Top-down and bottom-up landscape processes influence the formation of microbial partnerships in herbivorous insects

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Abstract
Many insects form intimate associations with microbial partners, spanning a continuum from obligate mutualisms to transient associations. These microbial partners confer a range of functional benefits, including protection from natural enemies, detoxification of plant secondary metabolites, and improved fitness. The prevalence and abundance of microbial symbionts can vary between insect populations, indicating that the insect-microbe relationship is influenced by external factors. However, little is known on the factors that determine the assembly, structure, and composition of the microbiome of herbivorous insects. We posit that the factors influencing the insect-microbe relationship occur at the landscape-scale, acting through a combination of bottom-up, top-down, and indirect effects between plants, herbivores, and their natural enemies. We test this in two agro-ecosystems by sampling individual insects from three sap-feeding and one leaf-chewing species. Our results explicitly show for the first time that habitat configurational complexity and the proportion of host-plant crop in the landscape, combined with natural enemy abundance, can act as direct and indirect drivers of microbial symbiosis in herbivorous insects. This highlights the wider implications landscape habitat and ecosystem structure has on species interactions across managed agricultural landscapes.
Funding Information
  • British Ecological Society (LRB20/1008)

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