Foraging in the darkness: Highly selective tuning of below-ground larval olfaction to Brassicaceae volatiles in striped flea beetle.

The olfactory system of above-ground insects is among the best described perceptual architectures. However, remarkably little is known about how below-ground insects navigate in the dark for foraging. Here, we investigated host plant preferences, olfactory sensilla and characterise olfactory proteins in below-ground larvae of the striped flea beetle (SFB) Phyllotreta striolata Fabricius (Coleoptera: Chrysomelidae). Both the adults and larvae of this coleopteran pest cause serious damage to Brassicaceous crops above and below ground, respectively. To elucidate the role of olfactory system in host location of below-ground larvae, we initially demonstrated that SFB larvae distinctly favoured Brassicaceae over other plant families by two-choice behavioural bioassay. Subsequently, scanning electron microscopy of sensilla in SFB larval head showed a significant reduction in the number of olfactory sensilla in larvae compared with adults. However, essential olfactory sensilla such as sensilla basiconica are underscoring the indispensability of the larval olfactory system. We selected four larval-specific odorant binding proteins for functional validation from our previous transcriptome data. Functional studies revealed that PstrOBP23 exhibits robust binding affinity to 24 volatiles of Brassicaceae plants, including seven isothiocyanate compounds. This suggests a pivotal role of PstrOBP23 in the foraging behaviour of the larvae below the ground. Moreover, two ligands displaying strong binding capacity exhibit apparent attractive or repellent activity towards SFB larvae. Our findings provide a crucial insight into the olfactory system of below-ground larvae in SFB, highlighting the highly selective tuning of larvae specific OBP to host plant volatiles. These results offer potential avenues for developing effective pest control strategies against SFB.