Trade-Offs among Immune Mechanisms: Bacterial-Challenged ISpodoptera frugiperda/I Larvae Reduce Nodulation Reactions during Behavioral Fever

• Published in: Insects (Basel, Switzerland) Switzerland), 2023-11, Vol.14 (11)
• Main Authors: Zhang, Lei, Goodman, Cynthia L, Ringbauer, Joseph A, Jiang, Xingfu, Lv, Weixiang, Xie, Dianjie, Reall, Tamra, Stanley, David
• Format: Article
• Language: English
• Subjects: Behavior; Biological research; Biology, Experimental; Fever; Hyperthermia; Immune system; Insects; Larvae; Mechanical properties; Moths; Physiological aspects
• ISSN: 2075-4450; 2075-4450
• DOI: 10.3390/insects14110864

Insect innate immunity is composed of cellular and humoral reactions to infections and invasions. Cellular immunity is the first response, launched immediately when an infection is detected and it involves direct interactions between hemocytes and infecting microbes. Some insect species respond to infection with behavioral fever by moving to warmer sites or increasing exposure to heat sources. We predicted that behavioral fevers, which entail changing postures with respect to the sun or moving to warmer locations, but not increasing metabolic rates as in mammalian fevers, would be a relatively low-cost immune function compared to the costs of replacing the many hemocytes lost in immune reactions. Based on this reasoning, we posed the hypothesis that hemocyte-based immunity is traded off for behavioral fevers in infected larvae of the fall armyworm, Spodoptera frugiperda, when they can fever. Here, we report that infected larvae that were allowed to fever produced far fewer nodules compared to controls that were not allowed to 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 expe