Transgenerational sublethal effects of emamectin benzoate and indoxacarb on Telenomus remus: Integrative insights from host-associated microbiome and transcriptome analyses.

The extensive application of synthetic insecticides like emamectin benzoate (EB) and indoxacarb (IN), threatens ecologically beneficial parasitoids such as Telenomus remus. This study evaluated the transgenerational impacts of continuous exposure (over seven generations) to EB and IN on T. remus by integrating toxicity assays, life-history analysis, microbiome profiling, and transcriptomics. Acute risk assessment indicated EB posed a moderate risk (Risk Quotient, RQ > 50), while IN showed low acute risk (RQ < 50). After multigenerational selection, T. remus developed only minor tolerance (ratios of 1.47 for EB and 1.46 for IN) but incurred significant fitness costs; prolonged development (EB: 10.33 days vs. control: 9.00 days), reduced parasitism (EB: 82.07%; IN: 85.00% vs. control: 90.29%), and shortened female longevity. Host-associated microbiome analysis revealed disrupted community homeostasis, with a notable decline in dominant Wolbachia abundance (from 33.20% in controls). Transcriptomics identified limited differentially expressed genes (53 for EB, 52 for IN), suggesting physiological adaptation, with key changes enriched in detoxification (e.g., cytochrome P450s, UGTs) and immune pathways. Integrated correlation analyses (Mantel tests) linked microbial dysbiosis to altered host gene expression and reduced fitness. These findings highlight that even insecticides with low acute toxicity (like IN) or those inducing only minor tolerance shifts can cause severe transgenerational impairments. Correlations between microbiome alterations and transcriptomic changes suggest potential interactive mechanisms that warrant further validation. Field application rates and ecological risk assessments should be re-evaluated to account for these chronic sublethal effects to conserve T. remus in sustainable agro-ecosystems.