Cyantraniliprole-mediated transgenerational hormesis in the invasive tomato pinworm, Tuta absoluta

Hormesis, a biphasic dose-response phenomenon, is gaining recognition for its bioregulatory and practical implications. Invasive species present a critical context for studying hormesis, because sublethal population-level responses may facilitate establishment and spread, particularly when transgenerational effects are involved. The invasive South American tomato pinworm, Tuta absoluta Meyrick, a global agricultural pest, exemplifies this scenario. Despite its relevance, the role of hormesis, particularly in response to novel insecticides like cyantraniliprole, a second-generation anthranilic diamide widely used against lepidopteran pests, remains underexplored. Thus, using age-stage, two-sex life table analyses and nanocarrier-mediated RNA interference, we examined the sublethal effects of cyantraniliprole on T. absoluta.

Cyantraniliprole exhibited high toxicity to third-instar larvae, with a median lethal concentration (LC₅₀) of 0.72 mg L^-1 after 72 h of exposure. Sublethal and low lethal concentrations (LC₁₀ and LC₃₀) prolonged developmental times and reduced adult longevity and fecundity in exposed individuals. Intriguingly, exposure to LC₁₀ in subsequent generations (F₁ and F₂) shortened developmental times and increased survival, reproduction and life table parameters, whereas exposure to LC₃₀ significantly impaired these traits. Gene expression analyses revealed reduced levels of development and reproduction-related genes (Vg, VgR and JHBP) in parental insects but increased levels in F₁ and F₂ at LC₁₀, whereas the levels of expression remained consistent at LC₃₀. Overexpression of detoxification-related P450 genes (CYP4M116, CYP6AW1 and CYP9A307v2) persisted over generations, whereas nanomaterial-encapsulated dsRNA targeting these genes significantly increased susceptibility to cyantraniliprole.

Cyantraniliprole induces a transgenerational hormesis-like response in T. absoluta. These findings highlight the need to evaluate the hormetic-like effects when designing ecologically sound pest management strategies for this invasive pest species. © 2025 Society of Chemical Industry.