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.
Male moths rely on olfactory cues to find females for reproduction. Males also use volatile plant compounds (VPCs) to find food sources and might use host-plant odor cues to identify the habitat of calling females. Both the sex pheromone released by conspecific females and VPCs trigger well-described oriented flight behavior toward the odor source. Whereas detection and central processing of pheromones and VPCs have been thought for a long time to be highly separated from each other, recent studies have shown that interactions of both types of odors occur already early at the periphery of the olfactory pathway. Here we show that detection and early processing of VPCs and pheromone can overlap between the two sub-systems. Using complementary approaches, i.e., single-sensillum recording of olfactory receptor neurons, in vivo calcium imaging in the antennal lobe, intracellular recordings of neurons in the macroglomerular complex (MGC) and flight tracking in a wind tunnel, we show that some plant odorants alone, such as heptanal, activate the pheromone-specific pathway in male Agrotis ipsilon at peripheral and central levels. To our knowledge, this is the first report of a plant odorant with no chemical similarity to the molecular structure of the pheromone, acting as a partial agonist of a moth sex pheromone.
Recognition of intra-specific olfactory signals within a complex environment of plant-related volatiles is crucial for reproduction in male moths. Sex pheromone information is detected by specific olfactory receptor neurons (Phe-ORNs), highly abundant on the male antenna. The information is then transmitted to the pheromone processing macroglomerular complex (MGC) within the primary olfactory center, the antennal lobe, where it is processed by local interneurons and projection neurons. Ultimately a behavioral response, orientation toward the pheromone source, is elicited. Volatile plant compounds (VPCs) are detected by other functional types of olfactory receptor neurons (ORNs) projecting in another area of the antennal lobe. However, Phe-ORNs also respond to some VPCs. Female-produced sex pheromones are emitted within a rich environment of VPCs, some of which have been shown to interfere with the detection and processing of sex pheromone information. As interference between the different odor sources might depend on the spatial and temporal features of the two types of stimuli, we investigated here behavioral and neuronal responses to a brief sex pheromone blend pulse in a VPC background as compared to a control background in the male noctuid moth Agrotis ipsilon. We observed male orientation behavior in a wind tunnel and recorded responses of Phe-ORNs and MGC neurons to a brief sex pheromone pulse within a background of individual VPCs. We also recorded the global input signal to the MGC using in vivo calcium imaging with the same stimulation protocol. We found that VPCs eliciting a response in Phe-ORNs and MGC neurons masked responses to the pheromone and decreased the contrast between background odor and the sex pheromone at both levels, whereas α-pinene did not interfere with first order processing. The calcium signal produced in response to a VPC background was tonic, lasting longer than the VPC stimulus duration, and masked entirely the pheromone response. One percent heptanal and linalool, in addition to the masking effect, caused a clear delay in responses of MGC neurons to the sex pheromone. Upwind flight toward the pheromone in a wind tunnel was also delayed but otherwise not altered by different doses of heptanal.
As in vertebrates, the insect steroid hormones, especially 20-hydroxyecdysone (20E), initiate and regulate sexual behavior by acting on the central nervous system. This 20E action is, in part, triggered by transcriptional events mediated through the binding of 20E to a heterodimer comprising the ecdysone receptor (EcR) and ultraspiracle (USP). However, to date, our knowledge about this genomic steroid pathway remains incomplete. In moths, males detect female sex pheromones, eliciting stereotyped sexual behavior. In Agrotis ipsilon males, the behavioral response and the neuronal sensitivity to sex pheromone in the olfactory center, the antennal lobe (AL), increase with age. We recently showed that 20E controlled this age-dependent olfactory plasticity via the activation of an EcR/USP-dependent pathway in the AL. Here, we cloned the gene encoding A. ipsilon synaptotagmin I (AisytI), a presynaptic vesicle protein known to act as a calcium sensor in neurotransmitter release. AisytI was expressed in the AL, where its amount increased with age, whereas its knockdown inhibited the sex pheromone-oriented flight of males. 20E administration to males induced AL AisytI expression in a dose-dependent and time-dependent manner. Moreover, A. ipsilon EcR silencing caused decreases in AL AisytI expression and the behavioral response to sex pheromone. Our results show that the synaptotagmin I gene is a target gene for the genomic steroid signaling that controls the expression of insect sexual behavior by acting on central sex pheromone processing. This study thus represents a significant advance in our understanding of the steroid actions that influence neural functions, and thereby behavioral plasticity, in various organisms. DatabaseThe nucleotide sequence of Agrotis ipsilon synaptotagmin I is available in the DDBJ/EMBL/ GenBank databases under the accession number KJ863735.
How animals perceive and learn complex stimuli, such as mixtures of odorants is a difficult problem, for which the definition of general rules across the animal kingdom remains elusive. Recent experiments conducted in human and rodent adults as well as newborn rabbits suggested that these species process particular odor mixtures in a similar, configural manner. Thus, the binary mixture of ethyl isobutyrate (EI) and ethyl maltol (EM) induces configural processing in humans, who perceive a mixture odor quality (pineapple) that is distinct from the quality of each component (strawberry and caramel). Similarly, rabbit neonates treat the mixture differently, at least in part, from its components. In the present study, we asked if the properties of the EI.EM mixture extend to an influential invertebrate model, the honey bee Apis mellifera. We used appetitive conditioning of the proboscis extension response to evaluate how bees perceive the EI.EM mixture. In a first experiment, we measured perceptual similarity between this mixture and its components in a generalization protocol. In a second experiment, we measured bees’ ability to differentiate between the mixture and both of its components in a negative patterning protocol. In each experimental series, bees' performances with this mixture were compared with those obtained with 4 other mixtures, chosen from previous work in humans, newborn rabbits and bees. Our results suggest that when having to differentiate mixture and components, bees treat the EI.EM in a robust configural manner, similarly to mammals, suggesting the existence of common perceptual rules across the animal kindgdom.
Characteristics of attachment were assessed in peer-and object-reared lambs, and compared to mothered subjects by taking into consideration distress, proximity seeking, and exploration during two separation-reunion tests in both the familiar and a novel environment. Plasma cortisol and oxytocin were assayed as physiological indicators of stress and being comforted during the separation-reunion test. Rewarding properties of the familiar figures were also determined in a conditioned place preference-like paradigm. Between-group analysis revealed the existence of secure attachment with the mother, alteration of secure attachment with the peer and weaker attachment with the object. Weaker attachment was expressed by a lack of distress during separation in the home pen and no preference for the place conditioned with the familiar object. Elevated basal plasma oxytocin levels, but not cortisol, observed in maternally deprived lambs were more likely linked to the absence of a maternal figure rather than social comfort during reunion. K E Y W O R D Sattachment, cortisol, distress, oxytocin, social bond
Vespavelutinanigrithorax, an invasive species, a direct result of increased trade and climate change, is spreading rapidly in Europe and endangering entomofauna in general and more alarmingly honeybee (Apismellifera) populations, and therefore their pollination services. All traps used now, to try to control this species, seem to be not efficient enough and non-selective. However, in the current context of massive disappearance of insects in general, it is urgent to find means of protection for the entomofauna. While no selective trapping is still occurring, we performed a pilot study to test a carnivorous plant as a potential biocontrol tool to trap V.velutina. In our study, we analyzed the hornet-capturing ability of two Sarracenia hybrids (S.juthatipsoper and S.evendine) on a 2-years period (2015 and 2016). Our results show that these plants trapped more dipterans than other taxa, and they do not attract many hornets. In such condition, both Sarracenia hybrids cannot therefore be used in a mass trapping system, because they are not selective, and too few hornets are trapped. To maximize captures of V.velutina while minimizing captures of non-target species, other systems need to be thus developed, as traps using hornet pheromone-based baiting.
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