Evolution, multifunctionality, and agricultural potential of insect microbiomes and the holobiont concept

Insect-associated microbiomes, as co-evolved members of the holobiont, play pivotal roles in host physiology, ecological resilience, and evolutionary innovation. This review synthesizes recent advances in understanding microbial symbionts' contributions to metabolic adaptation, insecticide detoxification, and immune modulation. Framed within hologenome theory—which posits host-microbe assemblages as units of natural selection—we explore co-evolutionary dynamics driving mutualistic specialization and adaptive plasticity. Cutting-edge tools like genome editing and metagenomics reveal how gut microbiota mediate cross-kingdom interactions, insecticide resistance, and reproductive fitness. Intriguingly, microbial symbionts can enhance host resistance through detoxification while sensitizing hosts to specific toxins, highlighting context-dependent trade-offs. Targeted manipulation of microbial consortia—via detoxification disruption or symbiont engineering—offers new avenues for sustainable pest control, though ecological risks demand rigorous biosafety protocols. A paradigm shift toward holobiont-centered models promises unified strategies for sustainable agriculture and biodiversity conservation in the Anthropocene.