*Author ([email protected]) for correspondence Universitetsparken 15,DK-2100 Copenhagen,Denmark. Copenhagen, University Denmark, of Museumof The Natural History is abundleofaxons(Richteret al., 2010);theventralnervecordmay nervous cellsincludingtheircell bodies,asopposedtoanerve,which characterized byapairedlongitudinalventralnervecord[acluster of of thecentralnervoussystem(CNS).TheZygoneura were three majorgroupsoftheBilateria,basedonstructureandposition (now Protostomia),AmbulacrariaandChordoniaChordata) for ago, Hatschek(Hatschek,1888)introducedthenamesZygoneura high importanceinstudiesofanimalevolution.Morethanacentury most conservativeanimalorgan systemsandhasthereforebeengiven adult nervoussystems. development oflarvalnervoussystemsandtheirrelationships to made importantcontributionstoknowledgeofthestructure and nervous systemevolutionanddiversification,newmethods have Studies onontogenyareveryimportantforourunderstandingof Dorsal–ventral orientation KEY WORDS:Deuterostomy, Metamorphosis,Nervoussystems, morphologically ventral. trochaea theory, andthattheneuraltubeofchordatesis pelago-benthic ancestoroftheprotostomesasdescribedby ancestor ofthedeuterostomeswasverysimilartolatestcommon evolved fromthespiraliantype.Thisindicatesthatlatestcommon demonstrates thatthechordatetypeofgastrulationcouldeasilyhave with the‘normal’ spiraliangastrulationtype,andinthechaetognaths both inanannelidandamollusk,whichareplacedfamilies gene expression.Thepresenceof‘deuterostomian’ blastoporefates cord oftheprotostomes,andthisisstronglysupportedbypatterns interpreted asavariationoftheontogenyblastoporalnerve enigmatic. TheontogenyofthechordateCNScanperhapsbe systems ofechinodermsandenteropneustsappearcompletely deuterostomes aregenerallydifficult tointerpret,andthenervous structures intheecdysozoansarestronglyindicated.The studies inanumberofspiralians,andhomologieswithsimilar part ofthebrain.Thishasbeenwelldocumentedthroughcell-lineage nerve cordsandasmallperianalloop.Theanteriorloopbecomes differentiated intoaperioralloop,pairedorsecondarilyfusedventral blastoporal (circumblastoporal)nervecord,whichbecomes cerebral ganglia,whichformthemajorpartofadultbrain,anda system (CNS).Two structurescanberecognized,viz.apairof ganglia/nerve cordsthatareretainedastheadultcentralnervous knowledge isscant.Theciliatedprotostomelarvaeshow appears tobesensory, probablyinvolvedinmetamorphosis,but true larvalorganthatdisappearsbeforeoratmetamorphosis.It The apicalorganofciliatedlarvaecnidariansandbilateriansisa Claus Nielsen* Larval nervoussystems:truelarvalandprecociousadult REVIEW © 2015.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2015)218,629-636doi:10.1242/jeb.109603 Introduction ABSTRACT The nervoussystemhasforalongtimebeenconsideredoneof the of thewholegenomes sister groupofalltheremainingmetazoans,andrecentstudies 2012; Nesnidaletal.,2013)haveplacedtheCtenophoraas studies (Dunnetal.,2008;Hejnol2009;Maxwell form thecladeCoelenterata,butanumberofrecentphylogenomic classical viewhasbeenthattheCtenophoratogetherwithCnidaria position oftheCtenophorahasrecentlycomeintofocus.The inter-relationships ofthebasalmetazoangroups.Inparticular, the relatively wellestablished,butthereisnotagreementaboutthe cords arehomologous(seebelow). been challenged,anditnowappearsthatthetwolongitudinalnerve interpretation ofthedorsal/ventralorientationtwogroupshas 2009; Wheeleretal.,Edgecombe2011). However, the now supportedbynumerousphylogenomicstudies(Hejnoletal., Ambulacraria) (Grobben,1908)isstilluniversallyacceptedand Bilateria intoProtostomiaandDeuterostomia(=Cordonia+ Chordonia byanunpaireddorsalneuraltube.Thedivisionofthe be specializedintorowsofgangliaconnectedbyconnectives]andthe present discussion. and theuncertaintydictatesthat theywillnotcontributetothe phylogenetic positionfallsoutside thescopeofpresentpaper, Ambulacraria (Philippeetal., 2011). A discussionoftheir 2013), orthealternativeview that theyarethesistergroupof bilaterian groups(Hejnoletal., 2009;Nielsen,2010;Ryan etal., more traditionalviewthatthey are thesistergroupofremaining Nemertodermatida andXenoturbellida)isstilldebated,with the type hasbeencalledprimarylarvae(Jägersten,1972). Chordata (exceptforthenon-feedingamphioxuslarva).This larval (Echinodermata +Hemichordata),butareabsentinEcdysozoa and Porifera, Cnidaria,Spiralia(Lophotrochozoa)andAmbulacraria systems ofCnidariaandBilateria,i.e.Neuralia. larval nervoussystemscanthereforeberestrictedtothe the neuralianapicalorgan (Jager etal.,2011). Thediscussionof (Hernandez-Nicaise, 1991)anditisnotconsideredhomologous of completely different from thatofcnidariansandbilaterians ctenophores issituatedattheapicalpole,butitsstructure (Martindale, 1987).The‘apicalorgan’ ofthemainlyholopelagic organs andbecauseitcanalreadycarryoutsexualreproduction a larva(Ryan etal.,2013),bothbecauseitlacksspeciallarval ctenophore lifecyclesmustbeinterpretedasajuvenileratherthan Jékely etal.,2015).Thecydippidstagecharacteristicofthe around theK–T (Cretaceous–Tertiary) boundary(Podaretal.,2001; ancestor ofthelivingctenophorescouldhavebeenasrecent may suffer fromlongbranchattraction,becausethelatestcommon system appearshighlyunlikely, andthephylogenomicanalyses Bilateria) haveevolvedconvergently. However, lossofthenervous systems andmusclesofCtenophoraNeuralia(Cnidaria+ have beenlostinspongesandplacozoansorthatthenervous position. Thisimplieseitherthatthenervoussystems(andmuscles) Pleurobrachia belcheri The topologyofthebilaterianpartanimaltreelifeis Within theNeuralia,positionofAcoelomorpha (Acoela, Ciliated primarylarvaearefoundinnumerouslineages of Mnemiopsis leidyi (Moroz etal.,2014)supporttothis (Ryan etal.,2013)and 629
The Journal of Experimental Biology 630 Fritzenwanker etal.,2014). homologous (Sinigagliaetal.,2013;Marlow 2014; apical poleofcnidariansandthebilateriansare new observationsofgeneexpressionclearlydemonstratethatthe opposite directionsinthe‘coelenterates’ (Dunnetal.,2007).However, apical–blastoporal axisinthebilaterians,whereastwoaxeshave because theanimal–vegetalaxishassameorientationas apical organs ofcnidariansandbilaterianshasbeenquestioned terminology ofRichteretal.(Richteral.,2010).Thehomology use thetermapicalorgan intherestrictedsenseaccordancewith expression (Tosches andArendt,2013).However, mostrecentpapers morphological literature,andthisisalsoseeninsomestudiesongene structure hasbeencalledtheapicalorgan inmostoftheolder ganglia incloseappositiontotheapicalorgan, andthiscompound cells (Richteretal.,2010).Manyspiraliansdeveloplateral(cerebral) definition ofaganglion,becauseitapparentlycomprisesonlysensory cilium, butinsomespecieswithseveral;itdoesnotfitthenarrow consists ofagroupcolumnarorflask-shapedcellsusuallywithone other speciesshowamoregenerallyciliatedarea.Theapicalorgan many species( together asacompoundcilium(cirrus)in (Nielsen, 2004;Nielsen,2005).Theapicalgroupoflongciliaworks apical blastomeres,asshowninnumerouscell-lineagestudies in mostoftheciliatedneuralianlarvae.Itdevelopsfrom The apicalorgan isacharacteristic,ciliated,putativesensorystructure REVIEW series ofadaptationalmodificationsexistingstructures. larva andthemorphologyofprotostomianCNSinacontinuous that explainsboththeoriginofciliarybandstrochophora trochaea theory(Nielsen,2012),whichappearstobetheonly apical organ andthelarval–adultnervoussystem. centers canberecognizedinthelarvae,viz.exclusivelylarval called adultation(Jägersten,1972),sothattwotypesofnervous established inthelarvalstages,throughevolutionaryprocess centers developedinthebenthicadultsandgraduallybecame have beendiscussedelsewhere(Nielsen,2013).Newnervous alternative theoriesfortheevolutionofpelago-benthiclifecycles cycle(s) evolvedthroughadditionofadultbenthicstages;thisand organization wasretainedinthelarvaewhenpelago-benthiclife corresponding ancestorneurogastraea(Nielsen,2008).Its a ciliatedsensoryorgan attheapicalpole,andIhavecalled Carroll, 1999;BruscaandBrusca,2003).Mostciliatedlarvaehave gastraea, althoughthisisrarelydiscusseddirectly(e.g.Knolland The apical organ: the ancestral neuralian brain neuralian theancestral organ: apical The A The followingdiscussionsarebasedontheframeworkof Most recentauthorsagreethattheeumetazoanancestorwasa B i.1),but Fig.
C (Martina, 2000;Nakanishietal.,2008). neurons; abrainislackingbothinthepolypsandmedusae degeneration ofthelarvalnervenetanddevelopmentanew (Yuan etal.,2008).Thenervoussystembecomesreorganized with It islostwhenthelarvasettleswithcellsaroundapicalpole medusozoans (Nakanishietal.,2008). differentiates fromthemostapicalcells,named1a 2005; Hejnoletal.,2007;Meyer2010).Theapicalorgan confirmed theearlierresultsinalmostalldetails(Ackermannetal., Nielsen, 2004;2005)andthefewmodernstudieshave been thesubjectofclassicalcell-lineagestudies(reviewedin serotonergic cellsmayalsobepresent(Page,2002). and Wanninger, 2012;Temereva andTsitrin, 2014).Othertypesof development, forexampleinthephoronid is foundinmanyspecies,butthenumbermayincreaseduring pattern ofeightflask-shapedserotonergic cells,eachwithonecilium, in thenumberandstructureofcellsorgan. A characteristic nemerteans (Cantelletal.,1982;Page,2002).Thereismuchvariation but multiciliatecellsareknownbothfrommollusksand Wanninger, 2012)(Fig. 1987; McDougalletal.,2006;Maslakova,2010;Temereva and larvae ofannelids,mollusks,nemerteansandphoronids(Nielsen, A slightlytwistedcirrusoflongapicalciliaisseeninmanyciliated ciliary cirrusseeninanthozoans(Fig. the organ seemsrathersimilarinallgroups,buttheprominent monociliated nervecells(Marlowetal.,2014).Theorganization of of theseaanemone The apicalorgan ofcnidarianlarvaeiswellstudied,especiallythat region. Phylactolaemate‘larvae’ showaconcentrationof of cells;itdisappearsatmetamorphosis(Nielsen,1971). cases becomesingestedbythejuvenile(Maslakova,2010). metamorphosis togetherwiththewholelarvalbody, whichinsome 1897). Inthepilidiumlarvae,apicalorgan isshedat stage, longbeforethelarvahatchesfromeggmass(Conklin, Crepidula, thefourapicalcellsdegenerateatanearlydevelopmental undergo apoptosis(GifondorwaandLeise,2006).Inthegastropod time ofsettling(DickinsonandCroll,2003),thecellsmay spiral-cleavage terminology. Theorgan degeneratesbeforeoratthe Protostomia Cnidaria The apicalorgan isnecessaryforsettling(Rentzschetal.,2008). Several annelids,mollusks,nemerteansandplatyhelminthshave Bryozoan larvaeshowwidevariationinthestructureofapical All entoproctlarvaehavealarge apicalorgan withseveral types The JournalofExperimentalBiology(2015)doi:10.1242/jeb.109603 Nematostella clavigerus tornaria larvaoftheenteropneust Lepidochitona dentiens trochophora larvaofthepolyplacophoranmollusk Vienna). (B)Scanningelectron micrographofa vectensis planula larvaofthecnidarian Fig. 1B). Thereisusuallyonlyoneciliumpercell,
.Apicalorgans. 1. (courtesy ofDrUliTechnau, Universityof (Stiasny, 1914). , whereitconsistsofagroup (A) Lightmicrographofa . (C)Drawingofanearly
1A) islackinginthe Phoronopsis Nematostella Balanoglossus 1 –1d (Temereva 1 in the
The Journal of Experimental Biology REVIEW nature ofthenervous systemofthevertebrates; thecerebralganglia 2013) andMarlowetal.(Marlow etal.,2014)recognizethedual nerve ringoftheprotostomes. patterns ofthechordateCNSindicate homologywiththeblastoporal difficult tointerpret,butbothembryologyandgeneexpression together becometheadultbrain. Thedeuterostomesaremore ring, wheretheanteriorpartofringandcerebralganglia pair ofcerebralgangliaandablastoporal(circumblastoporal) nerve embryonic) stageinallbilaterians.Inprotostomes,itconsists ofa The adultCNSbeginstodevelopalreadyinanearlylarval (or the theoryforevolutionofchordateCNSpresentedbelow. (Lacalli etal.,1994;Tagawa etal.,2000),butitisincompatiblewith some supportfromultrastructureandgeneexpressionstudies ciliary bandsandbecomingsituatedinthebrain.Thisideahasfound shows theapicalorgan being internalizedbythefusionoflateral by Garstang(Garstang,1928)andpresentedinmanytextbooks not present.ThetheoryfortheoriginofchordateCNSproposed (Byrne etal.,2007)andinenteropneusts(Miyamoto2010). always degeneratebeforeoratmetamorphosis,bothinechinoderms supports thehomology(Yaguchi etal.,2010),andtheapicalorgans the apicalorgan incnidariansandprotostomes,butgeneexpression (Byrne etal.,2007).Sothemorphologyisnotveryreminiscentof at themostapicalpartsofcircumoralciliaryband(neotroch) apical pole,withmorescatteredgroupsofflask-shapedcellslocated show somevariationinthestructureofnervoussystemat enteropneusts (Stiasny, 1914)(Fig. slightly twistedtuftandonlyinsomestages,forexample of echinoderms,althoughonlysomespeciesshowthetypical, apical organs arefoundinenteropneustsandspeciesofallclasses In theambulacrarians(hemichordates+echinodermates),ciliated 2000). for recognitionoftherightsubstratesettling(Hadfieldetal., but certaincellsintheorgan ofthegastropod between theapicalorgan andthenervoussystemofpolypides. Woollacott, 1983;Fuchsetal.,2011). Thereisnoconnection blastema developintothepolypideoffirstzooid(Reedand pulled downanddisintegrates,theciliatedcellslower ciliated cellssurroundsthenerve.Atsettling,neuralplateis nerve tothepyriformorgan. A ring-shapedblastemabelowthe cells areunderlainbyanervousplexus,whichsendsprominent Zimmer, 1971;ReedandCloney, 1982;Reedetal.,1988).These a radialarrayofwedge-shapedmulticiliatedcells(Woollacott and coronate larvaehaveamuchmorecomplicatedapicalstructure,with organs degenerateaftersettling(Atkins,1955).Thelecithotrophic testing thesubstrateforsettling(Strickeretal.,1988).Alllarval it isconnectedtothepyriformsensoryorgan, whichisusedin epitheliomuscular cell.Thefunctionofthisorgan isunknown,but ring-shaped areasofmonociliatedandnon-ciliatedcellsone area ofneuronsconnectedtoabasalnerveplexussurroundedby cyphonautes larvaehaveawell-definedapicalorgan withacentral Eurystome larvaeshowconsiderablevariation.Theplanktotrophic 1953). Nervecellshavenotbeenobservedincyclostomelarvae. apical poleisinvaginatedatmetamorphosisanddegenerates(Brien, present (Gruhl,2010);thewholeciliatedepitheliumincluding serotonergic sensorycellsattheapicalpole,butantuftisnot The larval–adult CNS larval–adult The Deuterostomia The recentpapersbyTosches andArendt(Tosches andArendt, The chordatesdonothaveciliatedlarvaeandanapicalorgan is The functionoftheprotostomianapicalorgan ispoorlyknown,
1C). Thevarioustypesoflarvae Phestilla are necessary have beenoverlooked, anditispresentinmanyother annelids. Capitella (see Meyeretal.,2010).Theshape ofthecircumblastoporalnerveringin and 1cinthegastropod the polychaete micromere quartetinthespiralcleavage,fromcells1cand1d mollusks (DickinsonandCroll,2003). 2010), butthepatterncanclearlyberecognized,forexamplein 2).Thisisbestseeninannelids(Meyeretal., perianal loop(Fig. into thepairedorfusedventralnervecordwithaperioraland cerebral gangliaandablastoporalnervecord,whichdifferentiates trochaea theory(Nielsen,2012).Typically, itconsistsofapair 2004; Nielsen,2005),anditsevolutionhasbeenexplainedbythe system isquitewellknowninmanyspiralians(reviewsNielsen, Both developmentandmorphologyoftheadultcentralnervous al., 2009). cannot becharacterizedasanervecord(Koizumi,2007;Marlowet A concentrationofnervecellsisseenaroundthemouth,butthey with thedescriptionsandinterpretationsbelow. ‘forebrain’ isdescribedasachimaera.Thisingoodaccordance cord iscalledtheblastoporallegacyormedio-lateralpatterning.The are calledtheapicallegacyorplateandblastoporalnerve lecithotrophic larvaof (Nielsen, 2012)],andthelowerillustration showstheCNSofalate and ajuvenile,asinterpretedbythe trochaeatheory[modifiedfromNielsen annelids. Theuppertwoillustrationsshowthe CNSofatrochophoralarva Fig. cerebral ganglia(Conklin,1897;Ackermannetal.,2005). found inmanyannelidandmollusklarvaedevelopfromcellsofthe Protostomia Cnidaria The cerebralgangliadifferentiate fromtwocellsofthefirst
Cerebral Metatroch .Central nervoussystems(CNSs)inprotostomes,exemplifiedby 2. ganglia Apical organ is exactlyaspredicted, exceptthattheanalloopismissing; itmay Mouth The JournalofExperimentalBiology(2015)doi:10.1242/jeb.109603 Prototroch Platynereis Cerebralganglia Circumoral connective Capitella blastoporal nervecord Crepidula Anterior loopof as demonstratedthroughacell-lineage study (Ackermann etal.,2005),andfrom1a Blastoporal nerve cord Telotroch Prototroch Ventral nerve Ventral nerve blastoporal nerve cord (Hejnol etal.,2007).Theeyes Anterior loop of Mouth cord cord Anus Telotroch Gut Anus 631
The Journal of Experimental Biology ventral nervecordsdevelopfromtheblastomeres2d Sicyonia with thelooparoundmouth. ganglia andtheircommissuresrepresenttheblastoporalnervecords 3).Thedeutocerebrum,tritocerebrumandthemoreposterior (Fig. the arthropods(Harzsch,2004;ScholtzandEdgecombe,2006) ganglia oftheannelidsarehomologouswithprotocerebrum larvae lackcerebralgangliaandventralnervecords. the foot(Wanninger etal.,2007).Theirfateisunknown.Bryozoan Loxosomella after metamorphosis(Nielsen,1971).Someobservationson which maybemodifiedcerebralganglia.Theorgan degenerates blastoporal nervoussystemoftheannelids. with anumberofcommissures,andthisisverysimilartothe and Wanninger, 2010)showpairedlongitudinalblastoporalnerves and thelarvaofbrachiopod 2009), aredifficult torelate to thoseonthespiralians. Romanomermis 632 adult echinoderms consistsofanoralnervering andfive(ormore) associated withtheadultnervous system.Thenervoussystemofthe metamorphosis andthenerves areapparentlynotinanyway disintegrates togetherwiththe associatednervesbeforeorat capture particlesthroughciliary reversal(Strathmann,2007).It those oftheprotostomianlarvae, viz.abandofmonociliatecellsthat neotroch, whichisofastructure andfunctionquitedifferent from tornaria oftheenteropneustshaveaperioralciliaryband, the feeding amphioxuslarva). whereas chordateslackprimarylarvae(exceptfortheearly non- Echinoderms andhemichordateshaveciliatedprimarylarvae, Fig. REVIEW 2010; MeyerandSeaver, 2010).In by thecelllineageinannelids(Ackermannetal.,2005;Meyer becomes theposteriorpartofbrain,hasonlybeendemonstrated Deuterostomia However, thelarge larvaof and areusuallybelievedtolacktheblastoporalnervoussystem. cleavage. Phoronidsandbrachiopodsseemtolackcerebralganglia nervous systemisdifficult todeduceingroupswithoutspiral this interpretation(seebelow). expression (Tosches andArendt,2013)areinfullagreementwith respectively (MeyerandSeaver, 2010).Observationsofgene and ScholtzEdgecombe(ScholtzEdgecombe,2006). cerebral gangliainyellowandtheblastoporalnervoussystemgreen(cf.Fig. The fewcell-lineagestudiesofecdysozoans,suchastheshrimp Both morphologyandgeneexpressionindicatethatthecerebral Entoproct larvaehaveapairedorunpairedfrontalorgan/ganglion, The varioustypesofdipleurulalarvaetheechinodermsand the The anteriorpartoftheperiorallooparoundmouth,which The embryologicaloriginofthecerebralgangliaandblastoporal
.ComparisonofspiralianandecysozoanCNSs. 3. (Hertzler, 2002)andthenematodes larvae indicatethepresenceoflongitudinalnervesin (Sulston etal.,1983;SchulzeandSchierenberg, Annelida Phoronopsis harmeri Novocrania anomala with chaetae Cerebral ganglia Peristomium Mouth Prostomial Parapodium Prostomium tentacle Capitella Caenorhabditis , therightandleft (Temereva, 2012) Nervous systemsofannelids,onychophoransandarthropods(exemplifiedbyacrustacean)withthe 1121 Onychophora (Altenburger and 2d 1122 and ,
2). BasedonErikssonetal.(Erikssonal.,2003),Harzsch(Harzsch,2004) The neuraltube inthetailisresorbedatsettling. Intheascidians, and variousothersensorystructures (BurighelandCloney, 1997). an anteriorbrainvesicle,insome specieswithaneye,astatocyte ascidian larvaehaveaneuraltube withoutnervecellsinthetailand (Seeliger andHartmeyer, 1893-1911; Veeman etal.,2010).The side astheneuraltube,whichthen oughttobedescribedasventral Clavelina gut, butthedevelopmentofcertainascidians,suchas make outbecauseoftheirmetamorphoseswiththerotation the organs arefoundalongitslength (Wicht andLacalli,2005). vesicle, andvarioustypesofphotoreceptorsothersensory 2009). Theanteriorpartoftheneuraltubedifferentiates intoabrain left gillopening(Ruppert,1997;Benito-GutiérrezandArendt, their ontogenyclearlyindicatesthatmouthisthemodified first be inferredthroughcomparisonswiththeotherchordates,because Cephalochordata, UrochordataandVertebrata. tube, whichisspecializedindifferent waysinthethreephyla orientation (Hollandetal.,2013). expression giveunambiguousinformationaboutthedorsal–ventral similar (Nomaksteinskyetal.,2009).Neithermorphologynorgene patterns inthedorsalandventralnervecordsofbodyarevery shows strongsimilarities(Panietal.,2012),butthegeneexpression seen inchordates(KaulandStach,2010).Also,geneexpression and anumberofthecelltypestheirdistributionresemblethose side. Thecollarcorddevelopsthroughachordate-likeneurulation, around thepharynxtoalongitudinalnervecordalongventral collar cordposteriorlyalongthelengthofbody, andnerves behind themouth,alongitudinalnervecordextendingfrom enteropneusts comprisesadorsalcollarcordintheregionjust at metamorphosis.Thenervoussystemofjuvenileandadult 2001), andboththeciliarybandnervebegintodegenerate 2007). Thereisanervealongthisciliaryband(LacalliandGilmour, telotroch, butitshomologyisuncertain(NielsenandHay-Schmidt, ring oflarge, compoundcilia,whichhasoftenbeencalleda Martinez, 2003;Nielsen,2006).Thetornarialarvahasaposterior must beinterpretedasanexampleofhomoplasy(Nielsenand homologs ofthechordateneuraltube(Haag,2005).However, this in neurulation,andtheradialnerveshavebeeninterpretedas organization ofthisstructureinvolvesanumbergenesalsoactive formation ofthechordateneuraltube(Smith,1988).The developing radiioftheadultrudimentandthisresembles holothurians developfrominvaginationsoftheectodermalong Welsch, 2001).Theradialnervesofechinoids,asteroidsand radial nervecords.Thereisnothinglikeabrain(Heinzellerand Cerebral Jaws Antenna ganglia Walking leg with The orientationofmosttheadulturochordatesisdifficult to The dorsal–ventralorientationofthecephalochordatescanonly The CNSofthechordatesdevelopsfromcharacteristicneural claws , showsthatthestomodaeum/mouth issituatedatthesame The JournalofExperimentalBiology(2015)doi:10.1242/jeb.109603 Arthropoda (Decapoda) Maxilla Mandible Tritocerebrum Antenna Mouth Deutocerebrum Antennule Protocerebrum Ciona and
The Journal of Experimental Biology a homologofthe ventralnervecord(s)ofthe protostomes.This variation ofprotostomy, withtheneuraltubeofchordates being (Doncaster, 1902).Thisindicatesthatdeuterostomyisinfacta Edgecombe etal.,2011; Riegeretal., 2011), showdeuterostomy phylogeny (HarzschandMüller, 2007;Hejnoletal.,2009; protostomes, asindicatedboth bytheirCNSandmolecular the ‘normal’ protostomy. Also,theChaetognatha,whichare 6).Bothgeneraarenestedwithingroupswith (Åkesson, 1967)(Fig. gastropod blastopore becomingonlytheanushasbeenobservedbothin the deuterostome, butitisremarkablethatanembryologywith the anus (Grobben,1908).Amphistomyhasneverbeenobservedin any (amphistomy). Inthedeuterostomes,blastoporebecomes the or inmoremoderninterpretationintothemouth+ anus developing species,withtheblastoporeintomouth, lateral blastoporelips,orfromhomologousareasindirect protostomian nervecordstypicallydifferentiate alongthefusing Deuterostomia hasalwaysbeenthefateofblastopore. The 5). dorsal intheprotostomes(Fig. that boththemouthandanusbecomesituatedonsidecalled embryo (andtheblastoporal/analareaaroundposteriorend)so anterior endoftheneuraltubeextendsaround in thesamepositionduringdevelopmentclearlyshowshow REVIEW frog 4). agreement withthisview(Tosches and Arendt, 2013)(Fig. expression incnidarians,protostomesandvertebratesarefull (Arendt andNübler-Jung, 1997;Nielsen,1999).Comparisonsofgene have supportedthisview, sobothCNSsoughttobecalledventral indicating homology, andseveralstudiesofanatomyembryology Robertis andSasai,1996;Denesetal.,2007;Lowe2006) cord ofanannelidandthefusedneuralfoldsavertebrate(De expression exhibitsthesamepatternindevelopingventralnerve are homologous.Manystudieshavedemonstratedthatgene suggested thatthecentralnervoussystemsofannelidsandvertebrates the dorsalside),butmorethanacenturyagoDohrn(Dohrn,1875) straightforward, withthemouthonventralside(andCNS Burighel, 2005). the anteriorenddifferentiates intoasmallbrain(Mackieand Apical patterningsystems Blastoporal patterningsystems The characterusedfordistinguishingProtostomiaand A freshviewontheclassicaldescription oftheembryology The orientationofthevertebratesappearsintuitively Xenopus dll pax3/7-paxD pax6 nk2.1/nk2.2 foxQ2 fezf rx six3 Viviparus (Hausen andRiebesell,1991)withtheapicalpolekept Cnidarians (Dautert, 1929)andintheannelid Annelids Insects Eunice it couldrepresentthecerebralgangliawitheyesof in theareacorrespondingtoepisphereofspiralianlarva,so area ofthevertebratebrain(Tosches andArendt,2013)issituated cerebral gangliacouldbepresentinvertebrates.The‘apicallegacy’ opening ofanamphistomeblastoporeclosure. the mouthofurochordatesandvertebratesasamodifiedanterior (Drysdale andElinson,1991).Thus,thereisgoodreasontointerpret line andappearstobecomepinchedoff fromtheneuraltube anterior partoftheneuralfold,whichextendsforwardinanarrow al., 2010).Invertebrates( which issituatedattheanterioredgeofneuralplate(Veeman et (ascidians), thestomodaeumisderivedfromanteriorneuropore, brain areaorbeacompletelynewstructure.Intheurochordates implies thatthemouth(stomodaeum)shoulddevelopinside developing intothe CNSareblack.ModifiedfromNielsen (Nielsen,1999). embryo. Theblastopore rimisblueandthecellsof neuralplate the apicalpole(redarrow).(A)Fate map.(B)Young embryo.(C)Older Fig. The questionthenariseswhetherahomologoftheprotostomian A
.Development ofthefrogXenopus. 5. C Vertebrates Polar bodies Endoderm +chorda Ectoderm + mesoderm The JournalofExperimentalBiology(2015)doi:10.1242/jeb.109603 Neural plate Anus Adhesive organ Tosches andArendt(Tosches andArendt,2013). eyes ofvertebratesisquestionable.Modifiedfrom Fig. protocerebrum ofarthropodsissupported(see the cerebralgangliaofannelidsand at theapicalsideofprototroch;homology correspond tothepositionofcerebralganglia patterning system’ intheannelidappearsto expression inthevertebrate.The‘apical and insectshowsstrongsimilaritieswiththe system’ (especiallynk2.1/nk2.2)oftheannelid the apicalpole.The‘blastoporalpatterning vertebrates. cnidarians, annelids,arthropodsand Fig. Mouth Xenopus), themouthdevelopsfrom
3), buthomologywiththehypothalamusand .Regionalgeneexpressionsystemsin 4. Blastopore B None ofthegenesisexpressedat Apical pole Apical pole The orientationisdeterminedby Adhesive organ Adhesive organ Mouth Mouth 633
The Journal of Experimental Biology ‘deuterostomy’ intheannelid blastopore closure(amphistomy), asillustratedbytheoccurrenceof deuterostomes couldbeaspecializationoftheprotostomianlateral there arenonervesinthemidline.ModifiedfromÅkesson(Åkesson,1967). behind theprototroch.Theventralnervesdevelopfromareabut blastopore atalaterstage;thestomodaeumdevelopsfromanareajust archenteron becomessolid,buttheanusbreaksthroughinareaof 634 meeting, whichwas supportedbytheNationalScienceFoundation. Iammost This workwaspresented atthe‘EvolutionofFirstNervous SystemsII’ offshoot fromthestem-lineageofprotostomes. chaetognaths. Thisindicatesthat thedeuterostomescouldbeanearly as envisagedbythetrochaeatheory(Fig. bilaterians resembledthepelago-benthicancestorofprotostomes vertebrates). and bytheneuraltubeinchordates(brainplusspinalcord in the (developing fromthesecondmicromerequartetinspiralians) part ofthebrainandventralnervecordsinprotostomes (circumblastoporal) nervecord,whichisrepresentedbytheposterior homologous structuresinthevertebratebrain.(3)A blastoporal main partoftheprotostomianbrain,butitisdifficult toidentify (from thefirstmicromerequartetinspiralians).Theyform pair ofcerebralgangliathatdevelopinbilaterianlarvae/embryos the ancestralneuralianbrainandonlycnidarian‘brain’.(2)A all ciliatedlarvae.Itdegeneratesbeforeoratmetamorphosis.is main components.(1)Theapicalorgan, whichispresentinalmost The CNSsoftheneuralians(cnidarians+bilaterians)comprisethree very questionable. i.e. intheblastoporalarea(EaglesonandHarris,1990),sothisis protostomes, butthevertebrateeyesdevelopfromapicalplate, Modified fromOttoandTönniges(OttoTönniges,1906).In blastoporal nervoussystem,althoughtherearenonervesinthemidline. just behindtheprototroch.Theventralfootareaisgeneralof archenteron becomesthestomach;stomodaeumdevelopsfromanarea Viviparus Fig. REVIEW Acknowledgements Conclusions A furtherconclusionisthatthelatestcommonancestorof Episphere
.‘Deuterostomy’ inprotostomes. 6. Stomodaeum Prototroch , theblastoporedirectlybecomesanusandwhole Stomodaeum Archenteron Archenteron Shell glandarea ‘Neural’ area Endoderm Blastopore Eunice Eunice Ventral footarea Blastopore Viviparus daeum Stomo- Mouth , thegastropod Median sectionsofembryos.In Stomodaeum Prototroch
2). Theblastoporefateofthe Endoderm Stomach Viviparus Shell gland Gut ‘Neural’ area Eunice and the Anus , the uh,J,Mridl,M .adHjo,A. Hejnol, and M.Q. Martindale, J., Fuchs, C.J. Lowe, and Jr R.M., Freeman, J., Gerhart, J.H., Fritzenwanker, Peterson, and R.L. Morris, R.C., Angerer, L.M., Angerer, V. N., Moy, E.F., Dunn, deob,G . iie,G,Dn,C . enl . rsesn .M,Neves, R.M., Kristensen, A., Hejnol, C.W., Dunn, G., Giribet, G.D., Edgecombe, asag W. Garstang, G.E. Budd, and N. Tait, B.J., Eriksson, W. A. Harris, and G.W. Eagleson, un .W,Hjo,A,Mts .Q,Pn,K,Bon,W . mt,S.A., Smith, W. E., Browne, K., Pang, D.Q., Matus, A., Hejnol, C.W., Dunn, R.P. Elinson, and T. A. Drysdale, commercial, ornot-for-profitsectors. This researchreceivednospecificgrantfromanyfundingagencyinthepublic, The authordeclaresnocompetingorfinancialinterests. present alecture. grateful toDrPeterAndersonfororganizingthemeetingandinvitingme iodra .J n es,E.M. Leise, and D.J. Gifondorwa, L. Doncaster, rbe,K. 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