Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle.

Animals engage in a plethora of mutualistic interactions with microorganisms that can confer various benefits to their host but can also incur context-dependent costs. The sawtoothed grain beetle Oryzaephilus surinamensis harbors nutritional, intracellular Bacteroidetes bacteria that supplement precursors for the cuticle synthesis and thereby enhance desiccation resistance of its host. Experimental elimination of the symbiont impairs cuticle formation and reduces fitness under desiccation stress but does not disrupt the host's life cycle. For this study, we first demonstrated that symbiont populations showed the strongest growth at the end of metamorphosis and then declined continuously in males, but not in females. The symbiont loss neither impacted the development time until adulthood nor adult mortality or lifespan. Furthermore, lifetime reproduction was not influenced by the symbiont presence. However, symbiotic females started to reproduce almost two weeks later than aposymbiotic ones. Thus, symbiont presence incurs a metabolic and context-dependent fitness cost to females, probably due to a nutrient allocation trade-off between symbiont growth and sexual maturation. The O. surinamensis symbiosis thereby represents an experimentally amenable system to study eco-evolutionary dynamics under variable selection pressures.

Ancient symbiosis confers desiccation resistance to stored grain pest beetles.

Microbial symbionts of insects provide a range of ecological traits to their hosts that are beneficial in the context of biotic interactions. However, little is known about insect symbiont-mediated adaptation to the abiotic environment, for example, temperature and humidity. Here, we report on an ancient clade of intracellular, bacteriome-located Bacteroidetes symbionts that are associated with grain and wood pest beetles of the phylogenetically distant families Silvanidae and Bostrichidae. In the saw-toothed grain beetle Oryzaephilus surinamensis, we demonstrate that the symbionts affect cuticle thickness, melanization and hydrocarbon profile, enhancing desiccation resistance and thereby strongly improving fitness under dry conditions. Together with earlier observations on symbiont contributions to cuticle biosynthesis in weevils, our findings indicate that convergent acquisitions of bacterial mutualists represented key adaptations enabling diverse pest beetle groups to survive and proliferate under the low ambient humidity that characterizes dry grain storage facilities.