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Many animals use multicomponent sex pheromones for mating, but the specific function and neural processing of each pheromone component remain unclear. The cockroach Periplaneta americana is a model for studying sex pheromone communication, and an adult female emits major and minor sex pheromone components, periplanone-B and -A (PB and PA), respectively. Attraction and courtship behaviors (wing-raising and abdominal extension) are strongly expressed when adult males are exposed to PB but weakly expressed when they are exposed to PA. When major PB is presented together with minor PA, behaviors elicited by PB were impaired, indicating that PA can both promote and suppress courtship behaviors depending on the pheromonal context. In this study, we identified the receptor genes for PA and PB and investigated the effects of knocking down each receptor gene on the activities of PA- and PB-responsive sensory neurons (PA- and PB-SNs), and their postsynaptic interneurons, and as well as effects on courtship behaviors in males. We found that PB strongly and PA weakly activate PB-SNs and their postsynaptic neurons, and activation of the PB-processing pathway is critical for the expression of courtship behaviors. PA also activates PA-SNs and the PA-processing pathway. When PA and PB are simultaneously presented, the PB-processing pathway undergoes inhibitory control by the PA-processing pathway, which weakens the expression of courtship behaviors. Our data indicate that physiological interactions between the PA- and PB-processing pathways positively and negatively mediate the attraction and courtship behaviors elicited by sex pheromones.

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Aggregation of flying insects such as gypsy moths at commercial light sources in summer not only has an aesthetically negative impact on public facilities but also permits the establishment of new insect populations there from the next year. Although energy-efficient light traps equipped with light-emitting diodes (LEDs) have recently been used for controlling pest insects in agriculture, there are very few maintenance-free light traps that are available on the market. Based on the results of field surveys, we fabricated a prototype light trap in which the preferences of insects for light irradiation angle and wavelength are implemented. Field experiments revealed that flying moths were attracted more to light with a narrow irradiation angle than to light with a wide irradiation angle. Moreover, there was a tendency for fewer moths to be collected when fluorescent paint was applied to the surface of the flight-interception board, indicating that a high contrast made by illumination and the background is preferred by flying moths. Taken together with our previous results, we found that the moth catch was influenced more by modification of the light design than by change in visible light wavelengths. A semi-portable light trap, named the "Kurihara trap" after the primary contributor to its development, is made of light-weight plastic and is driven by solar power. This light trap is omnidirectional and maintenance-free and is therefore suitable for deployment in the backyards of rest areas as well as at houses for long-term macromoth sampling.

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Insect outbreaks often occur in the absence of natural enemies and in the presence of excess suitable host materials. Outbreaks of gypsy moths are especially problematic in remote areas located in high-latitude regions in Japan because the majority of adults emerge during the short summer season and initiate synchronous mass flight toward artificial lights. The aggregation of moths in public facilities not only is an annoyance to visitors but also permits the establishment of new populations the following year. The aim of this study was to establish a method to reduce the numbers of large moths that are attracted to lights in the rest areas of expressways in Hokkaido based on the results of research on their behavioral ecology and physiology. First, we conducted extensive insect surveys using light traps that emit light at different wavelengths; the traps were set along the expressways in the summers of 2014-2018. The insects attracted to the light were roughly classified into those showing a preference for broadband light wavelengths (from UV-A to green) and short light wavelengths (from UV-A to blue). The former included aquatic insects and winged ants, and the latter included moths and beetles. Next, we analyzed correlations between moth emergence and daily meteorological data. When gypsy moths were abundant during an outbreak, the daily catch of gypsy moths was positively correlated with the highest ambient temperature on the catch day but not with the visibility range, wind speed, or moon phase. In contrast, the daily catch of oak silkmoths did not correlate with any of these parameters. Our results provide guidance for the management of forest insects inhabiting cool-temperate to subarctic regions based on light wavelengths with reference to weather variables.

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The basic organization of the olfactory system has been the subject of extensive studies in vertebrates and invertebrates. In many animals, GABA-ergic neurons inhibit spike activities of higher-order olfactory neurons and help sparsening of their odor representations. In the cockroach, two different types of GABA-immunoreactive interneurons (calyceal giants [CGs]) mainly project to the base and lip regions of the calyces (input areas) of the mushroom body (MB), a second-order olfactory center. The base and lip regions receive axon terminals of two different types of projection neurons, which receive synapses from different classes of olfactory sensory neurons (OSNs), and receive dendrites of different classes of Kenyon cells, MB intrinsic neurons. We performed intracellular recordings from pairs of CGs and MB output neurons (MBONs) of male American cockroaches, the latter receiving synapses from Kenyon cells, and we found that a CG receives excitatory synapses from an MBON and that odor responses of the MBON are changed by current injection into the CG. Such feedback effects, however, were often weak or absent in pairs of neurons that belong to different streams, suggesting parallel organization of the recurrent pathways, although interactions between different streams were also evident. Cross-covariance analysis of the spike activities of CGs and MBONs suggested that odor stimulation produces synchronized spike activities in MBONs and then in CGs. We suggest that there are separate but interactive parallel streams to process odors detected by different OSNs throughout the olfactory processing system in cockroaches.SIGNIFICANCE STATEMENT Organizational principles of the olfactory system have been the subject of extensive studies. In cockroaches, signals from olfactory sensory neurons (OSNs) in two different classes of sensilla are sent to two different classes of projection neurons, which terminate in different areas of the mushroom body (MB), each area having dendrites of different classes of MB intrinsic neurons (Kenyon cells) and terminations of different classes of GABAergic neurons. Physiological and morphological assessments derived from simultaneous intracellular recordings/stainings from GABAergic neurons and MB output neurons suggested that GABAergic neurons play feedback roles and that odors detected by OSNs are processed in separate but interactive processing streams throughout the central olfactory system.

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Female Periplaneta americana cockroaches emit two cooperatively working pheromone components, periplanone-B (PB) as a long-range attractant and periplanone-A (PA) as a short-range arrestant, and males develop enlarged glomeruli for processing them separately in the first-order olfactory center. Using intracellular recordings and neuronal labelings, we found that the Turkestan cockroach, Blatta lateralis, which is phylogenetically close to P. americana but having adapted to inground habitats, has an extraordinary large glomerulus. This is caused by drastic enlargement of the PB-responsive glomerulus but not the PA-responsive glomerulus during the late nymphal stage. The output neuron from the macroglomerulus is sensitive to both PA and PB, at a dose of only 0.1 fg. Nevertheless, B. lateralis males never exhibited courtship rituals in response to the presentation of periplanones or natural sex pheromone but exhibited courtship rituals in response to antennal contact with females. Our findings indicate that the unique behavioral ecology and habitats of B. lateralis are related to the functional unification of the pheromone processing system, opposite to the functional differentiation that often underlies species diversification.

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Vertebrates and insects are phylogenetically separated by millions of years but have commonly developed tympanal membranes for efficiently converting airborne sound to mechanical oscillation in hearing. The tympanal organ of the field cricket Gryllus bimaculatus, spanning 200 µm, is one of the smallest auditory organs among animals. It indirectly links to two tympana in the prothoracic tibia via tracheal vesicles. The anterior tympanal membrane is smaller and thicker than the posterior tympanal membrane and it is thought to have minor function as a sound receiver. Using differential labeling of sensory neurons/surrounding structures and three-dimensional reconstructions, we revealed that a shell-shaped chitin mass and associated tissues are hidden behind the anterior tympanal membrane. The mass, termed the epithelial core, is progressively enlarged by discharge of cylindrical chitin from epithelial cells that start to aggregate immediately after the final molt and it reaches a plateau in size after 6 days. The core, bridging between the anterior tracheal vesicle and the fluid-filled chamber containing sensory neurons, is supported by a taut membrane, suggesting the possibility that anterior displacements of the anterior tracheal vesicle are converted into fluid motion via a lever action of the core. The epithelial core did not exist in tympanal organ homologs of meso- and metathoracic legs or of nymphal legs. Taken together, the findings suggest that the epithelial core, a potential functional homolog to mammalian ossicles, underlies fine sound frequency discrimination required for adult-specific sound communications.

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In the cockroach Periplaneta americana, to represent pheromone source in the receptive space, axon terminals of sex pheromone-receptive olfactory sensory neurons (pSNs) are topographically organized within the primary center, the macroglomerulus, according to the peripheral locations of sex pheromone-receptive single walled (sw)-B sensilla. In this study, we sought to determine when and where pSNs emerge in the nymphal antenna. We revealed two different pSN proliferation patterns that underlie the formation of topographic organization in the macroglomerulus. In nymphal antennae, which lack sw-B sensilla, pSNs are identified in the shorter sensilla, termed sw-A sensilla. Because new sw-A sensilla emerge on the proximal antenna at every molt, topographic organization in the macroglomerulus must be formed by adding axon terminals of newly emerged pSNs to the lateral region in the macroglomerulus at each molt. At the final molt, a huge number of new sw-B sensilla appeared throughout the whole antenna. Sw-B sensilla in the proximal part of the adult antenna were newly formed during the last instar stage, whereas those located in the distal antenna were transformed from sw-A sensilla. This transformation was accompanied by an increase in the number of pSNs. Axon terminals of newborn pSNs in new sw-B sensilla were recruited to the lateral part of the macroglomerulus, whereas those of newborn pSNs in transformed sw-B sensilla were recruited to the macroglomerulus according to the sensillar location. These mechanisms enable an increase in sensitivity to sex pheromone in adulthood while retaining the topographic map formed during the postembryonic development.

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