Ecological drift drives microbiome variation in the red flour beetle

Many eukaryotes harbor diverse and complex microbial communities that provide significant benefits to the host. However, recent work demonstrates substantial variation in microbial communities across hosts and over time, and the causes 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 a 5-year period, 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. Our experiments show that this ecological drift is caused by a lack of maternal microbial transmission and large microbial load fluctuations in the primary reservoir of microbial inocula: the flour. Flour microbial load is important because newly hatched larvae (from eggs) and newly eclosed adults (from pupae) acquire microbes from ingested flour containing the fecal material of other individuals. The flour microbiome fluctuates depending on host population density and stage structure, with larval feces increasing microbial load, and antimicrobial secretions from mature adults decreasing it. Finally, periodic flour replacement during population maintenance also dramatically decreases flour bacterial load, contributing to stochasticity in microbial colonization. Our work thus represents a case study of significant and pervasive ecological drift even in a highly controlled laboratory environment. We suggest that such unstable microbial communities may not be uncommon, and can serve as good models to understand early stages of the evolution and ecology of host-microbial interactions.