Parasites alter host energy homeostasis for their own development, but the mechanisms underlying this phenomenon remain largely unknown. Here, we show thatCotesia vestalis, an endoparasitic wasp ofPlutella xylostellalarvae, stimulates a reduction of host lipid levels. This process requires excess secretion ofP.xylostellatachykinin (PxTK) peptides from enteroendocrine cells (EEs) in the midgut of the parasitized host larvae. We found that parasitization upregulates PxTK signaling to suppress lipogenesis in midgut enterocytes (ECs) in a non-cell-autonomous manner, and the reduced host lipid level benefits the development of wasp offspring and their subsequent parasitic ability. We further found that aC.vestalisbracovirus (CvBV) gene,CvBV 9–2, is responsible forPxTKinduction, which in turn reduces the systemic lipid level of the host. Taken together, these findings illustrate a novel mechanism for parasite manipulation of host energy homeostasis by a symbiotic bracovirus gene to promote the development and increase the parasitic efficiency of an agriculturally important wasp species.

Making the appropriate responses to predation risk is essential for the survival of an organism; however, the underlying mechanisms are still largely unknown. Here, we find that Drosophila has evolved an adaptive strategy to manage the threat from its parasitoid wasp by manipulating the oviposition behavior. Through perception of the differences in host search performance of wasps, Drosophila is able to recognize younger wasps as a higher level of threat and consequently depress the oviposition. We further show that this antiparasitoid behavior is mediated by the regulation of the expression of Tdc2 and Tβh in the ventral nerve cord via LC4 visual projection neurons, which in turn leads to the dramatic reduction in octopamine and the resulting dysfunction of mature follicle trimming and rupture. Our study uncovers a detailed mechanism underlying the defensive behavior in insects that may advance our understanding of predator avoidance in animals.

Studying the microbial symbionts of eukaryotic hosts has revealed a range of interactions that benefit host biology. Most eukaryotes are also infected by parasites that adversely affect host biology for their own benefit. However, it is largely unclear whether the ability of parasites to develop in hosts also depends on host-associated symbionts, e.g., the gut microbiota. Here, we studied the parasitic wasp Leptopilina boulardi (Lb) and its host Drosophila melanogaster. Results showed that Lb successfully develops in conventional hosts (CN) with a gut microbiota but fails to develop in axenic hosts (AX) without a gut microbiota. We determined that developing Lb larvae consume fat body cells that store lipids. We also determined that much larger amounts of lipid accumulate in fat body cells of parasitized CN hosts than parasitized AX hosts. CN hosts parasitized by Lb exhibited large increases in the abundance of the bacterium Acetobacter pomorum in the gut, but did not affect the abundance of Lactobacillus fructivorans which is another common member of the host gut microbiota. However, AX hosts inoculated with A. pomorum and/or L. fructivorans did not rescue development of Lb. In contrast, AX larvae inoculated with A. pomorum plus other identified gut community members including a Bacillus sp. substantially rescued Lb development. Rescue was further associated with increased lipid accumulation in host fat body cells. Insulin-like peptides increased in brain neurosecretory cells of parasitized CN larvae. Lipid accumulation in the fat body of CN hosts was further associated with reduced Bmm lipase activity mediated by insulin/insulin-like growth factor signaling (IIS). Altogether, our results identify a previously unknown role for the gut microbiota in defining host permissiveness for a parasite. Our findings also identify a new paradigm for parasite manipulation of host metabolism that depends on insulin signaling and the gut microbiota.

Leptopilina wasps are crucial for biological pest control, particularly against the globally emerging pest Drosophila suzukii. Despite their ecological significance, the genomic basis of host selection and parasitism in this genus remains underexplored. In this study, we assembled a high-quality, chromosome-level genome of Leptopilina myrica, a species collected in Taizhou, Zhejiang Province, China. We employed a combination of PacBio long-read sequencing, Illumina short-read sequencing, and Hi-C technology to produce a genome assembly of approximately 462.30 Mb, with a scaffold N50 of 47.32 Mb and a contig N50 of 4.07 Mb. By comparing the protein-coding genes of L. myrica with those of other Hymenoptera species, we gained insights into the evolutionary history of parasitoid wasps. This high-quality genome will provide a foundation for future research on the genetic and functional traits of parasitoid wasps, shedding light on the evolutionary dynamics of host-parasite interactions. The genome of L. myrica provides a valuable resource for future studies on host-parasite interactions and the genetic basis of parasitoid wasp biology.

Behavioral fever, a thermoregulatory response in which ectothermic animals seek warmer environments to elevate body temperature and combat parasite infections, is well documented against microparasites. However, its role and mechanisms against macroparasites remain largely unknown. Here, we show that Drosophila hosts use behavioral fever to defend against Leptopilina parasitoid wasps. This thermal preference increases wasp mortality and enhances host survival. We find that behavioral fever is mediated by up-regulation of Heat shock protein 70 ( Hsp70 ) genes in infected hosts as Hsp70 loss abolishes behavioral fever, whereas its overexpression induces heat-seeking behavior. We further find that behavioral fever up-regulates immune genes in infected hosts, including 12 antimicrobial peptide ( AMP ) genes, which disrupt the gut microbiota homeostasis of parasitoid wasps and, in turn, lead to substantial wasp mortality. Our findings elucidate the detailed mechanisms of behavioral fever in Drosophila hosts, advancing our understanding of ectothermic animal defenses against macroparasites.