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Single sensillum recordings from olfactory sensilla located on larval antennae.(a) General view of the antenna of a S. littoralis larva, showing two of the three antennal segments (I and II). Bar: 500 μm. (b) Magnified scanning electron microscopy view of the third antennal segment (III): olf, olfactory sensilla; ms, mechanosensory sensillum; arrow, the sensillum used for electrophysiological recordings. Bar: 50 μm. (c) Representative traces of single sensillum recordings from antennal sensilla showing responses to the SlitPGE. (d) Electrophysiological responses to different doses of SlitPGE and MbraPGE, and synthetic Z9,E11-14:Ac. The action potentials were generated by at least three ORNs. Each data point represents the mean (±s.e.m.) firing rate, which was calculated as described in the Methods section (n=8–12 larvae, one stimulation per larva). Significant differences compared with the control (hexane, data point 0) are indicated by ** (Mann–Whitney, P<0.001).
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Sex pheromones are released by adults of a species to elicit a sexual interaction with the other sex of the same species. Here we report an unexpected effect of a moth sex pheromone on the caterpillars of the same species. We demonstrate that larvae of the cotton leafworm Spodoptera littoralis are attracted by the moth sex pheromone and that this p...
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Context 1
... response of larvae antennae to a pheromone source. S. littoralis larval antennae, typical of Lepidoptera, consist of three segments (Fig. 4a). All electrophysiological recordings were obtained from one of the two olfactory sensilla located on segment II (Fig. 4b). Given the high level of spontaneous activity, we were not able to separate the activity of the different neurons (usually four) housed in the sensillum; therefore, the global firing activity was measured. The ...
Context 2
... response of larvae antennae to a pheromone source. S. littoralis larval antennae, typical of Lepidoptera, consist of three segments (Fig. 4a). All electrophysiological recordings were obtained from one of the two olfactory sensilla located on segment II (Fig. 4b). Given the high level of spontaneous activity, we were not able to separate the activity of the different neurons (usually four) housed in the sensillum; therefore, the global firing activity was measured. The firing activities upon the PGE or Z9,E11-14:Ac stim- ulation were significantly higher than those upon hexane stimulation for ...
Context 3
... spontaneous activity, we were not able to separate the activity of the different neurons (usually four) housed in the sensillum; therefore, the global firing activity was measured. The firing activities upon the PGE or Z9,E11-14:Ac stim- ulation were significantly higher than those upon hexane stimulation for all doses (Mann-Whitney, P < 0.001) ( Fig. 4c and 4d). The firing activities increased upon stimulation with increasing doses of Slit- PGE (ANOVA, F test, slope 47.6 ± 4.7, P = 0.0001), MbraPGE (slope 27.7 ± 4.7, P = 0.0001) or Z9,E11-14:Ac (slope 0.09 ± 0.01, P = 0.0001). The highest firing rates were obtained upon stimulation with 2 FE of SlitPGE, and a decrease was observed at 3 FE, ...
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Citations
... Despite the binding of these genes to sex pheromones, all five PBPs and GOBPs were found to bind some plant volatiles with significant affinities, and PBPs sense some plant volatiles (Liu et al. 2015a). Poivet et al. (2012) suggested that in Spodoptera littoralis, PBPs are used to detect sex pheromones absorbed or present on the egg, and when the female moth lays eggs on the leaves of the plant, this pheromone sensation is used by larvae in their search for food. The larvae of Sesamia inferens also use PBPs to search for food (Zhang et al. 2013). ...
... Despite the binding of these genes to sex pheromones, all five PBPs and GOBPs were found to bind some plant volatiles with significant affinities, and PBPs sense some plant volatiles (Liu et al. 2015a). Poivet et al. (2012) suggested that in Spodoptera littoralis, PBPs are used to detect sex pheromones absorbed or present on the egg, and when the female moth lays eggs on the leaves of the plant, this pheromone sensation is used by larvae in their search for food. The larvae of Sesamia inferens also use PBPs to search for food (Zhang et al. 2013). ...
The insect olfactory system plays pivotal roles in insect survival and reproduction through odor detection.
Morphological and physiological adaptations are caste-specifc and evolved independently in workers, soldiers,
and reproductives in termites. However, it is unclear whether the olfactory system is involved in the division of
labor in termite colonies. In the present study, the antennal sensilla of alates, workers, soldiers, nymphs, and
larvae of the termite Reticulitermes aculabialis Tsai et Hwang ( Isoptera: Rhinotermitidae) were investigated.
Transcriptomes were used to detect olfactory genes, and differential expression levels of olfactory genes were
confrmed in various castes by qRT–PCR analysis. Nine types of sensilla were identifed on the antennae of R.
aculabialis, and soldiers possessed all 9 types. In 89,475 assembled unigenes, we found 16 olfactory genes,
including 6 chemosensory protein (CSP) and 10 odorant-binding protein (OBP) genes. These OBP genes in�cluded 8 general odorant-binding protein genes (GOBPs) and 2 pheromone-binding protein-related protein
(PBP) genes. Five CSP genes were more highly expressed in alates than in workers, soldiers, larvae, and
nymphs, and the expression levels of CSP6 were signifcantly higher in nymphs. Seven GOBP and two PBP
genes exhibited signifcantly higher expression levels in alates, and there were no signifcant differences in
the expression levels of GOBP2 among workers, soldiers, alates, and larvae. These results suggest that alates,
as primary reproductives, have unique expression patterns of olfactory genes, which play key roles in nuptial
fight, mate seeking, and new colony foundation.
... Brief pre-exposure to the sex pheromone of S. littoralis causes cross-modal sensitization of sensory-guided behaviors that lasts for days and reinforces male's rhythmic attraction to the pheromone. 11,47,48 S. littoralis sex pheromone can also guide the food source selection of young larvae 49 and modulate cognitive behaviors such as decision-making and learning in adults. 50,51 Supporting the wide-ranging impact of the sex pheromone on the behavioral repertoire of the moths, our results underscore a keen sensitivity of their clock to sex-pheromonal input and highlight a close working collaboration between circadian and mating functions. ...
To extract any adaptive benefit, the circadian clock needs to be synchronized to the 24-h day-night cycles. We have investigated if it is a general property of the brain's circadian clock to recognize social interactions as external time givers. Sociosexual interactions with the opposite sex are universal, prevalent even in the lives of solitary animals. The solitary adult life of the Spodoptera littoralis moth is singularly dedicated to sex, offering an ideal context for exploring the impact of sociosexual cues on circadian timekeeping. We have identified specific olfactory cues responsible for social entrainment, revealing a surprisingly strong influence of pheromone-mediated remote sociosexual interactions on circadian rhythms. Males' free-running rhythms are induced and synchronized by the sex pheromone that the female releases in a rhythmic fashion, highlighting a hierarchical relation between the female and male circadian oscillators. Even a single pulse of the sex pheromone altered clock gene expression in the male brain, surpassing the effect of light on the clock. Our finding of a daytime-dependent, lasting impact of pheromone on male's courtship efficacy indicates that circadian timing in moths is a trait under sexual selection. We have identified specific components of the sex-pheromone blend that lack mate-attractive property but have powerful circadian effects, providing rationale for their continued retention by the female. We show that such volatiles, when shared across sympatric moth species, can trigger communal synchronization. Our results suggest that the sex pheromone released by female moths entrains males' behavioral activity rhythm to ensure synchronized timing of mating.
... However, Lepidoptera pests damage crops mainly at the larval stage, and so far, studies on the olfactory system of larvae have been very scarce [45]. In recent years, researchers have found that olfactory-related proteins are not only expressed in the larval stage of Lepidoptera insects but also play an important role in the selection of insect food [45,46]. For example, research has shown that Spodoptera littoralis larvae are significantly attracted to Z9, E11-14:Ac, a major component of adult sex pheromones-a discovery that could inform new pest-control strategies [46]. ...
... In recent years, researchers have found that olfactory-related proteins are not only expressed in the larval stage of Lepidoptera insects but also play an important role in the selection of insect food [45,46]. For example, research has shown that Spodoptera littoralis larvae are significantly attracted to Z9, E11-14:Ac, a major component of adult sex pheromones-a discovery that could inform new pest-control strategies [46]. Only two OBP genes were significantly decreased in larvae, which may be consistent with the results of taxis behavior. ...
The remarkable biological and evolutionary adaptations of insects to plants are largely attributed to the powerful chemosensory systems of insects. The tomato leaf miner (Tuta absoluta) is a destructive invasive pest with a global distribution that poses a serious threat to the production of nightshade crops, especially tomatoes. Functional plants can attract or repel insect pests by releasing volatiles that interact with the olfactory system of insects, thereby reducing the damage of insect pests to target crops. However, there is limited research on the interaction between T. absoluta olfactory genes and functional plants. In this study, 97 members of the putative odorant-binding protein (OBP) family have been identified in the whole genome of T. absoluta. Phylogenetic analysis involving various Lepidopteran and Dipteran species, including D. melanogaster, revealed that OBP gene families present conserved clustering patterns. Furthermore, the Plus-C subfamily of OBP showed extremely significant expansion. Moreover, the expression levels of the OBP genes varied significantly between different developmental stages; that is, the highest number of OBP genes were expressed in the adult stage, followed by the larval stage, and fewer genes were expressed in high abundance in the egg stage. On the other hand, through a Y-tube olfactometer, we identified a functional plant—Plectranthus tomentosa—that significantly repels adult and larval T. absoluta. Finally, we screened the OBP genes in response to tomato and P. tomentosa volatiles at the genomic level of T. absoluta using RT-qPCR. These results laid a good foundation for controlling T. absoluta with functional plants and further studying olfactory genes.
... Insects at different developmental stages have different needs for chemoreception. Adult insects, for example, greatly rely on olfaction to seek host plants and find mates and oviposition sites (Thompson & Pellmyr, 1991;Chapman, 2003), while larvae mostly need to avoid natural enemies and locate food sources (Poivet et al., 2012). ...
... In addition to morphological studies, electrophysiological methods have also been employed to provide direct functional evidence of chemosensory sensilla. Single sensillum recordings (SSR), for which an electrode penetrates the sensillum wall, were used to determine the function of an olfactory sensillum in a certain species and to make comparisons between different species (Poivet et al., 2012;Zielonka et al., 2016). Similarly, tip recordings were employed to reveal the response to tastants of gustatory receptor neurons (Bernays et al., 2002;Bernays et al., 2003;Tang et al., 2015;Wee et al., 2016). ...
... These volatiles also elicited significant attraction or repellence in the caterpillars (de Fouchier et al., 2017;Di et al., 2017;de Fouchier et al., 2018;Revadi et al., 2021). In addition, S. littoralis larvae were significantly attracted by diets laced with the female Spodoptera pheromone, although the pheromone receptor in larvae was not successfully identified (Poivet et al., 2012). ...
The olfactory system of adult lepidopterans is among the best described neuronal circuits. However, comparatively little is known about the organization of the olfactory system in the larval stage of these insects. Here, we explore the expression of olfactory receptors and the organization of olfactory sensory neurons in caterpillars of Pieris brassicae , a significant pest species in Europe and a well‐studied species for its chemical ecology. To describe the larval olfactory system in this species, we first analyzed the head transcriptome of third‐instar larvae (L3) and identified 16 odorant receptors (ORs) including the OR coreceptor (Orco), 13 ionotropic receptors (IRs), and 8 gustatory receptors (GRs). We then quantified the expression of these 16 ORs in different life stages, using qPCR, and found that the majority of ORs had significantly higher expression in the L4 stage than in the L3 and L5 stages, indicating that the larval olfactory system is not static throughout caterpillar development. Using an Orco‐specific antibody, we identified all olfactory receptor neurons (ORNs) expressing the Orco protein in L3, L4, and L5 caterpillars and found a total of 34 Orco‐positive ORNs, distributed among three sensilla on the antenna. The number of Orco‐positive ORNs did not differ among the three larval instars. Finally, we used retrograde axon tracing of the antennal nerve and identified a mean of 15 glomeruli in the larval antennal center (LAC), suggesting that the caterpillar olfactory system follows a similar design as the adult olfactory system, although with a lower numerical redundancy. Taken together, our results provide a detailed analysis of the larval olfactory neurons in P. brassicae , highlighting both the differences as well as the commonalities with the adult olfactory system. These findings contribute to a better understanding of the development of the olfactory system in insects and its life‐stage‐specific adaptations.
... A new example of autodetection was found recently in female Contarinia nasturtii (Hodgdon et al. 2021). Availability of ecological and molecular data suggested that sex pheromones had been detected only in adult moths (Poivet et al. 2012). ...
Global crop productivity is reduced by 20-40% annually due to agricultural pests. Mass trapping with insect sex-pheromones have been the major option for the pest control because of non-negative impact on both natural enemy and environment. In addition to this, we can lure and record a wide variety of insect pests with low concentrations of the insect sex pheromone which is released by female insects. However, the lack of understanding regarding the mechanism of how insect sex phero-mone lures and traps work in the field has negatively affected the application of these techniques in countries like China and Pakistan. This lack of understanding hinders growers' ability to accurately comprehend the effectiveness and proper utilization of insect sex pheromone lures in pest management. This review summarizes recent advancements in molecular understanding of insect sex pheromones (their relevant structures and compositions), mass trapping, mating disruption and peptide biosensors, various forms of insect sex pheromone traps with a focus on the integration of artificial intelligence, machine learning, deep learning, and smart trap technologies used in Asia. According to this review, the insect sex pheromone technique is not only well understood but can also be effectively utilized for agricultural pest management.
... Odor-binding proteins (OBPs) are a class of olfactory proteins that are thought to aid in capturing and transporting semiochemical odorants to receptors. OBPs are water-soluble and low-molecular-weight proteins (10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20) with six cysteine residues that stabilize the three-dimensional structure conformation and binding cavity. [1][2][3] In lepidopterans, there are two subgroups of OBPs: Pheromone Binding Proteins (PBPs), which bind insect specific pheromones, and general odor-binding proteins (GOPBs), which bind general odorant molecules. ...
... 9,10 When species-specific pheromones were added to the food, the larvae of Spodoptera littoralis were more attracted by their food. 11 The Plutella xylostella sex pheromones act as an attractant, guiding the larvae to locations where they can find better food and avoid competition. 12 In previous studies, PBPs in Lepidoptera were thought to be predominantly male-specific, while the GOBPs were expressed in both males and females. ...
BACKGROUND
General odor‐binding proteins (GOBPs) play critical roles in insect olfactory recognition of sex pheromones and plant volatiles. Therefore, the identification of GOBPs in Hyphantria cunea (Drury) based on their characterization to pheromone components and plant volatiles is remain unknown.
RESULTS
In this study, two H. cunea (HcunGOBPs) genes were cloned, and their expression profiles and odorant binding characteristics were systematically analyzed. Firstly, the tissue expression study showed that both HcunGOBP1 and HcunGOBP2 were highly expressed in the antennae of both sexes, indicating their potential involvement in the perception of sex pheromones. Secondly, these two HcunGOBPs genes were expressed in Escherichia coli and ligand binding assays were used to assess the binding affinities to its sex pheromone components including two aldehydes and two epoxides, and some plant volatiles. HcunGOBP2 showed high binding affinities to two aldehyde components (Z9, Z12, Z15‐18Ald and Z9, Z12‐18Ald), and showed low binding affinities to two epoxide components (1, Z3, Z6‐9S, 10R‐epoxy‐21Hy and Z3, Z6‐9S, 10R‐epoxy‐21Hy), whereas HcunGOBP1 showed weak but significant binding to all four sex pheromone components. Furthermore, both HcunGOBPs demonstrated variable binding affinities to the plant volatiles tested. Thirdly, in silico studies of HcunGOBPs utilized homology, structure modeling, and molecular docking revealed critical hydrophobic residues might be involved in the binding of HcunGOBPs to their sex pheromone components and plant volatiles.
CONCLUSION
Our study suggests that these two HcunGOBPs may serve as potential targets for future studies of HcunGOBPs ligand binding, providing insight in the mechanism of olfaction in H. cunea. © 2023 Society of Chemical Industry.
... In S. littoralis, Or5 is mostly expressed in adult male antennae and is necessary for male attraction toward the pheromone, whereas the duplicate Or75 is expressed in larvae chemosensory organs. Expression of this latter receptor could explain how S. littoralis larvae can smell the female sex pheromone (33). This finding points toward the importance of considering the evolution of receptor expression and not only the evolution of response spectra. ...
Pheromone communication is an essential component of reproductive isolation in animals. As such, evolution of pheromone signaling can be linked to speciation. For example, the evolution of sex pheromones is thought to have played a major role in the diversification of moths. In the crop pests Spodoptera littoralis and S. litura, the major component of the sex pheromone blend is (Z,E)-9,11-tetradecadienyl acetate, which is lacking in other Spodoptera species. It indicates that a major shift occurred in their common ancestor. It has been shown recently in S. littoralis that this compound is detected with high specificity by an atypical pheromone receptor, named SlitOR5. Here, we studied its evolutionary history through functional characterization of receptors from different Spodoptera species. SlitOR5 orthologs in S. exigua and S. frugiperda exhibited a broad tuning to several pheromone compounds. We evidenced a duplication of OR5 in a common ancestor of S. littoralis and S. litura and found that in these two species, one duplicate is also broadly tuned while the other is specific to (Z,E)-9,11-tetradecadienyl acetate. By using ancestral gene resurrection, we confirmed that this narrow tuning evolved only in one of the two copies issued from the OR5 duplication. Finally, we identified eight amino acid positions in the binding pocket of these receptors whose evolution has been responsible for narrowing the response spectrum to a single ligand. The evolution of OR5 is a clear case of subfunctionalization that could have had a determinant impact in the speciation process in Spodoptera species.
... Numerous examples show that Lepidoptera can actively orient toward volatiles from their host plants (Carroll & Berenbaum 2002, Castrejon et al. 2006, Becher & Guerin 2009, toward plants attacked by conspecific larvae (Carroll et al. 2008, Mooney et al. 2009), or selectively move away from odors of non-host plants (Piesik et al. 2009), and even detect the conspecific adult female pheromone (Poivet et al. 2012). Several species can learn the odor of their host plant on which they feed (Rojas & Wyatt 1999), and they are capable of associative learning with tastants (Salloum et al. 2011) or with noxious stimuli associated with feeding on a noxious host plant (Dethier 1980). ...
... Pheromones are expected to play a key role in this mechanism as they instigate aggregation for feeding and ovipositing in many different species 1,[28][29][30] , advertise the presence of conspecifics to aid reproduction [31][32][33][34] , and are used for communally fending off threats [35][36][37] . As pheromones have similarly been found to play a prominent role in the aggregation of D. melanogaster 31,38 , we hypothesize that they may also be able to indicate the number of flies that have visited a communal oviposition site. ...
Female fruit flies (Drosophila melanogaster) oviposit at communal sites where the larvae may cooperate or compete for resources depending on group size. This offers a model system to determine how females assess quantitative social information. We show that the concentration of pheromones found on a substrate increases linearly with the number of adult flies that have visited that site. Females prefer oviposition sites with pheromone concentrations corresponding to an intermediate number of previous visitors, whereas sites with low or high concentrations are unattractive. This dose-dependent decision is based on a blend of 11-cis-Vaccenyl Acetate (cVA) indicating the number of previous visitors and heptanal (a novel pheromone deriving from the oxidation of 7-Tricosene), which acts as a dose-independent co-factor. This response is mediated by detection of cVA by odorant receptor neurons Or67d and Or65a, and at least five different odorant receptor neurons for heptanal. Our results identify a mechanism allowing individuals to transform a linear increase of pheromones into a non-linear behavioral response.
