the Glanville fritillary butterfly ( Melitaea cinxia, L.), we tested whether the larvae host a gut microbial community that supports growth and survival, and modulates metabolism and immunity during the early stages of development. We successfully altered this microbiota through antibiotic treatments, and consecutively restored it through fecal transplants from conspecifics. Under laboratory conditions, Firmicutes dominated the bacterial microbiota associated with the gut and frass of non-treated larvae, even though these Gram-positive bacteria were not found in association with the host plant, Plantago lanceolata . Furthermore our study suggests that the microbiota is involved in the up-regulation of an antimicrobial peptide, but did not affect the life-history traits or the metabolism of early instars larvae. Conclusions This study confirms the poor impact of the microbiota on diverse life history traits of yet another Lepidoptera species. However, it also suggests that potential eco-evolutionary host-symbiont strategies that take place in the gut of herbivorous butterfly hosts might have been disregarded, particularly how the microbiota may affect the host immune system homeostasis.