612 *Author ([email protected]) for correspondence CarolinaWilmington, Wilmington, NC28409,USA. North University of BiologyandMarineCenterfor Marine Science, of Department canbeusedtofocus oncommonnervoussystem themes. Thistypeofanalysis of behavioralvariabilityonextant species-specific propertiesthataresuperimposedonthesecommon common themesinneuronalorganization andfunction,note variability. Throughcomparativeanalyses,wecansearchfor and throughvariousformsofmodulation,toimpactbehavioral organism. Yet, thisdoesnottellushowtheseproteinsactinconcert, components ofspecificneuronsorclasseswithin an thorough understandingoftheionchannelandsynapticprotein time courseofbehavioralevents.Forexample,wecanhave a information onhowthegeneproductsareused,particularlyin the where itisexpressedandwhenexpressed.Itdoesnotprovide within-group evolutionaryrelationships. analyses shouldallowimproveddescriptionofbetween-groupand Furthermore, combiningtheintegrativeapproachwithcomparative examination, andphysiologicaldevelopmentalexperimentation. systems atthesametimeasitpointswayformorphological help focusgenomicanalysesoncriticalcomponentsofnervous neuroethology, canprovideamutuallybeneficialdialoguethat is whereanintegrativeapproach,extendingfromgenomesto provides awealthofcandidategenesforphylogeneticanalysis.This huge datasetsofusefulgeneticandmolecularinformation.Italso 2014). A majoradvantageofthisnew approachisthegenerationof (and relatedmolecular)techniques(e.g.Moroz,2009;Morozetal., development, hasseenamajoradvancethroughtheuseofgenomic evidence oftheevolutionaryhistorynervoussystem The descriptionofbasalnervoussystems,andthesearchfor KEY WORDS:,Ctenophores,Nervoussystemevolution organizations. significant progressinoursearchforancestralnervoussystem selection ofgenesandgeneproducts,wecancontinuetomake and elaborationofphylogenomicreconstructions.Withcareful and species-specificnervoussystempropertiesforthedevelopment physiological anddevelopmentalexperimentationtoidentifycommon genomic/transcriptomic techniquesiscoupledwithmorphological, integrative andcomparativeapproach,wherethepowerof beyond thatavailablefromgenomicinvestigations,andcallsfora presented withconflictingstimuli.Thisrequiresanunderstanding combination ofsimpleresponses,anddecision-makingwhen producing complexbehavioralactsthatinvolvetheintegrationand Even themostbasalmulticellularnervoussystemsarecapableof Richard A.Satterlie* comparative approach The searchforancestralnervoussystems:anintegrativeand REVIEW © 2015.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2015)218,612-617doi:10.1242/jeb.110387 Introduction ABSTRACT Genomic andtranscriptomicinformationtellsuswhatisthere, nervous system. present beliestheapparentanatomicalsimplicityofanemone decision makingwhenswimmingandfeedingstimuliareboth generation ofthisintegratedbehavioralpatterncoupledwith stimuli (RossandSutton,1964b;Ross,1965).Together, the oral diskorfollowingnematocystdischarge inresponsetofood The swimmingresponseisinhibitedinthepresenceoffoodon away fromthepredator(RossandSutton,1964a;Ellisetal.,1969). repetitive seriesofalternate-sidecolumncontractionsto‘swim’ predator, releasesthebasaldiskfromsubstrateandproducesa the anemones,underlinethispoint. repertoires ofsometheleastcentralizedcnidarians,forexample capabilities ofbasalnervoussystemsisamajorgoal.Thebehavioral knowledge isnotenough,particularlywhenanunderstandingofthe genomic level. and thusprovidenewfociforphylogeneticreconstructionsatthe strategy tolookbackwardtowardancestralneuronalorganizations, arrangements withinandbetweenphylogeneticgroupsasastepwise represented by anatomically definednervenets (Horridge,1966; down modulatedbyconducting systemsthatarepresumably addition, combplatebeatingfrequency andintensitycanbeupor comb platebeatingintheeight combrows(Horridge,1966).In orientationinthewater column throughreflexadjustmentof by anapicalorgan, includingastatocystthatdirectlyinfluences The combrowsthatproducelocomotory movementsarecontrolled and inthesearchforlikelypropertiesofancestralnervoussystems. to theunderstandingofnervoussystemfunctioninbasalmetazoans, functional morphologycanbeusedtoprovideusefulcontributions and comparativeapproachtotheunderstandingofnervoussystem suggest theexistenceofsuch‘centralproperties’. integrative capabilitiesandsufficiently complexbehaviorsto extant animalsthatpossessmulticellularnervoussystemsexhibit justifies theconceptof‘centralproperties’.Certainly, themostbasal organizational complexityexistsinacentralizednervoussystemthat those ofsingleneurons?’ Thesequestionssuggestthatanadditional confer onthegroupsomerecognizablynewfeatures,whicharenot together beforepatternsofinteractioncanevolvebetweenthemthat a …centralnervoussystem?Howmanyneuronsmustbebrought at aconceptraisedbyHorridge(Horridge,1968):‘Whatconstitutes inhabit theshell,anemonewillmovetoanothershell. Ross andSutton,1961b;Ross,1965).Ifahermitcrabdoesnot to thesnailshell(andreleasetentacles)(RossandSutton,1961a; with thesubstratum,benditsbodyaroundandattachbasaldisk Buccinum, theanemonewillattachwithitstentacles,releasecontact Pleurobrachia A complex feeding inthectenophore behavior: When theanemone When dealingwithnervoussystems,genomicandanatomical In thefollowingsectionsareafewexampleswhereanintegrative These specificandintegratedbehaviorsencourageasecondlook Calliactis encounters ashellofthesnail Stomphia , whenstimulatedbya

The Journal of Experimental Biology suggests anorganism-wide levelofintegration.Eachnervenetcan tentacular nervenet,thecoordinationofcomponentresponses each individualresponsemaybeexplainedbyactivityinabodyor response, andcoordinationoftentaclemouthactivity. While stimulated ,anoverrideofthenormalstatocystgeotactic side ofthebody, ciliaryreversalontheotherside,shorteningof involves severalcoordinatedresponses:ciliaryexcitationonone consumed. Thisintegratedbehavior, whichisspeciesspecific, contracted untilthepreyisbroughttomouth,whereit in contactwiththemouth.Thetentacleholdingpreyisthen tentacle sheathssobothtentaclesbecomewrappedaroundthebody These reactionsproduceaspinningofthebodyinplane – ciliaryexcitationononesideandreversaltheotherside. plate rowsonoppositesidesofthebodyundergo oppositereactions The tentacleshortens,pullingthepreyclosertobody. Comb 2)(Tamm andMoss,1985). coordinated actionsareinitiated(Fig. become attachedtoatentacle(viacolloblastactivity),seriesof uppermost withtentaclesextendeddownward(aborally).Whenprey niiino obpaeatvt Fg 1). inhibition ofcombplateactivity(Fig. suction electrodesthatcorrespond,respectively, toexcitationand Moss, 2004).Distinctelectricalimpulsescanberecordedwith electrodes andstandardACamplificationdisplay. author withpolyethylenesuction (arrows), whileburstsofsmallerimpulsestriggeranaccelerationincombplatebeating(asterisk).Originalrecordingbythe withcombplateinhibition movements, producedbyplacingaphotoresistorabovecombrowwithsubstageillumination.Largeimpulseburstsareassociated Fig. REVIEW In the‘fishing’ mode,

.Extracellularrecordingimmediatelyadjacenttoacombplateinthectenophore 1. Pleurobrachia are orientedmouth- suggests theuseofaformHorridge’s ‘centralproperties’. independent conductingsystems,formsaneuronalhierarchythat systems. Thislevelofintegration,coordinatedcross-talkbetween coordinated andbehaviorallyrelevantinteractionbetweenthese concept intheintegrationofmultipleconductingsystemsis feeding reactions,veryspecificregionalchanges.Oneimportant produce animal-widechangesincombplateactivityand,asseen marginal rowinginlarger forms(Colinetal.,2013). an intermediatecondition–jetpropulsioninsmallermedusaeand interesting astheirbellistypicallywideittall,andtheyshow marginal rowing(CostelloandColin,1995).Cubomedusaeare Scyphomedusae, whicharenearlyalloftheoblatetype,similarlyuse produce marginal rowingmovements(ColinandCostello,2002). a formofjetpropulsion,whileoblateforms(bellwiderthanitistall) hydromedusae showthatprolateforms(belltallerthanitiswide)use force forforwardlocomotion.Biomechanicalanalysesof of thesubumbrellarcavity, andthusmoveswatertoprovidemotive has alayerofsubumbrellar, circularmusclethatdecreasesthevolume members (,Scyphozoa,Cubozoa)aresimilarinthateach The swimmingsystemsinallthreecnidariangroupswithmedusoid Behavioral convergence incnidarianmedusae Pleurobrachia pileus.Thelowertraceisarecordofcombplate The JournalofExperimentalBiology(2015)doi:10.1242/jeb.110387 prey intocontactwiththemouth. contracted tobringthesegmentbearing panel –thetentaclebearingpreyisthen around thebodytocontactmouth.Fourth tentacular plane,whichwrapsthetentacles of prey)triggersaspinningresponse,inthe Third panel–continuedstimulation(struggling a tentacleresultsincontractionofthattentacle. at thetop.Secondpanel–contactofpreywith panel –normal‘fishing’ behavior. Themouthis Pleurobrachia pileus.Fromlefttoright:first Fig.

.Summaryoffeedingbehaviorin 2. 613

The Journal of Experimental Biology 614 REVIEW the author(seeSpencerandSatterlie,1980). identified viaelectronmicroscopyinthesesametissues.Originalimageof within sheetsofstriatedswimmusculature.Gapjunctionshavebeen coupling isfoundwithinelectricallycouplednetworksofhydromedusaeand microelectrode. Theentirenetworkisdye-andelectricallycoupled.Dye- The dyewasiontophoreticallyinjectedfromatip-filledrecording motor neuronnetworkintheinnernerveringofPolyorchispenicillatus. Fig. can initiateaswimcontraction.Theseneuronsactivatethe swim 3).Anyneuron inthenetwork margin intheinnernervering (Fig. electrically couplednetwork,viagapjunctions,thatcirclesthe bell foractivationofthemusculature,areorganized asan neurons thatinitiateeachswimcontraction,andserveasmotor neural controlofswimming(Satterlie,2002).Inhydromedusae,the of swimming,adistinctdichotomyexistsinthemechanisms subumbrella bythenerverings. subumbrella, andinhydromedusaetheyareseparatedfromthe than homologous,asincubomedusaetheyaredirectextensionsofthe et al.,2011). Thetwostructuresareconsideredtobeanalogousrather contractions anddirectionalnozzleformation(Gladfelter, 1973;Petie also playasignificantroleinturningbehaviorthroughasymmetrical the rateofflowejectedwaterfromsubumbrellarcavity, butthey and thevelariuminlatter. These structuresbothservetoincrease in hydromedusaeandcubomedusae–calledthevelumformer marginal ringofmusculartissuethatservestonarrowthebellopening Despite thesimilaritiesinbehavioral/biomechanicalaspects One aspectofthisapparentbehavioralconvergence centersona

.LuciferYellow injectionofasingleneuronthepacemaker/ 3. in actenophoreand18hydrozoan)wouldbelostentirely. would seemunlikelythatanentireclassofinnexins/pannexins (12 lacked thesegapjunctionproteins.Fromalogicalstandpoint, it innexins/pannexins weresecondarilylostorifanancestralform also the threecnidarianclasses,animmediatequestioniswhether call forsuchasearch.Ifinnexinsandpannexinsaremissingfrom former shouldbestraightforwardtotest,andthispaperrepresentsa could bepresentbutunabletoformfunctionalgapjunctions.The and pannexinsaremissinginthesegroups,asanthozoans,orthey Two possibilitiescanaccountforthelackofgapjunctions:innexins investigations ofinnexins/pannexinsinscyphozoansandcubozoans. forms. Foremostistheneedforgenomicandtranscriptomic lacking. communication), whiledataforscyphozoansandcubozoansare Hydra, has18innexins/pannexins(L.L.Moroz,personal Nematostella Pleurobrachia innexins/pannexins havebeenfoundinthectenophore do havegapjunctions(SatterlieandCase,1978).Twelve animals developgapjunctions(Fushikietal.,2010).Ctenophores 1984). Thisiscontrarytothesuggestionthatallmulticellular polyploid andmedusoidformsoftheHydrozoa(Mackieetal., neurons, betweenmusclecellsandepithelialinboth appear tohavegapjunctions,whilejunctionsarefoundbetween cnidarian classes(Anthozoa,CubozoaandScyphozoa)donot basal metazoans.Theimportantobservationisthatthreeofthe also couldcontributetooursearchforancestralnervoussystemsof within thecnidaria,andbetweencnidariaotherbasalgroups.It that couldbeusefulforfurtheranalysesofevolutionaryrelationships the classicaldescriptionofanon-polarized,diffuse nervenet. neuronal distributionsystemforexcitationofswimmusculaturefits chemical synapticinputs(Satterlie,2002).Theorganization ofthe activation ofthesubumbrellarswimmusculatureisentirelythrough are restrictedtosensory/ganglion-likestructurescalledrhopalia,and anthozoans. Swimpacemakersinscyphomedusaeandcubomedusae 4)(Mackieetal.,1984),norhavetheybeenfoundin found (Fig. gap junctions(Satterlie,1985;Satterlie,2008). both chemicalsynapticinputsandintercellularcurrentflowthrough forms (primarilyoblateforms),sotheactivationofmuscleisdueto 1980; Linetal.,2001).Subumbrellarnervenetsarepresentinsome at themargins ofaquadrant(Spencer, 1978;SpencerandSatterlie, that insomeforms,themusclesheetsareaneural,onlyinnervated circular swimmusclecellsareinterconnectedbygapjunctionsso musculature (directlyand/orindirectly)viachemicalsynapses.The This raisesinterestingevolutionaryquestionsaboutthesebasal Within thismotorcontroldichotomyisaninterestingsituation In scyphomedusaeandcubomedusae,gapjunctionshavenotbeen cubomedusa motor nervenet(A)andfiveswimmusclecells(B)ofthe Carboxyfluorescein injectionoftwoneuronsthesubumbrellar the subumbrellarmusclesheetofcubomedusae. Fig. hydromedusae (asshowninFig. techniques identicaltothoseusedobtaindye-couplingin iontophoretically injectedfromatip-filledmicroelectrodewith injections, dye-couplingwasneverobserved.Thedye The JournalofExperimentalBiology(2015)doi:10.1242/jeb.110387 (Moroz etal.,2014).A representative hydrozoan, , whilenonehavebeenfoundintheanthozoan

4. Lackofdye-couplinginthemotornervenetand Tamoya haplonema

3). Originaldataoftheauthor. . Inthese,and54additional

The Journal of Experimental Biology common tothelarger phylogenetic group. combination ofindependentresponses,somewhichmay be complex behaviorscanbeconstructedthroughtheintegration and and combplateinhibition/reversal.Inthisway, veryspecific, throughout thephylum,suchascombplateexcitation(acceleration) However, itenlistsindividualresponses thataremorecommon and between-group relationships. parsimony doesnotalwaysreflect abestapproximationofwithin- organism (DumontandRobertson,1986).Thissuggests that ancestral forms,andarchitectural featuresbasedonthedesignof influences, developmentalconstraints, historicalinfluencesfrom nervous systemsareshapedby fourtypesofvariables:adaptive The anatomicalorganization andfunctionofneuralcircuits and ctenophore and otherbasalmetazoans. system developmentwithinthecnidariaandbetween hydromedusae tostrengthenevidencefortheoriginsofnervous between therhopalialpacemakersandpacemakernetworksof could yieldinterestingfeaturesthatallowmolecularcomparisons contractions (Satterlie,2002).Thedevelopmentofmarginal rhopalia ganglia calledrhopalia,whichcontainthepacemakersforswim scyphomedusae andcubomedusae,intheformofsensory produce endogenouspacemakeractivity. network, possiblyincludingionchanneltypesandpropertiesthat genomic/transcriptomic analysesofproteinprofilesspecificforthis swim musclecontractions.Assuch,itrepresentsatarget for medusoid ancestormayhavehadasimilarmethodforinitiating (Satterlie andSpencer, 1983).Thissuggeststhatacommon primary motornetworkforactivationoftheswimmusculature surrounding neurons,thatfunctionasthepacemakernetworkand inner nervering,frequentlyoversizedcomparedwiththe presence ofanetworkelectricallycoupledneuronswithinthe suborders revealedacommoncomponentoftheswimsystem– a comparativeexaminationof13speciesfromfourdifferent sheets (Satterlie,2002)].Despitethevariationinmuscleactivation, properties canbeseen[e.g.electricalconductionwithinthemuscle muscle isvariableandspeciesspecific,althoughsomegeneralized hydromedusae. Themethodofactivationsubumbrellarswim phyletic subgroupisillustratedbyexaminingtheswimsystemof One strategyforthesearchnervoussystemoriginswithina (Moroz etal.,2014). 2014) andctenophoresarelikelytheearliestlineageinMetazoa systems appeartohavemultipleorigins(Moroz,2009;Morozetal., search forcommonancestors,particularlyasorganized nervous relationships inbasalmetazoansshouldholdsignificantvaluethe innexins arepresentinctenophores,theinnexin/pannexin organizational dichotomyincnidarianmedusae(seebelow),and included. Asgapjunctionsarecentralplayersinthenervoussystem representative ofthecnidarians.Additionally, ctenophoreswerenot 2010). Thisstudyusedonlyoneinnexinsequencefrom evolutionary appearanceofinsectsandnematodes(Fushikietal., suggests thedivergence oftheinnexinsubfamiliesoccurredafter innexinsandvertebratepannexins,currentevidence innexin/pannexin types.Thereisacloserelationshipbetween However, innexinscouldhavebeenlostbeforethefullradiationof REVIEW metazoan subgroup systemwithina A searchfornervous anancestral Nervous systemorigins Nervous In contrast,thefeedingbehaviordescribedaboveforcydippid A similarcommonfeaturecanbefound intheswimsystemsof Pleurobrachia is certainlyaspecies-specificactivity. Hydra as a neuronal integration representativeofHorridge’s ‘central interaction betweenthesedifferent nervenetswillrepresent sitesof effectors inmixedsensory–motornets.Onceagain,areas of development andarrangementof sensorystructuresandappropriate swim musculatureofmedusae), andsensorynetworksfollowthe their effectors (diffuse in the bodywallof that theorganization ofmotornervenetsfollowsthedistribution of networks aremixedsensory–motornets. 1984; Spencer, 1988),raisingthepossibility thattheFMRFamide musculature usedinswimming(GrimmelikhuijzenandSpencer, associated withsmoothmusclebandsforfields,butnotthestriated addition toinclusionofsensorycells,thenetworkswerefrequently hydromedusa conducting systemscanbeconsiderable,asshowninthe outer nerveringsofhydromedusae.Here,thenumberdistinct between thelargely parallelconductingsystemsoftheinnerand 1985; Koizumietal.,1992).Similarintegrativeinteractionsoccur oral diskandtentacularnervenetsinteract(e.g.Grimmelikhuijzen, sometimes foundintheoralregion,wherebodywall,mesenteric, integration, orboth.Inpolypoidcnidarians,suchdensificationsare find eitheranincreaseddensityofneuronsorareasphysiological body parts,willhaveareasofinteractionwherewewouldexpectto multiple nervenets,someparallelandcoordinatingdifferent of thenervoussystemsthesebasalorganisms areimportant.First, cnidarians goeswellbeyondthatofasimplenervenet.Two features However, thenervoussystemorganization ofextantctenophoresand present, itwasnotaspecificadaptationtoradialbodyplan. 2004; Martindale,2005),soifsuchanervenetorganization was suggests thatacnidarianancestorwasbilaterian(Finnertyetal., (typically statedinthesingular).Furthermore,recentevidence a possibleancestralfeatureisthebasiepidermaldiffuse nervenet the FMRFamide-immunoreactivenetsof known motornetworks(Mackieetal.,1985).Furtherexamination of immunoreactive nervenetswhileimmunoreactivitywasabsent in orders, sensorycellswerecomponentsofallFMRFamide- 2003; Mackie,2004),andinfourspeciesrepresentingthreehydrozoan (Arkett andSpencer, 1986a;ArkettandSpencer, 1986b;Mackieetal., sensory networksarefoundinthenerveringsofhydromedusae (see SatterlieandEichinger, 2014).Similarly, separatemotorand scyphomedusae –the‘giantfibernervenet’ andthe‘diffuse nervenet’ separation ofthetwodiffuse networksofthesubumbrella Satterlie, 2014;SatterlieandEichinger, 2014).Thisisseeninthe networks wereassociatedwithsensorystructures(Eichingerand to bethemotornetworks,whileFMRFamide-immunoreactive cubomedusae, thetubulin-immunoreactivenervenetsareconsidered throughout thelarva(Pirainoetal.,2011). Inbothscyphomedusaeand anterior concentration,butratherwasmoreevenlydistributed Clava nerve netsandthatprimarilyhaveasensoryfunction.Inthe et al.,2011). forward-directed regionforthesebenthic,crawlinglarvae(Piraino in theanteriorend,whichcorrespondswithsensorycell-rich FMRamide andGLWamide immunoreactivity)showaconcentration hydrozoan Satterlie, 2002;2011). Butevenintheplanulalarvaof and cubomedusae,inthenerveringsofhydromedusae(see of sensorycells.Thisisbestseenintherhopaliascyphomedusae like structures,isfrequentlyassociatedwithasimilaraccumulation A commonthemethatemerges fromthesepreparationssuggests One commoncharacteristicofbasalmetazoansthatisconsidered This meansthereisadistinctionbetweentheorganization ofmotor Second, theaccumulationofneurons,sometimesintoganglion- planula, atubulin-immunoreactivenetworkdidnotshowthe Clava multicornis The JournalofExperimentalBiology(2015)doi:10.1242/jeb.110387 Aglantha digitale , thesensorynetworks(asrevealedby (Mackie, 2004). Polyorchis Clava planulae andinthe indicated that,in 615

The Journal of Experimental Biology 616 REVIEW supported bytheNational ScienceFoundation. presented atthe‘Evolution oftheFirstNervousSystems II’ meeting,whichwas I thankDrRobertCondonforcomments onthemanuscript.Thisworkwas of similarhomologoussystems (DumontandRobertson,1986). analogous behavioralsystemsand neuralcircuits,andthedivergence particularly throughtheidentification oftheconvergence of common ancestorsdeservingofmorein-depthgenomicevaluation, circuit analogyorhomologycanpointtopotentialproperties of behavioral systemsofbasalmetazoans.Theevaluationneural common versusspecies-specificneuronalorganizations within innexins/pannexins inbasalmetazoangroups,andthedescription of medusae, thepresence/absenceofgapjunctions and behavioral convergence in the swimmingsystemsofcnidarian research concentration.A fewexamplesareindicatedhere,including potential topinpointspecificareasforgenomic/transcriptomic physiological experimentation,studieshold the addition, justasthewealthofgenomicinformationisdirecting new hierarchies, whichwillnotshowupingenomicdatabases. In of ‘centralproperties’ involvedincomplexbehaviorsandbehavioral understanding ofnervoussystemorganization mustincludeanalyses teamed withamutuallyinteractiveprogramofgenomicanalysis.An nervous systemorganizations withintheMetazoa,particularlywhen integrative andcomparativeapproachestothesearchforancestral behavioral responses. motor systemstoaidintheproductionofcomplex,integrated involved intheintegrationofmultiplesensorysystemsand represent anatomicalnucleatingsitesforaccumulationofneurons emergence ofHorridge’s ‘centralproperties’.Theseareascouldalso integration andthebeginningsofcentralizationthrough multiple conductingsystemswillrepresentareasofneural (Piraino etal.,2011). (5)Theareasofinteractionbetweenthe anterior–posterior bodyaxisanditsforward-directedlocomotion anterior regionof seen intheanatomicalconcentrationofsensorynetworks dependent onbodypatterningandaxisformation.Thisisbest structures. (4)Thedistributionofeffectors andsensorycellswillbe tissue inareasorregionsofhighdensitysensorycells sensory structures,frequentlywithanaccumulationofnervous influenced bythedistribution,andparticularlyaggregation,of The organization ofsensory-relatedconductingsystemswillbe phyla (e.g.KoopowitzandChien,1974;Lawrenz-Miller, 1977).(3) nerve net/nerveplexusorganization isseenwellbeyondthebasal compressed neuronalnetworks(Satterlie,2002;Satterlie,2011). The and restrictedbandsofmuscleareassociatedwithtract-like effectors, tendstobeinnervatedbyanervenetorplexus, of muscle(orepitheliomuscularcells),orotherdistributed distribution oftheireffectors, sothatabroad,two-dimensionalsheet systems. (2)With thisseparation,motorsystemsfollowthe and theirlarvae,particularlywithaseparationofmotorsensory for multipleanddistinctconductingsystemsinextantbasalforms beyond thesingulardiffuse nervenetconcept.(1)Evidenceexists nervous systemsinbasalorganisms andtheirancestorsthatgowell Garm etal.,2006;SkoghSatterlie,2011. compressed nervenetworks(Mackie,2004;Parkefeltetal.,2005; the ganglion-likerhopaliaornerveringscomposedofmultiple, species thathavemorecentralizednervouscomponents,including These interactionsarecarriedtotheextreme(forcnidarians)inthose go wellbeyondthoseoftheindividualcontributingnervenets. properties’, whereemergent propertiesofthenervoussystemwill Acknowledgements Neurobiology andneuroethologystillholdimportantpositionsin Several organizational conceptsaresuggestedfortheevolutionof Clava planula larvae,relatedtoits ihne,J .adStele R.A. Satterlie, and J.M. Eichinger, uot .P .adRbrsn R.M. Robertson, S.P. and J.P. C. Colin, Dumont, and J.H. Costello, li,V . os .M n utn L. Sutton, and D.M. Ross, V. L., Ellis, oi,S . otlo .H,Ktj,K,Syor .adKee,K. Kiefer, and J. Seymour, K., Katija, J.H., Costello, S.P., Colin, orde G.A. Horridge, A.N. Spencer, and C.J.P. Grimmelikhuijzen, C.J.P. Grimmelikhuijzen, D.E. Nilsson, and M. Boudes, P., Ekström, A., Garm, M.Q. Martindale, and D. Paulson, P., Burton, K., Pang, J.R., Finnerty, J.H. Costello, and S.P. Colin, orde G.A. Horridge, uhk,D,Hmd,Y,Ysiua .adEd,Y. Endo, and R. Yoshimura, Y., Hamada, D., Fushiki, A.N. Spencer, and S.A. Arkett, ldetr W. G. Gladfelter, Frank HawkinsKenanEndowmentFund. R.A.S. issupportedbyNationalScienceFoundationgrantIOS-0920825andthe The authordeclaresnocompetingorfinancialinterests. ozm,O,Iaaa . iuoo . ioe . aos L.C., Javois, S., Minobe, H., Mizumoto, M., Itazawa, O., Koizumi, ret .A n pne,A.N. Spencer, and S.A. Arkett, References Funding Competing interests ake .O,Mr,R .adMeh R.W. Meech, and R.M. Marx, G.O., Mackie, G.O. Mackie, A.N. Spencer, and W. J. Gallin, Y.-C. J., Lin, P. Chien, and H. 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