Effects of sublethal fipronil exposure on cross-generational functional responses and gene expression in Binodoxys communis

The effective systemic insecticide fipronil is widely used on a variety of crops and in public spaces to control insect pests. Binodoxys communis (Gahan) (Hymenoptera: Braconidae) is the dominant natural enemy of Aphis gossypii Glover (Homoptera: Aphididae), an important cotton pest, and has good efficiency in inhibiting aphid populations. The direct effects of environmental residues of sublethal fipronil doses on adult B. communis have not previously been reported. This study therefore aimed to evaluate the side effects and transcriptomic impacts of sublethal fipronil doses on B. communis. The results showed that exposure to the LC10 dose of fipronil significantly reduced the survival rate and parasitism rate of the F0 generation, but did not affect these indicators in the F1 generation. The LC25 dose did not affect the survival or parasitic rates of the F0 generation, but did significantly reduce the survival rate of F1 generation parasitoids. These results indicated that sublethal doses of fipronil affected B. communis population growth. Transcriptome analysis showed that differentially expressed genes (DEGs) in B. communis at 1 h after treatment were primarily enriched in pathways associated with fatty acid elongation, biosynthesis of fatty acids, and fatty acid metabolism. DEGs at 3 days after treatment were mainly enriched in ribosomal functions, glycolysis/gluconeogenesis, and tyrosine metabolism. Six DEGs (PY, ELOVL, VLCOAR, MRJP1, ELOVL AAEL008004-like, and RPL13) were selected for validation with real-time fluorescent quantitative PCR. This is the first report of sublethal, trans-generational, and transcriptomic side effects of fipronil on the dominant parasitoid of A. gossypii. The results of this study show that adaptation of parasitoids to high concentrations of pesticides may be at the expense of their offspring. These findings broaden our overall understanding of the intergenerational adjustments used by insects to respond to pesticide stress and call for risk assessments of the long-term impacts and intergenerational effects of other pesticides.