A host-derived volatile primes context-dependent foraging behavior in parasitic nematodes via a lysosome-associated neural pathway.

Abstract

Entomopathogenic nematodes (EPNs) are valued for sustainable pest control, yet their efficacy hinges on matching foraging behavior to host ecology. The nematode <i>Steinernema carpocapsae</i>, long regarded as an ambusher, paradoxically infects the cryptic red palm weevil (<i>Rhynchophorus ferrugineus</i>), which resides deep in plant tissue. Here, we show that this contradiction stems from a context-dependent modulation of foraging-related behaviors, triggered by butylated hydroxytoluene (BHT)-a host-derived volatile emitted by <i>R. ferrugineus</i> larvae. BHT functions as a potent behaviorally active volatile, increasing locomotion, jumping, host attraction, and infection success in <i>S. carpocapsae</i>. Mechanistically, BHT engages a lysosome-associated signaling pathway involving <i>mfsd8</i>, <i>SLC17A5</i>, and <i>ptr</i>. Knockdown of these genes disrupted BHT-induced behavioral changes, supporting their functional involvement. Our findings extend existing context-dependent models of nematode foraging by providing mechanistic insight into chemically induced behavioral modulation. This work opens possibilities for improving EPN biocontrol efficacy via ecological or molecular priming.