Hadley Wilson Horch · Taro Mito Aleksandar Popadić · Hideyo Ohuchi Sumihare Noji Editors The Cricket as a Model Organism Development, Regeneration, and Behavior The Cricket as a Model Organism Hadley Wilson Horch (cid:129) Taro Mito Aleksandar Popadic´ (cid:129) Hideyo Ohuchi Sumihare Noji Editors The Cricket as a Model Organism Development, Regeneration, and Behavior Editors HadleyWilsonHorch TaroMito DepartmentsofBiologyand GraduateschoolofBioscienceandBioindustry Neuroscience TokushimaUniversity BowdoinCollege Tokushima,Japan Brunswick,ME,USA AleksandarPopadic´ HideyoOhuchi BiologicalSciencesDepartment DepartmentofCytologyandHistology WayneStateUniversity OkayamaUniversity Detroit,MI,USA Okayama,Japan DentistryandPharmaceuticalSciences SumihareNoji OkayamaUniversityGraduateSchool GraduateschoolofBioscience ofMedicine andBioindustry Okayama,Japan TokushimaUniversity Tokushima,Japan ISBN978-4-431-56476-8 ISBN978-4-431-56478-2 (eBook) DOI10.1007/978-4-431-56478-2 LibraryofCongressControlNumber:2016960036 ©SpringerJapanKK2017 Thisworkissubjecttocopyright.AllrightsarereservedbythePublisher,whetherthewholeorpartof the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilarmethodologynowknownorhereafterdeveloped. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publicationdoesnotimply,evenintheabsenceofaspecificstatement,thatsuchnamesareexempt fromtherelevantprotectivelawsandregulationsandthereforefreeforgeneraluse. Thepublisher,theauthorsandtheeditorsaresafetoassumethattheadviceandinformationinthis book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained hereinorforanyerrorsoromissionsthatmayhavebeenmade. Printedonacid-freepaper ThisSpringerimprintispublishedbySpringerNature TheregisteredcompanyisSpringerJapanKK Theregisteredcompanyaddressis:ChiyodaFirstBldg.East,3-8-1Nishi-Kanda,Chiyoda-ku,Tokyo 101-0065,Japan Preface Crickets inhabit all areas of the world with the exception of subarctic and arctic regions.Encompassingabout2,400species,theyarethemostdiverselineageofthe “leaping”insects.Theirdefiningcharacteristicisthechirpingsoundmadebymales duringmating.Forthepast100years,detailed studiesatthebehavioral,acoustic, andneurophysiologicallevelhaverevealedfundamentalaspectsofmatingbehav- ior and the complexity of the aggressive interactions among males. Around the world, crickets are also considered an important food source. They are frequently rearedonanindustrialscaletosatisfydemandsfromzoosandpetstoresaswellas fromfoodprocessingplants.Cricketsareservedasacommonstreetsnackthrough- out Southeast Asia and can frequently be found as an ingredient in commercially produced protein bars and baked goods. Remarkably, the food conversion effi- ciencyofhousecrickets(Achetadomesticus)isfivetimeshigherthanbeef,andif theirfecundityistakenintoaccount,thisefficiencyincreases15–20-fold(Nakagaki andDefoliart1991).Ifoneconsiderstheever-increasinghumanpopulationgrowth, oursurvivalonEarthmaydependonalteringoureatinghabitsandconsumingnew sourcesoffood,suchasinsects(O.Deroy2015). The present volume aims to provide recent scientific updates on research on cricketsingeneral,withtheemphasisonGryllusbimaculatus.Webelievethatthis species can serve as a representative model for basal, hemimetabolous insect lineages.Inthismodeofdevelopment,anembryodevelopsintoaminiatureadult (firstnymph),whichinturnundergoesanumberofsuccessivemoltsbeforeturning into an adult. In comparison, the development and overall biology of the premier insect genetic model system, Drosophila melanogaster, are highly derived and representativeofonlyoneinsectgroup(Diptera–flies).Asthisbookdemonstrates, it is rather the cricket, as exemplified by Gryllus, which should be considered to representatypical insect.Untilrecently,though,only verylimitedfunctionaland genetic manipulation studies were feasible in non-drosophilid species. This all changed dramatically in the past 10 years, as the cricket community made rapid progress adaptingexisting andnewexperimentaltechniques inGryllus.Themain impetus behind all these advancements can be traced to the 2006 Nobel Prize in v vi Preface PhysiologyorMedicinetoAndrewZ.FireandCraigC.Mellofortheirdiscoveryof RNA interference (RNAi). The advent of the RNAi methodology provided a powerful tool to study almost any insect species. As shown in this book, many researchers have performed functional analyses of a variety of cricket genes, yielding important information about the biology and development of this organism. In2015,thefirstavailableroughdraftassemblyofthewholegenomeofGryllus bimaculatuswascompletedatTokushimaUniversity.Thiswasamilestoneevent, enabling researchers to study hundreds of new genes (public access is planned for 2017). In addition to making transgenic crickets, it is now possible to use site-specific approaches such as TALENs and zinc-finger nucleases to alter the Gryllusgenomeatatargetedregion.Furthermore,theCRISPR/Cas-basedgenome- editing system has been adapted for use in the cricket. These newly available genome-editing techniques can spearhead the detailed examination of gene func- tionandtheproductionofgene-editedcricketsthatcanserveasmodelsforhuman diseases. In theory, such genetically engineered crickets can be used to screen various chemicals to find drug candidates for genetic disorders and to produce humantherapeuticproteinsormetabolites. In2012,weorganizedthe2ndInternationalConferenceonCricketResearchin Tokushima,Japan.(Infact,thefirstconferencewascanceledbecauseoftheGreat East Japan Earthquake of March 11, 2011.) At that second meeting, we proposed the publication of this book and invited participants to contribute chapters representingtheirfieldsandtheirwork.We wanttothankalltheauthorsfortheir contributions and supportthroughout the development of thisbook. We hopethat this volume will inspire scientists in various disciplines to use the cricket model systemtoaskinterestingandinnovativequestions. Brunswick,ME,USA HadleyWilsonHorch Tokushima,Japan TaroMito Tokushima,Japan SumihareNoji Okayama,Japan HideyoOhuchi Detroit,MI,USA AleksandarPopadic´ September,2015 References Nakagaki BJ, Defoliart GR (1991) Comparison of diets for mass-rearing Acheta domesticus (Orthoptera: Gryllidae) as a novelty food, and comparison for food conversion efficiency withvaluesreportedforlivestock.JEconEntomol84:891–896 O’DeroyO(2015)Eatinsectsforfun,nottohelptheenvironment.Nature521:395 Contents PartI DevelopmentandRegeneration 1 HistoryofCricketBiology. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 GeraldS.PollackandSumihareNoji 2 EarlyDevelopmentandDiversityofGryllusAppendages. . . . . . . . 17 JinLiuandAleksandarPopadic´ 3 LegFormationandRegeneration. . . . . . . . . . . . . . . . . . . . . . . . . . 31 TetsuyaBando,YoshimasaHamada,andSumihareNoji 4 EyeDevelopmentandPhotoreceptionofaHemimetabolous Insect,Gryllusbimaculatus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49 HideyoOhuchi,TetsuyaBando,TaroMito,andSumihareNoji 5 AnEarlyEmbryonicDiapauseStageandDevelopmental PlasticityintheBand-LeggedGroundCricketDianemobius nigrofasciatus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63 SakikoShigaandHideharuNumata PartII Physiology,NervousSystem,andBehavior 6 MolecularApproachtotheCircadianClockMechanism intheCricket. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77 KenjiTomioka,OutaUryu,YuichiKamae,YoshiyukiMoriyama, ASMSaifullah,andTaishiYoshii 7 HormonalCircadianRhythmintheWing-Polymorphic CricketGryllusfirmus:IntegratingChronobiology, Endocrinology,andEvolution. . . . . . . . . . . . . . . . . . . . . . . . . . . . 91 AnthonyJ.Zera,NeethaNanothVellichirammal, andJenniferA.Brisson vii viii Contents 8 PlasticityintheCricketCentralNervousSystem. . . . . . . . . . . . . . 105 HadleyWilsonHorch,AlexandraPfister,OlafEllers, andAmyS.Johnson 9 LearningandMemory. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129 MakotoMizunamiandYukihisaMatsumoto 10 NeuronsandNetworksUnderlyingSingingBehaviour. . . . . . . . . . 141 StefanSch€oneichandBertholdHedwig 11 TheCricketAuditoryPathway:NeuralProcessing ofAcousticSignals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155 GeraldS.PollackandBertholdHedwig 12 NeuromodulatorsandtheControlofAggressioninCrickets. . . . . 169 PaulA.StevensonandJanRillich 13 FightingBehavior:UnderstandingtheMechanisms ofGroup-Size-DependentAggression. . . . . . . . . . . . . . . . . . . . . . . 197 HitoshiAonuma 14 CercalSystem-MediatedAntipredatorBehaviors. . . . . . . .. . . . . . 211 YoshichikaBabaandHirotoOgawa 15 TheBiochemicalBasisofLifeHistoryAdaptation: GryllusStudiesLeadtheWay. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229 AnthonyJ.Zera 16 ReproductiveBehaviorandPhysiologyintheCricketGryllus bimaculatus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 245 MasakiSakai,MikihikoKumashiro,YukihisaMatsumoto, MasakatsuUreshi,andTakahiroOtsubo PartIII ExperimentalApproaches 17 ProtocolsforOlfactoryConditioningExperiments. . . . . . . . . . . . . 273 YukihisaMatsumoto,ChihiroSatoMatsumoto, andMakotoMizunami 18 OpticalRecordingMethods:HowtoMeasureNeural ActivitieswithCalciumImaging. . . . . . . . . . . . . . . . . . . . . . . . . . . 285 HirotoOgawaandJohnP.Miller 19 TrackballSystemsforAnalysingCricketPhonotaxis. . . . . . . . . . . 303 BertholdHedwig Contents ix 20 SyntheticApproachesforObservingandMeasuring CricketBehaviors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 313 HitoshiAonuma 21 ProtocolsintheCricket. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 327 HadleyHorch,JinLiu,TaroMito,AleksandarPopadic´, andTakahitoWatanabe Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 371 Part I Development and Regeneration