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Sperm morphology of Trichospilus diatraeae and Palmistichus elaeisi (Hymenoptera: Chalcidoidea: Eulophidae).

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ContentslistsavailableatScienceDirect

Micron

jo u rn al h om ep a g e :w w w . e l s e v i e r . c o m / l o c a t e / m i c r o n

Sperm

morphology

of

Trichospilus

diatraeae

and

Palmistichus

elaeisis

(Hymenoptera:

Chalcidoidea:

Eulophidae)

Helen

Pinto

Santos

a

,

Uyra

Zama

b

,

Heide

Dolder

c

,

José

Lino-Neto

a,∗

aDepartamentodeBiologiaGeral,UniversidadeFederaldeVic¸osa-UFV,MinasGerais,Brazil bDepartamentodeCiênciasBiológicas,UniversidadeFederaldeOuroPreto-UFOP,MinasGerais,Brazil cDepartamentodeBiologiaCelular,UniversidadeEstadualdeCampinas-UNICAMP,SãoPaulo,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received12December2012 Receivedinrevisedform12June2013 Accepted15June2013 Keywords: Spiraledsperm Ultrastructure Parasitoid Insect

a

b

s

t

r

a

c

t

Inthisstudy,thespermmorphologyoftheparasitoidsTrichospilusdiatraeaeandPalmistichuselaeisis (Eulophidae)wasinvestigatedusinglightandtransmissionelectronmicroscopy.Inthetwospecies,the spermarespiralalongtheirentirelengthandmeasureabout130␮mand195␮minlength,respectively. Theheadregionconsistsoftheacrosomeandnucleus.Theacrosomeiscomposedofanacrosomalvesicle and,inP.elaeisis,aperforatorium.Inbothspecies,anextracellularlayerinwhichseveralfilamentsare radiatedcoverstheacrosomeandtheanteriornuclearregion.Thenucleiarefilledwithhomogeneous andcompactchromatinandmeasureabout50␮minlengthinP.elaeisisand20␮minT.diatraeae.The flagellumconsistsofanaxonemewiththe9+9+2microtubulearrangementspiraledinalonghelix, twomitochondrialderivativescoilingaroundtheaxonemeand,inP.elaeisis,twoaccessorybodies.InT. diatraeaewereobservedtransversestriationsthroughoutthecentralregionoftheaxoneme,whereasthe centralpairofmicrotubuleswasrarelyobserved.InthefinalflagellarregioninT.diatraeae,differentfrom P.elaeisis,onemitochondrialderivativeendswellbeforetheotherandbothendbeforetheaxoneme. Thespermofthesetwospeciesexhibitfeaturesthatdiscriminateonespeciesfromeachother,aswellas characteristicssuggestthatEulophidaeiscloselyrelatedtoTrichogrammatidaeandbothofthesefamilies aremoresimilartoEurytomidaethanAgaonidae.

©2013ElsevierLtd.Allrightsreserved.

1. Introduction

The Chalcidoidea comprise up to a third of parasitic

Hymenopteraspecies(LaSalleand Gauld,1991), formingoneof

themostabundantgroupsofinsects(GrisselandSchauff,1997).

Although some Chalcidoidea are phytophagous or

hyperpara-sitoids, most are parasitoids of other arthropods, thus playing

animportantroleincontrollingthepopulationsofotherinsects.

Therefore,chalcidoidshavebeensuccessfullyusedinmost

biologi-calpestcontrolprograms(Greathead,1986;Neumannetal.,2010;

Polaszeketal.,2012).

Despitetheeconomicandecologicalimportanceofthisgroup

ofinsects,knowledgeofevolutionaryrelationshipsamong

Chal-cidoidearemainsunclear,withisnoconsensusontheplacement

ofseveralfamilies(Heratyetal.,1997;Munroetal.,2011).

There-fore,cleardefinitionsoffamiliesbasedoncharactersthatcanbe

usedincladisticanalysesarenecessary(GrisselandSchauff,1997).

∗ Correspondingauthorat:DepartamentodeBiologiaGeral,UniversidadeFederal deVic¸osa-UFV,Vic¸osa,MinasGerais,CEP36570-000,Brazil.Tel.:+553138993367; fax:+553138992549.

E-mailaddress:linoneto@ufv.br(J.Lino-Neto).

AuthorslikeHeratyetal.(1997,2012)drewattentiontotheuseof

newclassificationsystemstoclarifyrelationshipsbetweenfamilies

andsubfamiliesofChalcidoidea.

Inmanyanimalgroups,includinginsects,spermmorphological

datahavebeencommonlyusedinphylogeneticanalysis(Carcupino

etal.,1995;DallaiandAfzelius,1995;Dallaietal.,2011;Gottardo etal.,2012;Jamieson,1987).Inthis regard,earlierstudieshave

demonstratedthatthestructuraldiversityofspermatozoain

Chal-cidoideacanprovideasystemofcharacters,whichmaybeusedin

combinationwithotherstostudyphylogeneticrelationshipsofthe

groupandresolveuncertaintyatthefamilyandgenuslevels.

Inthispaperwedescribethespermstructureandultrastructure

ofthe parasitoidsTrichospilus diatraeaeand Palmistichuselaeisis

(Chalcidoidea: Eulophidae) to provide spermatological data for

futurephylogeneticanalysesofthisinsectgroup.

2. Materialsandmethods

Adultmale T.diatraeaeandP.elaeisiswerepurchasedinthe

departmentofentomologyattheEscolaSuperiordeAgricultura

LuizQueiroz–ESALQ/USP.

0968-4328/$–seefrontmatter©2013ElsevierLtd.Allrightsreserved. http://dx.doi.org/10.1016/j.micron.2013.06.006

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2.1. Lightmicroscopy

Seminalvesiclesweredissectedandsquashedoncleanglass

microscope slides, followed by spreading, then fixed with 4%

paraformaldehydein0.1Mphosphatebuffer,pH7.2.Afterdrying

atroomtemperature,theslideswereobservedwithanOlympus

BX41 photomicroscopeequippedwith a phase contrastlens to

allowmeasurementofthesperm.Fornucleimeasurements,some

slideswerestainedfor 15minwith0.2␮g/mlof

4,6-diamino-2-phenilidole(DAPI) and viewedwitha epifluorescenceOlympus

BX60microscopeequippedwithaBP360-370nmexcitationfilter.

TheimageswereanalyzedusingtheImagePro-Plusprogram.

2.2. Transmissionelectronmicroscopy

Seminal vesicles were dissected in 0.1M sodiumcacodylate

buffer,pH7.2andfixedina2.5%glutaraldehydeand0.2%picric

acidsolutionwiththesamebuffer,for24hat4◦C.Thematerial

waspost-fixedin1%osmiumtetroxidesolutioninthesamebuffer.

ThematerialwasdehydratedusingacetoneanembeddedinEpon.

Ultrathinsectionswerestainedwith2%uranylacetateindistilled

waterand0.2%leadcitrateina1Nsodiumhydroxidesolutionand

observedwithatransmissionelectronmicroscope,ZeissLeo906.

Forbasicproteindetection,theethanolicphosphotungsticacid

method(E-PTA)wasapplied.Seminalvesicleswerefixedonlyin

bufferedglutaraldehydesolutionfor24hat4◦C.Thematerialwas

dehydratedinanalcoholicseriesandtreatedenblocbya2%PTA

solutioninabsolutealcoholandembeddedinEpon.

3. Results

ThespermofP.elaeisis(Fig.1A)andT.diatraeae(Fig.2A)are

spiral,longandthin,approximately195␮mand130␮minlength,

respectively. They are divided into head and flagellum regions

(Fig.1Aand Fig.2A).Theheadregionconsistsoftheacrosome

andnucleus.Inbothspecies,theacrosomeandtheanteriornuclear

regionarecoveredbyanextracellularlayerinwhichseveral

fila-mentsareradiate(Figs.1C–Eand2C–F).Thisextracellularlayeris

longerinthespermofT.diatraeae(Fig.2C)spermthanP.elaeisis

(Fig.1C),measuringaround2␮mand0.3␮m,respectively.Itin

P.elaeisiscontainstworegions,withtheinnerregionbeingmore

electron-dense(Fig.1C).Thislayerandallthefilamentsarisingfrom

itareE-PTApositive,inbothspecies(Fig.2F).

Theacrosomeisverysmallinbothspecies,measuringaround

0.1␮minlength.Itiscomposedofanacrosomalvesicleand,in

P.elaeisis, a rod-shapedperforatorium. Thislatter hasthebase

insertedintoa smallcavityatthenucleartipandiscoveredby

theacrosomalvesicle(Fig.1C).

Inbothspeciesthenucleusisfilledwithhomogeneously

com-pacted chromatin(Figs.1F–H and2G–J).In P.elaeisisit islong,

measuringapproximately50␮minlengthand0.2␮matthebase,

graduallytaperingtowardthetip(Fig.1AandB).InT.diatraeaethe

nucleusmeasures20␮minlengthand0.4␮mindiameteratthe

base.Ittapersabruptlyfrombasetonearhalf(Fig.2AandB).

Inthetransitionregionofthenucleus-flagelluminbothspecies,

thenucleusisconnectedtotheflagellarstructuresbyacentriolar

adjunct(Figs.1F,H,Iand2H–K).Thecentriolaradjunctoverlaps

boththebaseofthenucleusandtheaxonemeanteriorregion

(cen-triole).InP.elaeisistheoverlappednuclearareaisgreaterthanin

T.diatraeae(Figs.1Fand2I,however,inT.diatraeaethecentriolar

adjunctsurroundsalmosttheentirenuclearbase(Figs.1Hand2J).

The flagellum consists of an axoneme, two

mitochon-drial derivatives, and in P. elaeisis, two accessory bodies

(Figs. 1J–M and 2H, I, L,N).Theaxoneme shows a

microtubu-lar arrangement of 9+9+2, nine accessory microtubules, nine

peripheralpairsandonecentralpair(Figs.1Nand2N).However,

inT.diatraeaethecentralpairwasdifficultlyobserved(Fig.2L–O),

whiletransversestriationswereobservedthroughoutthecentral

regionoftheaxoneme(Fig.2H,I,PandQ).Thesestriationsare

compoundbydenseandpalelineswithregularspacesbetween

theseones,measuringamongdenselinesabout38nm(Fig.2I).

Theaxonemeisalsocoiled,soallpairscannotsimultaneously

besectionedatrightangles(Figs.1M–Pand2L–O).Attheflagellar

posteriorendtheaxonemeisthelasttofinish,andtheaccessory

microtubulesarethefirsttodisappear(Figs.1O,Pand2L,M).InT.

diatraeaesperm,whentreatedwithethanolicPTA,anEPTA-positive

materialisclearlyobservedaroundandinsidetheaxoneme,butthe

microtubulesareEPTA-negative(Fig.2F).

Themitochondrialderivativesarearrangedinaspiralalongthe

entireaxoneme.Incross-sectiontheyareovalshapedwithequal

areasandmuchsmallerthantheaxoneme(Figs.1L,Mand2H–P).

In the final portionof theflagellum, themitochondrial

deriva-tivesofP.elaeisisendapproximatelytogetherandneartheend

oftheaxoneme,sinceflagellasectionedwithonlyone

mitochon-drialderivativeorjusttheaxonemerarelyareobserved(Fig.1L).

InT.diatraeaeonederivativeendswellbeforetheotherandboth

endbeforetheaxoneme,becauseFig.2Lshowsvariousflagellain

crosssectionwithonlyonemitochondrialderivativeoronlythe

axoneme.

InP.elaeisis,theaccessoriesbodiesareelectron-dense,located

betweenthemitochondrialderivativesandtheaxoneme,andin

cross-sectionsareovalwithaverysmalldiameter(Fig.1JandM).

TheywerenotobservedinT.diatraeae.

4. Discussion

ThespermofP.elaeisisandT.diatraeaeexhibitbasicmorphology

similartothatofotherChalcidoidea,forexample:(1)spiralsperm;

(2)thepresenceofanextracellularlayercoatingtheacrosomeand

partofthenucleusfromwhichseveralfilamentsareirradiated;(3)

thetwomitochondrialderivativeshavereducedandequal

diam-eters;and(4)attheendoftheaxoneme,accessorymicrotubules

finishfirst(Britoetal.,2009;Fiorilloetal.,2008;Lino-Netoetal.,

2000;Quickeetal.,1992;Silva,2010).Meanwhile,thereareother

featuresthatdiscriminatethesetwospeciesofotherschalcidoids.

Althoughthepresenceofanacrosomeis commonin

Chalci-doidea,itsmorphologycanvarywidely.Itmaybeverysmall,e.g.

Mellitobia(Britoetal.,2009),orabsent,asinPegoscapus(Fiorillo

etal.,2008).Also,therearespeciesinwhichthevesicleacrosomal

ispresentbuttheperfuratoriumisnotobserved,asinTrichogramma

pretiosum and Trichogramma dendrolimi (Lino-Neto and Dolder,

2001;Lino-Netoetal.,2000),MellitobiaaustralicaandMellitobia

hawaiiensis(Britoetal.,2009),inIdarnessp.1andsp.2(Silva,2010)

andinT.diatraeaestudiedhere.Likewise,theextracellularlayer

wasnotobservedinsomechalcidoidsas,forexample,Idarnessp.1

andsp.3(Silva,2010).However,thislayer,withfilamentsradiating

fromit,isnotuniquetochalcidoids,asobservedinIchneumonoidea

(Moreiraetal.,2010;Quickeetal.,1992)andCynipoidae(Newman andQuicke,1998).

Thecentriolaradjunct,observedinthesetwoeulophids,occurs

inmany insectordersincludingHymenoptera.In chalcidoids,it

canoffergooddiagnosticcharactersatthefamilyandsometimes

genuslevel.Forexample,inEurytomidae(Lino-Netoetal.,1999),

Trichogrammatidae(Lino-Netoetal.,2000;Lino-NetoandDolder,

2001)andEulophidae(Britoetal.,2009)thisstructureoverlapping

onlythecentrioleregion(about0.5␮m).However,in

Eurytomi-daeitoverlapsthenucleusbyamuchlargerdistance(about8␮m)

than in Eulophidae and Trichogrammatidae (lessthan 0.5␮m).

In theAgaonidae, Pegoscapus (Fiorillo et al., 2008) and Idarnes

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Fig.1.Light(AandB)andtransmissionelectron(C–Q)photomicrographsofspermatozoafromP.elaeisisinlongitudinal(C,GandK)andtransversal(D,E,G–JandL–P) sections.(A)Sperminphasecontrast.Thearrowindicatesthelimitbetweenthehead(h)andtail(t).(B)Nucleus(n)stainedwithDAPI.(C–E)Sectionoftheheadregion showingtheacrosomalvesicle(a),theperforatorium(p)insertedinadeepnuclearcavityandthefilaments(f)radiatingfromtheextracellularsheath(s).(F)Sectionof thenucleus–flagellumtransitionregionshowingcentriolaradjunct(ca),centriole(c)andaxoneme(ax).(G)Sectionoftwonuclei.(H–J)Sectionsofthenucleus–flagellum transitionregionatdifferentlevels.Notein(J)theanteriortipofthemitochondrialderivatives(m).(K)Alongitudinallysectionedflagellumshowingthemitochondrial derivativescoilingaroundtheaxoneme.(L)Spermatdifferentlevels.Notethepresenceoftwomitochondrialderivativesinallflagella.(M)Middleregionoftheflagellum showingtheaxonemeformedofdoubleexternalmicrotubules(curvedarrow),acentralpair(smallarrows),andaccessoriestubules(arrowhead).Thelargearrowsindicate thetwoaccessorybodies.(N–P)Sectionsshowingtheflagellatipswhereonemitochondrialderivative(m)terminatesbeforetheotherandbothbeforetheaxoneme.Inthe latter,theaccessorymicrotubules(arrowheads)arefirsttofinish.Bars:AandB=10␮m;C–JandM–P=0.1␮m;KandL=0.5␮m.

ItoverlapsonlythecentrioleregioninPegoscapus,butinIdarnesit

runsparalleltomitochondrialderivativesbyatleast4␮m.

Althoughtheaxonemewith9+9+2microtubulesisobserved

inmanyinsects,changesinthispatternarecommonlyobserved,

whichmayrepresentimportantcharactersforsystematicsofthese

organisms.Forexample,transversestriationsalongthecenterof

theaxoneme,asoccurinT.diatraeae,haveneverbeenobservedin

anyotherHymenopteraincludingchalcidoids,thisstriationsmay

constituteauniquecharacteristicforthespeciesorgenus.

How-ever,whetherthesestriationsaremodifications ofone existing

flagellarcomponentsasthecentralsheath,andhowtheycombine

withotherelementsinthecentralregionoftheaxoneme,areissues

thatneedfurtherinvestigation.

In most chalcidoids, including these two species, accessory

microtubulesarethefirsttofinish,followedbythecentralpair

andtheperipheraldouble.However,inPegoscapus(Fiorilloetal.,

2008),thecentralpairisthefirsttoend.Thelastperipheral

dou-bleendingdifferentiateschalcidoidsaswellastwoichneumonids

species(Moreiraetal.,2010),oftheAculeata,inwhichthelastto

finishareaccessorymicrotubules(seeZamaetal.,2005).

Inthesetwoeulophidspecies,themitochondrialderivatives,

incross-section,aresymmetrical,slightlyovalandsmallerthan,

andveryclosedto,axoneme. Thesesamefeaturesarethesame

ones showed in Eurytomidae (Lino-Neto et al., 1999) and

Tri-chogrammatidae(Lino-Neto etal., 2000;Lino-Neto and Dolder,

2001),indicatingthatthesethreefamiliesarecloselyrelated.

How-ever,mitochondrialderivativesofM.hawaiiensisandM.australica

(Britoetal.,2009)areasymmetric,possiblyrepresentingaunique

characteristicforthiseulophidgenus.InPegoscapus(Fiorilloetal.,

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Fig.2. Light(AandB)andtransmissionelectron(C–Q)photomicrographsofspermatozoafromT.diatraeaeinlongitudinal(C,D,G–I,PandQ)andtransversal(E,FandJ–O) sections.(A)Sperminphasecontrast.Thearrowindicatesthelimitbetweenthehead(h)andtail(t).(B)Nucleus(n)stainedwithDAPI.(C–F)Sectionoftheheadregion showingtheacrosomalvesicle(a)supportedatthenucleartip(arrow)andthefilaments(f)radiatingfromtheextracellularsheath(s).(G–K)Sectionsofanuclearregion (G)andnucleus-flagellumtransitionshowingcentriole(c),centriolaradjunct(ca)andmitochondrialderivatives(m)coilingaroundtheaxoneme(ax).Notethepresenceof transversestriations(arrows)throughoutthecentralregionoftheaxoneme.(L–Q)Sectionsofflagellaatdifferentlevels.Notethatitiscommonflagellawithonlyone(large arrow)orno(arrowheads)mitochondrialderivative.Alsonotethatthecentralpairofmicrotubules(arrowsinO)israrelyobservedandtheaccessorymicrotubulesarefirst tofinish(M).Bars:AandB=10␮m;C–FandI–O=0.1␮m;G,H,PandQ=0.5␮m.

aboveonlybybeingslightlyasymmetrical.InIdarnes(Silva,2010),

theyare larger in diameterand completely surrounded bythe

axoneme,indicatingthatthesetwoagaonidgeneraaredistantly

related.

Accessorybodiesareveryreduced(asinP.elaeisis)orpossibly

absentinsomespecies(asinT.diatraeae),characteristicsthat

dif-ferentiatechalcidoidsfrommostHymenoptera(Zamaetal.,2005;

Araújoetal.,2009;Moreiraetal.,2012).

Inconclusion,themorphologicalcharacteristicsofchalcidoid

spermindicatethatEulophidaeiscloselyrelatedto

Trichogram-matidae,aswasobservedbyHeratyetal.(2012),andbothofthese

familiesareclosertoEurytomidaethanAgaonidae.InAgaonidae,

Pegoscapusspermaremoresimilartothosethreefamiliesabove

thanIdarnes.

Acknowledgments

The authors thank the Nucleus of ElectronMicroscopy and

MicroanalysisoftheUFV,ElectronMicroscopyCentersofthe

UNI-CAMPandtheUniversityofBrasília(UNB),andthetwoanonymous

reviewerswhoprovidevaluablefeedbackonthemanuscript.This

researchwassupportedbyCAPES,CNPqandFAPEMIG.

References

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FNDE - Fundo Nacional de Desenvolvimento da Educação IBGE - Instituto Brasileiro de Geografia e Estatística IES - Instituições de Ensino Superior IF - Instituto Federal de