Effects of Antheraea pernyi on Parasitization of Kriechbaumerella dendrolimi by Using Immunology and Metabolomics

Abstract

Kriechbaumerella dendrolimi (Hymenoptera, Chalcididae) is a dominant pupal parasitoid species of various significant pine caterpillars, including Dendrolimus houi Lajonquiere (Lepidoptera, Lasiocampidae), with great potential for utilization. So far, the mass rearing of K. dendrolimi has been successfully established using Antheraea pernyi (Lepidoptera, Saturniidae) pupae as alternative hosts and released in the forest to suppress D. houi populations. However, the outcome is still expected to be improved due to lower parasitism rates, which might be related to the autonomous immune function of A. pernyi pupae. In our study, we investigated the effects of K. dendrolimi parasitization on the immune responses of A. pernyi pupae by measuring the expression of key immune factors: superoxide dismutase (SOD), polyphenol oxidases (PPOs), Attacin, Lysozymes (LYSs), and serine proteases (PRSSs). Our results show that parasitization significantly upregulated these immune factors, with distinct temporal patterns observable between 4 and 48 h post-parasitization. This upregulation highlights a robust immune response, adapting over time to the parasitic challenge. These findings suggest that specific immune mechanisms in A. pernyi pupae are activated in response to K. dendrolimi, shedding light on potential targets for enhancing host resistance. Metabolomic analyses complemented these findings by illustrating the broader metabolic shifts associated with the immune response. Specifically, Attacin was significantly upregulated twice, hypothesizing that the parasitoid’s venom contains at least two parasitic factors. Metabolomics analysis revealed a significant metabolite difference within parasitized A. pernyi pupae. The highest number of differential expression metabolites (DEMs) was observed at 16 h post-parasitism (1184 metabolites), with fewer DEMs at 8 h (568 metabolites) and 32 h (693 metabolites), suggesting a close relationship between parasitism duration and the number of DEMs. These fluctuations reflected the fundamental process of immune interaction. KEGG enrichment results showed that the DEMs were mainly enriched in energy metabolism and immune-related pathways, indicating that parasitism is a process of continuous consumption and immune interaction in the host. These DEMs could also become future targets for regulating the immune functions of A. pernyi pupae and could provide reference data for optimizing mass-rearing techniques.