The life-history trait trade-offs mediated byreproduction and immunity in the brown planthopper, Nilaparvata lugens Stål

Reproduction and immunedefense are costly functions, and they are expected to tradeoff with each otherto drive evolution. The brownplanthopper (BPH), Nilaparvata lugens Stål(Hemiptera, Delphacidae), is a global superpest that mostly damages ricecrops. Yeast-like symbionts (YLS) existin the abdominal fat body tissue and are tightly associated with thedevelopment, growth, and reproduction of BPH. Our previous research demonstrated that mating behavior promotes therelease of YLS from the fat body into the hemolymph in the BPH, therebytriggering an immune response. Additionally, the fitness costs related to life-history traits of BPH(such as survival rate) have a strong dependence on the relative abundance ofYLS. However, the possible relationshipbetween reproduction and the immune response in BPH has not beenidentified. In this study, anomics-based approach was used to analyze the transcriptome of fat body tissuesin mated and unmated BPH at 72 h post-eclosion, from which two antimicrobialpeptide genes, NlDefensin A (NlDfA) and NlDefensin B (NlDfB), were selected since they were highly expressed in matedBPH. Subsequently, the full-length cDNAsequences of the NlDfA and NlDfB genes were cloned andanalyzed. qPCR results showedup-regulation of the NlDfA and NlDfB genes in mated BPH whencompared to unmated BPH. Spatial-temporal expression analysis indicated that the NlDfA and NlDfB genes were expressed in all tissues and developmental stages, andthey were most highly expressed in the fat body at 24 h post-eclosion. Moreover, the symbionts in BPH weresignificantly inhibited by the in vitro expression of the NlDfAand NlDfB proteins. Furthermore, RNAinterference (RNAi)-mediated suppression of NlDfA and NlDfB dramatically increased the relative abundance of YLS in the fat body, while YLSin the hemolymph decreased significantly. These BPHs also displayed some fitness disadvantages in survival,fecundity, hatchability, and possibly the vertical transmission of YLS fromhemolymph to egg. Our results indicatedthat mating could heighten the immunity of BPH by up-regulating the expressionof the NlDfA and NlDfB genes, which protect the host frompathogen challenges during reproduction. However, the reduced content of YLS may act as a fitness disadvantage indictating the life-history traits of BPH. This work has significant theoretical and practical implications for theprecise green control technology that involves crucial gene targeting, as wellas for the “endosymbionts for pest control” strategy in insects.