@article{liu_heath_zhang_wijk_wang_buellesbach_wada-katsumata_groot_schal_2023, title={A mosaic of endogenous and plant-derived courtship signals in moths}, volume={33}, ISSN={["1879-0445"]}, url={https://doi.org/10.1016/j.cub.2023.07.010}, DOI={10.1016/j.cub.2023.07.010}, abstractNote={Insects rely on olfaction to guide a wide range of adaptive behaviors, including mate and food localization, mate choice, oviposition site selection, kin recognition, and predator avoidance.1Wyatt T.D. Pheromones and Animal Behaviour: Communication by Smell and Taste. Cambridge University Press, 2003Crossref Google Scholar In nocturnal insects, such as moths2Allison J.D. Cardé R.T. Pheromone Communication in Moths: Evolution, Behavior, and Application. University of California Press, 2016Crossref Google Scholar and cockroaches,3Gemeno C. Schal C. Sex pheromones of cockroaches.in: Cardé R.T. Millar J.G. Advances in Insect Chemical Ecology. Cambridge University Press, 2004: 179-247Crossref Google Scholar mate finding is stimulated predominantly by long-range species-specific sex pheromones, typically emitted by females. During courtship, at close range, males in most moth species emit a blend of pheromone compounds from an everted, often large, pheromone gland. While long-distance communication with sex pheromones has been remarkably well characterized in thousands of moth species,2Allison J.D. Cardé R.T. Pheromone Communication in Moths: Evolution, Behavior, and Application. University of California Press, 2016Crossref Google Scholar,4El-Sayed A.M. The Pherobase: Database of Insect Pheromones and Semiochemicals.2012http://www.pherobase.comGoogle Scholar close-range chemosensory sexual communication remains poorly understood. We reveal that in the moth Chloridea virescens, the male pheromone consists of three distinct classes of compounds: de novo biosynthesized alcohols, aldehydes, acetates, and carboxylic acids that resemble the female’s emissions; newly identified compounds that are unique to the male pheromone, such as aliphatic polyunsaturated hydrocarbons; and sequestered plant secondary compounds and hormone derivatives, including methyl salicylate (MeSA). Thus, males employ a mosaic pheromone blend of disparate origins that may serve multiple functions during courtship. We show that two olfactory receptors in female antennae are tuned to MeSA, which facilitates female acceptance of the male. Because MeSA is emitted by plants attacked by pathogens and herbivores,5Takabayashi J. Shiojiri K. Multifunctionality of herbivory-induced plant volatiles in chemical communication in tritrophic interactions.Curr. Opin. Insect Sci. 2019; 32: 110-117https://doi.org/10.1016/j.cois.2019.01.003Crossref PubMed Scopus (54) Google Scholar the chemosensory system of female moths was likely already tuned to this plant volatile, and males appear to exploit the female’s preadapted sensory bias. Interestingly, while female moths (largely nocturnal) and butterflies (diurnal) diverged in their use of sensory modalities in sexual communication,6Ehlers S. Schulz S. The scent chemistry of butterflies.Nat. Prod. Rep. 2023; 40: 794-818https://doi.org/10.1039/D2NP00067ACrossref PubMed Google Scholar MeSA is used by males of both lineages.}, number={16}, journal={CURRENT BIOLOGY}, author={Liu, Yang and Heath, Jeremy J. and Zhang, Sai and Wijk, Michiel and Wang, Guirong and Buellesbach, Jan and Wada-Katsumata, Ayako and Groot, Astrid T. and Schal, Coby}, year={2023}, month={Aug} }
 @article{hamilton_wada-katsumata_schal_2023, title={Cockroaches as Trojan Horses for Control of Cockroach Aggregations With Baits}, volume={2}, ISSN={["1938-291X"]}, url={https://doi.org/10.1093/jee/toad018}, DOI={10.1093/jee/toad018}, abstractNote={Gel bait formulations of insecticides have been shown to be highly effective in managing German cockroach (Blattella germanica L. [Blattodea: Ectobiidae]) populations. Three potential reasons for this are high palatability of baits, the use of slow-acting insecticides, and their horizontal transfer within aggregations, a phenomenon known as 'secondary mortality'. Our objective was to determine whether horizontal transfer can go beyond secondary, to tertiary and quaternary effects, and to compare various gel baits with different active ingredients. We fed adult females a bait and recorded their bait consumption, moribundity, and mortality. Groups of first instars were then exposed to the dead females and their feces, secondary mortality was quantified, and a new cohort of nymphs was then exposed to the feces and dead nymphs (for tertiary mortality); this process was repeated for quaternary mortality. This design did not distinguish among the major mechanisms of horizontal transfer of insecticides, namely coprophagy and contact with feces, exposure to regurgitated fluids, and cannibalism and necrophagy of nymphs. All the tested baits caused 100% mortality of the adult females that directly fed on the bait and high secondary mortality (average of >85%) within 48 hr. Baits containing either dinotefuran, emamectin benzoate, fipronil, or indoxacarb caused tertiary mortality (average of 15-70%), but only the fipronil and indoxacarb baits caused some quaternary mortality. The relative importance of secondary, tertiary, and quaternary transfer of the active ingredient remains to be determined in field populations of the German cockroach.}, journal={JOURNAL OF ECONOMIC ENTOMOLOGY}, author={Hamilton, Jamora A. and Wada-Katsumata, Ayako and Schal, Coby}, editor={Appel, ArthurEditor}, year={2023}, month={Feb} }
 @article{wada-katsumata_hatano_schal_2023, title={Gustatory polymorphism mediates a new adaptive courtship strategy}, volume={290}, ISSN={["1471-2954"]}, url={https://doi.org/10.1098/rspb.2022.2337}, DOI={10.1098/rspb.2022.2337}, abstractNote={Human-imposed selection can lead to adaptive changes in sensory traits. However, rapid evolution of the sensory system can interfere with other behaviours, and animals must overcome such sensory conflicts. In response to intense selection by insecticide baits that contain glucose, German cockroaches evolved glucose-aversion (GA), which confers behavioural resistance against baits. During courtship the male offers the female a nuptial gift that contains maltose, which expediates copulation. However, the female's saliva rapidly hydrolyses maltose into glucose, which causes GA females to dismount the courting male, thus reducing their mating success. Comparative analysis revealed two adaptive traits in GA males. They produce more maltotriose, which is more resilient to salivary glucosidases, and they initiate copulation faster than wild-type males, before GA females interrupt their nuptial feeding and dismount the male. Recombinant lines of the two strains showed that the two emergent traits of GA males were not genetically associated with the GA trait. Results suggest that the two courtship traits emerged in response to the altered sexual behaviour of GA females and independently of the male's GA trait. Although rapid adaptive evolution generates sexual mismatches that lower fitness, compensatory behavioural evolution can correct these sensory discrepancies.}, number={1995}, journal={PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES}, author={Wada-Katsumata, Ayako and Hatano, Eduardo and Schal, Coby}, year={2023}, month={Mar} }
 @article{saveer_hatano_wada-katsumata_meagher_schal_2023, title={Nonanal, a new fall armyworm sex pheromone component, significantly increases the efficacy of pheromone lures}, volume={4}, ISSN={["1526-4998"]}, url={https://doi.org/10.1002/ps.7460}, DOI={10.1002/ps.7460}, abstractNote={Abstract Background The fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith), is a global pest that feeds on >350 plant species and severely limits production of cultivated grasses, vegetable crops and cotton. An efficient way to detect new invasions at early stages, and monitor and quantify the status of established infestations of this pest is to deploy traps baited with species‐specific synthetic sex pheromone lures. Results We re‐examined the compounds in the sex pheromone glands of FAW females by gas chromatography‐electroantennogram detector (GC‐EAD), GC–mass spectrometry (MS), behavioral and field assays. A new bioactive compound from pheromone gland extracts was detected in low amounts (3.0% relative to ( Z )‐9‐tetradecenyl acetate (Z9‐14:OAc), the main pheromone component), and identified as nonanal. This aldehyde significantly increased attraction of male moths to a mix of Z9‐14:OAc and ( Z )‐7‐dodecenyl acetate in olfactometer assays. Adding nonanal to this two‐component mix also doubled male trap catches relative to the two‐component mix alone in cotton fields, whereas nonanal alone did not attract any moths. The addition of nonanal to each of three commercial pheromone lures also increased male catches by 53–135% in sorghum and cotton fields. Conclusion The addition of nonanal to pheromone lures should improve surveillance, monitoring and control of FAW populations. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.}, journal={PEST MANAGEMENT SCIENCE}, author={Saveer, Ahmed M. and Hatano, Eduardo and Wada-Katsumata, Ayako and Meagher, Robert L. and Schal, Coby}, year={2023}, month={Apr} }
 @article{mcpherson_wada-katsumata_hatano_silverman_schal_2022, title={Nutritional condition affects tergal gland secretion and courtship success of male cockroaches}, volume={17}, ISSN={["1932-6203"]}, url={https://doi.org/10.1371/journal.pone.0271344}, DOI={10.1371/journal.pone.0271344}, abstractNote={An integral part of the courtship sequence of the German cockroach ( Blattella germanica ) involves the male raising his wings to expose tergal glands on his dorsum. When a female cockroach feeds on the secretion of these glands, she is optimally positioned for mating. Core chemical components have been identified, but the effect of male diet on the quality of the tergal gland secretion remains unexplored. After validating the pivotal role of tergal feeding in mating, we starved or fed reproductively mature males for one week. We then paired each male with a sexually receptive female and observed their interactions through an infrared-sensitive camera. While starvation had no effect on male courtship behavior, it did influence the duration of female tergal feeding and mating outcomes. Females fed longer on the gland secretion of fed males, and fed males experienced greater mating success than starved males (73.9% vs. 48.3%, respectively). These results suggest that the quality of the tergal gland secretions, and by association mating success, are dependent on the nutritional condition of the male.}, number={8}, journal={PLOS ONE}, author={McPherson, Samantha and Wada-Katsumata, Ayako and Hatano, Eduardo and Silverman, Jules and Schal, Coby}, editor={Borges, Renee M.Editor}, year={2022} }
 @article{katte_shimoda_kobayashi_wada-katsumata_nishida_ohshima_ono_2022, title={Oviposition stimulants underlying different preferences between host races in the leaf-mining moth Acrocercops transecta (Lepidoptera: Gracillariidae)}, volume={12}, ISSN={["2045-2322"]}, DOI={10.1038/s41598-022-18238-0}, abstractNote={Abstract The importance of plant chemistry in the host specialization of phytophagous insects has been emphasized. However, only a few chemicals associated with host shifting have been characterized. Herein, we focus on the leaf-mining moth Acrocercops transecta (Gracillariidae) consisting of ancestral Juglans (Juglandaceae)- and derived Lyonia (Ericaceae)-associated host races. The females of the Lyonia race laid eggs on a cover glass treated with an L . ovalifolia leaf extract; the extract was fractionated using silica gel and ODS column chromatography to isolate the oviposition stimulants. From a separated fraction, two analogous Lyonia -specific triterpenoid glycosides were characterized as oviposition stimulants. Furthermore, we observed probable contact chemosensilla on the distal portion of the female antennae. Lyonia race females laid their eggs on the non-host Juglans after the leaves were treated with a Lyonia -specific oviposition stimulant, although they do not lay eggs on Juglans . These results suggest that Lyonia race females do not lay eggs on Juglans leaves because the leaves do not contain specific oviposition stimulant(s). Otherwise, the activity of the oviposition stimulants overcomes oviposition deterrents contained in Juglans leaves. This paper describes the roles of plant chemicals in the different preferences between host races associated with distantly related plant taxa.}, number={1}, journal={SCIENTIFIC REPORTS}, author={Katte, Tomoko and Shimoda, Shota and Kobayashi, Takuya and Wada-Katsumata, Ayako and Nishida, Ritsuo and Ohshima, Issei and Ono, Hajime}, year={2022}, month={Aug} }
 @article{wada-katsumata_hatano_mcpherson_silverman_schal_2022, title={Rapid evolution of an adaptive taste polymorphism disrupts courtship behavior}, volume={5}, ISSN={["2399-3642"]}, url={https://doi.org/10.1038/s42003-022-03415-8}, DOI={10.1038/s42003-022-03415-8}, abstractNote={Abstract The evolution of adaptive behavior often requires changes in sensory systems. However, rapid adaptive changes in sensory traits can adversely affect other fitness-related behaviors. In the German cockroach, a gustatory polymorphism, ‘glucose-aversion (GA)’, supports greater survivorship under selection with glucose-containing insecticide baits and promotes the evolution of behavioral resistance. Yet, sugars are prominent components of the male’s nuptial gift and play an essential role in courtship. Behavioral and chemical analyses revealed that the saliva of GA females rapidly degrades nuptial gift sugars into glucose, and the inversion of a tasty nuptial gift to an aversive stimulus often causes GA females to reject courting males. Thus, the rapid emergence of an adaptive change in the gustatory system supports foraging, but it interferes with courtship. The trade-off between natural and sexual selection under human-imposed selection can lead to directional selection on courtship behavior that favors the GA genotype.}, number={1}, journal={COMMUNICATIONS BIOLOGY}, author={Wada-Katsumata, Ayako and Hatano, Eduardo and McPherson, Samantha and Silverman, Jules and Schal, Coby}, year={2022}, month={May} }
 @article{mcpherson_wada-katsumata_hatano_silverman_schal_2021, title={Comparison of Diet Preferences of Laboratory-Reared and Apartment-Collected German Cockroaches}, volume={114}, ISSN={["1938-291X"]}, url={http://dx.doi.org/10.1093/jee/toab139}, DOI={10.1093/jee/toab139}, abstractNote={The German cockroach, Blattella germanica (L.) (Blattodea: Ectobiidae), is a common pest of human-built structures worldwide. German cockroaches are generalist omnivores able to survive on a wide variety of foods. A number of studies have concluded that laboratory-reared B. germanica self-select diets with an approximate 1P:3C (protein-to-carbohydrate) ratio. We predicted that field-collected insects would exhibit more variable dietary preferences, related to the wide-ranging quality, quantity, and patchiness of foods available to them. We compared diet self-selection of B. germanica within apartments and in the laboratory by offering them a choice of two complementary diets with 1P:1C and 1P:11C ratios. We observed high variation in the population-level self-selection of these diets among individual apartment sites as well as among various life stages tested in laboratory-based assays. Significant differences between populations in various apartments as well as between populations maintained in the laboratory suggested that factors beyond temporary food scarcity influence diet choice. Nevertheless, we found significant correlations between the amounts of diets ingested by cockroaches in apartments and cockroaches from the same populations assayed in the laboratory, as well as between males, females, and nymphs from these populations. These findings suggest that females, males, and nymphs within apartments adapt to the local conditions and convergently prefer similar amounts of food of similar dietary protein content.}, number={5}, journal={JOURNAL OF ECONOMIC ENTOMOLOGY}, publisher={Oxford University Press (OUP)}, author={McPherson, Samantha and Wada-Katsumata, Ayako and Hatano, Eduardo and Silverman, Jules and Schal, Coby}, editor={Appel, ArthurEditor}, year={2021}, month={Oct}, pages={2189–2197} }
 @article{hamilton_wada‐katsumata_ko_schal_2021, title={Effects of novaluron ingestion and topical application on German cockroach (Blattella germanica) development and reproduction}, volume={77}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85092035578&partnerID=MN8TOARS}, DOI={10.1002/ps.6092}, abstractNote={Abstract BACKGROUND Insect growth regulators disrupt insect development and reproduction. Chitin synthesis inhibitors (CSIs) allow the insect to grow normally, but because chitin is an essential component of the cuticle, formation of a new cuticle and ecdysis are prevented and the insect dies. CSIs can also kill embryos by disrupting their normal development. We evaluated the potential utility of novaluron in bait formulations against the German cockroach ( Blattella germanica L . ). RESULTS The minimum novaluron intake that interfered with molting and reproduction was assessed by exposing nymphs and adult females to novaluron. Results showed that 1 day of feeding on 0.1% novaluron was sufficient to disrupt molting in nymphs and prevent adult females from developing viable oothecae. The long‐term effects on gravid females were investigated by feeding females 0.1% novaluron for different 5‐day intervals during successive stages of gestation. Results demonstrated that gravid females fed novaluron during any period of gestation were able to produce viable eggs. To determine if ingestion of novaluron affected mating success and fertility of adult males, males were fed novaluron and then allowed to mate with untreated virgin females. Males that fed on novaluron successfully mated, and the females produced viable oothecae. Finally, direct comparisons revealed that novaluron is equally effective by ingestion and topical application. CONCLUSIONS Novaluron caused mortality in nymphs and interfered with ootheca production in adult females, but only before they formed an ootheca. It successfully reduced German cockroach populations in cages and has potential to be incorporated in cockroach baits.}, number={2}, journal={Pest Management Science}, author={Hamilton, Jamora A and Wada‐Katsumata, Ayako and Ko, Alexander and Schal, Coby}, year={2021}, pages={877–885} }
 @article{wada-katsumata_schal_2021, title={Olfactory Learning Supports an Adaptive Sugar-Aversion Gustatory Phenotype in the German Cockroach}, volume={12}, ISSN={["2075-4450"]}, url={https://www.mdpi.com/2075-4450/12/8/724}, DOI={10.3390/insects12080724}, abstractNote={An association of food sources with odors prominently guides foraging behavior in animals. To understand the interaction of olfactory memory and food preferences, we used glucose-averse (GA) German cockroaches. Multiple populations of cockroaches evolved a gustatory polymorphism where glucose is perceived as a deterrent and enables GA cockroaches to avoid eating glucose-containing toxic baits. Comparative behavioral analysis using an operant conditioning paradigm revealed that learning and memory guide foraging decisions. Cockroaches learned to associate specific food odors with fructose (phagostimulant, reward) within only a 1 h conditioning session, and with caffeine (deterrent, punishment) after only three 1 h conditioning sessions. Glucose acted as reward in wild type (WT) cockroaches, but GA cockroaches learned to avoid an innately attractive odor that was associated with glucose. Olfactory memory was retained for at least 3 days after three 1 h conditioning sessions. Our results reveal that specific tastants can serve as potent reward or punishment in olfactory associative learning, which reinforces gustatory food preferences. Olfactory learning, therefore, reinforces behavioral resistance of GA cockroaches to sugar-containing toxic baits. Cockroaches may also generalize their olfactory learning to baits that contain the same or similar attractive odors even if they do not contain glucose.}, number={8}, journal={INSECTS}, author={Wada-Katsumata, Ayako and Schal, Coby}, year={2021}, month={Aug} }
 @unpublished{wada-katsumata_schal_2021, title={Olfactory Learning Supports an Adaptive Sugar-Aversion Gustatory Phenotype in the German Cockroach}, volume={7}, url={https://doi.org/10.20944/preprints202107.0696.v1}, DOI={10.20944/preprints202107.0696.v1}, abstractNote={An association of food sources with odors prominently guides foraging behavior in animals. To understand the interaction of olfactory memory and food preferences, we used glucose-averse (GA) German cockroaches. Multiple populations of cockroaches evolved a gustatory polymorphism where glucose is perceived as a deterrent and enables GA cockroaches to avoid eating glucose-containing toxic baits. Comparative behavioral analysis using an operant conditioning paradigm revealed that learning and memory guide foraging decisions. Cockroaches learned to associate specific food odors with fructose (phagostimulant, reward) within only a 1 hr conditioning session, and with caffeine (deterrent, punishment) after only three 1 hr conditioning sessions. Glucose acted as reward in wild type (WT) cockroaches, but GA cockroaches learned to avoid an innately attractive odor that was associated with glucose. Olfactory memory was retained for at least 3 days after three 1 hr conditioning sessions. Our results reveal that specific tastants can serve as potent reward or punishment in olfactory associative learning, which reinforces gustatory food preferences. Olfactory learning therefore reinforces behavioral resistance of GA cockroaches to sugar-containing toxic baits. Cockroaches may also generalize their olfactory learning to baits that contain the same or similar attractive odors even if they do not contain glucose.}, publisher={MDPI AG}, author={Wada-Katsumata, Ayako and Schal, Coby}, year={2021}, month={Jul} }
 @article{wada-katsumata_schal_2021, title={Salivary Digestion Extends the Range of Sugar-Aversions in the German Cockroach}, volume={12}, ISSN={["2075-4450"]}, url={https://www.mdpi.com/2075-4450/12/3/263}, DOI={10.3390/insects12030263}, abstractNote={Saliva has diverse functions in feeding behavior of animals. However, the impact of salivary digestion of food on insect gustatory information processing is poorly documented. Glucose-aversion (GA) in the German cockroach, Blattella germanica, is a highly adaptive heritable behavioral resistance trait that protects the cockroach from ingesting glucose-containing-insecticide-baits. In this study, we confirmed that GA cockroaches rejected glucose, but they accepted oligosaccharides. However, whereas wild-type cockroaches that accepted glucose also satiated on oligosaccharides, GA cockroaches ceased ingesting the oligosaccharides within seconds, resulting in significantly lower consumption. We hypothesized that saliva might hydrolyze oligosaccharides, releasing glucose and terminating feeding. By mixing artificially collected cockroach saliva with various oligosaccharides, we demonstrated oligosaccharide-aversion in GA cockroaches. Acarbose, an alpha-glucosidase inhibitor, prevented the accumulation of glucose and rescued the phagostimulatory response and ingestion of oligosaccharides. Our results indicate that pre-oral and oral hydrolysis of oligosaccharides by salivary alpha-glucosidases released glucose, which was then processed by the gustatory system of GA cockroaches as a deterrent and caused the rejection of food. We suggest that the genetic mechanism of glucose-aversion support an extended aversion phenotype that includes glucose-containing oligosaccharides. Salivary digestion protects the cockroach from ingesting toxic chemicals and thus could support the rapid evolution of behavioral and physiological resistance in cockroach populations.}, number={3}, journal={INSECTS}, author={Wada-Katsumata, Ayako and Schal, Coby}, year={2021}, month={Mar} }
 @unpublished{wada-katsumata_schal_2021, title={Salivary Digestion Extends the Range of Sugar-Aversions in the German Cockroach}, volume={3}, url={https://doi.org/10.20944/preprints202103.0048.v1}, DOI={10.20944/preprints202103.0048.v1}, abstractNote={Saliva has diverse functions in feeding behavior of animals. However, the impact of salivary digestion of food on insect gustatory information processing is poorly documented. Glucose-aversion (GA) in the German cockroach, Blattella germanica, is a highly adaptive heritable behavioral resistance trait that protects the cockroach from ingesting glucose-containing-insecticide-baits. In this study, we confirmed that GA cockroaches rejected glucose, but they accepted oligosaccharides. However, whereas wild-type cockroaches that accepted glucose also satiated on oligosaccharides, GA cockroaches ceased ingesting the oligosaccharides within seconds, resulting in significantly lower consumption. We hypothesized that saliva might hydrolyze oligosaccharides, releasing glucose and terminating feeding. By mixing artificially collected cockroach saliva with various oligosaccharides, we demonstrated oligosaccharide-aversion in GA cockroaches. Acarbose, an alpha-glucosidase inhibitor, prevented the accumulation of glucose and rescued the phagostimulatory response and ingestion of oligosaccharides. Our results indicate that pre-oral and oral hydrolysis of oligosaccharides by salivary alpha-glucosidases released glucose, which was then processed by the gustatory system of GA cockroaches as a deterrent and caused the rejection of food. We suggest that the genetic mechanism of glucose-aversion support an extended aversion phenotype that includes glucose-containing oligosaccharides. Salivary digestion protects the cockroach from ingesting toxic chemicals and thus could support the rapid evolution of behavioral and physiological resistance in cockroach populations.}, publisher={MDPI AG}, author={Wada-Katsumata, Ayako and Schal, Coby}, year={2021}, month={Mar} }
 @article{kakumanu_marayati_wada-katsumata_wasserberg_schal_apperson_ponnusamy_2021, title={Sphingobacterium phlebotomi sp. nov., a new member of family Sphingobacteriaceae isolated from sand fly rearing substrate}, volume={71}, ISSN={["1466-5034"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85105243609&partnerID=MN8TOARS}, DOI={10.1099/ijsem.0.004809}, abstractNote={A Gram-stain-negative, rod-shaped, non-motile, non-spore-forming, aerobic bacterium, designated type strain SSI9 T , was isolated from sand fly ( Phlebotomus papatasi Scopoli; Diptera: Psychodidae ) rearing substrate and subjected to polyphasic taxonomic analysis. Strain SSI9 T contained phosphatidylethanolamine as a major polar lipid, MK-7 as the predominant quinone, and C 16 : 1 ω6 c /C 16 : 1 ω 7c , iso-C 15 : 0 , iso-C 17 : 0 3-OH and C 16 : 0 as the major cellular fatty acids. Phylogenetic analysis based on 16S rRNA gene sequences revealed that SSI9 T represents a member of the genus Sphingobacterium , of the family Sphingobacteriaceae sharing 96.5–88.0 % sequence similarity with other species of the genus Sphingobacterium . The results of multilocus sequence analysis using the concatenated sequences of the housekeeping genes rec A, rpl C and gro L indicated that SSI9 T formed a separate branch in the genus Sphingobacterium . The genome of SSI9 T is 5 197 142 bp with a DNA G+C content of 41.8 mol% and encodes 4395 predicted coding sequences, 49 tRNAs, and three complete rRNAs and two partial rRNAs. SSI9 T could be distinguished from other species of the genus Sphingobacterium with validly published names by several phenotypic, chemotaxonomic and genomic characteristics. On the basis of the results of this polyphasic taxonomic analysis, the bacterial isolate represents a novel species within the genus Sphingobacterium , for which the name Sphingobacterium phlebotomi sp. nov. is proposed. The type strain is SSI9 T (=ATCC TSD-210 T =LMG 31664 T =NRRL B-65603 T ).}, number={5}, journal={INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY}, author={Kakumanu, Madhavi L. and Marayati, Bahjat Fadi and Wada-Katsumata, Ayako and Wasserberg, Gideon and Schal, Coby and Apperson, Charles S. and Ponnusamy, Loganathan}, year={2021} }
 @article{hatano_wada-katsumata_schal_2020, title={Environmental decomposition of olefinic cuticular hydrocarbons of Periplaneta americana generates a volatile pheromone that guides social behaviour}, volume={287}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85080045912&partnerID=MN8TOARS}, DOI={10.1098/rspb.2019.2466}, abstractNote={Once emitted, semiochemicals are exposed to reactive environmental factors that may alter them, thus disrupting chemical communication. Some species, however, might have adapted to detect environmentally mediated breakdown products of their natural chemicals as semiochemicals. We demonstrate that air, water vapour and ultraviolet (UV) radiation break down unsaturated cuticular hydrocarbons (CHCs) of Periplaneta americana (American cockroach), resulting in the emission of volatile organic compounds (VOCs). In behavioural assays, nymphs strongly avoided aggregating in shelters exposed to the breakdown VOCs from cuticular alkenes. The three treatments (air, water vapour, UV) produced the same VOCs, but at different time-courses and ratios. Fourteen VOCs from UV-exposed CHCs elicited electrophysiological responses in nymph antennae; 10 were identified as 2-nonanone, 1-pentanol, 1-octanol, 1-nonanol, tetradecanal, acetic acid, propanoic acid, butanoic acid, pentanoic acid and hexanoic acid. When short-chain fatty acids were tested as a mix and a blend of the alcohols and aldehyde was tested as a second mix, nymphs exhibited no preference for control or treated shelters. However, nymphs avoided shelters that were exposed to VOCs from the complete 10-compound mix. Conditioned shelters (occupied by cockroaches with faeces and CHCs deposited on the shelters), which are normally highly attractive to nymphs, were also avoided after UV exposure, confirming that breakdown products from deposited metabolites, including CHCs, mediate this behaviour. Our results demonstrate that common environmental agents degrade CHCs into behaviourally active volatile compounds that potentially may serve as necromones or epideictic pheromones, mediating group dissolution.}, number={1921}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Hatano, Eduardo and Wada-Katsumata, Ayako and Schal, Coby}, year={2020}, pages={20192466} }
 @article{yanagawa_huang_yamamoto_wada-katsumata_schal_mackay_2020, title={Genetic Basis of Natural Variation in Spontaneous Grooming in Drosophila melanogaster}, volume={10}, ISSN={["2160-1836"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85090276700&partnerID=MN8TOARS}, DOI={10.1534/g3.120.401360}, abstractNote={Spontaneous grooming behavior is a component of insect fitness. We quantified spontaneous grooming behavior in 201 sequenced lines of the Drosophila melanogaster Genetic Reference Panel and observed significant genetic variation in spontaneous grooming, with broad-sense heritabilities of 0.25 and 0.24 in females and males, respectively. Although grooming behavior is highly correlated between males and females, we observed significant sex by genotype interactions, indicating that the genetic basis of spontaneous grooming is partially distinct in the two sexes. We performed genome-wide association analyses of grooming behavior, and mapped 107 molecular polymorphisms associated with spontaneous grooming behavior, of which 73 were in or near 70 genes and 34 were over 1 kilobase from the nearest gene. The candidate genes were associated with a wide variety of gene ontology terms, and several of the candidate genes were significantly enriched in a genetic interaction network. We performed functional assessments of 29 candidate genes using RNA interference, and found that 11 affected spontaneous grooming behavior. The genes associated with natural variation in Drosophila grooming are involved with glutamate metabolism (Gdh) and transport (Eaat); interact genetically with (CCKLR-17D1) or are in the same gene family as (PGRP-LA) genes previously implicated in grooming behavior; are involved in the development of the nervous system and other tissues; or regulate the Notch and Epidermal growth factor receptor signaling pathways. Several DGRP lines exhibited extreme grooming behavior. Excessive grooming behavior can serve as a model for repetitive behaviors diagnostic of several human neuropsychiatric diseases.}, number={9}, journal={G3-GENES GENOMES GENETICS}, author={Yanagawa, Aya and Huang, Wen and Yamamoto, Akihiko and Wada-Katsumata, Ayako and Schal, Coby and Mackay, Trudy F. C.}, year={2020}, month={Sep}, pages={3453–3460} }
 @article{wada-katsumata_schal_2019, title={Antennal grooming facilitates courtship performance in a group-living insect, the German cockroach Blattella germanica}, volume={9}, ISSN={["2045-2322"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85062208237&partnerID=MN8TOARS}, DOI={10.1038/s41598-019-39868-x}, abstractNote={The antennae of adult male German cockroaches detect a contact sex pheromone embedded in the female's cuticular lipids. The female pheromone stimulates courtship behavior in males, notably a wing-raising (WR) display. Within aggregations, however, cuticular lipids are disseminated by contact among group members, including nymphs and adults of both sexes, and "contamination" of cockroaches with the cuticular lipids of another stage or sex may interfere with sex discrimination and disrupt courtship. We used behavioral observations, bioassays and chemical analysis to determine how males maintain their sensitivity to sex pheromone in aggregations. Males contaminated with female pheromone displayed lower courtship, because residual female pheromone on their antennae adapted their peripheral sensilla and habituated the central nervous system. Female pheromone that contaminated the male's antennae also elicited courtship from other non-contaminated males, disrupting their sex discrimination in the group. However, antennal grooming effectively removed female pheromone from males' antennae and maintained their chemosensory acuity and sexual discrimination among group members. Thus, grooming of the antennae and other sensory appendages is an important strategy to enhance sensory acuity, especially in group-living insects like the German cockroach.}, number={1}, journal={SCIENTIFIC REPORTS}, author={Wada-Katsumata, Ayako and Schal, Coby}, year={2019}, month={Feb} }
 @article{hatano_wada-katsumata_schal_2019, title={Environmental decomposition of cuticular hydrocarbons generates a volatile pheromone that guides insect social behavior}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85095643670&partnerID=MN8TOARS}, DOI={10.1101/773937}, abstractNote={Abstract Once emitted, semiochemicals are exposed to reactive environmental factors that may alter them, thus disrupting chemical communication. Some species, however, might have adapted to detect environmentally mediated breakdown products of their natural chemicals as semiochemicals. We demonstrate that air, water vapor, and ultraviolet (UV) radiation break down unsaturated cuticular hydrocarbons (CHCs) of Periplaneta americana (American cockroach), resulting in the emission of volatile organic compounds (VOCs). In behavioral assays, nymphs strongly avoided aggregating in shelters exposed to the breakdown VOCs from cuticular alkenes. The three treatments (air, water vapor, UV) produced the same VOCs, but at different time-courses and ratios. Fourteen VOCs from UV-exposed CHCs elicited electrophysiological responses in nymph antennae; 10 were identified as 1-pentanol, 1-octanol, 1-nonanol, tetradecanal, acetic acid, propanoic acid, butanoic acid, pentanoic acid and hexanoic acid. When short-chain fatty acids were tested as a mix and a blend of the alcohols and aldehyde was tested as a second mix, nymphs exhibited no preference for control or treated shelters. However, nymphs avoided shelters that were exposed to VOCs from the complete 10-compound mix. Conditioned shelters (occupied by cockroaches with feces and CHCs deposited on the shelters), which are normally highly attractive to nymphs, were also avoided after UV-exposure, confirming that breakdown products from deposited metabolites, including CHCs, mediate this behavior. Our results demonstrate that common environmental and anthropogenic agents degrade CHCs into volatile semiochemicals that may serve as necromones or epideictic pheromones, mediating group formation and dissolution. Significance Statement Cuticular hydrocarbons (CHCs) cover the outer surface of insects, where they prevent water loss and serve as sex pheromones and in nest-mate recognition in social insects. Although CHCs are not volatile, they can be broken into volatile fragments by reacting with environmental agents. We demonstrate that volatile breakdown products of CHCs affect the social behavior of the American cockroach. A synthetic mix of volatiles dispersed cockroaches away from shelters, signaling an unsuitable shelter. These results highlight that some insect species have evolved communication strategies that exploit environmental and anthropogenic agents to produce bioactive compounds that mediate ecological interactions.}, journal={bioRxiv}, author={Hatano, E. and Wada-Katsumata, A. and Schal, C.}, year={2019} }
 @article{wexler_delaney_belles_schal_wada-katsumata_amicucci_kopp_2019, title={Hemimetabolous insects elucidate the origin of sexual development via alternative splicing}, volume={8}, ISSN={2050-084X}, url={http://dx.doi.org/10.7554/eLife.47490}, DOI={10.7554/eLife.47490}, abstractNote={Insects are the only known animals in which sexual differentiation is controlled by sex-specific splicing. The doublesex transcription factor produces distinct male and female isoforms, which are both essential for sex-specific development. dsx splicing depends on transformer, which is also alternatively spliced such that functional Tra is only present in females. This pathway has evolved from an ancestral mechanism where dsx was independent of tra and expressed and required only in males. To reconstruct this transition, we examined three basal, hemimetabolous insect orders: Hemiptera, Phthiraptera, and Blattodea. We show that tra and dsx have distinct functions in these insects, reflecting different stages in the changeover from a transcription-based to a splicing-based mode of sexual differentiation. We propose that the canonical insect tra-dsx pathway evolved via merger between expanding dsx function (from males to both sexes) and narrowing tra function (from a general splicing factor to dedicated regulator of dsx).}, journal={eLife}, publisher={eLife Sciences Publications, Ltd}, author={Wexler, Judith and Delaney, Emily Kay and Belles, Xavier and Schal, Coby and Wada-Katsumata, Ayako and Amicucci, Matthew J and Kopp, Artyom}, year={2019}, month={Sep} }
 @article{wexler_delaney_belles_schal_wada-katsumata_amicucci_kopp_2019, title={Hemimetabolous insects elucidate the origin of sexual development via alternative splicing}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85095617834&partnerID=MN8TOARS}, DOI={10.1101/587964}, abstractNote={ABSTRACT Insects are the only animals in which sexual differentiation is controlled by sex-specific RNA splicing. The doublesex ( dsx ) transcription factor produces distinct male and female protein isoforms (DsxM and DsxF) under the control of the RNA splicing factor transformer ( tra ). tra itself is also alternatively spliced so that a functional Tra protein is only present in females; thus, DsxM is produced by default, while DsxF expression requires Tra. The sex-specific Dsx isoforms are essential for both male and female sexual differentiation. This pathway is profoundly different from the molecular mechanisms that control sex-specific development in other animal groups. In animals as different as vertebrates, nematodes, and crustaceans, sexual differentiation involves male-specific transcription of dsx -related transcription factors that are not alternatively spliced and play no role in female sexual development. To understand how the unique splicing-based mode of sexual differentiation found in insects evolved from a more ancestral transcription-based mechanism, we examined dsx and tra expression in three basal, hemimetabolous insect orders. We find that functional Tra protein is limited to females in the kissing bug Rhodnius prolixus (Hemiptera), but is present in both sexes in the louse Pediculus humanus (Phthiraptera) and the cockroach Blattella germanica (Blattodea). Although alternatively spliced dsx isoforms are seen in all these insects, they are sex-specific in the cockroach and the kissing bug but not in the louse. In B. germanica , RNAi experiments show that dsx is necessary for male, but not female, sexual differentiation, while tra controls female development via a dsx- independent pathway. Our results suggest that the distinctive insect mechanism based on the tra-dsx splicing cascade evolved in a gradual, mosaic process: sex-specific splicing of dsx predates its role in female sexual differentiation, while the role of tra in regulating dsx splicing and in sexual development more generally predates sex-specific expression of the Tra protein. We present a model where the canonical tra - dsx axis originated via merger between expanding dsx function (from males to both sexes) and narrowing tra function (from a general splicing factor to the dedicated regulator of dsx ).}, journal={bioRxiv}, author={Wexler, J. and Delaney, E.K. and Belles, X. and Schal, C. and Wada-Katsumata, A. and Amicucci, M. and Kopp, A.}, year={2019} }
 @article{hamilton_wada-katsumata_schal_2019, title={Role of Cuticular Hydrocarbons in German Cockroach (Blattodea: Ectobiidae) Aggregation Behavior}, volume={48}, ISSN={0046-225X 1938-2936}, url={http://dx.doi.org/10.1093/ee/nvz044}, DOI={10.1093/ee/nvz044}, abstractNote={Aggregation can be adaptive by providing protection from predators, facilitating thermoregulation, and expediting the location of food, shelter, and mates. German cockroaches Blattella germanica L. (Blattodea: Ectobiidae), are obligatory commensals in human-built structures, where they aggregate in crevices during the day. The source of the aggregation pheromone that drives this behavior and its chemical identity remain unclear. Cuticular hydrocarbons (CHCs) in feces have been proposed to serve as aggregation pheromone, but this function has not been investigated in relation to visual and tactile cues that mediate aggregation. Our objective was to delineate how CHCs in the feces and on the cockroach body operate in conditions that reflect the German cockroach’s ecology—either applied to shelters, representing fecal deposition, or to previously extracted cockroaches, representing shelter co-habitation with other cockroaches. Cockroaches and feces-conditioned filter papers were extracted, CHCs were purified by flash chromatography, and two-choice behavior assays were performed with first instar nymphs. Our results confirmed that nymphs preferred to rest within feces-conditioned shelters. However, purified CHCs did not elicit more aggregation than solvent-treated control shelters. Nymphs significantly preferred to rest in shelters that contained a CHC-free dead female, but the addition of CHCs to the female did not enhance aggregation. Nymphs preferred to aggregate with the CHC-free female over CHC-treated shelters. Finally, a methanol extract of feces was highly effective at eliciting aggregation, contesting previous reports that fecal CHCs serve as aggregation pheromone. We assert that CHCs play a minor, if any, role in the aggregation behavior of German cockroaches.}, number={3}, journal={Environmental Entomology}, publisher={Oxford University Press (OUP)}, author={Hamilton, Jamora A and Wada-Katsumata, Ayako and Schal, Coby}, year={2019}, month={Apr}, pages={546–553} }
 @article{wada-katsumata_robertson_silverman_schal_2018, title={Changes in the Peripheral Chemosensory System Drive Adaptive Shifts in Food Preferences in Insects}, volume={12}, ISSN={1662-5102}, url={http://dx.doi.org/10.3389/fncel.2018.00281}, DOI={10.3389/fncel.2018.00281}, abstractNote={A key challenge in understanding the evolution of animal behaviors is to identify cellular and molecular mechanisms that underlie the evolution of adaptive traits and behaviors in polymorphic populations under local selection pressures. Despite recent advances in fish, mice, and insects, there are still only a few compelling examples of major genes and cellular mechanisms associated with complex behavioral changes. Shifts in food or host preferences in insects, accompanied by changes in the peripheral chemosensory system, offer some of the best examples of adaptive behavioral evolution. A remarkable example is the German cockroach, Blattella germanica, a major indoor pest with a highly diverse omnivorous diet. Strong and persistent selection pressure with toxic-baits has induced rapid evolution of behavioral resistance in multiple cockroach populations. While typical cockroaches detect and accept the sugar glucose as a feeding-stimulant, behaviorally resistant cockroaches avoid eating glucose-containing toxic baits by sensing glucose as a deterrent. We review the peripheral gustatory neural mechanisms of glucose-aversion and discuss how the rapid emergence of taste polymorphisms can impede pest control efforts and affect foraging and mate-choice in adapted cockroach populations.}, journal={Frontiers in Cellular Neuroscience}, publisher={Frontiers Media SA}, author={Wada-Katsumata, Ayako and Robertson, Hugh M. and Silverman, Jules and Schal, Coby}, year={2018}, month={Aug} }
 @article{sierras_wada-katsumata_schal_2018, title={Effectiveness of Boric Acid by Ingestion, But Not by Contact, Against the Common Bed Bug (Hemiptera: Cimicidae)}, volume={111}, ISSN={0022-0493 1938-291X}, url={http://dx.doi.org/10.1093/jee/toy260}, DOI={10.1093/jee/toy260}, abstractNote={Abstract Boric acid has been used as an insecticide in the successful control of agricultural, public health and urban pests long before the advent of synthetic organic pesticides. Boric acid products, formulated as dusts, sprays, granular baits, pastes, gels, and liquids, are widely available to consumers and pest management professionals, especially to control pest infestations within homes. Boric acid dust is commonly used against bed bugs (Cimex lectularius L. [Hemiptera: Cimicidae]), but its efficacy has not been demonstrated. We evaluated the efficacy of boric acid as an ingestible and residual contact insecticide on bed bugs, and compared its efficacy on the German cockroach (Blattella germanica L. [Blattodea: Ectobiidae]) which is known to be susceptible to boric acid by both routes. Dose–response studies of 0–5% boric acid in blood demonstrated that ingested boric acid caused rapid mortality at concentrations of ≥2%, and even 0.5% and 1% boric acid caused 100% mortality, albeit at a slower time course. In contrast, bed bugs survived contact with high concentrations of boric acid dust. Smaller boric acid particles did not increase mortality of either unfed or recently fed bed bugs. The same boric acid products were effective at causing mortality of German cockroaches by both contact and ingestion. We thus conclude that although boric acid is an excellent candidate active ingredient for an ingestible bait formulation, residual applications of dust or spray would be ineffective in bed bug interventions.}, number={6}, journal={Journal of Economic Entomology}, publisher={Oxford University Press (OUP)}, author={Sierras, Angela and Wada-Katsumata, Ayako and Schal, Coby}, year={2018}, month={Sep}, pages={2772–2781} }
 @article{robertson_baits_walden_wada-katsumata_schal_2018, title={Enormous expansion of the chemosensory gene repertoire in the omnivorous German cockroach Blattella germanica}, volume={330}, ISSN={1552-5007}, url={http://dx.doi.org/10.1002/JEZ.B.22797}, DOI={10.1002/jez.b.22797}, abstractNote={The acquisition of genome sequences from a wide range of insects and other arthropods has revealed a broad positive correlation between the complexity of their chemical ecology and the size of their chemosensory gene repertoire. The German cockroach Blattella germanica is an extreme omnivore and has the largest chemosensory gene repertoire known for an arthropod, exceeding even the highly polyphagous spider mite Tetranychus urticae. While the Odorant Receptor family is not particularly large, with 123 genes potentially encoding 134 receptors (105 intact), the Gustatory Receptor family is greatly expanded to 431 genes potentially encoding 545 receptors (483 intact), the largest known for insects and second only to the spider mite. The Ionotropic Receptor family of olfactory and gustatory receptors is vastly expanded to at least 897 genes (604 intact), the largest size known in arthropods, far surpassing the 150 known from the dampwood termite Zootermopsis nevadensis. Commensurately, the Odorant Binding Protein family is expanded to the largest known for insects at 109 genes (all intact). Comparison with the far more specialized, but phylogenetically related termite, within the Dictyoptera, reveals considerable gene losses from the termite, and massive species-specific gene expansions in the cockroach. The cockroach has lost function of 11%-41% of these three chemoreceptor gene families to pseudogenization, and most of these are young events, implying rapid turnover of genes along with these major expansions, presumably in response to changes in its chemical ecology.}, number={5}, journal={Journal of Experimental Zoology Part B: Molecular and Developmental Evolution}, publisher={Wiley}, author={Robertson, Hugh M. and Baits, Rachel L. and Walden, Kimberly K.O. and Wada-Katsumata, Ayako and Schal, Coby}, year={2018}, month={Mar}, pages={265–278} }
 @article{harrison_jongepier_robertson_arning_bitard-feildel_chao_childers_dinh_doddapaneni_dugan_et al._2018, title={Hemimetabolous genomes reveal molecular basis of termite eusociality}, volume={2}, ISSN={2397-334X}, url={http://dx.doi.org/10.1038/S41559-017-0459-1}, DOI={10.1038/s41559-017-0459-1}, abstractNote={Abstract Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the 2-Gb genome of the German cockroach, Blattella germanica , and the 1.3-Gb genome of the drywood termite Cryptotermes secundus . We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.}, number={3}, journal={Nature Ecology & Evolution}, publisher={Springer Science and Business Media LLC}, author={Harrison, Mark C. and Jongepier, Evelien and Robertson, Hugh M. and Arning, Nicolas and Bitard-Feildel, Tristan and Chao, Hsu and Childers, Christopher P. and Dinh, Huyen and Doddapaneni, Harshavardhan and Dugan, Shannon and et al.}, year={2018}, month={Feb}, pages={557–566} }
 @article{harrison_jongepier_robertson_arning_bitard-feildel_chao_childers_dinh_doddapaneni_dugan_et al._2017, title={Hemimetabolous genomes reveal molecular basis of termite eusociality}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85095626274&partnerID=MN8TOARS}, DOI={10.1101/181909}, abstractNote={Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the first, 2GB genome of a cockroach, Blattella germanica , and the 1.3GB genome of the drywood termite, Cryptotermes secundus . We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.}, journal={bioRxiv}, author={Harrison, M.C. and Jongepier, E. and Robertson, H.M. and Arning, N. and Bitard-Feildel, T. and Chao, H. and Childers, C.P. and Dinh, H. and Doddapaneni, H. and Dugan, S. and et al.}, year={2017} }
 @article{jensen_wada-katsumata_schal_silverman_2017, title={Persistence of a sugar-rejecting cockroach genotype under various dietary regimes}, volume={7}, ISSN={2045-2322}, url={http://dx.doi.org/10.1038/srep46361}, DOI={10.1038/srep46361}, abstractNote={Abstract Glucose-aversion is a heritable trait that evolved in a number of German cockroach ( Blattella germanica L.) populations in response to strong selection with glucose-containing insecticide baits. However, in the absence of glucose-containing bait, glucose-averse (GA) cockroaches have lower performance than wild-type (WT) cockroaches in several fitness-determining traits. We allocated 48 caged populations initiated with homozygous GA and WT adults to four dietary treatments consisting of either pure rodent chow, rodent chow mixed to yield a content of either 20% glucose or 20% fructose, or a treatment consisting of choice between the 20% glucose- and the 20% fructose-containing food. After 6 months we found significantly higher frequency of WT individuals in populations restricted to the 20% glucose food, and after 12 months all dietary treatments contained significantly more WT individuals than expected. In accompanying experiments, we found lower survival and longer development time of GA nymphs restricted to glucose-containing food. We furthermore found evidence for assortative mating of females with males from their own genotype, with significant differences within WT cockroaches. Our study shows experimental evidence that within heterogeneous populations, WT German cockroaches will over time prevail in abundance over GA individuals, even when glucose is not a dietary component.}, number={1}, journal={Scientific Reports}, publisher={Springer Science and Business Media LLC}, author={Jensen, Kim and Wada-Katsumata, Ayako and Schal, Coby and Silverman, Jules}, year={2017}, month={Apr} }
 @article{wada-katsumata_zurek_nalyanya_roelofs_zhang_schal_2015, title={Gut bacteria mediate aggregation in the German cockroach}, volume={112}, ISSN={0027-8424 1091-6490}, url={http://dx.doi.org/10.1073/pnas.1504031112}, DOI={10.1073/pnas.1504031112}, abstractNote={Significance There is great interest in elucidating the diverse roles of microbes in biology, in general and, specifically, in mediating animal communication. We demonstrate that the gut bacterial community plays a pivotal role in production of aggregation pheromones in the German cockroach. The feces of normal and gut bacteria-inoculated cockroaches emits highly attractive volatile carboxylic acids (VCAs) that elicit aggregation whereas bacteria-free feces contains few VCAs and is relatively unattractive. VCAs may reflect the gut microbiota and, in turn, the cockroach's local environment, explaining why divergent chemical structures have been proposed as aggregation pheromones. This new insight emphasizes the importance of gut microbes in insect–insect communication and highlights the plasticity of the chemistry and function of fecal aggregation pheromones.}, number={51}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Wada-Katsumata, Ayako and Zurek, Ludek and Nalyanya, Godfrey and Roelofs, Wendell L. and Zhang, Aijun and Schal, Coby}, year={2015}, month={Dec}, pages={15678–15683} }
 @article{wada-katsumata_silverman_schal_2013, title={Changes in Taste Neurons Support the Emergence of an Adaptive Behavior in Cockroaches}, volume={340}, ISSN={0036-8075 1095-9203}, url={http://dx.doi.org/10.1126/science.1234854}, DOI={10.1126/science.1234854}, abstractNote={Sugar Aversion Several populations of the German cockroach have become averse to the glucose used as bait in toxic traps, which has severely reduced the traps' effectiveness. Wada-Katsumata et al. (p. 972 ) show that this aversion is a result of changes in the peripheral gustatory system, whereby glucose, as well as “sweet” receptors, stimulated an aversive bitter compound receptor.}, number={6135}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Wada-Katsumata, A. and Silverman, J. and Schal, C.}, year={2013}, month={May}, pages={972–975} }
 @article{böröczky_wada-katsumata_batchelor_zhukovskaya_schal_2013, title={Insects groom their antennae to enhance olfactory acuity}, volume={110}, ISSN={0027-8424 1091-6490}, url={http://dx.doi.org/10.1073/pnas.1212466110}, DOI={10.1073/pnas.1212466110}, abstractNote={Grooming, a common behavior in animals, serves the important function of removing foreign materials from body surfaces. When antennal grooming was prevented in the American cockroach, Periplaneta americana, field emission gun scanning electron microscopy images revealed that an unstructured substance accumulated on nongroomed antennae, covering sensillar pores, but not on groomed antennae of the same individuals. Gas chromatography analysis of antennal extracts showed that over a 24-h period nongroomed antennae accumulated three to four times more cuticular hydrocarbons than groomed antennae. Moreover, nongroomed antennae accumulated significantly more environmental contaminants from surfaces (stearic acid) and from air (geranyl acetate) than groomed antennae. We hypothesized that the accumulation of excess native cuticular hydrocarbons on the antennae would impair olfactory reception. Electroantennogram experiments and single-sensillum recordings supported this hypothesis: antennae that were prevented from being groomed were significantly less responsive than groomed antennae to the sex pheromone component periplanone-B, as well as to the general odorants geranyl acetate and hexanol. We therefore conclude that antennal grooming removes excess native cuticular lipids and foreign chemicals that physically and/or chemically interfere with olfaction, and thus maintains the olfactory acuity of the antennae. Similar experimental manipulations of the German cockroach (Blattella germanica), carpenter ant (Camponotus pennsylvanicus), and the housefly (Musca domestica), which use different modes of antennal grooming, support the hypothesis that antennal grooming serves a similar function in a wide range of insect taxa.}, number={9}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Böröczky, Katalin and Wada-Katsumata, Ayako and Batchelor, Dale and Zhukovskaya, Marianna and Schal, Coby}, year={2013}, month={Feb}, pages={3615–3620} }
 @article{wada-katsumata_silverman_schal_2011, title={Differential Inputs from Chemosensory Appendages Mediate Feeding Responses to Glucose in Wild-Type and Glucose-Averse German Cockroaches, Blattella germanica}, volume={36}, ISSN={1464-3553 0379-864X}, url={http://dx.doi.org/10.1093/chemse/bjr023}, DOI={10.1093/chemse/bjr023}, abstractNote={Glucose is a universal phagostimulant in many animal species, including the cockroach Blattella germanica. However, some natural populations of B. germanica have been found that are behaviorally deterred from eating glucose. In dose–response studies, glucose was a powerful phagostimulant for wild-type cockroaches, but it strongly deterred feeding in a glucose-averse strain. Both strains, however, exhibited identical dose–response curves to other phagostimulants and deterrents. As a lead to electrophysiological and molecular genetics studies to investigate the mechanisms that underlie glucose-aversion, we used 2 assay paradigms to delineate which chemosensory appendages on the head contribute to the reception of various phagostimulatory and deterrent chemicals. Both simultaneous dual stimulation of the antenna and mouthparts of the insects and 2-choice preference tests in surgically manipulated insects showed that the glucose-averse behavior could be elicited through the gustatory systems of the antennae and mouthparts. The paraglossae alone were sufficient for maximum sensitivity to both phagostimulants and deterrents, including glucose as a deterrent in the glucose-averse strain. In addition to the paraglossae, the labial palps were more important than the maxillary palps in the reception of deterrents (caffeine in both strains and glucose in the glucose-averse strain). The maxillary palps, on the other hand, played a more important role in the reception of phagostimulants (fructose in both strains and glucose in the wild-type strain). Our results suggest that distinct inputs from the chemosensory system mediate opposite feeding responses to glucose in the wild-type and glucose-averse strains.}, number={7}, journal={Chemical Senses}, publisher={Oxford University Press (OUP)}, author={Wada-Katsumata, Ayako and Silverman, Jules and Schal, Coby}, year={2011}, month={Apr}, pages={589–600} }
 @article{wada-katsumata_yamaoka_aonuma_2011, title={Social interactions influence dopamine and octopamine homeostasis in the brain of the ant Formica japonica}, volume={214}, ISSN={["1477-9145"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-79955636938&partnerID=MN8TOARS}, DOI={10.1242/jeb.051565}, abstractNote={SUMMARY In ants, including Formica japonica, trophallaxis and grooming are typical social behaviors shared among nestmates. After depriving ants of either food or nestmates and then providing them with either food or nestmates, a behavioral change in type and frequency of social interactions was observed. We hypothesized that starvation and isolation affected levels of brain biogenic amines including dopamine (DA) and octopamine (OA) – neuromediators modifying various insect behaviors – and tested the relationship between brain biogenic amines and social behaviors of stressed ants. Ants starved for 7 days contained lower brain DA levels and they did not perform trophallaxis toward nestmates. Feeding starved ants sucrose solution re-established trophallaxis but not brain DA levels. The performance of trophallaxis induced recovery of brain DA content to the level of untreated ants. Ants that were isolated for 2 days displayed markedly increased OA levels, which following nestmate interactions, returned to levels similar to those of control (non-isolated) ants and ants isolated for 1 h. We conclude that: (1) starvation reduced brain DA level but had no significant effect on brain OA (trophallaxis recovered the brain DA levels), and (2) isolation increased brain OA level but had no effect on brain DA (trophallaxis and grooming events recovered the brain OA levels). We suggest that social interactions with nestmates influenced brain biogenic amine homeostasis in stressed F. japonica.}, number={10}, journal={JOURNAL OF EXPERIMENTAL BIOLOGY}, author={Wada-Katsumata, Ayako and Yamaoka, Ryohei and Aonuma, Hitoshi}, year={2011}, month={May}, pages={1707–1713} }
 @inbook{ozaki_wada-katsumata_2010, title={Perception and olfaction of cuticular compounds}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-79955574496&partnerID=MN8TOARS}, DOI={10.1017/CBO9780511711909.011}, abstractNote={When humans communicate with each other, we rely on an arsenal of acoustic sounds and signals, as well as words and body language. Just as the simple words themselves tell only part of the story for humans, so, too, in the insect world, species-specific single- or few-component chemical messaging (i.e. sex pheromones) do not convey all the needed information. Our intonation, tone, intensity, gesturing and posture all combine to allow our fellow humans greater perception and analysis of the larger meaning we are trying to convey. In a comparable way, the chemosensory systems of insects also release mixtures of multiple compounds forming larger patterns for con-specifics to interpret. The communication among insects, like that of humans, has the ability to receive both selectively and collectively. Furthermore, the chemical information, when sent to the central nervous system, is integrated with other information or referred to memorized information, until, finally, it affects behavior. In this chapter, we will focus on the sensory system in cuticular hydrocarbon (CHC) perception.}, booktitle={Insect Hydrocarbons Biology, Biochemistry, and Chemical Ecology}, author={Ozaki, M. and Wada-Katsumata, A.}, year={2010}, pages={207–221} }
 @article{wada-katsumata_ozaki_yokohari_nishikawa_nishida_2009, title={Behavioral and electrophysiological studies on the sexually biased synergism between oligosaccharides and phospholipids in gustatory perception of nuptial secretion by the German cockroach}, volume={55}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-67549120761&partnerID=MN8TOARS}, DOI={10.1016/j.jinsphys.2009.04.014}, abstractNote={Females of Blattella germanica feed compulsively on a nuptial secretion from the male's eighth tergal gland (TG-8) during courtship. Using TG-8 extract and its essential ingredients, maltotriose (MT) and 1,2-dioleoylphosphatidylcholine (PC), we investigated the perception of the secretion by gustatory sensilla in both sexes. Female-biased chemosensitivity was found in the feeding responses to the TG-8 extract. The TG-8 extract induced specific impulses in four functionally different receptor cells: the sugar, salt and other two types of receptor cells in a single gustatory sensillum on the paraglossae in both sexes. The impulse frequencies of the sugar receptor cell and a receptor cell of unknown type were significantly higher in females than those in males. There were no sexual differences in the behavioral and electrophysiological responses to MT alone; no responses were elicited by PC. However, a mixture of MT and PC elicited the behavioral responses more strongly than MT in females. The impulse frequency of sugar receptor cells toward the mixture of MT and PC also increased in females but not in males. These results suggest that the synergistic effect of PC on 'sweetness' of MT in the female cockroach contributes to her compulsive nuptial feeding. The female-biased gustatory sensitivity seems to ensure successful coupling during the nuptial feeding.}, number={8}, journal={Journal of Insect Physiology}, author={Wada-Katsumata, A. and Ozaki, M. and Yokohari, F. and Nishikawa, M. and Nishida, R.}, year={2009}, pages={742–750} }
 @article{hojo_wada-katsumata_akino_yamaguchi_ozaki_yamaoka_2009, title={Chemical disguise as particular caste of host ants in the ant inquiline parasite Niphanda fusca (Lepidoptera: Lycaenidae)}, volume={276}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-58149130165&partnerID=MN8TOARS}, DOI={10.1098/rspb.2008.1064}, abstractNote={The exploitation of parental care is common in avian and insect ‘cuckoos’ and these species engage in a coevolutionary arms race. Caterpillars of the lycaenid butterfly Niphanda fusca develop as parasites inside the nests of host ants ( Camponotus japonicus ) where they grow by feeding on the worker trophallaxis. We hypothesized that N. fusca caterpillars chemically mimic host larvae, or some particular castes of the host ant, so that the caterpillars are accepted and cared for by the host workers. Behaviourally, it was observed that the host workers enthusiastically tended glass dummies coated with the cuticular chemicals of larvae or males and those of N. fusca caterpillars living together. Cuticular chemical analyses revealed that N. fusca caterpillars grown in a host ant nest acquired a colony-specific blend of cuticular hydrocarbons (CHCs). Furthermore, the CHC profiles of the N. fusca caterpillars were particularly close to those of the males rather than those of the host larvae and the others. We suggest that N. fusca caterpillars exploit worker care by matching their cuticular profile to that of the host males, since the males are fed by trophallaxis with workers in their natal nests for approximately ten months.}, number={1656}, journal={Proceedings of the Royal Society B: Biological Sciences}, author={Hojo, M.K. and Wada-Katsumata, A. and Akino, T. and Yamaguchi, S. and Ozaki, M. and Yamaoka, R.}, year={2009}, pages={551–558} }
 @article{goodwyn_katsumata-wada_okada_2009, title={Morphology and neurophysiology of tarsal vibration receptors in the water strider Aquarius paludum (Heteroptera: Gerridae)}, volume={55}, url={http://dx.doi.org/10.1016/j.jinsphys.2009.06.001}, DOI={10.1016/j.jinsphys.2009.06.001}, abstractNote={Substrate vibratory information receptors are extensively studied in insects and spiders, however for water surface dwelling species little data is available. We studied the vibration receptive organs in tarsi of the water strider Aquarius paludum, using light, transmission and scanning electron microscopes, and recorded the neural activity of the organs in response to vibrational stimuli, which were afterwards analysed with a custom made spike sorting program. We found that the tarsal chordotonal organ has one set of three scoloparia: one in the tarsomere I and two in the tarsomere II, all of which consisted of a few scolopidia. The chordotonal organ clearly responded to vibratory stimulation. Furthermore, we found that a pair of large subapical emergent dorsal setae, which had been deemed mechanosensory by previous authors, are not so. In turn, four ventral subapical trichobothria that are in direct contact with the water surface during locomotion, proved to be mechanosensory. The anatomical and ultrastructural observations support these electro-physiological results.}, number={9}, journal={Journal of Insect Physiology}, publisher={Elsevier BV}, author={Goodwyn, Pablo Perez and Katsumata-Wada, Ayako and Okada, Koutaroh}, year={2009}, month={Sep}, pages={855–861} }
 @article{wada_akino_yamaoka_2008, title={Ants semiochemical microcosmos investigated by the antennae}, volume={80}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-49049092667&partnerID=MN8TOARS}, number={5}, journal={Seikagaku}, author={Wada, A.K. and Akino, T. and Yamaoka, R.}, year={2008}, pages={385–398} }
 @article{hojo_wada-katsumata_ozaki_yamaguchi_yamaoka_2008, title={Gustatory synergism in ants mediates a species-specific symbiosis with lycaenid butterflies}, volume={194}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-56649085103&partnerID=MN8TOARS}, DOI={10.1007/s00359-008-0375-6}, number={12}, journal={Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology}, author={Hojo, M.K. and Wada-Katsumata, A. and Ozaki, M. and Yamaguchi, S. and Yamaoka, R.}, year={2008}, pages={1043–1052} }
 @article{ozaki_wada-katsumata_2008, title={Insect proteins transporting hydrophobic substances: Chemosensory stimulant carrier proteins in insect olfactory and gustatory receptors}, volume={53}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-41449095225&partnerID=MN8TOARS}, number={2}, journal={Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme}, author={Ozaki, M. and Wada-Katsumata, A.}, year={2008}, pages={111–118} }
 @article{ozaki_wada-katsumata_fujikawa_iwasaki_yokohari_satoji_nisimura_yamaoka_2005, title={Behavior: Ant nestmate and non-nestmate discrimination by a chemosensory sensillum}, volume={309}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-22044438575&partnerID=MN8TOARS}, DOI={10.1126/science.1105244}, abstractNote={In animal societies, chemical communication plays an important role in conflict and cooperation. For ants, cuticular hydrocarbon (CHC) blends produced by non-nestmates elicit overt aggression. We describe a sensory sensillum on the antennae of the carpenter ant Camponotus japonicus that functions in nestmate discrimination. This sensillum is multiporous and responds only to non-nestmate CHC blends. This suggests a role for a peripheral recognition mechanism in detecting colony-specific chemical signals.}, number={5732}, journal={Science}, author={Ozaki, M. and Wada-Katsumata, A. and Fujikawa, K. and Iwasaki, M. and Yokohari, F. and Satoji, Y. and Nisimura, T. and Yamaoka, R.}, year={2005}, pages={311–314} }
 @article{ozaki_takahara_kawahara_wada-katsumata_seno_amakawa_yamaoka_nakamura_2003, title={Perception of noxious compounds by contact chemoreceptors of the blowfly, Phormia regina: Putative role of an odorant-binding protein}, volume={28}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-1942506801&partnerID=MN8TOARS}, DOI={10.1093/chemse/28.4.349}, abstractNote={The blowfly, Phormia regina, has sensilla with four contact-chemoreceptor cells and one mechanoreceptor cell on its labellum. Three of the four chemoreceptor cells are called the sugar, the salt and the water receptor cells, respectively. However, the specificity of the remaining chemoreceptor cell, traditionally called the "fifth cell", has not yet been clarified. Referring to behavioral evaluation of the oral toxicity of monoterpenes, we measured the electrophysiological response of the "fifth cell" to these compounds. Of all the monoterpenes examined, D-limonene exhibited the strongest oral toxicity and induced the severest aversive behavior with vomiting and/or excretion in the fly. D-Limonene, when dispersed in an aqueous stimulus solution including dimethyl sulfoxide or an odorant-binding protein (OBP) found in the contact-chemoreceptor sensillum, the chemical sense-related lipophilic ligand-binding protein (CRLBP), evoked impulses from the "fifth cell". Considering the relationship between the aversive effects of monoterpenes and the response of the "fifth cell" to these effects, we propose that the "fifth cell" is a warning cell that has been differentiated as a taste system for detecting and avoiding dangerous foods. Here we suggest that in the insect contact-chemoreceptor sensillum, CRLBP carries lipophilic members of the noxious taste substances to the "fifth cell" through the aqueous sensillum lymph. This insect OBP may functionally be analogous to the von Ebner's grand protein in taste organs of mammals.}, number={4}, journal={Chemical Senses}, author={Ozaki, M. and Takahara, T. and Kawahara, Y. and Wada-Katsumata, A. and Seno, K. and Amakawa, T. and Yamaoka, R. and Nakamura, T.}, year={2003}, pages={349–359} }
 @article{wada_isobe_yamaguchi_yamaoka_ozaki_2001, title={Taste-enhancing effects of glycine on the sweetness of glucose: A gustatory aspects of symbiosis between the ant, Camponotus japonicus, and the larvae of the lycaenid butterfly, Niphanda fusca}, volume={26}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-0034782090&partnerID=MN8TOARS}, DOI={10.1093/chemse/26.8.983}, abstractNote={The lycaenid butterfly, Niphanda fusca, has a parasitic relationship with its host ant, Camponotus japonicus: the caterpillars may use chemical mimicry to enter the ant nest where they are fed mouth-to-mouth by the adult ants until pupation. Nevertheless, larvae offer their host ants a nutritious secretion that contains 160 mM glucose and 43 mM glycine. Using glucose and glycine mixture as artificial secretions, we investigated the gustatory effect of glucose and/or glycine on the ants. Glycine induced neither feeding behavior nor gustatory response in the ants if its concentration was <500 mM. In the presence of glycine at the concentration in the secretion, however, the ants improved their preference to glucose, and the sugar receptor cell exhibited electrophysiological enhancement of response to glucose in a glycine-concentration-dependent manner. By adding glycine to glucose in their secretions, therefore, the butterfly larvae can manipulate the gustatory sense of the ants. The alluring taste of `glycine-flavored glucose' could motivate the host ants to feed the larvae and thereby receive the secretions as a reward. The taste enhancement created by the combination of sugar and amino acid may play a role in the evolution of the parasitic relationships of these insects. The taste-enhancing effect appears to be analogous to taste enhancement by `umami' substances in humans.}, number={8}, journal={Chemical Senses}, author={Wada, A. and Isobe, Y. and Yamaguchi, S. and Yamaoka, R. and Ozaki, M.}, year={2001}, pages={983–992} }
 @article{hori_wada_shibuta_1997, title={Changes in Phenoloxidase Activities of the Galls on Leaves of Ulmus davidana Formed by Tetraneura fuslformis (Homoptera: Eriosomatidae)}, volume={32}, url={http://dx.doi.org/10.1303/aez.32.365}, DOI={10.1303/aez.32.365}, abstractNote={The galls on Ulmus leaves formed by Tetraneura fusiformis enlarged gradually from the 1st week of gall development to the 3rd week and rapidly from the 3rd to the 4th week, although no further enlargement was, thereafter, observed. Offspring began to be produced by the fundatrix from the 4th week and reached a maximum in number in the 5th week. thereafter, the number of offspring did not change until the 7th week. Dry weight of leaves with or without galls increased similarly from the 2nd to the 7th week, though the dry weight of the latter was higher than that of the former throughout the season. Maximums of peroxidase and polyphenoloxidase activities in non-galled leaves were observed in the 1st week and the zero week, respectively, and then those enzymatic activities gradually fell, whereas those in the galls were at a maximum in the zero or fist week, then dropped rapidly and were almost lost at the 2nd (peroxidase) or 4th week (polyphenoloxidase). These observations suggest that the process of formation and utilisation of galls by insects is apparently divided into two broad physiological stages before and after the 4th week.}, number={2}, journal={Applied Entomology and Zoology}, publisher={Japanese Society of Applied Entomology & Zoology}, author={HORI, Koji and WADA, Ayako and SHIBUTA, Toumi}, year={1997}, pages={365–371} }
 @article{wada_hori_1997, title={Feeding Strategy of Palomena angulosa Motschulsky (Hemiptera: Pentatomidae). I: Oviposition Site Selection, Nymph Development and Walking Ability of Nymphs.}, volume={41}, url={http://dx.doi.org/10.1303/jjaez.41.209}, DOI={10.1303/jjaez.41.209}, abstractNote={野外より採集したエゾアオカメムシの雌成虫の産卵場所の選択性を実験室内のケージと野外の網室において調べたところ,野外で寄生が確認されている数種の植物上に選択的に産卵することはなく,飼育ケージの網などにも多数の産卵が認められた。産卵が認められた5種の植物とインゲンマメ(対照区)で若虫を飼育したところ,ヤナギを与えた若虫は若齢のうちにすべて死亡した。成虫羽化までの生育期間は最も短かったナナカマドと最も長かったクローバの間に約60日の差があった。成虫羽化時の体重はナナカマドで約100mg,クローバ約90mgであった。2齢から5齢の若虫の歩行能力について調べたところ,若齢若虫ほど活発に歩く傾向が認められた。以上より,エゾアオカメムシの雌成虫は,若虫の生育に好適な場所へ必ずしも選択的に産卵をせず,生育に不適な場所で孵化した若虫は歩行によって寄主植物へ移動する戦略を取ることが示唆された。}, number={4}, journal={Japanese journal of applied entomology and zoology}, publisher={Japanese Society of Applied Entomology & Zoology}, author={WADA, Ayako and HORI, Koji}, year={1997}, pages={209–216} }
 @article{harrison_jongepier_robertson_arning_bitard-feildel_chao_childers_dinh_doddapaneni_dugan_et al., title={Hemimetabolous genomes reveal molecular basis of termite eusociality}, volume={2}, number={3}, journal={Nature Ecology & Evolution}, author={Harrison, M. C. and Jongepier, E. and Robertson, H. M. and Arning, N. and Bitard-Feildel, T. and Chao, H. and Childers, C. P. and Dinh, H. and Doddapaneni, H. and Dugan, S. and et al.}, pages={557–566} }