Behavioral changes induced by gut symbionts confer adaptive traits to host insects in tri-trophic interactions

Insect herbivores face the challenge of balancing foraging and predator avoidance throughout their life span. This challenge leads herbivores to develop diverse strategies to maintain this balance, especially by establishing symbiotic interactions with microorganisms. There is emerging evidence that symbiotic microorganisms provide beneficial effects on nutrient utilization and defensive against pathogens, which can serve as adaptive traits for herbivore with regard to either foraging or predation avoidance. However, there is limited knowledge regarding how symbiont acquisition alters the behavior of host, which can affect both foraging and predation avoidance of host insect. In this study, we revealed that the symbiotic bacteria, Caballeronia insecticola provides an adaptive trait for foraging and predation avoidance of host bean bug, Riptortus pedestris (Hemiptera: Alydidae), by modulating the behavior of its host insect herbivore. We observed that acquisition of symbiotic microbe induced the host bean bug to display intense and efficient feeding behavior followed by subdued movement. In contrast, the bean bug without the symbiont (apo-symbiotic) displayed unordered and frequent switches between feeding and walking behaviors. Through the intense and efficient feeding behavior, symbiotic insects exhibited higher weight gain rates than apo-symbiotic insects during the early period of each nymphal stage, leading to enhanced development and growth. Furthermore, the subdued movement after intense feeding significantly reduced the predation risk of symbiotic insect compared to apo-symbiotic insects. Our results demonstrated a novel mechanism by which insect-microbe interactions confer adaptive traits for both foraging and predation avoidance by modulating the behavior of host herbivores.