Tetraniliprole Triggers Transgenerational Hormesis in an Invasive Insect Herbivore: Molecular and Biological Insights

The South American tomato pinworm, <i>Tuta absoluta</i> (Meyrick), is among the most destructive invasive pests of tomato globally. The diamide insecticide tetraniliprole is increasingly used for its management. This study examines the sublethal effects of tetraniliprole on <i>T. absoluta</i> larvae, with a focus on its transgenerational impacts. Bioassays demonstrated that tetraniliprole was highly toxic to third-instar <i>T. absoluta</i> larvae, with an LC₅₀ of 0.029 mg/L. Sublethal (LC₁₀) and low lethal concentrations (LC₃₀) were used to investigate their impact on developmental, reproductive, and population parameters across two subsequent generations (F₁ and F₂). In the parental (F₀) generation, exposure to tetraniliprole at both concentrations significantly prolonged larval and pupal durations and reduced adult longevity and fecundity. In both F₁ and F₂ generations, concentration-dependent effects were observed-LC₁₀ accelerated development and enhanced fecundity and population growth, indicative of a hormetic response, whereas LC₃₀ delayed development and suppressed reproduction and survival. Life table analyses revealed significant changes in the <i>r</i>, <i>λ</i>, and <i>T</i>, particularly under LC₃₀. Additionally, the RT-qPCR analysis revealed the downregulation of development and reproduction-related genes (<i>Vg</i>, <i>VgR</i>, and <i>JHBP</i>) in the F₀ generation following exposure to tetraniliprole (LC₁₀ and LC₃₀). In contrast, these genes were upregulated in the progeny generations (F₁ and F₂) at LC₁₀. Furthermore, the overexpression of key detoxification genes, particularly <i>CYP4M116</i> and <i>CYP6AW1</i>, persisted across all three generations. Taken together, these findings reveal a substantial risk of unintended population resurgence (hormesis effects) at sublethal concentrations, underscoring the importance of integrating transgenerational consequences into insecticide resistance management programs for sustainable control of this key insect pest.