Pathogen-associated odor experience induces inherited olfactory avoidance in a parasitoid wasp

Odors allow animals to evaluate resources and risks, but the neural and inherited consequences of experience with ecologically meaningful odors remain poorly understood. Since both parasitoids and entomopathogenic fungi are widely used as agents in integrated biocontrol, we asked whether exposure to pathogen-associated volatiles can reassign odor value in a parasitoid wasp and whether the acquired bias is transmitted to descendants. Adult female Scleroderma guani were exposed, without host contact, to volatiles from Beauveria bassiana-infected hosts or to methyl cinnamate (MC), a representative component of the infected-host odor. Twelve-hour exposure shifted subsequent choices away from infected-host odor and MC, whereas shorter exposure produced different effects, indicating duration-dependent olfactory plasticity. The shift occurred without an explicit reward or punishment and is therefore consistent with non-associative learning. Unexposed F1 and F2 descendants of MC-exposed females expressed the same avoidance bias. MC stimulation elicited stronger calcium responses in mushroom-body regions of trained females and their descendants. Head transcriptomes identified reduced expression of the crustacean cardioactive peptide receptor (CCAPR) as a shared molecular signature, and CCAPR RNA interference phenocopied the odor-avoidance behavior. Finally, maternal treatment with sinefungin, a broad S-adenosylmethionine-dependent methyltransferase inhibitor, left maternal behavioral shift intact but abolished the F1 bias, implicating a methylation-sensitive process in transmission. Together, these results reveal that a pathogen-associated odor can induce durable, cross-generational reweighting of olfactory value in a non-model insect and identify candidate neural and neuropeptidergic mechanisms linking sensory experience to inherited behavior, and providing a new perspective on utilizing training in integrated biocontrol as well.