Dynamic regulation and remodeling of the symbiotic midgut in stinkbugs: Short title: Dynamics of stinkbug symbiotic midgut.

Abstract

The establishment of mutualistic symbiosis with microorganisms has contributed to the ecological success and diversification of a wide range of insect lineages. In such systems, microbial partners are often stably inherited across generations and have co-evolved with their hosts over long evolutionary timescales. These intimate associations are often supported by specialized symbiotic organs that intracellularly or extracellularly harbor beneficial microorganisms. As an interface between hosts and symbionts, these symbiotic organs play a pivotal role in harnessing diverse symbiont functions, as represented by nutritional supplementation. However, what constitutes an optimal symbiotic state can vary across life stages, infection status, or environmental conditions. Recent studies have revealed that symbiotic organs undergo dynamic, life-stage-specific remodeling during the lifetime of a single insect, highlighting the remarkable flexibility and sophistication of insect-microbe interactions. This review synthesizes recent advances in our understanding of such dynamic regulation, with particular emphasis on the midgut symbiotic organ in stinkbugs. It illustrates how regional differentiation within the midgut enables diverse functions, including symbiont sorting, population control, and vertical transmission, beyond its primary role in nutritional interactions. Moreover, life stage-specific adjustments and remodeling of the symbiotic midgut flexibly accommodate potentially incompatible constraints arising from varying food sources, symbiont status, and host metabolic demands. Elucidating the dynamic nature of insect-microbe interactions across the entire life cycle will shed light on previously unexplored aspects of the evolutionary trajectories and adaptive mechanisms underlying mutualistic symbiosis.