In vertebrates, it is well documented that the parental consumption of high-fat diet increases the risk of Attention-Deficit Hyperactivity Disorder (ADHD) in offspring. While insects have long been used as popular study organisms in various biological research, few studies have explored how the nutritional quality of parental diet affects offspring behavioral phenotypes associated with ADHD in insects. Here we used the bean bug, Riptortus pedestris (Hemiptera: Alydidae), as a study organism to test the effect of parental high-fat diet on offspring hyperactivity, impulsivity, and diffuse attention, which are widely held as the three core symptoms of ADHD in vertebrates. Peanut was used as the high-fat diet while soybean was the control. Parental high-fat diet consumption induced hyperactivity in R. pedestris offspring. Compared to the controls, the hyperactive offspring of parents fed on high-fat diet were behaviorally more impulsive and less attentive, as they were found to be highly attracted to visual stimuli but losing attention easily. Collectively, these results provide the experimental evidence that the parental consumption of high-fat diet results in increased hyperactivity, impulsivity, and diffuse attention in an insect. This study implies that the well-known association between parental high-fat diet and offspring ADHD is conserved across the tree of life and opens up the new horizons that insects can arise as novel and feasible models for studying the mechanism and evolution of this common neurodevelopmental disorder in humans.

Riptortus pedestris is known to acquire their symbiotic bacteria, Caballeronia insecticola, from soil environments in every generation. The symbionts have been demonstrated to affect behavioral and physiological traits of the host insect such as the enhancement of development. In particular, symbiotic effects on female adults could directly entail changes in their population growth. Therefore, we investigated a suite of symbiotic effects of C. insecticola on behaviors and fitness-related parameters of female R. pedestris. Overall, symbiotic females showed an behavioral enhancement in both feeding efficacy and movement capacity including walking and flight. In addition, the survival rates under exposure to overwintering conditions and insecticide resistance level were significantly higher in symbiotic females than the aposymbiotic. Finally, although symbiotic females exhibited shorter longevity, their fecundity was found higher compared to the apo-symbiotic.

The choice of suitable companion plants is crucial for enhancing pest management strategies in agricultural fields. Riptortus pedestris, an important agricultural pest, has drawn attention for its serious damage on soybean. To identify an ideal companion plant for soybean, we investigated the pest’s behavioral patterns when exposed to corn seedlings in laboratory. Series of choice experiments were conducted for 4th instar nymphs and unmated female adults of R. pedestris when presented with corn and/or soybean pot against soybean or blank pot. In 4th instar nymphs, 56% preferred the treatment of corn pot plus soybean pot over soybean alone pot while 69% of unmated female adults preferred the same combination. These findings provide valuable insights into the behavior of this insect pest, which could be beneficial for establishing polycultures in agricultural fields.

Riptortus pedestris has established symbiotic interactions with specific bacteria from soil environment in every generations. The soil environment is extremely heterogeneous with microbial diversity, suggesting that bacterial composition of the R. pedestris can be affected by surrounding environments. Therefore, we investigated spatiotemporal variation of bacterial communities in wild R. pedestris collected from five mainland areas and Jeju Island in South Korea across insect generations. Among the 390 R. pedestris adults collected, we detected a total of 28 bacterial genera from the symbiotic region of insects. Among the bacterial genera, genus Caballeronia bacteria was the most abundantly detected regardless of sampling site and generation. Nevertheless, bacterial richness varied among the insect generations with 10 genera detected in overwintered generation, 15 genera in the 1st generation and 18 genera in the 2nd generation. Moreover, we found five bacterial genera that were exclusively detected from the Jeju island compared to the mainland areas surveyed.

Nutrient acquisition by insect herbivores affect all aspect of the the lifespan of individauls. For seed-sucking insect herbivores, they face challenges with nutrient acquisition due to requirement for extra-oral digestion of seed contents into a readily-ingestible state. In this study, we demonstrated environmentally-transmitted Caballeronia insecticola allow seed-sucking R. pedestris to overcome challenges with extra-oral digestion. Through the evaluation, first, we found symbiotic insects exhibited enhanced feeding efficiency by consuming significantly larger amount of food per feeding attempt compared to apo-symbiotic insects (P<0.05). Then, we observed feeding behavior modification in the symbiotic insects from the behavior tracking evaluation. Symbiotic insects displayed dichotomic behavior which can be generally divided into early focused feeding and later subdued resting periods. By contrast, apo-symbiotic insects displayed unordered behavior by frequent switches between feeding and walking behavior.

Many insects form mutualistic relationships with microbial symbionts, crucial for their physiological processes. The bean bug, Riptortus pedestris, establishes a unique gut symbiosis with the genus Caballeronia and consistently acquires these symbionts from surrounding soil with each generation. As a result, the bean bug unavoidably consumes a variety of environmental microbes, including potential pathogens. To address this, the bean bug has developed a specialized organ in its midgut that selectively filters out non-symbiotic microbes, thereby preventing contamination of its symbiotic organ. In this study, we identified a pathogenic strain from the genus Burkholderia that lethally affects the bean bug post-invasion of the symbiotic organ. This pathogen employs a strategy of mimicking the motility of native symbionts to infiltrate the symbiont sorting organ and displays a pronounced resistance against antimicrobial agents produced by the host. Upon establishing itself in the symbiotic organ, the pathogen breaches the midgut cells, leading to host mortality, and subsequently disperses into the external environment. Our findings unveil a cunning pathogenic tactic that exploits the mimicry of native symbionts within an insect's symbiotic framework.