Non-redundant odorant detection in a locust

Abstract

Olfactory coding, from insects to humans, is canonically considered to involve considerable across-fiber coding already at the peripheral level, thereby allowing recognition of very large numbers of odor compounds. Here we show that the migratory locust, Locusta migratoria, has evolved an alternative strategy built on highly specific odorant receptors feeding into a complex primary processing center in the brain. By collecting odors from food and different life stages of the locust, we identified 208 ecologically relevant odorants, which we used to deorphanize 48 locust olfactory receptors via ectopic expression in Drosophila. Contrary to the often broadly tuned olfactory receptors of other insects, almost all locust receptors were found to be narrowly tuned to one ligand and most of these best ligands exclusively excited only one receptor. Knocking out a single receptor using CRISPR-Cas9 resulted in an abolished physiological and behavioral response to the corresponding ligand. We conclude that the locust olfactory system, with an apparent lack of redundancy among most olfactory receptors, differs from so-far described olfactory systems.

A chemical defense deters cannibalism in migratory locusts

“…Among these, we identified 17 compounds that are only emitted by the gregarious phase, during which cannibalism occurs. Four of the compounds identified—4-vinylanisole, 2-methyl-5-isopropylpyrazine, 2,4,6-trimethylpyridine, and phenylacetonitrile (PAN)—had been reported earlier ( 23 , 25 , 26 ), and 4-vinylanisole, 2-methyl-5-isopropylpyrazine, and 2,4,6-trimethylpyridine were identified as intraspecifically attractive compounds ( 23 , 26 ); the remaining compounds were shown to be behaviorally neutral in our tests (fig. S2).…”

“…3B). We then asked whether LmOR70a was exclusively tuned to PAN and screened 204 locust volatiles reported previously from our laboratory ( 23 ) (tested at 10 −1 dilution) in continued recording experiments (table S1). We identified two additional compounds, which are structurally similar to PAN (benzaldehyde and cinnamaldehyde), that activated neurons expressing LmOR70a, though at higher concentrations (Fig.…”

A chemical defense deters cannibalism in migratory locusts

“…Second, we used CYP305M2 −/− locusts scented with PAN or paraffin oil to test predation choice. CYP305M2 −/− locusts were each perfumed with 300 ng PAN, an amount similar to the biosynthesis level in WT nymphs 20 . In predation experiments as described above, oil-treated CYP305M2 −/− locusts were in most cases completely consumed by starved conspecifics, whereas PAN-treated CYP305M2 −/− nymphs were seldomly injured or consumed (Fig 4e, f).…”

“…3b). We then asked whether LmOR70a was exclusively tuned to PAN and screened 207 locust volatiles reported previously from our laboratory 20 (tested at 10 -1 dilution) in continued SSR experiments (S1 table). We identified two additional compounds, structurally similar to PAN (benzaldehyde and cinnamaldehyde), which activated neurons expressing LmOR70a, even though at higher concentrations (Fig.…”

“…The selective repulsion driven by cannibalistic interactions suggests that gregarious locusts may release warning signals to deter conspecific predation. Our recent study on the migratory locust Locusta migratoria identified hundreds of volatile compounds emanating from all life stages of the locusts 20 . Several of these compounds were shown to be behaviorally repulsive, but their biological functions remain largely unknown.…”