Effects of Elevated CO(2) Concentration on Host Adaptability and Chlorantraniliprole Susceptibility in Spodoptera frugiperda

SIMPLE SUMMARY: Elevated carbon dioxide concentrations (eCO(2)) have a significant direct effect on herbivorous insects during their host seeking and oviposition. On the other hand, eCO(2) could dramatically alter leaf chemistry of plants, especially in C3 plants (such as wheat), which in turn is likely to affect the population performance of insects that feed on the host plant. However, the effects of eCO(2) on host adaptability and insecticide resistance in the fall armyworm, Spodoptera frugiperda, are unclear. In this study, we demonstrate that elevated CO(2) concentrations increased the population performance of S. frugiperda on wheat and reduced the susceptibility of S. frugiperda to chlorantraniliprole by inducing the expression of detoxification enzyme genes. This report warns that S. frugiperda may continue to be a major global pest through better host adaptation and increased insecticide resistance in the future as atmospheric CO(2) continues to rise. ABSTRACT: Elevated atmospheric carbon dioxide concentrations (eCO(2)) can affect both herbivorous insects and their host plants. The fall armyworm (FAW), Spodoptera frugiperda, is a highly polyphagous agricultural pest that may attack more than 350 host plant species and has developed resistance to both conventional and novel-action insecticides. However, the effects of eCO(2) on host adaptability and insecticide resistance of FAW are unclear. We hypothesized that eCO(2) might affect insecticide resistance of FAW by affecting its host plants. To test this hypothesis, we investigated the effect of eCO(2) on (1) FAW’s susceptibility to chlorantraniliprole after feeding on wheat, (2) FAW’s population performance traits (including the growth and reproduction), and (3) changes in gene expression in the FAW by transcriptome sequencing. The toxicity of chlorantraniliprole against the FAW under eCO(2) (800 µL/L) stress showed that the LC(50) values were 2.40, 2.06, and 1.46 times the values at the ambient CO(2) concentration (400 µL/L, aCO(2)) for the three generations, respectively. Under eCO(2), the life span of pupae and adults and the total number of generations were significantly shorter than the FAW under aCO(2). Compared to the aCO(2) treatment, the weights of the 3rd and 4th instar larvae and pupae of FAW under eCO(2) were significantly heavier. Transcriptome sequencing results showed that more than 79 detoxification enzyme genes in FAW were upregulated under eCO(2) treatment, including 40 P450, 5 CarE, 17 ABC, and 7 UGT genes. Our results showed that eCO(2) increased the population performance of FAW on wheat and reduced its susceptibility to chlorantraniliprole by inducing the expression of detoxification enzyme genes. This study has important implications for assessing the damage of FAW in the future under the environment of increasing atmospheric CO(2) concentration.