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White-gutted soldiers: simplification of the digestive tube for a non-particulate diet in higher Old World termites (Isoptera: Termitidae)

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White-gutted soldiers: simplification of the digestive tube for a non-particulate diet in higher Old World termites (Isoptera: Termitidae)
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Insectes sociaux, 64(4), 525-533
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Scheffrahn, Rudolf
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Springer
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English
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Previous observations have noted that in some species of higher termites the soldier caste lacks pigmented particles in its gut and, instead, is fed worker saliva that imparts a whitish coloration to the abdomen. In order to investigate the occurrence of this trait more thoroughly, we surveyed a broad diversity of termite specimens and taxonomic descriptions from the Old World subfamilies Apicotermitinae, Cubitermitinae, Foraminitermitinae, Macrotermitinae, and Termitinae. We identified 38 genera that have this “white-gutted” soldier (WGS) trait. No termite soldiers from the New World were found to possess a WGS caste. Externally, the WGS is characterized by a uniformly pale abdomen, hyaline gut, and proportionally smaller body-to-head volume ratio compared with their “dark-gutted” soldier (DGS) counterparts found in most termitid genera. The WGS is a fully formed soldier that, unlike soldiers in other higher termite taxa, has a small, narrow, and decompartmentalized digestive tube that lacks particulate food contents. The presumed saliva-nourished WGS have various forms of simplified gut morphologies that have evolved at least six times within the higher termites.
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Collected for University of Florida's Institutional Repository by the UFIR Self-Submittal tool. Submitted by Rudolf Scheffrahn.

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RESEARCHARTICLEWhite-guttedsoldiers:simplicationofthedigestivetubeforanon-particulatedietinhigherOldWorldtermites(Isoptera:Termitidae)R.H.Scheffrahn1€T.Bourguignon2€C.Bordereau3€R.A.Hernandez-Aguilar4€V.M.Oelze5€P.Dieguez5€J.Sobotnik6€A.Pascual-Garrido7Received:24June2016/Revised:26June2017/Accepted:30June2017/Publishedonline:12July2017TheAuthor(s)2017.Thisarticleisanopenaccesspublication.ThisarticleisanopenaccesspublicationAbstractPreviousobservationshavenotedthatinsomespeciesofhighertermitesthesoldiercastelackspigmentedparticlesinitsgutand,instead,isfedworkersalivathatimpartsawhitishcolorationtotheabdomen.Inordertoinvestigatetheoccurrenceofthistraitmorethoroughly,wesurveyedabroaddiversityoftermitespecimensandtaxo-nomicdescriptionsfromtheOldWorldsubfamiliesApicotermitinae,Cubitermitinae,Foraminitermitinae,Macrotermitinae,andTermitinae.Weidentied38generathathavethiswhite-gutted''soldier(WGS)trait.Noter-mitesoldiersfromtheNewWorldwerefoundtopossessaWGScaste.Externally,theWGSischaracterizedbyauniformlypaleabdomen,hyalinegut,andproportionallysmallerbody-to-headvolumeratiocomparedwiththeirdark-gutted''soldier(DGS)counterpartsfoundinmosttermitidgenera.TheWGSisafullyformedsoldierthat,unlikesoldiersinotherhighertermitetaxa,hasasmall,narrow,anddecompartmentalizeddigestivetubethatlacksparticulatefoodcontents.Thepresumedsaliva-nourishedWGShavevariousformsofsimpliedgutmorphologiesthathaveevolvedatleastsixtimeswithinthehighertermites.KeywordsApicotermitinaeCubitermitinaeForaminitermitinaeMacrotermitinaeTermitinaeEntericvalvearmatureProctodeumIntroductionTrophallaxisisthemouth-to-mouth(stomodeal)oranus-to-mouth(proctodeal)exchangeofalimentarycontentsbetweenmembersofasocialinsectcolony(Wilson1971).Termitesoldierslackchewingmandiblesandmustobtaintheirfoodasliquidsorpastesofferedbynestmateworkers(Grasse1949).Inthelowerwood-feedingtermites(e.g.,KalotermitidaeandRhinotermitidae),soldiersarefedwithworkergutcontentswhichconsistofmixturesofmasticatedwoodparticlesandsaliva(Grasse1982;Noirot1969).Thedietsofmosthighertermites(Termitidae)aremuchmorevaried(Donovanetal.2001),andsoldiersarenourishedbystomodealtrophallaxiswithparticlesofworker-masticatedwood,leaflitter,soil,fungus,bacteria,herbaceousplants,lichens,algae,orsomederivationofthese(e.g.,soundvs.severelydecayedwood).Workersofsoil-feedingtermites,whichconstitutethemajorityoftermitidgenera,ingestmasticatedmixturesofhumus,roots,mycelia,lignied ElectronicsupplementarymaterialTheonlineversionofthisarticle(doi:10.1007/s00040-017-0572-9)containssupplementarymaterial,whichisavailabletoauthorizedusers.&R.H.Scheffrahnrhsc@u.edu1FortLauderdaleResearchandEducationCenter,UniversityofFlorida,3205CollegeAvenue,Davie,FL33314,USA2OkinawaInstituteofScienceandTechnologyGraduateUniversity,1919-1Tancha,Onna-son,Okinawa904-0495,Japan3UMRCNRS5548,CommunicationChimique,UniversitedeBourgogneDeveloppement,21000Dijon,France4DepartmentofBiosciences,CentreforEcologicalandEvolutionarySynthesis(CEES),UniversityofOslo,P.O.Box1066,Blindern,0316Oslo,Norway5DepartmentofPrimatology,MaxPlanckInstituteforEvolutionaryAnthropology,DeutscherPlatz6,04103Leipzig,Germany6FacultyofForestryandWoodSciences,CzechUniversityofLifeSciences,Prague,CzechRepublic7LeverhulmeTrustEarlyCareerFellow,SchoolofArchaeology,UniversityofOxford,OxfordOX13QY,UK Insect.Soc.(2017)64:525533DOI10.1007/s00040-017-0572-9InsectesSociaux123

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tissue,silicagrains,etc.(Sleafordetal. 1996 ;Donovanetal. 2001 ;Donovan 2002 )whicharetransferredtotheirsoldiers. Theseparticulatesuspensionsimpartacontrastinglydarker colorationtotheguttubesofbothmatureworkersand soldiers,whicharevisiblethroughtheiropaqueornearly transparentintegument. Grasse ( 1949 )reportedthatinsomehighertermites (probablymostlyinsoil-feedingtaxa),thedietofsoldiers mayconsistwhollyoftheworker'ssalivainitsclearor opalescentform.Noirot( 1955 )observedthatsoldiersof Procubitermescurvatus Silvestri(Cubitermitinae)havean exclusivelyliquiddietandtheirdigestivetube,contraryto thatoftheirworkers,lacksparticulatefoodcontent.Noirot ( 1955 )furthernotedthatsoldiersof Pericapritermesurgens Silvestri(Termitinae)alsohaveanexclusivelyliquiddiet whichimpartsawhitish-yellowishcolortotheirabdomens. NoirotandNoirot-Timothe e( 1969 )reportedthatsoldiersof Basidentitermes,Fastigitermes,Orthotermes,Proboscitermes,Procubitermes, and Promirotermes alsohaveastrict liquid(salivary)dietbutdidnotmentiontheirabdominal coloration.Finally,inherkeyofsouthernAfricantermitine genera,Uys( 2002 )usedabdominalcoloration,anartifactof asalivarydiet,inherrstcouplet(creamyyellowto creamywhite''fortheAfricangenera Angulitermes,Basidentitermes,Lepidotermes,Noditermes,Pericapritermes, Promirotermes,Unguitermes, and Unicornitermes ;and greyish-black''for Amitermes,Batillitermes,Crenetermes, Cubitermes,Euchilotermes,Microcerotermes,Okavangotermes,Ovambotermes, and Termes ). Despiteitsimportance,themorphologicalandphylogeneticunderpinningsofthisbipartitesoldierconditionhave receivedlittleornoadditionalattention.Thisledusto examinesoldiersfromanextensivecollectionoftermites worldwideandtointerpretsoldierdescriptionliterature.We showthatOldWorldtermitidsoldierscanbesortedintotwo groups:thewhite-gutted''soldiergroup(WGS)andthe morecommondark-gutted''soldiergroup(DGS).Herein, weidentifyWGSgenera,comparetheexternalandinternal morphologyofWGSandDGSfromselectedgeneraof highertermites,andpresentinformationfromtheliterature thatweusetoreconstructtheancestralstateofsoldiergut typefromarecentlypublishedtermitephylogenetictree.MaterialsandmethodsPhotosofwholeorpartialtermitebodiesweretakenas multi-layermontagesusingaLeicaM205CstereomicroscopecontrolledbyLeicaApplicationSuiteversion3 software.Preservedspecimensweretakenfrom85%ethanolandsuspendedinapoolofPurellHandSanitizer(70% ethanol)topositionthespecimenswithinaclearplastic Petridish.Entericvalvearmature(EVA)imagesweretaken fromslidemountsusingaLeicaCTR5500compound microscopewithdifferentialinterferencecontrastopticsand thesamemontagesoftware.Allphotographedspecimens andthoselistedinTableS1(electronicsupplementary material)arehousedintheUniversityofFloridaTermite CollectioninDavie,Florida,whichcontains42,595colony samplesof229describedandnewgenera.Africantermite specimenswerecollectedintheeldforprimatenutrition and/ortermitediversitystudiesbetween1989and2016. TerminologyoftheworkergutfollowsthatofSands( 1998 ) andNoirot( 2001 ). WeusedonephylogenetictreeofTermitidaerecently publishedbyBourguignonetal.( 2017 )toreconstructthe ancestralstateofthesoldiergut.Weprunedthetreesothat onerepresentativeofeachgenusforwhichweknowthe typeofsoldiergutremains.ThetreewasaBayesianphylogeneticchronograminferredfromfullmitochondrial genomeswiththirdcodonpositionexcluded.Twostates wereconsidered,WGSandDGS.Weusedthefunction ace''ofthepackagephytools(Revell 2012 )implemented inRversion3.2.0.Themodelimplementedbyacewasa maximumlikelihoodmodelwithequalrateoftransition betweenstates.ResultsOurexaminationoftermitespecimens(TableS1),andthe descriptivewordingoftaxawelackedrevealedthatatleast 38OldWorldgenerahavetheWGSmorph(Table 1 ).All aresoil/humusfeedingspecies(non-occulentandsilica particlesabundantinworkergut)withtheexceptionofthe plant-feeding Angulitermes (DebeloandDegaga 2014 ), Eremotermes (AkhtarandSarwar 2003 ), Forculitermes (ScheffrahnandKr ec ek 2015 ), Promirotermes (Davies etal. 2015 ), Synhamitermes (ShanbhagandSundararaj 2012 ),andthefungusfeeding Acanthotermes Pseudacanthotermes ,and Synacanthotermes ,thathaveabundant occulentcontentsintheworkergutbutlacksilicaparticles.Theseeightgeneraalllacksoldierswithasymmetrical snappingmandibles(Table 1 ).TheWGSmorphisrecognizableexternallybyitsuniformlypaleabdomenand proportionallysmallerbody-to-headvolumeratio(Figs.S1, S2)comparedwiththedarkerabdomensandlargerbody-toheadproportionsoftheDGStaxa(Fig.S3).UnlikeNoirot's 1969 whitesoldier''ortheequivalenttermpresoldier'' (NoirotandPasteels 1987 )whichdescribethestagebefore thenalsoldiermolt(Fig. 1 binset),theWGSarefully developedandpossessfunctionalmandibles. Internally,thedigestivetubesofWGSarevariously simplied,shortened,narrowed,and/ordecompartmentalized,andlackparticulatefoodcontents(Figs. 1 2 ,S4) presentintheworkersoftheirspecies(Figs. 1 b,f, 2 c)orin 526 R.H.Scheffrahnetal.123

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Table1 White-guttedsoldiergeneraincludingsubfamily,regionaldistribution(totalno.species),mandibletype,abdomen/bodycolorationas giveninreference GenusSubfamilyRegiona,no.speciesMandibleColorationReferences Acanthotermes MacrotermitinaeEth,1Piercing,cuttingWhitebCurrentpaper Angulitermes TermitinaeEth,Ore,Pale,29Symmetrical snap CreamywhiteUys( 2002 ),Harris( 1964 ) Basidentitermes CubitermitinaeEth,8Piercing,cuttingWhiteCurrentpaper Captritermes TermitinaeEth,1Asymmetrical snap WhiteCurrentpaper Dicuspiditermes TermitinaeOre,20Asymmetrical snap YellowishwhiteAkhtar( 1975 ) Eremotermes TermitinaeEth,Ore,Pale,10Piercing,cuttingWhitishChhotani( 1997 ) Eburnitermes ApicotermitinaeEth,1Piercing,cuttingYellowishwhiteNoirot( 1966 ) Euhamitermes ApicotermitinaeOre,24CrushingBodylighterthanheadChhotani( 1975 ) Eurytermes ApicotermitinaeOre,6CrushingWhitishChhotani( 1997 ) Fastigitermes CubitermitinaeEth,1Piercing,cuttingWhiteCurrentpaper Forculitermes TermitinaeEth,1Piercing,cuttingAbdomenpalerthanheadEmerson( 1960 ),Scheffrahn andKr ec ek( 2015 ) Homallotermes TermitinaeOre4Asymmetrical snap WhitishChhotani( 1997 ) Indocapritermes TermitinaeOre,1Asymmetrical snap WhitishChhotani( 1997 ) Indotermes ApicotermitinaeOre,10Piercing,cuttingWhiteCurrentpaper Krishnacapritermes TermitinaeOre,2Asymmetrical snap WhitishChhotani( 1997 ) Labiocapritermes TermitinaeOre,1Asymmetrical snap WhitishChhotani( 1997 ) Labritermes ForaminitermitinaeOre,3Piercing,cuttingYellowishwhiteAnonymouscLepidotermes CubitermitinaeEth,9Piercing,cuttingWhiteUys( 2002 ) Mirocapritermes TermitinaeOre,8Asymmetrical snap YellowishwhiteChhotani( 1997 ) Mucrotermes CubitermitinaeEth,2Piercing,cuttingAbdomenpalerthan pronotum Emerson( 1960 ) Noditermes CubitermitinaeEth,7Piercing,cuttingWhiteCurrentpaper Orthotermes CubitermitinaeEth,2Piercing,cuttingWhiteCurrentpaper Pericapritermes TermitinaeEth,Ore,Pale,Pap, 40 Asymmetrical snap WhiteCurrentpaper Pilotermes CubitermitinaeEth,1Piercing,cuttingAbdomenwhitishEmerson( 1960 ) Proboscitermes CubitermitinaeEth,2Piercing,cuttingHyalineScheffrahnandO'Malley ( 2010 ) Procapritermes TermitinaeOre,13Asymmetrical snap PaleyellowThapa( 1982 ) Procubitermes CubitermitinaeEth,9Piercing,cuttingWhiteCurrentpaper Profastigitermes CubitermitinaeEth,1Piercing,cuttingAbdomenpalerthan pronotum Emerson( 1960 ) Promirotermes TermitinaeEth,10Symmetrical snap WhiteCurrentpaper Pseudacanthotermes MacrotermitinaeEth,6Piercing,cuttingWhitebCurrentpaper Pseudocapritermes TermitinaeOre,2Asymmetrical snap CreamywhiteChhotani( 1997 ) Quasitermes TermitinaeEth,1Asymmetrical snap PaleKatieCribbs Sinocapritermes TermitinaeOre,16Asymmetrical snap Abdomenwithoutsoil content Chiuetal.( 2015 ) Speculitermes ApicotermitinaeOre,12CrushingWhiteChhotani( 1997 ) White-guttedsoldiers:simplicationofthedigestivetubeforanon-particulatedietin ƒ 527123

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soldiersandworkersofDGSspecies(Figs. 3 ,S3).Several gutmorphologiesarerepresentedintheWGSgroup.In Basidentitermes ,theWGSgutsegmentsformaverylong tubewithanenlargedcrop(C)andrectum(P5)ateitherend (Fig. 1 c).Themidgut(mesenteron,M,andmixedsegment, MS),canbarelybedifferentiatedbecausetheydifferfrom Table1 continued GenusSubfamilyRegiona,no.speciesMandibleColorationReferences Synacanthotermes MacrotermitinaeEth,3Piercing,cuttingWhiteCurrentpaper Synhamitermes TermitinaeOre,4Piercing,cuttingYellowwhiteChhotani( 1997 ) Unguitermes CubitermitinaeEth,7Piercing,cuttingCreamywhiteUys( 2002 ) Unicornitermes CubitermitinaeEth,1Piercing,cuttingCreamywhiteUys( 2002 )aEth Ethiopian, Ore oriental, Pale palarctic, Pap papuanbUnderlyingdarkcuticlechttp://termitesandants.blogspot.com/2012/05/labritermes.html Fig.1a White-guttedsoldier(WGS)of Basidentitermes n.sp.; b B. malelaensis Emersonlivehabitusofsoldiers,workers,andqueen (insetpresoldier(PS)andnestmatesof B .n.sp.; c uncoiledgutof B .n. sp.WGS; d entericvalvearmature(EVA)of B .n.sp.worker; e EVAof B.malelaensis worker;and f lateralviewof B.malelaensis workerwith abdominalintegumentremoved( trianglemarks locationofEVA). C crop(includesgizzard), M mesenteron, MS mixedsegment,P1P5 rstthroughfthproctodealsegments 528 R.H.Scheffrahnetal.123

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eachotheronlyslightlyinshapeanddiameter.TheproctodealsegmentsP1P4ofthe Basidentitermes WGSshow nodiscernablejuncturesandtheEVAisabsent.Inthe Promirotermes WGS(Fig.S4a),thecrop,mesenteron, mixedsegment,andrectumareallwelldevelopedbutthe proctodealsegmentsP1P4formalongandserpentinetube withoutclearsectionaldelineations.TheEVAisabsentin the Promirotermes soldier.The Pericapritermes WGS (Fig.S4b)hasarathershortguttubeandallsegmentsare recognizablebutittoolackstheEVA.Unliketheprevious genera,thegutsegmentsofthe Procubitermes WGSareall recognizableandithasremnantsoftheentericvalve armature(Fig. 2 a),albeitlessdevelopedthanthatoftheLIL (Fig. 2 b)orthatofthefullysclerotizedEVAofthefully formedworker(Fig. 2 c).Incomparison,theDGStaxahave morerobusthindgutmorphologiessimilartotheirworkers, and,akintoworkers,theentireDGSalimentarytractcontainsgrainyparticulatematter(e.g., Cubitermesschereri Rosen,Fig. 3 a,b).Additionally,theDGSsoldierhasafully developedEVAsimilartothatofitsworkerandLIL (Fig. 3 ce). Ourphylogenetictreeincludes83taxabelongingto82 genera(Fig. 4 ).Theancestralstatereconstructionshows, withstrongsupport,thatWGSevolvedatleastoncein Cubitermitinae,twiceinTermitinae,andonceinApicotermitinae.Wealsoincludedsomemembersofthebasal Termitidaesubfamilies,i.e.,Foraminitermitinae, Macrotermitinae,andSphaerotermitinaeandfoundthat WGSalsoevolvedinthesesubfamilies:onceinthesoilfeeding Labritermes (Foraminitermitinae),andatleast twiceinMacrotermitinae.Discussion13WGSgeneraofApicotermitinae,Cubitermitinae, Macrotermitinae,andTermitinaeareincludedinboth Table 1 andthephylogenetictreeweusedtoreconstruct theancestralstateofsoldiergut.Ourtreeshowsthat WGSevolvedfromDGSatleastfourtimesinthese lineages.Becauseourtreedidnotincludeallthespecies recordedwithWGS,thereisapossibilitythatWGS evolvedindependentlyinmorelineages.Oneofthemis Forculitermes ,agenusrecentlytransferredfrom CubitermitinaetoTermitinae(ScheffrahnandKr ec ek 2015 ).TheabsenceofWGStaxaintheNewWorldis enigmaticgiventhecommonancestryofbothNewand OldWorldApicotermitinaeandTermitinae(Bourguignon etal. 2017 ). InNoirot's 1966 descriptionof Eburnitermesgrassei (Apicotermitidae),hereportsthatsoldiersofthisspecies possessayellowish-whiteabdomenduetothefactthatthe digestivetractdoesnotcontainsolidfood''.Duetolackof material,wedidnotexaminethegutcontentsofthe E. grassei soldier;however,otherapicotermitinegenerawith soldiersexaminedincluding Allognathotermes sp., Coxotermesboukokoensis Grasse andNoirot, Duplidentitermes sp., Heimitermes sp., Jugositermestuberculatus Emerson, Phoxotermescerberus Collins,and Rostrotermescornutus Grasse allpossesstheDGSformandcontainsoliddark particulatesintheirguts. FortheTermitidae,salivarysecretionsfromworkersare thesoleorprimarynutrientsforallimmaturestages(Grasse 1982 ;Noirot 1969 ).Theimmaturestages,whiteincolor,are generallyfoundnearreproductivecentersofthenestforall termitefeedinggroups,includingsoil-feeders(Fig.S5ad) Fig.2 Procubitermes sp. a White-guttedsoldier(WGS)wholegut (insets upperleft ishalfofsoldierentericvalvearmature(EVA), lower left isWGSwithabdominalintegumentremoved,and rightinset isthe contentsoftheWGScrop); b unwoundgutoflastinstarlarva(LIL) ( topinset wholeLIL); c workerwithgutunwound( topinset whole worker; bottominset workerEVA). D diverticulum.SeeFig. 1 for abbreviationdenitions White-guttedsoldiers:simplicationofthedigestivetubeforanon-particulatedietin ƒ 529123

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andwood-feeders(Fig.S5e,f).Casualobservationsofthe gutsofthelastinstarlarvae(LIL,usuallythesecondinstar, Noirot 1969 )andpresoldierstagessampledfromabout120 termitidgenera,bothOldandNewWorld,shownotracesof particulatecontent(Scheffrahn,pers.obs.). AlthoughtrophallaxisandsalivarysecretionsintheWGS havenotbeenstudied,someinferencefromtheDGSgroup maybeusefulinunderstandingthedietcommontoall dependentcastesintheTermitidae.Forexample,using radionuclidetracing,Alibert( 1963 )conrmedthatlarvae andpresoldiersof C.fungifaber Sjo stedtreceivedsalivary secretionsfromworkers,whilematuresoldiersandworkers receivedregurgitatedforegutcontents.StudiesofNew WorldTermitidaeshowthatworkersalivary(labial)gland secretionscontaincomplexaqueousadmixturesofproteins andothernon-volatilecompounds(Sillam-Dusse ` setal. 2012 )whichnourishdependentcastes.Billenetal.( 1989 ) foundthattheworkersalivaryglandsof Macrotermesbellicosus (Smeathman)aresubstantialandconsistofthree secretorycelltypes,whilethesoldierglandhasonlyasingle typethatsecretesadefenseuid(Prestwich 1979 ).However,uponreachingmaturity,theDGSgutsarelledwith darkparticulatematterfromstomodealtrophallaxis(e.g., Figure 3 a).Therefore,theworker-to-larval ? presoldier trophallaxisinDGSandtheworker-to-larval ? presoldier ? soldiertrophallaxisintheWGSisaspecialformof nutrientsharingwithfoodoriginatingfromthesalivary gland(buccaltrophallaxis?)andnotfromtheforegut(stomodealtrophallaxis). Forthersttime,thisstudyintroducestheexternaland internalmorphologyoftheWGSunderlyingtheobservationsofNoirot( 1955 1966 ),NoirotandNoirot-Timothe e ( 1969 ),andGrasse ( 1949 1982 ).Althoughwedidnot analyzetheWGSworkersalivaorguts,thematterfoundin WGSsoldiercrops(Fig. 2 ainset)hastheappearanceofa secretorysubstance.Althoughobviousinbothliveand preservedmaterial,thecolorationoftheWGSisomittedin taxonomicdescriptionsbysomerenownedtaxonomists suchasEmersonAE,KrishnaK,andSandsWA.Wesuspectthattheirfocuswasonthecomplexexternal morphologyofthesoldierheadcapsule,andthattheinternal anatomyofsoldiershadbeensupplantedbythegreater interestinworkerinternalanatomy. Comparedwithotherinsects,thedigestivetubeofhigher termiteworkersismorphologicallycomplex(Noirot 2001 ) andprovidesformultifacetednutrientmetabolism(Bignell 2010 ).Althoughthesoldiergutinalltaxaislargelyoverlooked,thesimilarityoftheDGStoitsworkers(e.g., Fig. 3 c,d)suggestssimilarstructureandfunction.The relativelywell-developedmidgut(M ? MS)inWGS (Figs. 1 c, 2 a,andS4)issimilartoDGSandsuggeststhatits proteolyticfunction(JiandBrune 2005 )isretainedasmightbeexpectedfromasalivarydiet.Thetermitidworkergut hasevolvedtooptimizemicrobialsymbiosis(Brune 2013 ). Insoil-feedingtermites,thegutdigestsparticulateswhich arecomparablynutrientpoorandrecalcitrant.Toaccomplishthis,soil-feedingtermiteshavecompartmentalized physiochemicalgutenvironmentstonurturetheir Fig.3 Cubitermesschereri (Rosen) a Dark-guttedsoldier(DGS); B workerofwithabdominalintegumentremoved.Entericvalvearmatureof c DGS, d worker,and e lastinstarlarva.SeeFig. 1 forabbreviationdenitions 530 R.H.Scheffrahnetal.123

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prokaryoticsymbionts(Brune 2013 ),nodoubtatsome energycost.OneadvantageoftheWGS/LILnutritional schemeoverthatoftheparticulatefeedersmightbeto redirecttheenergydemandslosttosoildigestiontoward defensivefunction(WGS)andgrowth(LIL).Forthis,the matureworkersmustcarryagreatermetabolicburdento feedhigh-energysecretionstotheirwhite-guttednestmates. TheEVAiswelldevelopedinsoil-feedingtermites. Donovan( 2002 )andBignell( 2010 )suggestthattheEVA spinesandcombsfractionategutcontentsbysizetoexpose Fig.4 PhylogenetictreeofTermitidaereproducedfromBourguignon etal.(inpress).Nodepiechartsshowtheprobabilitiesforancestral statestobewhite-guttedanddark-guttedsoldiers.Theancestralstates werereconstructedusingaLikelihoodmodelwithequalrateof transitionbetweenstates White-guttedsoldiers:simplicationofthedigestivetubeforanon-particulatedietin ƒ 531123

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moredigestibleorganicparticlestomicrobialfermentation. Alternately,Scheffrahn( 2013 )arguesthatthesestructures enhancemicrobialinoculationofingestedmaterialbefore entryintotheP3.Ineithercase,theEVAprobablyenhances fermentationofthegutcontentsbeforeenteringtheP3for microbialdigestion.Aswouldbeexpectedfromaliquid diet,theWGSgenerallylackanEVAandtheirP3isrelativelysmall.RemnantsoftheEVAandenlargementofthe hindgutsegmentsinboththeWGSandtheLILof Procubitermes (Fig. 2 a)suggestthattheconversiontoasalivary dietismorerecentinthisgenus.Wehopethatthispaper willstimulatestudiesonthecompositionoffoodand dynamicsoftrophallaxisinalltermites.Acknowledgements WededicatethispaperinhonorofthelateDr. CharlesNoirot,aleadingpioneerofmoderntermitology.Collectionof termitesfromIssa,Ugalla(Tanzania)wasfundedbytheEuropean ResearchCouncil(GrantNo.#283959).Wethankthefollowing institutions,projectsandpeopleforsamplecollectionintheeld:PAN AFRICANPROGRAMME,TaiChimpanzeeProject,MaxPlanck Society,JuanLapuente,AmeliaMeierandJessicaJunker. 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