Unexpected effects of sublethal doses of insecticide on the peripheral olfactory response and sexual behavior in a pest insect

Abstract

Pesticides have long been used as the main solution to limit agricultural pests, but their widespread use resulted in chronic or diffuse environmental pollutions, development of insect resistances, and biodiversity reduction. The effects of low residual doses of these chemical products on organisms that affect both targeted species (crop pests) but also beneficial insects became a major concern, particularly because low doses of pesticides can induce unexpected positive--also called hermetic--effects on insects, leading to surges in pest population growth at greater rate than what would have been observed without pesticide application. The present study aimed to examine the effects of sublethal doses of deltamethrin, one of the most used synthetic pyrethroids, known to present a residual activity and persistence in the environment, on the peripheral olfactory system and sexual behavior of a major pest insect, the cotton leafworm Spodoptera littoralis. We highlighted here a hormetic effect of sublethal dose of deltamethrin on the male responses to sex pheromone, without any modification of their response to host-plant odorants. We also identified several antennal actors potentially involved in this hormetic effect and in the antennal detoxification or antennal stress response of/to deltamethrin exposure.

Glutathione-S-Transferases in the Olfactory Organ of the Noctuid Moth Spodoptera littoralis, Diversity and Conservation of Chemosensory Clades

“…SlitMGST1-1 and SlitMGST1-2 were indeed broadly expressed in all tissues and development stages tested whereas SlitMGST1-3 was restricted to the antenna suggesting that these three genes could have evolved different functions after a noctuid-specific duplication event. A previous study showed that SlitMGST1-3 expression is induced after deltamethrin exposure (Lalouette et al, 2016), thus suggesting a possible specialization of SlitMGST1-3 toward toxic molecules. In the beetle P. striolata two MGSTs are also preferentially expressed in the antennae of adult insects (Wu et al, 2016) meaning that members of this protein family could have conserved important function linked to olfaction.…”

“…We named all S. littoralis sequences according to the corresponding S. litura and S. frugiperda sequences (Zhang et al, 2016; Gouin et al, 2017). Subsequently the 7 S. littoralis GSTs that were previously published in (Lalouette et al, 2016), namely SlGSTe1, e2, e3, e4, d1, d2 , and d3 were respectively renamed SlitGSTe15, e8, e14, e12, d2, d3 , and SlitMGST1-3 . All sequences have been deposited in Genbank with reference accession number from MH177577 to 177613.…”

The Sublethal Effects of Insecticides in Insects

“…The regular olfactory process was also affected, since the repolarization on the antenna was reduced, while a rapid response of the olfactory receptor neurons (ORN) was induced. Thus, a faster behavioral response of males to pheromone stimulation was observed (Figure 1) [23].…”

Degradation of sex pheromone and plant volatile components by an antennal glutathione S‐transferase in the oriental fruit moth,Grapholita molesta Busck (Lepidoptera: Tortricidae)

“…The results indicated that GmolGSTD1 may not be involved in the detoxification of these insecticides, which were inconsistent with the detoxification or resistance functions to insecticides of CpomGSTd2 of C. pomonella (Huang, Fan, Liu, & Feng, ), SlGSTE1 of Spodoptera litura (Xu, Zou, Zhang, Feng, & Zheng, ) and BdGSTe9 of Bactrocera dorsalis (X. P. Lu et al, ). Previous studies have shown that the insecticides can inhibit the sensitivities of insect olfactory system (Lalouette et al, ; Z. Li et al, ). For example, imidacloprid can significantly reduce the binding capacity of the odorant‐binding protein, AcerASP2, to host plant volatiles (G. Li et al, ).…”

“…Clothianidin at a sublethal dose (0.25 ng) can significantly reduce the directional behavior of male Agrotis ipsilon to sex pheromones (Rabhi et al, ). Pyrethroid at a sublethal dose can alter the peripheral olfactory response and the courtship behavior of male Spodoptera littoralis (Lalouette et al, ). The ability of olfactory learning of the adult bees can be severely impaired after imidacloprid treatment of the larvae (K. Tan et al, ).…”