Multi-Omics Reveals the Effect of Population Density on the Phenotype, Transcriptome and Metabolome of Mythimna separata

SIMPLE SUMMARY: Mythimna separata living in the environment with high population density show characteristics of melanization and overeating and cause serious damage to crops. In order to explore the impact of population density on M. separata, we studied the gene expression and metabolite accumulation of M. separata under different population densities through transcriptome and metabolome analysis. The results showed that the insulin-like signaling pathway influences the phase change of M. separata. Compared with solitary M. separata, the gregarious type had a faster energy consumption rate and stronger protein digestion and absorption capacity, while the transcription and translation processes were inhibited. This study explains the molecular mechanism of the phase change and the overeating behavior of M. separata under high population density. ABSTRACT: Population-density-dependent polymorphism is important in the biology of some agricultural pests. The oriental armyworm (Mythimna separata) is a lepidopteran pest (family Noctuidae). As the population density increases, its body color becomes darker, and the insect eats more and causes greater damage to crops. The molecular mechanisms underlying this phase change are not fully clear. Here, we used transcriptomic and metabolomic methods to study the effect of population density on the differentiation of second-day sixth instar M. separata larvae. The transcriptomic analysis identified 1148 differentially expressed genes (DEGs) in gregarious-type (i.e., high-population-density) armyworms compared with solitary-type (low-population-density) armyworms; 481 and 667 genes were up- and downregulated, respectively. The metabolomic analysis identified 137 differentially accumulated metabolites (DAMs), including 59 upregulated and 78 downregulated. The analysis of DEGs and DAMs showed that activation of the insulin-like signaling pathway promotes the melanization of gregarious armyworms and accelerates the decomposition of saccharides, which promotes the gregarious type to take in more food. The gregarious type is more capable of digesting and absorbing proteins and decreases energy consumption by inhibiting transcription and translation processes. The phase change traits of the armyworm are thus attributable to plasticity of its energy metabolism. These data broaden our understanding of the molecular mechanisms of insect-density-dependent polymorphism.