Ecological drift in the flour beetle microbiome and associated instability in host benefits

Abstract Recent work demonstrates substantial variation in host-associated microbiota, though the causes and consequences of this instability are not always clear. We describe large temporal, among-individual and across-population variation in the microbiome of the flour beetle Tribolium castaneum, a widespread pest of stored grain flour. Across 5 years, the load and composition of the bacterial community of laboratory beetles fluctuated dramatically, caused by a lack of maternal transmission and large microbial load fluctuations in flour—the primary reservoir of microbial inocula. Newly hatched larvae and newly eclosed adults acquire microbes from ingested flour containing conspecific faeces. The flour microbiome fluctuates with host population density and stage structure, with larval faeces increasing microbial load and antimicrobial secretions from adults decreasing it. Periodic flour replacement during population maintenance dramatically decreases flour bacterial load, contributing to stochasticity in microbial colonization. The resulting drift was associated with unstable host fitness benefits, though we cannot disentangle cause and effect. Our work thus represents a case of significant ecological drift even in a highly controlled laboratory environment. We suggest that such unstable microbial communities and host benefits may be common, and offer an opportunity to analyse early stages of the establishment of host-microbial interactions.