Viruses and virus-like entities in the parasitic Hymenoptera

15 Pages·1992·6.2 MB·English

by  D B Stoltz

J.HYM.RES.
1(1),1992 pp.125-139
VirusesandVirus-likeEntitiesintheParasiticHymenoptera
DonStoltzandJamesB.Whitfield
(DS)DepartmentofMicrobiologyandImmunology,DalhousieUniversity,Halifax,NS,CanadaB3H4H7;(JBW)Depart-
mentofBiology,UniversityofMissouri,St.Louis,MO,63121-4499,U.S.A.1
amazAibsntgrlayctc.—ompWleexpvraoriveitdyeofhesruechanageonvtesrvisienwowofknvoirwuns.esByanfdarvtihreumsa-ljiokreitaygaernetsnoanf-fpeacttihnoggetnhiec,parreapsliitciactiHngympernimoaprtielryai.ntAhne
femalereproductivetract,fromwhichtheyareoftenifnotinvariablydeliveredintohostinsectsduringoviposition;most,in
fact,wouldappeartobebeneficialtotheparasitoidsinwhichtheyarefound.Emphasisisnecessarilyplacedonthebetter
kDnNoAwnapppoelayrdsnatvoibreuspeesr,mawnheincthlyarienctaergrriaetdedbiyntpoerpharaapssittoeindsgoefntohmoeuss,antdhseroefbbyreancsounriidngantdraincshminsesuimoonntiodalslpepcrioegse.nPyo;liyndkneaevpiirnugs
withthisobservation,these,wherepresent,areknowntoberequiredforsuccessfulparasitism.Relationshipsamongthe
polydnavirusesarediscussedintermsoftheirpossiblerelevancetoparasitoidphylogenyandclassification.
Likeotherinsects,theparasiticHymenoptera scribedbelow,thisvirusappearstoreplicateonly
mustpresumablyfromtimetotimebesubjectto inthefemalereproductivetractand/oritsacces-
infectiousviraldisease.Thereare,tobesure,nu- soryglands;likealloftheagentsdescribedbelow,
merousopportunities.Forexample,virusescould the Mesoleius baculovirus is apparently non-
readilyspreadhorizontallybetweenlarvalcohorts pathogenic(atleastfortheparasitoidhost).
of those species which are either gregarious or The best-known of the parasitoid-associated
polyembryonic.Thehostitselfcouldrepresenta virusesarethepolydnaviruses,whichnowcon-
sourceofinfectiousvirusfordevelopingparasi- stitutearecognizedvirusfamily(Polydnaviridae)
toidlarvae,andpossiblyaswellforadultwasps withinwhich2groupsarerecognized,namelythe
feedinguponhemolymphexudedfromoviposi- bracoviruses and ichnoviruses, which differ in
tionsites.Finally,infectiousdiseaseagentscould terms ofboth morphology and host range; the
betransmittedmechanicallyviacontaminatedovi- polydnaviruseswillbesubsequentlyexaminedin
positorsofhyperparasites.Yet,oddlyenough,vi- considerabledepth,andsoarenotdiscussedfur-
ral diseases in the parasitic Hymenoptera are therhere. Emergingaspotentiallyasecondvirus
seeminglyrare. Reasonsforthisarenotimmedi- familyisagrowingassemblageofentitieshaving
atelyevident.Conceivably,manyparasitoidssuc- asadistinctcommonmorphologyalong,filamen-
cumb to disease prior to emergence from their tous,envelopednucleocapsid. Examplesofthese
ehovsetns;insauclhabeovraetnotrsymsiitguhattioena.sily go undetected, Vviirnussoens1ar9e77kannodwn197f9rao;mSbtoytehrebtraalc.o1n9i8d7;(SHtoaltmzmanedt
al.1990;)andichneumonid(Krell1987)parasitoids;
ASURVEY onehasbeenshown toreplicatein host tissues
(Styeretal.1987). Intermsofnucleocapsidmor-
Infact,weareawareofonlyoneexampleofa phology, the filamentous virusobserved in the
recognized viral pathogen of parasitoids: a re- braconidCotesiacongregata(Say)(StoltzandVinson
centlydescribed baculovirusfromthebraconid, 1977,1979a)verycloselyresemblesafilamentous
Microplitiscroceipes(Cresson)(Hammetal.1988); virusfromthetsetseflyGlossinapallidipesAusten
thusfar,replicationhasbeenobservedonlyinfat (Odindoetal. 1986). Itshould benoted thata
bodytissue.Abaculovirushasalsobeendescribed somewhatsimilarvirushasbeendescribedfrom
from the ichneumonid parasitoid, Mesoleius honeybees(Clark1978;Baileyetal.1981).
tenthredinis(Morley)(Stoltzetal.1981). Likemost A variety of other viruses (again all non-
ofthevirusesandvirus-likeagentsthatarede- pathogenic)havebeenreported fromparasitoid
species(Table1). Stoltzetal.(1988a)describean
U1nCiuvrerresnittyadodfrAersksan(JsBaWs),:FDayeeptatrevtimlelen,tAofKE7n2t7o0m1,olUo.gSy.,A. uenntulsyuraelplviicrautses(idneaslilginnadtievdidCumalVs2o)fcwehritacihnaCoptpeasri-a
126 JournalofHymenopteraResearch
Table1.
Volume1,Number1,1992 127
particles,whichareapparentlyformedwithinan polydnaviruses should be of interest to the
accessoryglandofthewaspovary,areimmuno- hymenopteristc—ommunity.
suppressivewithinhostDrosophila larvae. Spe- Classification. Withregardtovirusesreplicat-
cifically,theLeptopilinaparticlescanbeshownto ing in animal hosts, the great majority maybe
destroylamellocytes,whichareotherwisecapable convenientlyassignedtoaparticularfamilyonthe
ofencapsulatingparasitoideggs(RizkiandRizki basisofthreecriteria: siteofreplication(nucleus
1984). Atthispoint,itisnotknownwhetherthe vs. cytoplasm), morphology, and information
particlescontainnucleicacid,anddetailsofmor- concerningthenatureofthegenome.Inthecaseof
phogenesisareunavailable. Accordingly, these thepolydnaviruses,thelatterhasparticularsig-
particlesarebestreferredtoas"virus-like". Since nificanceasadiagnostictool,sinceitallowsusto
theparticlescanbereadilypurified,itseemslikely readilydistinguishthesevirusesfromallothers.
thatadditionalinformationrelatingtothisfasci- Briefly,encapsidatedpolydnavirusgenomescon-
natingbiologicalsystemwillemergeinthenear sist of a po/i/disperse population of double-
future. strandedcircularDNAmolecules(hence,polydna-
Finally,muchoftheinspirationleadingtothe virus;Stoltzetal.,1984);withinthispopulation,
discovery and characterization of the thereexistatleast20-30classesofmoleculesdif-
polydnaviruses(seebelow)hassurelybeenderived feringintermsofmolecularsize(KrellandStoltz
fromtheearlystudiesofSaltandRotheramonthe 1979,1980,Stoltzetal.1981,Krelletal.1982). As
ichneumonid parasitoid, Venturia canescens will beseen (see: LifeCycle,below), therealso
(Gravenhorst) and its host Anagasta kuhniella exists a linear, chromosomal, copy of the
(Zeller);fordetails,thereadershouldconsultre- polydnavirusgenome. Intermsofmorphology,
viewsbySalt(1968,1970).Briefly,Rotheram(1967) the polydnaviruses comprise two quite distinct
identifiedaparticulatesecretioncomprisedlargely groups, the so-called bracoviruses and
ofvirus-likeparticlesproduced in thenucleiof ichnoviruses;asthenamessuggest,thesearefound,
cells found in the calyx, a region ofthe ovary respectively,incertainbraconidandichneumonid
situatedbetweentheovariolesandtheoviducts. waspsonly. Bracovirusparticlesconsistofcylin-
Salt(1968,1970),andmorerecently,Feddersenand dricalnucleocapsids,ofvariablelength,surrounded
Schmidt(1986),showedthat"calyxfluid"conferred eitherindividuallyoringroupsbyasingleunit
resistanceonparasitoideggstohostimmunere- membrane;ichnovirusparticlesconsistoffusiform
sponses. Ithas now been determined that the nucleocapsidssurroundedbytwounitmembrane
virus-likeparticlesshareantigenicdeterminants envelopes(StoltzandVinson1979a). Typicalex-
withoneormorehost proteins (Feddersenand amplesaregiveninFigure1. Bracovirusstructure
Schmidt1986),suggestingthattheparasitoidegg clearlyresemblesthatofthebaculoviruses,atleast
surface(whichiscoatedwithparticles:Rotheram in some respects (Stoltz and Vinson 1979a);
1973)isrecognizedasself,henceevadingsurveil- ichnovirusparticlesonlysuperficiallyresemblea
lancebythehostimmunesystem. Despitetheir numberoflargeviruseshavinglenticularnucleo-
toariingiDnNinAcel(lFenudcdleeris,eVnenatnudriaScphamrtiidctles19d86o).noAtcroena-- c1a97p8s;idFsed(ee.rgi.ciAv1—e98r3y).etal.1977;StoltzandFaulkner
sonable working hypothesis might posit that Distribution. Preliminarylistsofspeciescar-
Venturia carriesa "defective" polydnavirus, the ryingpolydnaviruseshavebeenprovidedbyStoltz
genome of which resides within the parasitoid andVinson(1979a)andStoltzetal.(1981);more
genome,butfailstobecomepackagedintovirus recentcompilationsaregivenbyKrell(1991)andin
particles. Table2. AmongtheBraconidae,polydnaviruses
areknownfromthreesubfamilies: Cheloninae,
THEPOLYDNAVIRUSES Microgastrinae,andCardiochilinae. Withinthe
samelineageareincludedseveralothersubfami-
Inwhatfollows,weprovideabriefoverviewof lies (Miracinae, Khoikhoiinae, Adeliinae and
whatiscurrentlyknownaboutthepolydnaviruses. probablyalsoNeoneurinae;seeFig.2),someorall
Insodoing,wewillhighlightthosefeatureswhich ofwhichmightreasonablybepredictedtocarry
distinguishthisgroupfromwhatmaybereferred polydnaviruses. Ichnoviruseshavebeen,thusfar,
toas"typical"viruses.Finally,considerableem- detectedprimarilyintheCampopleginae. How-
phasis will be placed on the question of why ever,isolatesfromGlyptaspp.(Stoltzetal.1981,
128 JournalofHymenopteraResearch
kbp
10
6
Fig.1.Typicalexamplesofpolydnavirusparticlesandencapsidatedgenomes.Belowleftisshownanelectronmicrographof
agDreebNlprreAaelcseoiecsvntiptrrrodeupisshfeo(fnrefterrteioinnmctePpparrocoophtfuailpllaaeannsteti.oeoflLneeDssfNtpo,aAflbseiranactecraxioctttvraiae(ri)c.utea.se,nddDu,fnNrdtAioogmtefhcsreatolremiydgx)Mhitfcc,liruaoripncdlusiiltacairhrsenDocsrvNeoiecArenuispmaefo(stl;feerrrcoieugmlthehtHs,iy.dpioicSsuhiomnztoeebvrrmieoraxmurisigkudeDaereNs)s.At(aiiAnfnbrkiooinglmv;oeHba.atpshpreeirsvopeaaxl,ii.s0r.s.1)8Tu%ahgreaeogfbgaavirinvordesasnel
forthesuperhelica!formsofviralgenomesegments.Experiencethusfarsuggeststhatbracovirusgenomesegmentstypically
exhibitarelaxedopencirculartopology,andareforthemostpartlargerthan10kb. Ichnovirusgenomesegmentsareoften
smaller(e.g.,2-10kbinthegenusHyptosoter);superhelicalformstendtopredominate,especiallywhenDNAshavebeen
extractedfrompurifiedvirusparticles.
Volume1,Number1,1992 129
Table2.Parasitoidspeciesinwhichpolydnaviruseshavebeenfound.Forreferences,consultStoltzandVinson(1979a),Stoltz
etal.(1981),andKrell(1991).Ichnoviruseswerenot,priortothepresentreport,knownfromeitherDusona,LissonotaorSynetaeris.
A/1,demolitorisalsoanewlisting(seeStrandandDover1991).
BRACONIDAE Microplitiscroceipes(Cresson)
ChelACAosshncceooilggnoaanassuettseerrblaqarucgakedbnrutiridnfeirnotCnasatma(ePWrreoosvnmanacehler) ICHMPPiNhrcooErltoeaUptpleMaisnOtotireNsloIedrsenDimpAgoaillEsieta(coWrrietWeaidel)k(Riinlseoy)n
ChelonusaltitudinisViereck
Chelonusnr.curvimaculatusCameron Banchinae
ChelonusinsularisCresson Glyptafumiferanae
PhanerotomaflavitestaceaFischer Glyptasp.
Catnpoletissonorensis(Cameron) Lissonotasp
Cardiochilinae Campopleginae
CardiochilesnigricepsViereck Catnpoletisaprilis(Viereck)
Catnpoletisflavicincta(Ashmead)
MicrCCCACACooooooppgtttttaaaeeeeennssssssttiiiiiteeaaaaallreeifgkhcsslnaloyaraonpfcvimeghuriyeraapmarenseiigtassfiartWe(ctiaraoCaaatr(eann(aLmaiS(ineseRanariy(Vnbl)oiaPeeneery)ruo)sev)cakncher) CCCCDDDEaaaariiusssimaasiiibpddonnnooeenaaarlggrrraueiiismmtaaasaaiptsfsi.eaiopnrcsnrf.eprtceb.oeisrtrpnaaaryntucs(aptCta(WriGaeo(rnslAasls(voeehHnynmo)hleomargdsr)te)n)
CCCooottteeesssiiiaaammreualbraegcniuonlsiacvee(lnMatan(rsRsah(atClzrlee)bsusrogn)) HHiy/ppoossootteerraenxniugluaiepe(sVi(eCrreecsks)on)
CMDGGGHoiilllytoyyycpelppprosctttomioaaagiagpppacaaaassrsnnntcottttehgeeeeraarllleseeecfftsssaaeecnrfileraliintdap(doeevaiMscnireaadicsnrydois(sitxsishWioss)leM(o(eu(BpMdMoeha)ausarrceeshsb(heheM)))cueksebeck) HHHOOSTyyylylrnppepeaeoososntssisioaoococseatttaermeeemimprrrpsaeeflrtsuiygbepgvemen.ainnalutieniiifcstfvaureu(clismtCaauotre(rraeSe(saH(sCyQWio)uaunnlsze)lhdemyna)anu)&Lim
andunpublisheddata)areknown;thisgenusis AlysiaandAleiodesareendoparasitic,theyappear
includedinadifferenttaxon: Banchinae(Gauld to comprise a lineage independent from the
1984;Wahl1988). Thetwosubfamiliesarefairly microgastrinecomplexofsubfamilies(Tobias1967;
closelyrelated,sothatsurveysofadditionalrelated Capek1970;Shaw1983;Gauld1988;Gauldand
subfamilies (Figure 3) for the presence of Bolton 1988; Quicke and van Achterberg 1990;
polydnaviruseswouldpresumablybeworthwhile. Whitfieldinpress).Amongtheichneumonidtaxa,
—idnigf:fPeerarecelnhitmp"iaonflafyredycntaoevbdsi"errupvasartcahisaoirntasocitsdeurgsigpseetsciitceostfhectahrfarotilelssopwea-- poanfugocalslLiyuiendbfafenrlaa,iCmtvytiacilllnerieduei.sss—a.kcpPanproeorlaiwyarndgsnec,atoovinifbcraeeunrsyln,irimewnipigtlteihtdcihatentoiitothnnheceiimsdoaesvjtnaorcrireciitatolnyyf
—pcioelsiy.fdonnaevisrpuesc,ietshweiytahlilnaarepalrikteilcyultao.rgenuscarries cRaaenlpdylxiVcioafntsicooernntba1ei9gn8i3sn;pseTcdhiueerisilnomfgaptnahnreaaspniutdpiacSluHsymtmmaegenero(spNto1e9r8rt6ao).n,
Needlesstosay,mostgroupsofparasiticHy- and has longbeen assumed tobe triggered by
menoptera have not yet been examined in any hormonalchangesoccurringduringmorphogen-
systematicwayforthepresenceofpolydnaviruses. esisoftheovary;morerecently,viralreplicationin
Incidentalobservations,however,suggestthatthese explantedCampoletissonorensis(Cameron)ovaries
virusesarenotpresentinAlysia(Alysiinae),Bracon hasbeenshowntobeinducedbyecdysone(Webb
(Braconinae), or Aleiodes (Rogadinae) in the andSummersinpress). Asidefromthisobserva-
Braconidae(Stoltz,unpublished). Althoughboth tion,themoleculardetailsofviralreplicationremain
130 JournalofHymenopteraResearch
CHELONINAE
ADELIINAE
NEONEURINAE
CARDIOCHILINAE
KHOIKHOIINAE
MIRACINAE
{. MICROGASTRINAE
Polydnaviruses known
Fig.2.PhylogenetichypothesisforthesubfamiliesofBraconidaethatcarrypolydnaviruses.AdaptedfromAustin(1990);based
alsoondatafromMason(1983).ThereisnogeneralagreementthattheIchneutinaealsobelonginthiscomplex(see,e.g.,Quicke
andvanAchterberg1990),butthepossibilityexists.
CTENOPELMATINAE
BANCHINAE
TERSILOCHINAE
CREMASTINAE
CAMPOPLEGINAE
t
OPHIONINAE
Polydnaviruses known
Fig.3.PhylogenetichypothesisforthesubfamiliesofIchneumonidaethatcarrypolydnaviruses. AdaptedfromGauld(1985);
theAnomaloninaeprobablyalsobelonghere(Wahl1988).
obscure. Followingreplication,matureparticles 1)polydnavirusreplicationoccursintheovaries
enterthelumenofthereproductivetractwhere of all females of all affected species, and 2)
theycomprise,asseenpreviouslywithVenturia,a polydnavirusesare"designed"forexport(i.e.,to
so-called"calyxfluid".Theoviducts,then,contain theparasitizedhost). Eachoftheseobservations
botheggsandvirus;itshouldthereforecomeasno hasfar-reachingimplications. Thefirstindicates
surprisetolearnthatbothareinjectedintohost thatpolydnavirustransmissionwithinparasitoid
animalsduringoviposition(StoltzandVinson1977, populations occurs with 100% efficiency, sug-
1979b). Extensive electron microscopic studies gestingfurtherthatpolydnavirusesmusthavean
carriedoutinthemidtolate1970sestablishedthat: importantroletoplayintheparasitoidlifecycle.
Volume1,Number1,1992 131
Thesecondobservationsuggeststhatafunctional demonstratedthatpolydnavirusparticlesarein
roleforpolydnavirusparticlesshouldbesought most cases absolutely required for successful
intWheehmoasty.thinkofpolydnavirus"transmission", Gpaurzaositainsdm(StEodlstozn1e9t87al)..19T8h1e;rSteolitszgaonoddGuevziode1n9c8e6,;
and indeed thepolydnaviruslifecycleitself,as albeitcircumstantial,thattranscriptionalactivity
ocnoens,isptoilnygdonfavtiwrouspaDthNwAayiss(tSrtoalntszmiitntperdesws)i.thiInn aisnadlsSotoaltrzeq19u8i7r)e.meAnsty(eStt,onltozbainodloGgiuczaola1c9t8i6v;itGyuhzaos
parasitoidpopulations;intheother,polydnavirus beenassociatedwithanypolydnavirusgeneprod-
particlesaretransmittedtohostinsectsduringovi- uct;however,thatissurelyonlyamatteroftime.
position,theconsequencesofwhichwillbedis- Sincepolydnavirusesaregenerallyimmunosup-
cussedbelow.Thesetwopathwaysareconsidered pressiveinhostinsects(Edsonetal. 1981;Stoltz
hereintheordergiven,recognizinghoweverthat andGuzo1986;GuzoandStoltz1987),itcanrea-
theyaremutuallyinterdependent. Withinpara- sonablybeassumedthathostdefensesrepresenta
sitoidpopulations,polydnavirusesaretransmitted primaryandperhapscontinuingtargetforvirus-
geneticallyintheformofproviruses. Thiscon- specificgeneexpression. Inaddition,itmaybe
clusionisbasedupontwolinesofevidence. First, assumedthatpolydnavirusesmayexertprofound
geneticcrossingexperimentshaveclearlydemon- effectsonotheraspectsofhostphysiology,soasto
stratedthatbothichnovirusandbracovirusgenome makethatmorecompatiblewiththeneedsofde-
segmentsaretransmitted to parasitoid progeny velopingparasitoideggsand/orlarvae. Inkeep-
Saceccoornddilnyg,tolisniemaprleDMNenAdelsieaqnuernulceess(Sctoogltnzat19e90)t.o vianrgiweittyhotfhbiisoalsosgiucmaplteivoenn,twsehanovteentohawtbaebeenwialsdcerriibnedg
polydnavirus genome segments are covalently totheactivity(directorindirect)ofpolydnaviruses;
linkedtoparasitoidchromosomalDNA;this,too, thesearelistedinTable3,andhavebeendescribed
hasbeenshownforbothichnoviruses(Fleming elsewhereinsomedetail(Stoltzinpress).
andSummers1986,1991;XuandStoltz1991)and Beingimmunosuppressive,thepolydnaviruses
abracovirus(Stoltzetal.unpublisheddata).Itnow mayprovideparticularlyusefultoolswithwhich
seemsreasonabletoassumethatthelinear,chro- to examine the nature of invertebrate immune
mosomal,copiesofpolydnavirusgenomesegments responses, a subject which has in recent years
cmiarcyulsaerrDveNaAsstwehmipclahtuelstifmoarttehleybreepcloimcaetipoanckoafgtehde srieocneiavpepdeairnscrteoasbiengduaet,teanttlieoans.tinImpamrutn,otsoucphparnegse-s
intovirusparticles(Stoltz1990;FlemingandSum- inhemocytenumber,behaviour,and/orviability
mers1991;XuandStoltz1991). (StoltzandGuzo1986;Daviesetal.1987;Guzoand
Asmentioned previously, polydnavirus par- Stoltz1987;WagoandTanaka1989),butthemo-
ticles aredesigned fordelivery intoparasitized lecularbasisfortheseeffectsremainstobeeluci-
iDnNseActse;sthaebrlei,shtehsewchiartcualamroufnotrsmtoofapgoelnyedtniacvciorluos- dsiamtielda.rmIenchadadniitsiomns,oipterisatneottoypertotcelcetarbowthhetehgegrs
nizationofthehostanimal. Comprisingthissec- and larvae. In one study, the restoration ofan
ond arm of the polydnavirus life cycle are the immuneresponseagainstyeastcellshadnoap-
followingelements:rapidentryofvirionsintoa parenteffectondevelopingparasitoidlarvae(Stoltz
varietyofhosttissues(StoltzandVinson1979a), andGuzo1986);again,thebasisforanapparently
uncoatingofviralnucleicacideitheratorwithin selectiveimmunosuppressioninsuchsystemsis
cellnuclei(StoltzandVinson1979a),persistenceof notunderstood. Itisofcoursequitepossiblethat
viralgenomesegmentsthroughouttheentirecourse insomesystemsthelarvalsurfaceisnotseenas
ofparasitoiddevelopment(TheilmannandSum- foreign,whiletheeggis(orviceversa).Inanycase,
mers 1986;Stoltzetal. 1986),and virus-specific itisclearthataninvestigationofhost/parasitoid
transcription(Flemingetal. 1983; Blissardetal. interactionsatthecell/molecularlevelcanbeex-
1986a,1986b,TheilmannandSummers1988;Stoltz pected toshed newlightonsomefundamental
etal.1988b),allintheabsenceofviralreplication. entomologi—calquestions.
Theultimatepurposeoftheseactivities,presum- Origins. Wheredidthepolydnavirusescome
ably,istoensuresuccessfulparasitism. Thiscon- from?Atpresent,onecanonlyspeculate.Thereare
clusionhasbeendrawnfromconsiderableexperi- twoprincipalpossibilities:1)theyarosefromthe
mentation,theresultsofwhichhaveconclusively parasitoidgenomeitselfor,2)theyoriginallyex-
132 JournalofHymenopteraResearch
Table3. Physiologicalchangesinhostanimalsattributedtothepresenceofpolydnavirusesandvirus-likeagents(modified
fromStoltz(inpress)).
Activity References
Suppressionofcellularimmuneresponse Salt1970(VLP);Vinson1977;Edsonetal.1981(V);RizkiandRizki
1984and1990(VLP);GuzoandStoltz1985,1987;StoltzandGuzo
1986(V);Vinson,Stoltz1986(V);FeddersenandSchmidt1986
(VLP);Tanaka1987;StrandandWong1991(V).
Inhibitionofweightgain Vinsonetal.1979(V).
Changesinhemocytecountorbehaviour RizkiandRizki1984,1990(VLP);StoltzandGuzo1986;Guzoand
Stoltz1987;Tanaka1987;Daviesetal.1987(V);WagoandTanaka
1989;StrandandWong1991(V);StoltzandBeckage(V;unpublished
data).
Appearanceofnewhemolymphpolypeptides Cooketal.1984(V);Beckageetal.1987.
Inhibitionofphenoloxidaseactivity StoltzandCook1983(V);Beckageetal.1990(V).
Inhibitionofproteinstorageinfatbody Tanaka1986.
Reductioninhemolymphviscosity Daviesetal.1987(V);Stoltz(unpublisheddata).
Changeinhemolymphtrehaloseconcentration DahlmanandVinson1977.
Degenerationofhemopoietictissue GuzoandStoltz1987.
Pigmentationchanges Beckageetal.1990(V).
Degenerationoftheprothoracicgland Doveretal.1988a(V).
Prolongationand/orarrestofdevelopment Tanaka1987;Doveretal.1988b(V);TanakaandVinson1991a;
StrandandDover1991(V).
Perturbationofhormonelevels Doveretal.1987,1988(V);TanakaandVinson1991b.
V=gradient-purifiedpolydnavirusused(otherwise,calyxfluid).VLP=virus-likeparticle. Itshouldbenotedthatvenomis
requiredforfullactivityofsomebraconidpolydnaviruses(e.g.Kitano1982;Stoltzetal.1988b).
istedastypicalviruses1(Whitfield1990).Whilethere thatsucharelationshipapparentlyexistsbetween
isnoeasywaytoassesstherelativemeritsofthese a baculovirus and the ichneumonid parasitoid,
scenarios,thelatterisperhapsmoresatisfyingfor Mesoleius tenthredinis (Stoltz 1981); as with the
anumberofreasons. First,therearestrikingpar- bracoviruses,allfemalesthusfarexaminedappear
allelsbetweenbracovirusesandthewell-known tocarryvirus, and replication isapparentlyre-
insectbaculoviruses. Forexample,thediameter strictedtotheparasitoidovary.Furthercharacter-
and overall appearanceofthecapsid is similar izationofthisinterestingsystemshouldbegiven
(StoltzandVinson1979a);inbothcases,theenve- highpriority. Finally,defectiveinterfering(DI)
lopemaysurroundnucleocapsidseitherindividu- formsofbaculoviruseshaverecentlybeendiscov-
allyorin groups; in addition, somebracovirus ered(Kooletal.1991;Krell,pers.commun.). DI
nucleocapsids are fully as long as baculovirus particlescontainsub-genomicnucleicacid mol-
nucleocapsids(Stoltzetal.1976);finally,uncoating ecules, and havebeen known toamelioratethe
ofbothbracovirusandgranulosisvirusnucleocap- severity ofviral disease (Dimmock and Barrett
sidsoccursatnuclearpores(Summers1969;Stoltz 1986). Conceivably, non-pathogenic bracovirus
andVinson 1979b). Whilethesemayrepresent
arereexnlaadasmtopitnolhaneebsslhpeiaoprftaaorscoiosstneuovipbdeperotgrsweeeepnertntohdaeauvtpcortlsoiugotvemienoeintt,rosaorcirtbtt,aicoasufnljdousvstitatrbhuaalstse (fp'otForholruwysdhtnhigaeecvnhpieurtrrhuaepstroeiessn,geexipohsfrtootwhgheoiesvsntedysri,ssvucisuracsulelsspiptohainorb,stltitecsyltpeoipsc)epa.rrlmoIidvnuisrcstutihsiveevesceaafisroneerfeotcfvhtiotirshoaeenl
somesuchrelationshipultimatelygaverisetothe replication already carry the viral genome, that being
bracoviruses.Inthisregard,itisofinteresttonote transmittedasaprovirus.
Volume1,Number1,1992 133
genomescouldhaveevolvedfromdefectiveinter- Summers1990). —
feriTnhgebabcraucloovviirruussepsaratnicdleisc.hnoviruseshavebeen thatImppollicyadtniaovnsirfuosrDPaNraAsitisoiadppSayrsteenmtaltyictsr.ansmGiitvteend
assigned to the same virus family because of inastableMendelianfashion,itcannotlogicallybe
similaritiesinbothgenomeorganizationandlife regardedasdifferinginanysignificantwayfrom
cycle.Itshouldbestressed,however,thatthisdoes parasitoidgenomicDNA.Putmoredirectly,when
not mean that the family is necessarily mono- weexaminepolydnavirusDNA,wearealsoexam-
phyletic.Ifmonophyletic,thenthepolydnaviruses iningparasitoidDNA.Itfollowsthatrelationships
musthavearisenfromacommonancestor,which amongthepolydnavirusesshouldparallelthose
couldhavebeeneitheravirusoranappropriate amongtheparasitoidswithwhichtheyareassoci-
collection ofparasitoid genes. This hypothesis ated. Itmaythusbeinstructivetoconsiderwhat
doesnot,however,readilyaccountforthemajor littleisknownatpresentaboutpolydnavirusrela-
structural differences which define the two tionshipsinthecontextofparasitoidsystematics.
polydnavirussubgroups(seeFig.1).Alternatively, Itisofinterestinthisregardtonoteanapparent
thebraco-andichnovirusescouldhavearisenfrom congruenceofclassicaltaxonomicdeterminations
entirelydifferenttypesofviruses,withextantsimi- withtheresultsofpreviouselectronmicroscopic
larities resulting from convergentevolution. It studies. Earlyworkclearlyestablishedtheexist-
couldbearguedthat,forthelattertohaveoccurred, enceoftwobracovirusmorphotypes,distinguished
theovaryshouldbeafavouredsitefornon-cyto- onthebasisofwhetheroneorseveralnucleocap-
pathicvirusreplication;infact,aswehaveseen sidswereenclosedwithintheviralenvelope(see
(Table1),thiswouldcertainlyappeartobethecase. Figure1). Withinmembersofthe(former)genus
Theestablishmentofavarietyofnon-pathogenic Apanteles,thesetwomorphotypeswererepresen—ted
viralagentsintheparasitoidovarycouldthenbe in roughl—y equivalent numbers, suggesting in
seenasaprerequisitefortheoriginofancestral hindsight thatthegenuscouldwellbepolyphyl-
polydnavirus/parasitoid complexes. Variations etic,orthatatleastonebiologicallyrelevantdivi-
onthisthememightalsohavegivenrisetothe sionmightbefoundwithinthegenus. InTable4,
Venturia and Leptopilina particles,amongothers informationonbracovirusmorphologyispresented
waitingtobedescribed. in relation to Mason's (1981) reclassification of
The polydnavirus/parasitoid relationship is Apanteles. Interestingly,thosegenerawhichMa-
undoubtedlyancient,atleastintermsoforigin(s). sonassignedtothetribeCotesiiniareforthemost
Thus it is reasonable to assumethat during its part characterized by polydnaviruses in which
establishment,opportunitiesmusthaveexistedfor nucleocapsidsarenotindividuallyenveloped;of5
genetictransferbetweenviralandhostgenomesas suchgeneraforwhichdataarepresentlyavailable,
(wesuppose)theyco-evolvedtobecomeasingle onlyone(Diolcogaster)seemsoutofplace: unlike
genome. Indeed,itcouldgenerallybearguedthat allotherCotesiinithusfarexamined,polydnavirus
theestablishmentofageneticfusionbetweentwo nucleocapsidsinDiolcogasterareindividuallyen-
originallyseparateentities(e.g.,mitochondriaand veloped. Itmight,accordingly,besuggestedthat
eukaryotes)mightrequirethatsomefunctionsbe thetaxonomicpositionofDiolcogastercouldprof-
transferredfromonetotheother,andviceversa. itablybereconsidered. Alternatively,absenceof
Onemightpredict,forexample,thatsomegenes anindividualenvelopeforeachviralnucleocapsid
requiredforviralmorphogenesismighthavelost might represent a synapomorphy for a lineage
encapsidation signals: since morphogenesis oc- somewhat lessinclusivethantheCotesiini asa
cursonlyinthewaspovary,therewouldbeno whole.
pointinpackagingsuchgenesforexpressioninthe Additionalinformationmayin futurebede-
parasitizedhost. Similarly,parasitoidgenespro- rivedfromanalysesofviralDNA.Forphylogenetic
motingsuccessfulparasitismmightmoreusefully inference,suchstudiesshouldideallyincorporate
havebecomeincorporatedintotheviralgenome, ananalysisofsequencedatafrombothwaspsand
tobesubsequentlydeliveredtoparasitizedinsects. viruses(seebelow). Thusfar,ourstudieshave
Itisofconsiderableinterestinthisregardtonote been limited to the identification ofshared (or
thattheichnovirus,CsV,isthoughttohaveacquired greatlysimilar)genomesegmentsbetweenwasp
a parasitoid venom gland gene, which is duly taxa, using nucleic acid hybridization/blotting
expressedinparasitized hostlarvae(Webband techniques.Thisapproachcanprovidesomeindi-
134 JournalofHymenopteraResearch
cation of which taxa share genetically similar carriedbythesetwoparasitoidspecies. Itisthere-
polydnaviruses, although thedata obtained are fore reasonable to assume that their cognate
not directly useful for phylogenetic studiesbe- polydnaviruseslikelyengagethesamehostmilieu
causenodistinctioncanbemadebetweenances- inratherdifferentways. Conversely,wheretwo
tralandderivedsimilarities. Someobservations virusesshowsignificantsequencehomology,we
arealreadyavailable(Figures4and5);theseare mightreasonablypredictthatsharedgeneprod-
providedheremerelyaspreliminaryindicationof uctsareinteractingwithcommonhosttargets. In
arupsorsesliabtlieoncsohrirpse.spIonndFeignucreeb4e,tpwoeleyndnwaavsirpuasnDdNvAi- athneyDcaNseA,isttwuidlilebsesoofacsotnosiindcelruadbeleadidntietrieosntatlogeexnteernad;
circles(i.e.,genomesegments)fromavarietyof incombination with analysesofwaspmorpho-
bsreapacroantieddpaarnadsitthoeindpsrhoabveedbweietnhe3l2ePc-tlraobpehlorleetdiDcaNllAy ltohgeircraelfainndemmeonlteocfumliacrrodgataas,trtihnisecmlaasysipfeicramtiiton.aTfuhre-
fromCotesiamelanoscela.Hybridizationsignalswere developmentofnewdatainatimelyfashioncould
detectedonlywithinmembersofthesamegenus; prove particularly useful for this group, since
nohybridizationsignalwasdetectedeveninthe Mason's(1981) workonthisgroupiscurrently
caseofGlyptapanteles,which,accordingtoMason undergoingreappraisal(Walkeretal.1990;Mason
(1981),belongstothesametribeasCotesia. Our andWhitfieldinpreparation).
results,asfarastheygo,arethereforeentirelyin Preliminary studies involving ichneumonid
accordwithMason'sgenericdivisionofApanteles. polydnaviruses(ichnoviruses)areequallyinter-
Parenthetically,itshouldbenotedthatwhileboth esting,whileneverthelesssomewhatmoredifficult
C.melanoscelaandG.flavicoxis(Marsh)aregypsy tointerpretbecauseofuncertaintiesinthecurrent
mothparasitoids,theirrespectivepolydnaviruses genericclassification(see,e.g.,discussionbyWahl
arequitedissimilar;thusthereisnoindicationthat 1987).Evenso,someinferencesmayreasonablybe
host-sharinginfluencestheidentityoftheviruses drawnfromalreadyavailable,iflimited,data:for
A B
bFriergsa.pce4o.cntDiidvNeAlgye,hneoormfao.vliorAgaliaeDnsNdaAmBsorneegxptrpreoaslcetynedtdnagfevrlioramunscdeaslSyfoxruoftmlhuediridfnsfefbrlreoontmt, dSFiiogfu.ftehr5ee.nrtnDiNbclAohtn,ehuroemmsoopnleicotdgiivgeeeslnye,aramo.fonvAigraalpnodDlyNBdAnrsaevpierrxeutsrseaencsttegfderlofamrnodm5
thefollowing:Cotesiamelanoscela,C.marginiventris.Microplitis calyxfluidsofthefollowing: Campoletissp.,Diadegmasp.,
croceipes,andCardiochilesnigriceps(lanes1to4,respectively). Hyposoter fugitivus, H. annulipes, H. lymantriae, Diadegma
TSstDhrSei)nbgulesonitcnygw(a26.s58°xpCr1,o005b.e5cdpMmo/Nvmae-lrp.nhioogfshp"tPh-aultnaedb,eelrplHecdo7n.w2dh,iotclioeonntvsaiirnaolifnDghNi7gA%h tEtehxrepeebprrraionmsbe,enatunasdleOdcloehnsediricetaiwmopanessge,w2nPei-crluealbaaetslalegeid(vleHann.efsiun1gFititogi7.v,u4rs,eswephxeocceltpietvevltiyhr)aa.lt
fromC.melanoscela. Exposurewasfor24hrs DNA.