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

Abstract

Plant tissues 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 Lepidopteran species may not host a resident microbial community, but rather a transient one, acquired from their environment and diet. Studies directly testing these hypotheses are however scarce and come from an even more limited number of species. By coupling comparative metabarcoding, immune gene expression, and metabolomics analyses with experimental manipulation of the gut microbial community of prediapause larvae of the Glanville fritillary butterfly (Melitaea cinxia, L.), we tested whether the gut microbial community supports early larval growth and survival, or modulates metabolism or immunity during early stages of development. We successfully altered this microbiota through antibiotic treatments and consecutively restored it through fecal transplants from conspecifics. Our study suggests that although the microbiota is involved in the up‐regulation of an antimicrobial peptide, it did not affect the life history traits or the metabolism of early instars larvae. 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.

Editorial: Symbiosis in a Changing Environment

“…Furthermore, the role of microbial communities is severely debated in some species. For example, the gut microbiota of Lepidoptera larvae is thought to be transient and non-functional, rather than resident and of any benefit to the host (Hammer et al, 2017;Duplouy et al, 2020).…”

The Gut Microbiota Composition of Cnaphalocrocis medinalis and Their Predicted Contribution to Larval Nutrition

“…Due to the great difficulty in achieving aseptic rearing conditions, many studies use the method of incorporating antibiotics into diet to determine the biological function of gut bacteria ( Ignasiak and Maxwell, 2018 ; Koskinioti et al, 2019 ; Duplouy et al, 2020 ; Duan et al, 2021 ). The nutrition indices of RGR , RCR , ECI , and ECD were used to estimate the effect of food utilization.…”

“…Insect gut microbiomes differ between and within-host species and they often have multiple effects on insect biology ( Douglas, 2015 ; Voirol et al, 2018 ). To gain more insight into the interactions between symbiotic microorganism and their insect hosts, we need to study the gut bacterial diversity firstly ( Duplouy et al, 2020 ). In the present study, the diversity of gut bacteria in the fourth instar larvae of C. medinalis was analyzed by metagenomic sequencing.…”

Long‐term spatiotemporal genetic structure of an accidental parasitoid introduction, and local changes in prevalence of its associatedWolbachiasymbiont

“…Mesochorus cf. s tigmaticus wasps are however not known to carry Wolbachia , nor to vector the symbiont between hosts in the Åland population of their food web insect community (based on microbiota data from the butterfly host Duplouy et al, 2018, 2020, and from the screening of over N = 200 specimens of both the butterfly and the hyperparasitoid species by the first author, Duplouy, personal observation).…”