Insect herbivores are frequently reported to metabolize plant defense compounds, but the physiological and ecological consequences are not fully understood. It has rarely been studied whether such metabolism is genuinely beneficial to the insect, and whether there are any effects on higher trophic levels. Here, we manipulated the detoxification of plant defenses in the herbivorous pest diamondback moth (Plutella xylostella) to evaluate changes in fitness, and additionally examined the effects on a predatory lacewing (Chrysoperla carnea). Silencing glucosinolate sulfatase genes resulted in the systemic accumulation of toxic isothiocyanates in P. xylostella larvae, impairing larval development and adult reproduction. The predatory lacewing C. carnea, however, efficiently degraded ingested isothiocyanates via a general conjugation pathway, with no negative effects on survival, reproduction, or even prey preference. These results illustrate how plant defenses and their detoxification strongly influence herbivore fitness but might only subtly affect a third trophic level.

Lepidopteran pests are the major crop devastators. Farmers have to resort to heavy synthetic pesticide application for their control. It increases the pesticide residue contamination on produce and causes health hazards. Synthetic pesticides also endanger beneficial insects and pollute the environment. Therefore, the use of safe and eco-friendly botanicals as biopesticides is rapidly increasing. Despite their high demand, only a few botanicals are commercially available. Consequently, biopesticide discovery research boomed in the last decade. Spodoptera litura Fabricius (armyworm) is a polyphagous multi-insecticide-resistant lepidopteran pest. It is a serious concern for several commercially important crops. In this study, we employed a chemical ecology approach to discover a biopesticide against it. As a biopesticide source, we explored secondary metabolite-rich Solanum melongena L. (eggplant), one of the armyworm’s hosts. We found that the armyworm larvae show differential occurrence on seven eggplant varieties; the Himalayan eggplant variety RC-RL-22 (RL22) showed no armyworm infestation. When reared in a no-choice condition on RL22, larval mortality was two-fold higher, and mass was three-fold lower than the varieties showing high infestation. We tested whether RL22’s secondary metabolite(s) were associated with this hampered larval performance. Using LC-ESI-QTOF-based non-targeted metabolomics of eggplant varieties, we identified candidate metabolites. 5- O -caffeoylquinic acid (chlorogenic acid; CGA) showed a strong negative correlation (r= -0.88; p = 0.008) with the larval performance. CGA-spiked (average physiological concentration) artificial diet (CGA-AD)-fed larvae showed a three-fold mass reduction and two-fold mortality increase than the control artificial diet (AD)-fed larvae; pupation and eclosion also significantly reduced (1.3-fold and 1.4-fold, respectively) in the CGA-ingested larvae. We used a reverse genetics approach to assess the in planta insecticidal potential of CGA. When RL22’s CGA biosynthesis gene hydroxycinnamoyl-CoA quinate transferase ( Sm HQT) was silenced using virus-induced gene silencing (VIGS), CGA levels decreased by three-fold. This CGA depletion rendered RL22 two-fold armyworm-susceptible than controls. Foliar CGA application restored RL22’s armyworm resistance. Overall, this study showed that CGA exhibits larvicidal properties against the armyworm. It is also safe for beneficial organisms. CGA is a well-known dietary supplement and an antioxidant for humans. Thus, it is safe for human consumption. Together, high CGA-containing varieties can be used to reduce the armyworm infestation risk. CGA is a promising biopesticide candidate for the field trial phase against the lepidopteran pests, especially armyworm. If successful, it can be integrated into the pest control measures.