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Abstract Plants possess a suite of traits that make them challenging to consume by insect herbivores. Plant tissues are recalcitrant, have low levels of protein, and may be well defended by chemicals. Insects use diverse strategies for overcoming these barriers, including co‐opting metabolic activities from microbial associates. In this review, we discuss the co‐option of bacteria and fungi in the herbivore gut. We particularly focus upon chewing, folivorous insects (Coleoptera and Lepidoptera) and discuss the impacts of microbial co‐option on herbivore performance and plant responses. We suggest that there are two components to microbial co‐option: fixed and plastic relationships. Fixed relationships are involved in integral dietary functions and can be performed by microbial enzymes co‐opted into the genome or by stably transferred associates. In contrast, the majority of gut symbionts appear to be looser and perform more facultative, context‐dependent functions. This more plastic, variable co‐option of bacteria likely produces a greater number of insect phenotypes, which interact differently with plant hosts. By altering plant detection of herbivory or mediating insect interactions with plant defensive compounds, microbes can effectively improve herbivore performance in real time within and between generations.more » « less
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