Abstract

A large body of ongoing research focuses on understanding the mechanisms and processes underlying host-microbiome interactions, and predicting their ecological and evolutionary outcomes. To draw general conclusions about such interactions and understand how they are established, we must synthesize information from a diverse set of species. We analysed the microbiome of an important insect model–the red flour beetle Tribolium castaneum–which is a widespread generalist pest of stored cereals. The beetles complete their entire life cycle in flour, which thus serves multiple functions: habitat, food, and a source of microbes. We determined key factors that shape the T. castaneum microbiome, established protocols to manipulate it, and tested its consequences for host fitness. We show that the T. castaneum microbiome is derived from flour-acquired microbes, and varies as a function of (flour) resource and beetle density. Beetles gain multiple fitness benefits from their microbiome, such as higher fecundity, egg survival, and lifespan; and reduced cannibalism. In contrast, the microbiome has a limited effect on development rate, and does not enhance pathogen resistance. Importantly, the benefits are derived only from microbes in the ancestral resource (wheat flour), and not from novel resources such as finger millet, sorghum, and corn. Notably, the microbiome is not essential for beetle survival and development under any of the tested conditions. Thus, the red flour beetle is a tractable model system to understand the ecology, evolution and mechanisms of host-microbiome interactions, while closely mimicking the host species’ natural niche.

Highlights

  • We first analysed the microbiome of wheat flour and flour beetles reared in wheat flour

  • Fresh wheat flour had distinct dominant OTUs from conditioned flour, which was in turn more similar to the dominant taxa in beetles (Fig 1A for individual samples; Fig 1B for averages)

  • The most dominant taxa in wheat flour samples belonged to the family Sphingomonadales and the family Enterobacteriaceae

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Summary

Introduction

Most animals harbor specific microbes that alter various aspects of their biology, ranging from development to behavior and reproduction [1–3]. To harness host-associated microbiomes for practical applications such as improving host health [4], we need to better understand the factors that shape the establishment and maintenance of diverse host-microbiome relationships. Insects represent one of the best-studied animals in this context, with a large number of studies showing that insect-microbiome interactions are shaped by host taxonomy, host diet, and environmental factors [5–8]. Flour beetle microbiome had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

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