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

Many eukaryotes harbor complex microbial communities that provide significant benefits to the host. However, recent work demonstrates substantial variation in microbiota across hosts and over time, 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 red flour beetle Tribolium castaneum, a widespread pest of stored grain flour and a laboratory model organism. Across 5 years, the total load and composition of the bacterial community of laboratory beetle populations fluctuated dramatically, cycling between a few dominant taxa and hundreds of rare taxa. We show that this ecological drift is caused by a lack of maternal microbial transmission and large microbial load fluctuations in flour, which is the primary reservoir of microbial inocula. Newly hatched larvae (from eggs) and newly eclosed adults (from pupae) acquire microbes from ingested flour containing conspecific feces. The flour microbiome fluctuates with host population density and stage structure, with larval feces increasing microbial load and antimicrobial secretions from adults decreasing it. Periodic flour replacement during population maintenance also dramatically decreases flour bacterial load, contributing to stochasticity in microbial colonization. The resulting drift was associated with unstable fitness benefits for beetles, though we cannot disentangle cause vs. effect. Our work thus represents a case study of significant ecological drift even in a highly controlled laboratory environment. We suggest that such unstable microbial communities and variable host benefits may not be uncommon, and offer an opportunity to analyze early stages of the evolution and ecology of host-microbial interactions.