Interactions between migration and immunity among oriental armyworm populations infected with the insect pathogenic fungus, Beauveria bassiana.

BACKGROUND: Migration and immunity are behavioral and physiological traits that protect organisms from environmental stressors or pathogen infection. Shifting from migration to residency has become more common in some wildlife populations owing to environmental changes. However, other biological shifts, such as interactions between migration and immunity among populations within a species are largely unexplored for many agricultural migratory pests. In the field, entomopathogenic fungi infection and transmission, particularly Beauveria bassiana, can cause reduced fitness and population declines across a broad range of insect species. RESULTS: Here, we investigated migration-immunity interactions between migrant and resident populations of the oriental armyworm, Mythimna separata, infected with B. bassiana (the sole fungus used in this work). We found that migratory M. separata exerted stronger pathogen resistance, faster development and lower pupal weight than residents. High-dose infections (5.0 × 105 and 5.0 × 106 conidia mL-1) led to seriously decreased reproductive capacity in migrants and residents. Low-dose infections (1.0 × 104 and 5.0 × 104 conidia mL-1) led to significantly increased host flight capacities. Consecutive flight tests showed that five flight nights inhibited the reproduction of paternal infected M. separata populations. The flights also led to far-reaching transgenerational impairment of larval development and immune defense among offspring populations. By contrast, two flight nights enhanced the reproductive capacities of both M. separata populations and did not exert negative transgenerational effects on offspring populations, which may facilitate migration. CONCLUSIONS: This study provides insights into interactions between migration and immunity among M. separata populations. These insights will guide development of future monitoring and management technologies of this pest. © 2024 Society of Chemical Industry.

Green manure application improves insect resistance of subsequent crops through the optimization of soil nutrients and rhizosphere microbiota.

Green manure (GM) enhances organic agriculture by improving soil quality and microbiota, yet its effects on plant resistance are unclear. Investigating the GM crop hairy vetch-maize rotation system, a widely adopted GM practice in China, we aimed to determine maize resistance to fall armyworm (FAW), Spodoptera frugiperda (Smith), a major pest. Greenhouse experiments with three fertilization treatments (chemical fertilizer, GM, and a combination) revealed that GM applications significantly improved maize resistance to FAW, evidenced by reduced larval feeding preference and pupal weight. GM also enriched soil nutrients, beneficial rhizobacteria, and resistance-related compounds, such as salicylic acid, jasmonic acid, and 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), in maize. The results suggest that GM-amended soils and microbial communities may have an underestimated role in regulating host plant adaptation to pests by increasing plant resistance. This study can provide information for developing and implementing environmentally friendly and sustainable cropping systems with enhanced resistance to pests and diseases.

Gut Microbiota Affects Host Fitness of Fall Armyworm Feeding on Different Food Types.

The fall armyworm (FAW), Spodoptera frugiperda, seriously threatens food and cash crops. Maize, wheat, and even rice damage by FAWs have been reported in many areas of China. It is urgent to clarify the mechanism which FAWs adapt to different feeding hosts and develop effective control technologies. Two-sex life tables and 16s rDNA sequencing were used to determine the host fitness and gut microbial diversity of FAWs when fed four different food types. Considering the life history parameters, pupa weight, and nutrient utilization indexes, the host fitness of FAWs when fed different food types changed in descending order as follows: artificial diet, maize, wheat, and rice. The gut microbial composition and the diversity of FAWs when fed different food types were significantly different, and those changes were driven by low-abundant bacteria. The gut microbes of FAWs that were fed with maize had the highest diversity. The functions of the gut microbes with significant abundance differences were enriched in nutrient and vitamin metabolism and other pathways that were closely related to host adaptation. Furthermore, we identified five genera (Acinetobacter, Variovorax, Pseudomonas, Bacillus, and Serratia) and one genus (Rahnella) that were positively and negatively correlated with the host fitness, respectively. This study revealed the possible role of gut microbes in the host adaptation of FAWs.

Transboundary migration of Loxostege sticticalis (Lepidoptera: Crambidae) among China, Russia and Mongolia.

BACKGROUND: The beet webworm, Loxostege sticticalis, a worldwide pest of many crops, performs a seasonal migration, causing periodic outbreaks in Asia, Europe and North America. Although long-distance migration is well documented in China, patterns of transboundary migration among China, Russia and Mongolia are largely unknown. We performed a phase analysis of L. sticticalis periodic outbreaks among three countries based on 30 years of historical population data, analyzed the wind systems during migration over boundary regions, and traced the migratory routes in a case study of outbreaks in 2008 by trajectory simulation. RESULTS: Highly synchronized outbreak years of L. sticticalis were observed between China and Mongolia, China and eastern Siberia, China and western Siberia, Mongolia and eastern Siberia, eastern Siberia and western Siberia from 1978 to 2008, indicating possible transboundary migration between these regions. Winds at 300-600 m altitude, where adult migration usually occurs, also showed a high probability of northwestern winds in Haila'er (China), Chita (Russia) and Choybalsan (Mongolia), favoring successful adult migration from these areas to northern and northeastern China. Back trajectory analysis further showed that the first-generation adults that caused the severe outbreak of second-generation larvae in 2008 originated from eastern Siberia, eastern Mongolia, and the boundary regions of China-Russia and China-Mongolia. CONCLUSION: Our findings demonstrated that the source of L. sticticalis outbreaks in northern China was closely related to the outbreaks in Siberia and Mongolia via long-distance transboundary windborne migration. This information will help guide international monitoring and management strategies against this notorious pest. © 2024 Society of Chemical Industry.

Immunological regulation by Toll-1 and Spätzle-4 in larval density-dependent prophylaxis of the oriental armyworm, Mythimna separata.

High population density has been shown to alter insect prophylactic immunity. Toll-Spätzle pathway performs a key function in insect innate immune response. To determine the role of Toll and Spätzle, two main components of Toll-Spätzle pathway, in the density-dependent prophylaxis of Mythimna separata. We identified full-length cDNA encoding the Toll-1 and Spätzle-4 genes in M. separata (designed MsToll-1 and Ms Spätzle-4). Both MsToll-1 and MsSpätzle-4 were expressed throughout all developmental stages. MsToll-1 expression was highly in fat body and brain and MsSpätzle-4 was highly expressed in brain and Malpighian tubule. With increased larval density, MsToll-1 expression was markedly up-regulated. MsSpätzle-4 expression was found to be raised in larvae that were fed in high density (5 and 10 larvae per jar). Co-immunoprecipitation assays demonstrated that MsToll-1 interacted with MsSpätzle-4. Immune-related genes transcriptions were considerably reduced in high-density larvae MsToll-1 (or MsSpätzle-4) was silenced by dsRNA injection. Meanwhile, a discernible reduction in the survival rate of the larvae exposed to Bacillus thuringiensis infection with silence of MsToll-1 (or MsSpätzle-4) was observed. This study implies that prophylactic immunity was influenced by crowded larvae via modulating the Toll-Spätzle pathway in M. separata and allow for a new understanding of into density-dependent prophylaxis in insects.

Effect of Juvenile Hormone on Worker Behavioral Transition in the Red Imported Fire Ant, Solenopsis invicta (Hymenoptera: Formicidae).

The division of labor among workers is a defining characteristic of social insects and plays a pivotal role in enhancing the competitive advantage of their colony. Juvenile hormone (JH) has long been hypothesized to be the essential driver in regulating the division of labor due to its ability to accelerate behavioral transitions in social insects, such as honeybees. The regulation of behavioral transitions by JH in the red imported fire ant (RIFA), Solenopsis invicta, a typical social pest, is unclear. Through video capture and analysis, we investigated the effects of the juvenile hormone analogue (JHA) methoprene on brood care, phototaxis behavior, and threat responsiveness of RIFA nurse workers. Our results showed that the JHA application significantly reduced the time and frequency of brood care behavior by nurse workers while increasing their walking distance and activity time in the light area. Additionally, the application of JHA made ants become excited, indicating a significant improvement in their activity level (movement distance, time, and speed). Furthermore, it was observed that the application of JHA did not affect the threat responsiveness of nurse workers towards stimuli (nestmates or non-nestmates). Our study demonstrates that the application of JHA reduced brood care behavior and enhanced phototaxis in nurse workers, which may reveal the role of JH in facilitating behavioral transitions in RIFA from intranidal tasks to extranidal activity. This study provides an experimental basis for further elucidating the mechanism underlying the division of labor in social insects.

Trade-Offs among Immune Mechanisms: Bacterial-Challenged Spodoptera frugiperda Larvae Reduce Nodulation Reactions during Behavioral Fever.

Insect innate immunity is composed of cellular and humoral reactions, the former acting via circulating hemocytes and the latter via immune signaling that lead to the production of antimicrobial peptides and phenol oxidase-driven melanization. Cellular immunity involves direct interactions between circulating hemocytes and invaders; it includes internalization and killing microbes (phagocytosis) and formation of bacterial-laden microaggregates which coalesce into nodules that are melanized and attached to body walls or organs. Nodulation can entail investing millions of hemocytes which must be replaced. We hypothesized that biologically costly hemocyte-based immunity is traded off for behavioral fevers in infected larvae of fall armyworms, Spodoptera frugiperda, that were allowed to fever. We tested our hypothesis by infecting larvae with the Gram-negative bacterium, Serratia marcescens, placing them in thermal gradients (TGs) and recording their selected body temperatures. While control larvae selected about 30 °C, the experimental larvae selected up 41 °C. We found that 4 h fevers, but not 2, 6 or 24 h fevers, led to increased larval survival. Co-injections of S. marcescens with the prostaglandin (PG) biosynthesis inhibitor indomethacin (INDO) blocked the fevers, which was reversed after co-injections of SM+INDO+Arachidonic acid, a precursor to PG biosynthesis, confirming that PGs mediate fever reactions. These and other experimental outcomes support our hypothesis that costly hemocyte-based immunity is traded off for behavioral fevers in infected larvae under appropriate conditions.

The Sex Ratio Indicates the Conclusion and Onset of Population Cycles in the Beet Webworm Loxostege sticticalis L. (Lepidoptera: Pyralidae).

Beet webworms, Loxostege sticticalis L. (Lepidoptera: Pyralidae), are one of the most destructive pest insects in northern China, and their populations outbreak periodically. Developing an indicator that defines the ending and beginning of the occurrence period cycle is urgent for the population forecast and theoretical study. The sex ratio can be a primary pathway through which species regulate population size. We measured the maximum mating potential of both females and males and the population net reproductive rate under different sex ratios (e.g., 3:1, 2:1, 1:1, 1:2, 1:3). The maximum mating frequency of males was 2.91 times that of females. The progeny contribution per mating decreased with increased mating times in males. The variation in population net reproductive rate affected by the sex ratio fits the parabolic curve analysis and peaked at 1.82 for females vs. males. Our results illustrate the quantitative connection phenomenon shown by the historical data: population outbreaks occur at a sex ratio of two or more and collapse at a sex rate lower than one. Simultaneously, the sex ratio may be utilized as a definite indicator for the beginning and end of the future occurrence cycle in the beet webworm.

Green Manure Crops as Food Source: Impact on the Performance of the Migratory Beet Webworm, Loxostege sticticalis (Lepidoptera: Pyralidae).

The application of green manure is crucial for achieving sustainable agriculture and animal husbandry, but pest management is often overlooked. Conducting a risk assessment for insect pests in green manure is essential. The beet webworm, Loxostege sticticalis, a polyphagous insect, is currently experiencing an outbreak in northern China, and represents a significant migratory pest. A two-sex life table and flight mill test approach was used to comprehensively evaluate the effects of three major legume green manure crops (Pisum sativam, Vicia sativa, and Vicia villosa) on the growth, development, fecundity, and flight ability of L. sticticalis in China. Our findings indicate that L. sticticalis cannot utilize V. villosa for generational development. L. sticticalis shows reduced performance on P. sativam and V. sativa compared to its suitable host Chenopodium album. However, both the population parameters (R0, r, λ, and T) and the population prediction results suggest that L. sticticalis can adapt to P. sativam and V. sativa. In the process of promoting green manure, careful consideration should be given to the selection of appropriate green manure varieties and the implementation of effective pest control measures during their planting. Our findings lay the groundwork for the promotion of green manure and implementation of an ecological management plan for L. sticticalis.

Genome-scale analysis of ABC transporter genes and characterization of the ABCC type transporter genes in the oriental armyworm, Mythimna separata (Walker).

The oriental armyworm Mythimna separata is a polyphagous, migratory corn pest in China and other Asian countries. Transgenic Bacillus thuringiensis (Bt) corn may effectively control this insect pest. Several reports have suggested that ATP-binding cassette (ABC) transporter proteins may act as receptors that bind Bt toxins. However, our knowledge about ABC transporter proteins in M. separata is limited. We identified 43 ABC transporter genes in the M. separata genome by bioinformatics prediction. Evolutionary tree analysis grouped these 43 genes into 8 subfamilies, ABCA to ABCH. Among the 13 ABCC subfamily genes, the transcript levels of MsABCC2 and MsABCC3 were upregulated. In addition, RT-qPCR analyses of these two potentials showed that both were predominantly expressed in the midgut tissue. Knock-down of MsABCC2, but not MsABCC3, decreased Cry1Ac susceptibility as indicated by increased larval weight and reduced larval mortality. This suggested that MsABCC2 might play a more important role in Cry1Ac toxicity and that it is a putative Cry1Ac receptor in M. separata. Together, these findings provide unique and valuable information for future elucidating of the role of ABC transporter genes in M. separata, which is highly valuable and important for the long-term application of Bt insecticidal protein.