Host’s genetic background determines the outcome of reciprocal faecal transplantation on life-history traits and microbiome composition

Background Microbes play a role in fundamental ecological, chemical, and physiological processes of their host. Host life-history traits from defence to growth are therefore determined not only by abiotic environment and genotype but also by microbiota composition. However, the relative importance and interactive effects of these factors may vary between organisms. Such connections remain particularly elusive in Lepidoptera, which have been argued to lack a permanent microbiome and have microbiota primarily determined by their diet and environment. We tested the microbiome specificity and its influence on life-history traits of two colour genotypes of the wood tiger moth ( Arctia plantaginis ) that differ in several traits, including growth. All individuals were grown in the laboratory for several generations with standardised conditions. We analysed the bacterial community of the genotypes before and after a reciprocal frass (i.e., larval faeces) transplantation and followed growth rate, pupal mass, and the production of defensive secretion. Results After transplantation, the fast-growing genotype grew at a significantly slower rate compared to the controls, but the slow-growing genotype did not change its growth rate. The frass transplant also increased the volume of defensive secretions in the fast-growing genotype but did not affect pupal mass. Overall, the fast-growing genotype appeared more susceptible to the transplantation than the slow-growing genotype. Microbiome differences between the genotypes strongly suggest genotype-based selective filtering of bacteria from the diet and environment. A novel cluster of insect-associated Erysipelotrichaceae was exclusive to the fast-growing genotype, and specific Enterococcaceae were characteristic to the slow-growing genotype. These Enterococcaceae became more prevalent in the fast-growing genotype after the transplant, which suggests that the slower growth rate was potentially related to their presence. Conclusions We show that some genotype-specific life-history traits in a lepidopteran host can be reversed by a reciprocal frass transplantation. The results indicate that genotype-specific selective filtering can fine-tune the bacterial community at specific life stages, particularly the larval gut, even against a background of a highly variable community with stochastic assembly. Altogether, our findings suggest that the genotype of the host can influence its susceptibility to be colonized by microbiota with impact on key life-history traits.