Pesticides enhance maternal care in the wolf spider by inhibiting HSD3B, an enzyme for progesterone synthesis

Natural enemies are essential for the integrated pest management (IPM) strategy in insect pest control. However, chemical pesticides remain the primary method for insect pest control, diminishing natural enemies and causing environmental contamination. The wolf spider (Pardosa pseudoannulata), a major enemy in agro-ecosystem, exhibits maternal care (MC) behaviors such as eggsac-carrying and pulli-carrying, which are crucial for population growth. Here we found that m-Aminophenylacetylene (m-A), a MC inducer, downregulated HSD3B (3β-hydroxysteroid dehydrogenase/Δ5,4-isomerase) expression through two transcription factors, GATA6_Pardosa and LRH_Pardosa. HSD3B expression reduction inhibited progesterone production, which then induced pulli-carrying behavior in P. pseudoannulata. Although m-A did not inhibit HSD3B activity directly, several pesticides showed inhibitory effects on HSD3B from results of molecular docking and activity inhibition assay on recombinant enzyme. The fungicide difenoconazole, herbicide topramezone and insecticide buprofezin efficiently inhibited HSD3B activity, and then reduced progesterone production, thereby enhancing the pulli-carrying behavior. From MC induction perspective, some pesticides are not inherently harmful to natural enemy spiders of insect pests, and in turning trash into treasure, may be used as beneficial agents to improve pest control effectiveness. [Display omitted] •Impairing HSD3B function enhanced maternal care behaviors in P. pseudoannulata.•Inhibiting HSD3B reduced progesterone synthesis.•m-A stimulated maternal care behaviors in female by inhibiting HSD3B expression.•Pesticides enhance pulli-carrying behavior by directly inhibiting HSD3B activity.