Chapter2PheromonesandBehaviorTristramD.WyattAbstractChemicalcommunicat - PDF document

Chapter2PheromonesandBehaviorTristramD.WyattAbstractChemicalcommunicationiswidelyusedbycrustaceans,forexample,insexualinteractions,larvalrelease,andplanktonicsettlement.However,weknowtheidentityofveryfewofthemoleculesinvolved.Inthischapter,Iintroducepheromonesandcontrastthemwithsignaturemixtures.Pheromonesaremoleculesthatareevolvedsignals,indeÞnedratiosinthecaseofmultiplecomponentpheromones,whichareemittedbyanindividualandreceivedbyasecondindividualofthesamespecies,inwhichtheycauseaspeciÞcreaction,forexample,astereotypedbehaviororadevelopmentalprocess.Signaturemixturesarevariablechemicalmixtures(asubsetofthemoleculesinananimalÕschemicalproÞle)learnedbyotherconspeciÞcsandusedtorecognizeanorganismasanindividual(e.g.,lobsters,mammals)orasamemberofaparticularsocialgroupsuchasafamily,clan,orcolony(e.g.,mammals,desertwoodlouseHemilepistusreaumuriants,bees).Akeydifferencebetweenpheromonesandsignaturemixturesisthatinalltaxasofarinvestigateditseemsthatsignaturemixturesneedtobelearnt(unlikemostpheromones).Thesesignaturemixturesmaybebestthoughtofascues.Pheromonesevolvefrommoleculeswhichgiveaselectiveadvantagetothereceiverandsignaler.Theevolutionofpheromonesisfacilitatedbythecombinatorialbasisoftheolfactorysystemfoundincrustaceansandotheranimals.Incrustaceans,somepheromonesarealsodetectedbythedistributedchemosensorysystem.Crustaceanshavegreatpotentialasmodelorganismsforchemicalcommunicationresearch,inparticularnowthattheDaphniapulexgenomehasbeensequenced.2.1IntroducingChemicalEcologyLikeotheranimals,crustaceansliveinachemosensoryworldfullofchemicalinformationandsignalsfromconspeciÞcs,prey,andpredators(Fig.2.1).Toahuman T.D.Wyatt(DepartmentofZoology,TheTinbergenBuilding,SouthParksRoad,Oxford,OX13PS,UKe-mail:tristram.wyatt@zoo.ox.ac.ukT.BreithauptandM.Thiel(eds.),ChemicalCommunicationinCrustaceansDOI10.1007/978-0-387-77101-4_2,SpringerScience+BusinessMedia,LLC2011 itmaybestrangetothinkofaworldofsmellsunderwater(asweexperiencesmellsinair)butchemicalcommunicationiswidelyusedbyaquaticanimalsincludingcrustaceans.However,thetypesofmoleculesusedbycrustaceansforcommunica-tionunderwaterarelikelytobedifferentfromthoseusedinterrestrialenvironmentsbymostinsectsandmammals.Foraquaticanimals,solubilityofsignalmoleculesistheequivalentofvolatilityforairbornemessages.Thedivisionofchemicalsensesinvertebratesintotasteandsmelldoesnotworkwellforcrustaceansandotherinvertebrates.Likevertebrates,crustaceanshaveolfactoryreceptorneurons(ORNs)(thesearealsoknownasolfactorysensoryneurons)withoneendexposedtothechemicalworldoutsidetheanimalandtheotherleadingtothebrain.TheseORNsintheaesthetascsensillaofcrustaceansapproximatetovertebrateÒolfactionÓastheORNsprojecttoglomeruliinthecrustaceanolfactorylobe,analogoustotheorganizationofthebraininvertebrates(CaprioandDerby;DerbyandSorensen;SchmidtandMellon,Chap.7).Longdistancesexpheromonesandchemicalcuesforsocialinteractionstendtobeprocessedbytheolfactory/aesthetascpathways,forexample,spinylobsterresponsestoconspeciÞcurinesignals(Horneretal.).However,crustaceansalsohaveÒdistributedchemoreceptionÓ(SchmidtandMellon,Chap.7)whichgoesbeyondvertebratetaste.Distributedchemoreceptorsaretypicallypackagedwithmechanosensorsintosensillaoverotherpartsofthebodyandhaveanonglomerularorganizationinthebrain/ganglia.Whiledistributedchemoreceptiondoesincludetheequivalentoftaste,withcontactchemoreceptionforfoodforexample,italsoincludesotherchemicalsensessuchascontrolofantennulargroomingandthecoordinationofmatingandcopulation(SchmidtandMellon,Chap.7).SchmidtandMellonpointoutthatintegratedinputsfromsensillainboththeolfactoryanddistributedchemoreceptorsystemsmayparticipatetogetherinthecontrolofcom-plexbehaviors,includingassociativeodorlearning.Asyouwillseeintherestofthisbookthereisalreadyanimpressiveunder-standingofcrustaceanchemicalcommunicationÐbutreallywearejustatthebeginningoftheexploration.Inthecomingyears,asdemonstratedinthechapters Fig.2.1Justaspeacockmalesdisplaytheirfantails,themalelobster()displayswithpheromonesinthedirectedjethesendstowardthefemale.DrawingbyJorgeA.VarelaRamos(PictureinspiredbythemousepheromoneÒpeacocktailÓinPennandPottsT.D.Wyatt ofthisbook,chemicalcommunicationbycrustaceanswillbeseentobejustasspectacularasthecurrentlywell-knownexamplesofmothmalesßyingupwindtoÞndthefemalemothreleasingpheromone.WhatissurprisingisthatonlyasmallnumberofpheromoneshavebeenchemicallyidentiÞedforcrustaceanscomparedwiththethousandsforinsects.Partofthedifferencemaybetheimportanceofmothsasagriculturalpests,whichhaspromptedgovernmentstoprovidefunding,butIwonderifthedisparityalsosuggeststhatcrustaceansarehardertostudy.IsitthetypeofmoleculesusedbycrustaceansorthecurrentdifÞcultiesofworkingwiththechemicalcommunicationofaquaticanimals?HardegeandTerschak(Chap.19)discusstheimportanceofdiscriminatingbioassaysforidentifyingpheromones.Itmaybethatfurtherworkneedstobedoneonbioassaysthatyielddiscriminatingdataforcrustaceans.InthischapterIwouldliketointroduceconceptsofchemicalecology,todiscusspheromonesandsignaturemixtures,andcontrasttheresearchonterrestrialpher-omoneswithresearchonaquaticpheromones.2.2DeÞnitionofPheromonesPheromonesarechemicalsignalsusedtocommunicatewithinaspecies.Phero-monesareÒmoleculesthatareevolvedsignals,indeÞnedratiosinthecaseofmultiplecomponentpheromones,whichareemittedbyanindividualandreceivedbyasecondindividualofthesamespecies,inwhichtheycauseaspeciÞcreaction,forexample,astereotypedbehaviororadevelopmentalprocessÓ(WyattmodiÞedafterKarlsonandLuscher).ThewordisderivedfromtheGreekpherein,totransferandhormon,toexcite.KarlsonandLuscherintendedthatpheromonesshouldincludechemicalsignalsinanimalsofallkindsandtheyincludedCrustacea(theprawnPalaemonserratus),aswellasÞsh,mammals,andinsects,amongtheirexamples.KarlsonandLuscheranticipatedthatspecieswouldnotnecessarilyhaveexclu-siveuseofaparticularmoleculeastheirpheromone.Wenowknowmanyexamplesofshareduseofmolecules(Kelly;Wyatt).OneofthemostspectacularisthewaythatthefemaleAsianelephantsharesitssmallmoleculesexpheromone,()-7-dodecen-1-ylacetate,withsome140speciesofmoth(Ras-mussenetal.1996).BecausethemothsusedeÞnedcombinationsofmolecules,ofwhich()-7-dodecen-1-ylacetateisjustone,thereisnotlikelytobeconfusionbetweenelephantsandmoths.BecausethedeÞnedcombinationisdifferentforeachmothspeciesthereisnoconfusionbetweenthemothspecies:incaseswherethecombinationisthesame,thespeciesÒcallÓwiththeirpheromonesatdifferenttimesorhavenonoverlappinghabitats.Miceandsomebarkbeetlespeciesalsosharesometerpenecompoundsaspheromones.Thereareanumberofreasonswhytheseoverlapsoccur.TheÞrstisthatallanimalsshareacommonheritageandsohavebasicallythesamemetabolic2PheromonesandBehavior25 pathwaysandmolecularcapabilities.Second,thenumberofpotentialsmallvolatilemolecules,whicharealsochemicallystableandnontoxic,islimited.Incidentally,thismaybelessofaproblemforunderwatercommunicationasevenverylargemoleculescanbesoluble.Wemightexpectsomeaquaticspeciestohaveuniquelargepheromonemoleculesusedsingly,forexamplespecies-speciÞcpeptideswithdifferentaminoacidsequences,ratherthanblendsofcommonsmallmoleculesasinmothsexpheromones.2.2.1Signalsvs.CuesPheromonesaresignalsasdeÞnedbyMaynardSmithandHarper(,p3)intheirAnimalSignals:Òanyactorstructurewhichaltersthebehaviorofotherorganisms,whichevolvedbecauseofthateffect,andwhichiseffectivebecausethereceiverÕsresponsehasalsoevolved.ÓThedeÞnitionisfurtherdiscussedbyScott-Phillips()inathoughtfulpaperwhichmakesexplicitthattheresponseitselfhastohaveevolvedtobeaffectedbytheactorstructureconcerned(notjustevolvedtorespondtosomethingelse).Forsomethingtobeasignal,boththeemissionandresponseneedtohaveevolved.Thisdistinguishessignalsfromcues.CuesarethingssuchastheCOreleasedbyananimalasitbreathes,andusedasacuebyablood-suckinginsecttoÞnditshost.ThemosquitoÕsresponseiscertainlyevolved(andindeedithashighlyspecializedreceptorstodetectCO),butthereleaseofCObythehostdoesnotevolvetohavetheeffectofattractingmosquitoessoCOreleasedoesnotcountasasignal.Theodorsusedbymammalsandcrustaceanswhenrecognizingkinorfamiliaranimalsarealsoprobablybestseenascuesratherthansignals,inmyopinion(seebelow).Howdoweknowthatachemicalsignalhasevolvedforaneffect?InmothfemaleswecanseethespecializedpheromoneglandsevolvedforsecretingandreleasingthefemalesexpheromonesÐfortheeffectofsignalingÐandinthemale,thehighlyevolvedfeatheryantennaeandspecializedolfactorysensorycellsonthoseantennaefordetectingthepheromones,combinedwiththespecializedsex-speciÞcbrainstructures,themacroglomerularcomplex(MGC),inthemalebrainforprocessingthedata(Hansson2002;Wyatt).Oftentheevidenceofevolvedstructuresandprocessesforsignalreceptionismoresubtle.Forexample,maleandfemaleDrosophilaantennaearemorphologicallyverysimilar.TheevolvedeffectsofpheromonesinDrosophilaareatthereceptorlevelandcircuitsofthebrainofthemaleandfemale(Vosshall).Inlobsters,pheromonesmaybeaddedtotheurinebeforereleaseratherthantherebeingaspecialglandvisible.Pheromonecomponentscanbeacquiredaswellassynthesizedbytheemitter.Forexample,toattractfemales,maleeuglossinebeesintheAmericantropicsmustcollectperfumeoilssuchasmono-andsesqui-terpenesfromorchidßowers(seeWyattT.D.Wyatt 2.2.2PheromoneTypesbyFunctionPheromonesareoftendescribedbyfunction,bytheeffecttheyhave.Forexample,sexpheromonesdescribethoseinvolvedinmate-Þndingorattraction.Othersincludeaggregation,alarm,andtrailpheromones.Someresponsesarecontext-speciÞcÐforexampleinsomeantspeciesalarmpheromonescauseantstodisperseifreleasedfarfromthenestbuttoattackifreleasedclosetothenest.Inaway,thesedescriptorsallowussimplytodescribetherangeofbehaviorsmediatedbypher-omonesandthengeneralizefromthesetodescribepatternsinuse,say,ofsexpheromonesacrosstaxa.OurdeÞnitionsreßectourattemptstomakesenseoftheworldandidentifypatterns.UsefuldeÞnitionsenableustogeneralizeandpredictcharacteristics.However,nodeÞnitionisgoingtobeaperfectmatchtotherangeofobservedscenarios.TherewillalwaysbefuzzyareasanddifÞcultcases.PartoftheproblemmaybetryingtoincludeallphenomenainthesamedeÞnition.AnotherproblemisthatwemaybedescribingpheromonesatdifferentstagesofevolutionÐitislikelythatmanypheromonesstartaschemicalcuesandonlylaterevolveintosignals,anevolutionaryprocessknownasritualization(MaynardSmithandHarper2003,p.15).2.2.3Releaservs.PrimerEffectsPheromonesmayelicitabehavioralresponse(releasereffects),longer-lastingdevelopmental(primereffects)mediatedviahormones,orboth(seeFig.).Soforexample,priorexposureforsomedaystothefemalepheromone(s)inthepremolturineoftheshorecrabCarcinusmaenasprimeshissexualbehavioralresponsessuchascradlingwhenheislaterexposedtothefemalepremoulturine(EkerholmandHallberg2.2.4Semiochemicalsvs.InfochemicalsAsthevarietyofchemicalinteractionsbetweenorganismsbecamebetterunder-stoodduringthe1960sand1970s,manyauthorsattemptedtoclassifytheinterac-tionsandthechemicalagentsinvolved.IfpheromonesdescribeintraspeciÞcsignals,whattermsshouldbeusedforinterspeciÞcchemicalinteractions?Intherecentaquaticchemosensoryliterature,authorsseemtobealmostequallydividedbetweenusingÒsemiochemicalsÓandÒinfochemicals.ÓSemiochemicals(fromtheGreeksemeionmarkorsignal)arethechemicals,acquiredorproducedbythesender,involvedinthechemicalinteractionsbetweenorganisms(NordlundandLewis)(Table).IntheiroriginaldeÞnition,LawandRegnier()usedthephraseÒchemicalsignalsfortransmittinginformationbetweenindividualsÓ[myitalics],whichisÞneforpheromonesbutcausesa2PheromonesandBehavior27 problemformanyinterspeciÞcinteractionsaswenowreservethetermsÒcommu-nicationÓandÒsignalsÓformutuallyevolvedsignals.NordlundandLewis(recognizedtheproblemandreworkedtheirdeÞnitionofsemiochemicalstoremoveÒsignals.ÓPheromonesarethussemiochemicalsusedwithinaspecies.InterspeciÞcsemi-ochemicalsareallelochemicals.TheyarefurthersubdivideddependingonthecostsandbeneÞtstothesenderandthereceiver(NordlundandLewis).IfthesenderbeneÞtsattheexpenseofthereceiver,forexampleabolasspiderreleasingmoth-identicalpheromonestolureamalemoth,thespiderÕschemicalmessageisanallomone.IfapreyspeciessuchasthegammaridGammarusroeseliiavoidsitspredatorsÕodors,thenthegammaridisusingthoseodorsasakairomone(Hes-selschwerdtetal.).IfbothpartnersbeneÞt,asinthecaseofmutualismsbetweenseaanemonesandanemoneclown-Þsh,thechemicalsinvolvedaretermedsynomones.Themultiplicityoftermsisonlyusefulasshorthandandtheyareclearlyoverlapping,notmutuallyexclusive(amoleculeusedasapheromonewithinaspeciescanbeusedasakairomonebyitspredator,forexample).Inproposingthewordkairomone,Brownetal.()hadinmindthewordÕsGreekroot,especiallyinitssensesofÒopportunisticÓand Fig.2.2Pheromonescanbeastimulusleadingtoapromptbehavioralresponsebynerveimpulsesfromthebrain(CNS,centralnervoussystem)(releasereffects)orcanactindirectlybystimulationofhormonesecretionresultinginphysiologicalchanges,ÒprimingÓtheanimalforadifferentbehavioralrepertoire(primereffects).Agivenpheromonecanofcoursehaveprimerorreleasereffectsatthesametimeorindifferentcontexts.Thedistinctionbetweenprimerandreleasereffectshasbecomeblurredasweunderstandmoreaboutthelinks,interactions,andfeedbackloopsinthesequencefromodortobehavioralandendocrineeffects.Hormonaleffectscanberapid,andmemories,sometimesfacilitatedbylocalneurochemistrychanges,canbelong-lasting.Thedia-grambringstogetherideasfromÞguresinWilsonandBossert()andSachs().TextanddiagramadaptedfromWyatt(,Fig1.10,p.18)T.D.Wyatt ÒexploitativeÓÐwhichisjusthowapredatorusesakairomone.KairomoneshavenotevolvedassignalsandthisisreßectedinmyusageofkairomoneusuallyinthecontextofÒusing[moleculex]asakairomoneÓratherthandeÞningaparticularmoleculeitselfasakairomone.ÒInfochemicalÓwasproposedbyDickeandSabelis()asatermtoreplaceÒsemiochemicalÓattheheadoftheclassiÞcation.Theyarguedthatthecost-beneÞtoftheinteractionshouldbetheonlycriterion,nottheoriginofthechemicalsconcerned.Thiswaspromptedperhapsbytheirworkontritrophicinteractions,whichhavevolatilesproducedbytheherbivoresthemselvesandalsoinducedintheirhostplants.However,indirectlyproducedorinducedvolatileswerealready Table2.1DeÞnitionsofchemicalmediatorsimportantinchemicalinteractionsamongorganisms,basedonNordlundandLewis()andWyatt(A.Hormone:Achemicalagent,producedbytissueorendocrineglands,whichcontrolsvariousphysiologicalprocesseswithinanorganism(NordlundandLewisB.Semiochemical:Achemicalinvolvedinthechemicalinteractionbetweenorganisms(NordlundandLewis1.Pheromone:Moleculesthatareevolvedsignals,indeÞnedratiosinthecaseofmultiplecomponentpheromones,whichareemittedbyanindividualandreceivedbyasecondindividualofthesamespecies,inwhichtheycauseaspeciÞcreaction,forexample,astereotypedbehaviororadevelopmentalprocess(Wyatt,modiÞedafterKarlsonandL2.SignatureMixture:Avariablechemicalmixture(asubsetofthemoleculesinananimalÕschemicalproÞle)learnedbyotherconspeciÞcsandusedtorecognizeananimalasanindividual(e.g.,lobsters,mammals)orasamemberofaparticularsocialgroupsuchasafamily,clan,orcolony(e.g.,Hemilepistusreaumuri,ants,bees)(WyattderivedfromWyattÒsignatureodorÓandJohnstonÕsÒmosaicsignalÓ2003)3.Allelochemical:ChemicalsigniÞcanttoorganismsofaspeciesdifferentfromtheirsource,forreasonsotherthanfoodassuch(NordlundandLewisa.Allomone:Asubstance,producedoracquiredbyanorganism,which,whenitcontactsanindividualofanotherspeciesinthenaturalcontext,evokesinthereceiverabehavioralorphysiologicalreactionadaptivelyfavorabletotheemitterbutnottothereceiver(NordlundandLewisb.Kairomone:Asubstance,produced,acquiredby,orreleasedasaresultoftheactivitiesofanorganism,which,whenitcontactsanindividualofanotherspeciesinthenaturalcontext,evokesinthereceiverabehavioralorphysiologicalreactionadaptivelyfavorabletothereceiverbutnottotheemitter(NordlundandLewisc.Synomone:Asubstanceproducedoracquiredbyanorganism,which,whenitcontactsanindividualofanotherspeciesinthenaturalcontext,evokesinthereceiverabehavioralorphysiologicalreactionadaptivelyfavorabletobothemitterandreceiver(NordlundandLewisd.Apneumone:Asubstanceemittedbyanonlivingmaterialthatevokesabehavioralorphysiologicalreactionadaptivelyfavorabletoareceivingorganism,butdetrimentaltoanorganism,ofanotherspecies,whichmaybefoundinoronthenonlivingmaterial(NordlundandLewisÒInfochemicalÓasanalternativetoÒsemiochemicalÓwasproposedbyDickeandSabelis(thoughitsmainchangewastoreplaceÒproducedoracquiredbyÓwithÒpertinenttobiologyofÓineachcaseforallelochemics.Apneumoneisrarelyused.ParagraphsfromNordlundandLewis)withpermission2PheromonesandBehavior29 includedbyNordlundandLewis()intheirdeÞnitionforkairomonewhichincludessubstancesÒreleasedasaresultoftheactivitiesofanorganismÓ(TableOnbalanceIfeelthebestsolutionistostickwithÒsemiochemicals,ÓbutwitharelaxationofthedeÞnitionofpheromonetoinclude,whereneeded,compoundsproducedbysymbiontsorotherassociatedorganisms(Wyatt2.2.5Pheromones,SignatureMixtures,andRecognitionOneofthemostcontentiousproblemsinchemicalcommunicationhasbeenwhattonamethevariableodorsusedbymammalstodistinguishindividualsoftheirownspeciesandusedbysocialinsectstodistinguishfellowcolonymembersfromÒforeignersÓ(andprobablyusedbylobstersandhermitcrabstorecognizeindivi-dualsinÞghts,seeAtemaandSteinbach;GherardiandTricarico,Chap.15).ThesechemicalcuesdonotÞtthepheromonedeÞnitionofaÒdeÞnedcombinationofmoleculescausingaspeciÞcbehaviororresponseÓ(Table;WyattInstead,thevariationinchemicalmixturesbetweenindividualsorcoloniesmessage.IproposethatweusethetermÒsignaturemixturesÓtodescribethese)(Table).Thesesignaturemixturesarelearnt(incontrasttopheromones,whichtendnottoneedlearningforresponse)(TableForkinrecognition,animalslearnanycues(signaturemixtures)thatgiveastatisticalprobabilityallowingrecognition(Shermanetal.).Sometimesthesesignaturemixturesareproducedbytheanimalitselfbutinsomespeciestheymaybeacquiredfromthesharedlocalenvironmentinstead,forexampleinwoodfrogtadpolesRanasylvatica(Shermanetal.).Desertwoodlice(Hemilepistus)showfamilyrecognitionbycuticularchemicalsignatures,whichappeartobeamixtureofcompoundsfromallfamilymembers;signaturemixtureshavetobereacquiredaftereachmoltingevent(Linsenmair).TherecognitionbyguardsinHemilepistusisclearlyhighlyevolved(asitisinhoneybees).However,thecuticularmoleculesinHemilepistus,perhapswithawaterprooÞng Table2.2ContrastingpheromoneswithsignaturemixturesMolecule(s)Receiversystem/perceptionSpeciesspeciÞce.g.,Sexpheromonese.g.,ÒCategoryÓpheromones(suchasimmature,adult)ÒHardwired,ÓlearningnotusuallyrequiredIndividual,family,colonyodorsLearningrequiredlldoblerandCarlin()introducedtheideaofanonymoussignals(pheromones)contrastedwithvariablesignaturemixtures(thoughtheirterminologywasdifferent).Theanonymouspheromonesignalsareuniformthroughoutacategory(e.g.,species,male,female,andperhapsmoltstateanddominancestatus).Incontrast,signaturemixturesvaryandcanbeusedtorecognizetheorganismasanindividualormemberofaparticularsocialgroupsuchasafamilyorcolony.AmoreextensivecomparisonisgiveninWyatt(T.D.Wyatt function,mighthavebeencooptedforasignaturefunction.Itispossiblethatcomplexityofsignaturesmightlaterbeselected,undernaturalselection,foreaseofrecognition(TibbettsandDale).Dotheeusocialsponge-livingshrimpsuseodorincolonyrecognitioninasimilarwaytoHemilepistus,antsandbees?Agivenanimalwillproducebothpheromonesandsignaturemixtures(Fig.Inadditiontoitssexpheromone(s),eachlobsterhasitsownhighlyindividualodormixtureandthiscomplexbouquetcanbeusedbyotherlobstersforrecognition(seeAtemaandSteinbachItislikelythatsignaturemixtures,astheyinvolvelearning,areprocesseddifferentlyfrompheromonesthoughthisisstillnotfullyunderstood(Wyatt).Theneurobiologyoftheolfactoryimprintingofsignaturemixturesbyadultmammalsiswellstudiedinmice(fortheBruceeffect,theodorsofhermatearelearntinheraccessoryolfactorylobe)andsheep(themotherlearnstheodorsofherlambinhermainolfactorylobe)(BrennanandKendrick).Individualrecognitioninlobstersismediatedbytheesthetic/olfactorypathways(JohnsonandAtema)thoughcurrentlynotenoughisknownaboutolfactoryprocessinginlobsterstoknowifpheromonesareprocesseddifferently.2.3EvolutionofPheromonesPheromonesareusedrightacrosstheanimalkingdombecauseanymoleculethatgivesaselectiveadvantagecanpotentiallyevolveintoapheromone.Thisisinpartaconsequenceofthecombinatorialmechanismsofolfaction.Invertebrateandverte-brateolfaction,despiteallthesuperÞcialdifferencesbetweencrustaceanaesthe-tascsandmammaliannoses,worksinroughlythesameway.Crustaceans,withanimpermeableexoskeleton,haveevolvedolfactoryÒwindowsÓintheexoskeleton. Fig.2.3Mostanimalshavebothanonymouspheromonesignalsandsignaturemixtures(Wyatt).ThisisdemonstratedinthecuticularhydrocarbonsoftheÒqueenlessÓant(Monninetal.).Agaschromatographicanalysisofthecuticularhydrocarbonsonthealphafemale,theonlyfertilizedandegg-layingindividualinthecolony,showstheanonymoushydrocarbonpheromone9-hentriacontene(indicatedbythe)characteristicofalphafemalesinallcolonies,togetherwiththediverserangeofotherhydrocarbonswhichmakeupthecolonyodor.Herfellowcolonymembershavethecolonyodorbutlackthe9-hentriacontene.Antsphotograph,courtesyThibaudMonnin.Gaschromatogram,Monninetal.(),with2PheromonesandBehavior31 OdormoleculesinteractwitholfactoryreceptorproteinsonthesurfaceofeachORN.Inarthropodstherearehundredsofdifferentolfactoryreceptorproteinsdependingonspecies,eachwithabroadsensitivity/rangeofmoleculeswhichwillinteractwith(HallemandCarlson).EachreceptorÕssensitivitiesoverlapwiththoseofotherreceptorproteins,sothatahugeÒolfactoryworldÓcanbecovered.EachORNpresentsjustoneofthedifferentolfactoryreceptorproteins.ChemosensorysystemsarediscussedinchaptersbyHallbergandSkog(Chap.9),andSchmidtandMellon(Chap.7).DerbyandSorensen()remindusthatdetectorsofpheromonesandolfactorysocialcuesarenotexclusivelylocatedintheaesthetasc/olfactorypathway,givingasanexamplemalecrayÞshwhichhavesensorsontheirclawsthatdetectfemaleodors.AlltheORNscarryingthereceptorofaparticulartypefeedtothesameglomerulus(neuropil)oneachsideoftheolfactorylobe(CaprioandDerby).Thenumberofglomeruli(andbyimplicationthenumberofdifferentORs)inCrustacearangesfromabout150to1,300(CaprioandDerby).Thebrainbuildsupanolfactorypictureoftheworldfromthese,integratingtheresponsesacrossthedifferentglomeruli.Soforexample,hypotheticallyamoleculemightstimulateORNtypes1,3,and25.AdifferentmoleculemightstimulateORNtypes2and91.Thiscombinatorialprocessingallowsorganismstodiscriminateanddistinguishinnumerablemolecules,includingonesneverencounteredbefore.Thustheolfactorysystemisprimedtorespondtoanyodorchemical(s)intheenvironmentthatgiveaselectiveadvantage,forexampledetectingfemalesabouttoproduceeggs.Selectioncanstartonthereceivertobecomemoresensitive,withmoreselectiveolfactoryreceptorproteins,moreexpressedoneachORNandmoreoftheincreasinglyspeciÞcORNsintheanimalÕschemosensoryorgan(s).Inthiswaywecanevolvethesensitivepheromonedetectionsystemofthemalecrab.Therewillbecorrespondingselectionontheemittertoreleasemoreofthemolecules,nowbecominganevolvedsignalorpheromone.Ahypotheticalsce-nario,fromÒspyingÓtoanevolvedsignal,isshowninFig.Pheromonescanoftenberelatedtotheirlikelyoriginalsourceorfunction,thoughtheymayhavebeenmodiÞedsomewhattogivespeciÞcity.Forexample,manyÞshsexpheromonesareorhaveevolvedfromsteroidandprostaglandinhormones(StaceyandSorensen).AlarmpheromonesinantsoftenappeartohaveevolvedfromdefensivecompoundsusedbythatspeciesÐandpresumablyevolvedthepheromonefunctionasthesecompoundswouldbereleasedduringcombat.TheSettlement-InducingProteinComplexinbarnaclesappearstohaveevolvedfrom2-macroglobulin-likeproteinswhichoccurinthebarnaclecuticle(perhapsthroughduplicationofanancestralbarnacleA2Mgene)(Dreannoetal.;Clare,Chap.22).Inaquaticsystems,solubilitytakestheplaceofvolatility.Aquaticpheromonescanbelargemoleculessolongastheyaresolubleinwater(thoughcontactpheromones,suchasthoseusedinmaterecognitioninshrimpandcopepodsarepresumablyalmostinsolubleÐseee.g.,Bauer,Chap.14andSnell,Chap.23).Manyaquaticorganismsusepolypeptidesaspheromones,forexamplethecrabÒpumpingpheromoneÓ(RittschofandCohen).PheromonespeciÞcitycanbegainedbyT.D.Wyatt uniqueaminoacidsequences.Peptideshaveshorthalf-livesduetorapidconsump-tionbymicrobesandthiscanbeausefulpropertyforsomesignals(Rittschofand)thoughitmaybeonereasonwhyterritorialmarkingbyscentmarksdoesnotseemtobefoundinaquaticorganisms(ThielandDuffyAsthepheromonesofÞshandcrustaceansbecomebetterunderstood,speciesspeciÞcitythroughmulticomponentblendsmayberevealed(StaceyandSorensen).Multicomponentsynergy,withtwoormorepheromonecomponentsneededtogether,hasbeendemonstratedtostimulateagonadotropinsurgeinmalegoldÞsh. Fig.2.4Proposedstagesintheevolutionofacommunicationfunctionformoleculesreleasedbyanindividual.TheXintheupperpanelindicatesthatthereceivingindividualhasnoadaptationstoreceivethecue.IntheÒspyingphase,ÓonlythereceiverbeneÞts.ThetransitiontobilateralbeneÞttobothsenderandreceivercouldoccurlaterifthereisaselectiveadvantagetothesender.IntheÒspyingphaseÓthereneednotbechangesinthemoleculesreleasedbythesender.AnoriginalÞgurebyIvanHinojosa,inspiredbyandwithtextfromStaceyandSorensen(,Fig.9.1,p.363)(withpermissionfromtheauthors)2PheromonesandBehavior33 2.3.1PheromonesandSpeciationFormothsweknowenoughaboutthepheromonesacrossspeciesandfamiliestoanalyzethewaypheromoneschangeinspeciation.Closelyrelatedsympatricmothspecieshavemulticomponentpheromoneblendsthatdifferbyadded,lost,orchangedcomponents(Wyatt2010).Insomespecieswecanseethechangesatthegenelevel(e.g.,Xueetal.).Sexpheromonesareusedwidelybycrusta-ceansbutcopepodcuticularpheromonesaside(Snell,Chap.23)theyhavesofarresistedidentiÞcation(thoughweareclose,seeHardegeandTerschak,Chap.19;KamioandDerby,Chap.20).WethereforedonotyetknowenoughaboutthepheromonesofanygroupofCrustaceatolookatthevariationbetweenspecies.OvertimeIamconÞdentwewillbeabletodothis.2.4PeculiaritiesofChemicalCommunicationasComparedwithVisualandAcousticCommunicationThekeydifferencebetweenchemicalcommunicationandvisualandacousticcommunicationistheneedformoleculestotravelfromsignalertoreceiver.Thisrequireseitherdiffusion,likelytobeimportantonlyforsmallorganismsatthescaleofmillimeters(seeYenandLasley,Chap.9)orßowofcurrents(seeKoehl,Chap.5).Chemicalsignalsarethusrarelyalmostinstantaneousinthewaythatvisualandacousticsignalscanbe.Ontheotherhand,chemicalsignalscanbelong-lasting.Thechemicalcuesfrombarnaclecuticularproteins,forexample,resistavarietyofchemicalattacksincludingacidsandcausticalkalis(Knight-JonesClare,Chap.22).SpeciÞcityisachievedindifferentwaysinchemicalcommunicationcomparedwithvisualandacousticroutes,whichareacontinuousrangeofspectra,differingbywavelengthandtemporalstructure.Chemicalcommunicationofferswaysofdiffer-inginmanydimensions,andinparticulartheopportunitytocombinedifferentmoleculestogivespeciÞcity.Afurtherdifferencemaybethehonestyofchemicalsignals.Deceptioninsignaling,andcontrastsbetweenvisual,acoustic,andchemicalsignals,arediscussedbyChristyandRittschof(Chap.16).2.5NovelTechniquesandQuestionsinChemicalCommunicationResearchForresearchonpheromones,thebioassayiscrucialandistheÞrststeptoestablishthatthereisachemicallymediatedeffecttobestudied.ThebioassaytestforT.D.Wyatt activitycanbebehavioralorphysiologicaldependingonthepheromonebeingstudied.ThegoldstandardorpheromoneequivalentofÒKochÕspostulatesÓrequirestheisolation,identiÞcation,synthesis,andbioassayconÞrmationofactivity(Wyatt).Demonstrationofactivityatthebiologicallyrelevantcon-centrationisalsoimportant.ChemicalcommunicationismoredifÞculttoinvestigatethansoundandvisualsignalsbecausemoleculesareinvolvedratherthanbeingphenomenaamenabletospectralanalysis.Firstthereisthechallengeofidentifyingthemoleculesinvolved(whichmaybeatlowconcentrations,nearthelimitsofinstrumentation)andsecondthereistheproblemofplayback.WhereasvideooranMP3playercanreproducevisualorsoundsignals,andmanysignalscanbecreatedbysoftwareandthenreplayed,forstudiesofchemicalcommunicationtheexactmoleculeshavetobeoffered.PartofthedifÞcultyisthattheolfactorysystemissensitivetoeveryaspectofthepreciseidentityofmolecules,includingtheirchirality.Simplebioassay-guidedfractionationapproachesseparateabiologicalsampleintofractionsbasedonanumberofproperties,includingsolubilityinsolventsofdifferentpolarity,molecularmass,andmolecularcharge(DerbyandSorensen2008HardegeandTerschak,Chap.19;KamioandDerby,Chap.20).However,manypheromonesaremulticomponent,requiringanumberofmoleculestobepresentinthecorrectratioandconcentrationforactivity,sosimplefractionationmaynotworkasthecomponentsmayendupindifferentfractions,inactivebythemselves(weareveryluckythattheÞrstpheromoneidentiÞed,bombykol,hadamaincomponentthatwasactivebyitself,otherwiseButenandtÕsbioassayswouldnothaverevealedthemolecule).ThisproblemismademoredifÞcultbecausetheactivemoleculesmaynotbetheonespresentinthelargestquantities.Oneapproachtotackletheproblemofbioassayingmulticomponentpheromonesistouseasubtractive-combinationbioas-sayinwhichacompleteputativemixtureistestedwithsuccessivelymorefractionsormoleculesmissing,toseewhichonescanberemovedwithoutextinguishingthesignal(Byers1992;KamioandDerby,Chap.20).Progressinchemicaltechniquesofextraction,analysis,andsynthesisarelikelytoenablemanymorepheromonestobeidentiÞed.Thehistoryofpheromoneresearch,likemanyotherareasofscience,showstheimportanceofnewtechnol-ogiesandmethodsincludinggaschromatography(sohelpfulforworkoninsectpheromones),massspectroscopy,and,morerecently,theuseofmolecularbiologicaltechniques.Thenewtechniqueofmetabolomicshaspromisetoidentifybiomarkers,moleculesenrichedinaparticularcontextandthuscandidatephero-monecomponents(DerbyandSorensen;KamioandDerby,Chap.20).Theproblemofthehighestpeaks,notnecessarilybeingthepheromones,stillremainsthough.RecordingfromtheanimalsÕownsensorsasapheromone-identifyingtoolshowspromisethoughtheantennogramisproblematicinaquaticcrustaceansbecauseofthetechnicaldifÞcultyofisolatingtherecordingelectrodesfromthestimuluswater.Therehas,however,beenextensivesinglecellrecordingofchemosensoryorgansofcrustaceans(CaprioandDerby2PheromonesandBehavior35 2.6ThePromiseofCrustaceansasModelSystemsforChemicalCommunicationResearchCrustaceanscouldprovideanewrangeofmodelorganismscontributingtoanunderstandingofchemicalcommunicationandchemoreceptioningeneral.How-ever,currentlyakeychallengetousingcrustaceansasmodelsystemsinchemicalcommunicationisthelackofknowledgeaboutthechemicalidentityofthepher-omonesinvolved.AsmorecrustaceanpheromonesareidentiÞed,arichrangeofresearchquestionswillcomewithinreach.NonethelessthereismuchthatcanbedoneinthemeantimeevenifthechemicalidentitiesofthemoleculeshavenotbeenconÞrmed.Behavioralworkinparticularcangoaheadusingactivebiologicalsamplesorextractsasthechemicalstimuli.WiththeDaphniapulexwaterßeagenomenowavailable(wFleaBase),geneticdissectionofchemoreceptioninCrustaceabecomespossible(e.g.,Penalva-Arana,etal.).AswFleaBaseÕsintroductionpointsout:ÒDaphniashareswithaninterestingandrichgenestructureandwealthofgeneduplications.Ithasclosestgenehomologytotheinsects,ApisDrosophila.However,ithasnearlyasmanyuniqueorstronggenehomologiestoMouseastoinsectsÓ(wFleaBaseManycrustaceanscanbeculturedincontrolledlaboratoryenvironments(Barki,Jones,andKarplus,Chap.25).Whilemanylargedecapodshaveplanktoniclarvalstages,theperacarids(whichincludeisopodsandamphipods)aredirectdevelopers,withtheeggsbroodedbythefemale,facilitatinglabculture(Thiel,Chap.10).Onepossibleareaofresearchcouldusesuchdirectdevelopingspeciestogenerateparticularstrains,forexamplethathavegrowninparticularselectiveenvironments.Onetopicwhichisalreadyshowingtheimportantcontributionofworkoncrustaceansistheorientationbehaviorofanimalstochemicalstimuli.Howdoanimalsfollowanodorplumetoitssource?OrientationbehaviorbycrustaceansisexploredinWeissberg(Chap.4).Oneadvantageofdecapodsisthattheyarelargeenoughtocarrytrackingdevices.Thereseemtobeintriguingdifferencesbetweenthemechanismsusedbydifferentcrustaceangroups,evenwithinthedecapods.2.7ConclusionsandOutlookChemicalcommunicationisthecommonestmethodofcommunicationacrosstheanimalkingdom.Crustaceansprovidesomeofthemostinterestingexamplesofthis,fromsextosettlement,butwithfewexceptions,wedonotknowthemoleculesthatarebeingused.Crustaceanshavethepotentialtobeamongthekeymodelorganismsforworkonchemoreceptioninthefuture,inparticulariftheirphero-monescanbeidentiÞedandsynthesized.Oneareaofdebate,forchemicalcommunicationinallanimals,isthedeÞnitionofpheromoneandwhetherthesignaturemixturesusedforrecognitionshouldcountaspheromonesignalsorcues(Wyatt).WhilethisispartlyofsemanticT.D.Wyatt 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