Mating-Induced Common and Sex-Specific Behavioral, Transcriptional Changes in the Moth Fall Armyworm (Spodoptera frugiperda, Noctuidae, Lepidoptera) in Laboratory

SIMPLE SUMMARY: In this study, we found mating-induced sex-specific behavioral and transcriptional changes, and the transcriptional variation is consistent with postmating physiological and behavioral alteration in each sex. Virgin females and males showed high calling or courting behavior, whereas mated females and males showed very low calling or courting behavior. Mated females started to lay eggs at the beginning of the next night after the first mating. Obvious differences on female oviposition patterns were found between different mate treatments, suggesting that females may use a fertilization or oviposition strategy to obtain indirect genetic benefits. Differential expression analysis indicated that mating induced upregulation of many reproductive related genes and soma maintenance related genes in females. Mating in males also induced upregulation on soma maintenance related genes immediately after mating (0 h postmating), but induced downregulation on these genes after a period of time (6–24 h postmating). ABSTRACT: The intermediate process between mating and postmating behavioral changes in insects is still poorly known. Here, we studied mating-induced common and sex-specific behavioral and transcriptional changes in both sexes of Spodoptera frugiperda and tested whether the transcriptional changes are linked to postmating behavioral changes in each sex. A behavioral study showed that mating caused a temporary suppression of female calling and male courting behavior, and females did not lay eggs until the next day after the first mating. The significant differences on daily fecundity under the presence of males or not, and the same or novel males, suggest that females may intentionally retain eggs to be fertilized by novel males or to be fertilized competitively by different males. RNA sequencing in females revealed that there are more reproduction related GO (gene ontology) terms and KEGG (Kyoto encyclopedia of genes and genomes) pathways (mainly related to egg and zygote development) enriched to upregulated DEGs (differentially expressed genes) than to downregulated DEGs at 0 and 24 h postmating. In males, however, mating induced DEGs did not enrich any reproduction related terms/pathways, which may be because male reproductive bioinformatics is relatively limited in moths. Mating also induced upregulation on soma maintenance (such as immune activity and stress reaction) related processes in females at 0, 6 and 24 h postmating. In males, mating also induced upregulation on soma maintenance related processes at 0 h postmating, but induced downregulation on these processes at 6 and 24 h postmating. In conclusion, this study demonstrated that mating induced sex-specific postmating behavioral and transcriptional changes in both sexes of S. frugiperda and suggested that the transcriptional changes are correlated with postmating physiological and behavioral changes in each sex.