Olfactory perception of herbivore‐induced plant volatiles elicits counter‐defences in larvae of the tobacco cutworm

Abstract Herbivore attack leads to increased emission of herbivore‐induced plant volatiles (HIPVs) that protect plants by eliciting direct anti‐herbivore defences and indirect defences via attraction of natural enemies. Whether herbivorous insects can develop counter‐defences against host plants in response to HIPVs is largely unexplored. Using a directed airflow apparatus, we investigated the influence of HIPVs emitted from tobacco cutworm Spodoptera litura‐infested tomatoes on larval performance on herbivore‐pretreated tomatoes versus untreated tomatoes or on trypsin inhibitor‐amended artificial diets versus unamended diets, as well as the transcriptional responses of HIPV‐exposed larvae. Spodoptera litura larval feeding on tomato plants led to increased emission of HIPVs. The HIPV‐exposed larvae showed significantly increased survival rates and weight gains on both herbivore‐pretreated tomato leaves and trypsin inhibitor‐supplemented diet but not on untreated tomato leaves and control diets, nor when they had been exposed to HIPVs emitted from spr8 mutant plants which barely emit terpenes. These results suggest that larval exposure to HIPVs from wild‐type plants enhanced their ability to cope with plant‐induced defences. The latter is supported by the observation that larval exposure to HIPVs led to enhanced transcript levels of eight genes encoding cuticle proteins, and seven genes encoding cytochrome P450s, an important class of detoxification enzymes. Our studies revealed a mechanism by which larval olfactory perception of HIPVs elicits counter‐defences that enhance the ability of insect herbivores to withstand host plant chemical defences.