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Sexual behavior of the digger wasp Sphex ingens Smith (Hymenoptera, Sphecidae)

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ww w . r b e n t o m o l o g i a . c o m

REVISTA

BRASILEIRA

DE

Entomologia

AJournalonInsectDiversityandEvolution

Systematics,

Morphology

and

Biogeography

Sexual

behavior

of

the

digger

wasp

Sphex

ingens

Smith

(Hymenoptera,

Sphecidae)

Carlos

Alberto

S.

Souza

a,∗

,

Fábio

Prezoto

a

,

Mauro

Sérgio

C.S.

Lima

b

,

Jonas

Pederassi

c

aLaboratóriodeEcologiaComportamentaleBioacústica,UniversidadeFederaldeJuizdeFora(UFJF),JuizdeFora,MG,Brazil bUniversidadeFederaldoPiauí(UFPI),Floriano,PI,Brazil

cMuseuNacional,DepartamentodeVertebrados,UniversidadeFederaldoRiodeJaneiro(UFRJ),RiodeJaneiro,RJ,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received17September2014 Accepted11February2015 Availableonline9April2015 AssociateEditor:KevinWilliams Keywords: Copulation Coercivecopulation Breedingseason PraiadoAventureiro Solitarywasp

a

b

s

t

r

a

c

t

Aspecies’matingsystemdependsonitsspatialdistributionandtemporalavailabilityofmating opportu-nities,aswellasontheresourcesthatcreatetheseopportunities.Inaddition,formanyspecies,courtship isdrivenbyspecificbehaviorsthatprecedeandfollowcopulation.AlthoughSphexingensisa taxono-micallywellknownspeciesofdiggerwasp,itsecologyandbehaviorremainpoorlyknown.Hence,we analyzedpatternsandtrendsofsexualbehavior,inordertounderstandwhethercourtshipcanpersist inapolygamousmatingsystem.WemonitoredbyvideowasppopulationsinIlhaGrande,southeastern Brazil.Basedontheobservedbehaviors,wecalculatedstochasticprobabilitieswithaMarkovchainto inferonbehavioraltrends.Werecordedfourbehavioralphasesbasedon19,196behavioralactsobserved in224copulationattempts.Therewerenosignificantdifferencesincommonbehavioralactsbetween malesandfemales.Thecopulationpatterns,conflicts,andtrendsobservedinS.ingensclearlyshowthe influenceofsexualselectioninitspromiscuousmatingsystem.

©2015SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Allrightsreserved.

Introduction

Inseveralanimalspecies,matingsystemsareaffectedbyfood availabilityanddistribution,breedingsites,andpotentialpartners. Thecourtshipandcopulationphasesareobservedinmostmating events.Currently,there isconsensusontheconflictsofinterest betweensexesduringmating,andsexualselectionisanimportant mechanisminthechoiceofanidealpartner.

Amonghymenopterans,thespheciformcomplex(Ampulicidae, Crabronidae,andSphecidaesensu Melo,1999)comprises wasps thatareusuallysolitaryandhaveabroadbehavioral repertoire, especiallyintermsofreproductiveandnestingbehaviors(Evans andO’Neill,1978;Amarante,1999;Melo,2000;AlcockandKemp, 2005).Males increasetheirreproductivesuccessthrough adap-tivestrategiesorspecialization(Evans,1966;Alcock,1975;Kroiss etal.,2010),whereasfemalesincreasetheirreproductivesuccess throughmultiplemating(Melo,2000)orbychangingandsharing nestsafterthechoiceofapartnerwithbetterattributesorabilities. ThediggerwaspSphexingens Smith1856isa largesphecid, whichisusuallyblackandwhosegasterandlegsvaryfrompartially

∗ Correspondingauthor.

E-mail:seteorus@yahoo.com.br(C.A.S.Souza).

tocompletelyred(BohartandMenke,1976).Ithasbeenrecorded intheBrazilianstatesofBahia,EspíritoSanto,RiodeJaneiro,and SãoPaulo(Amarante,2002).

TheecologyandthebehaviorofS.ingensinBrazilwerestudied byPiliackasetal.(2007)andBuys(2009),respectively.Although thesestudiescompriseshort-termpreliminaryassessmentsand casualobservations,theyarestillconsideredpioneeringinBrazil, asfewscientistshavetriedtounderstandthenaturalhistoryofS. ingens.

Thegreatestchallengesofadetailedstudyontheecologyand behaviorofa wildpopulationofS.ingens aretheseasonalityof its breeding and its restricted distribution. However, the poor information available ontheecology and behavior of S.ingens, inparticularintermsofitssexualbehaviordeservesmore atten-tion,forinstance,onthetypeofmating,phasesandactsofmating repertoire,sexualbehaviortrends,influenceofthecourtshipinthe processofmateselectionandselectioncriteriaoffemales.

PreliminaryobservationsindicatethattheS.ingensmating sys-temispolygamous,andtheselectionofpartnersdoesnotoccur throughthecourtshipbehavior.For thisreason,weasked:how extensivelydoescourtshipbehaviorcoexistinapolygamous mat-ing system? Hence,the present study aimedat describing and analyzingthematingpatternsand trendsofthediggerwaspS. ingens,aimingatadvancingtheknowledgeofitsnestingdynamics. http://dx.doi.org/10.1016/j.rbe.2015.03.005

0085-5626/©2015SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Allrightsreserved.

CORE Metadata, citation and similar papers at core.ac.uk

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Materialsandmethods

Studyareaandsamplingdesign.IlhaGrande,a coastalisland, islocatedinthemunicipalityofAngradosReis,stateofRio de Janeiro,southeasternBrazil.Itisafragmentofthecoastalmassif witharuggedrelief,andhasapproximately19,300ha.Its predom-inantvegetationtypeismontaneandsubmontaneforest(Veloso etal.,1991).ThePraiadoSulStateBiologicalReserve(RBEPS) cov-ers18.6%(3.600ha:23◦10S–44◦17W)ofIlhaGrande’sarea,and harborsinnearlyallitsareaacontinuouscomplexofAtlantic For-est,whichcomprisesforestenvironments(sensustricto),restinga forests,mangroves,lagoons,shrubbyrestingas,rockyshores,and thebeaches Meros,Aventureiro, Demo,Sul, and Leste (FEEMA, 2008).

Wedelimitedtransectsabovethehightidelineandinforedune areasonAventureiroBeachtofindnestingsites.Whenwefound anestingsitewedelimitedthearea.Ineachnestingsite,we cap-turedmalesandfemales,markedtheirmesoscutumwithcolored non-toxicpaint(Martins,1993),andreleasedthemforindividual identificationandbehavioralanalysis.

We daily monitored in copulo pairs formed randomly with exchangeofindividuals,usingadigitalcamcorderanda chronome-ter.Thesamplingefforttotaled131hofobservation,comprisingthe firstfortnightofJanuary2010andthefirstandsecondfortnights ofJanuary2011.However,only50hwereselectedforanalysis,i.e., 45hofobservationincludingallrecordedcopulationsplus5hof observationusedtointerpretthematingbehaviorofthespecies.

Atfirst,inordertointerpretthebehaviorsweusedthead libi-tum method(Altmann, 1974), which is based onthebehaviors thatprecede, trigger,and endcopulation attempts,whereas for quantitativeobservationsweusedthesequencesamplingmethod (Altmann,1974).Theseproceduresallowedtheconstructionofa flowchartwiththeobservedbehaviors,inordertosupportthe analysisand theconstructionofanotherflow chartonthe con-ditional probabilitiesof occurrence and formation of stochastic processes(GottmanandRoy,1990).

All procedures of the present study complied with the guidelines of the permit for scientific research #002/2011 issued by the Directorate of Biodiversity and Protected Areas (INEA-RJ). The captured specimens were deposited as vouch-ers in the Natural History Collection of the Federal University of Piauí (CHNUFPI: Hymenoptera Collection), campus Amil-car Ferreira Sobral: CHNUFPI(HYM)0002, CHNUFPI(HYM)0003, CHNUFPI(HYM)0004,andCHNUFPI(HYM)0005.

Statisticalanalysis

Wetransformedtheabsolutefrequenciesofthebehavioralacts thatcomposethebehavioralstatesintorelativefrequencies.We submittedthe frequency of behavioral acts(state) common to malesandfemalestoachi-squaredtestandlogarithmizedthem toreducethevariation of frequencieswhenever necessary.We modeledtherelativefrequenciesofbehavioralstateswithaPoisson distributionandaMarkovchain,inordertoestimateconditional probabilitiesand formationof stochasticprocesses. We ranthe analysisusinganadd-infor MicrosoftExcel® developed bythe OperationResearchGroupoftheUniversityofTexas.Wesubmitted thecomparisonbetweenthePoissondistributionandtheMarkov chaintoaKolmogorov–Smirnovtest(p<0.01).Allstatistical anal-ysesweremadeusingfreesoftware.

Results

Weanalyzed224copulationattemptsin137randomlyformed pairs with interchange of males and females. The behavioral

0.0 1.0 0.1 F requency (Log) Behavioral categories Male Female

Pre-copulation Copulation Post-copulation

WIFA CONN SUCC UNSU PERM DISP

ANCO 10.0 100.0

Fig.1.Comparativefluctuationbetweenthelogarithmizedandnon-significant fre-quency(x2=16.622,df=n1,p<0.01)ofthecommonbehavioralactsofSphex

ingensSmith1856(Hymenoptera,Sphecidae).Thecommonbehavioralactswere: antennation(ANCO),wingfanning(WIFA),connubium/strictcopulation(CONN), genital clasping/successful copulation(SUCC), nogenital clasping/unsuccessful copulation(UNSU),permanenceofmalesinthenestingarena(PERM),and disper-sion/malesleavethenestingarena(DISP).

repertoire was divided in four phases: identification, pre-copulation,copulation,and post-copulation,based ona total of 19,196behavioralactsdistributedin24sexualbehaviors(Table1). Femalematingbehaviorwascomposedofnineexclusive behav-iors(2319 behavioralacts, 12.0%),whereasmalesshowedeight exclusivebehaviors(940behavioralacts,4.8%).Sevenbehaviors werecommontobothsexes(15,937behavioralacts,83.0%),but there was no difference between sexes (x2=16.622, df=n1, p<0.01)(Fig.1).Themostfrequentmatingphasesinbothsexes werepre-copulationandcopulation,andbehavioralactsrelatedto communicationweresignificantandrecurrentinthesephases. Descriptionofthesexualbehaviorbasedontheobservedbehavior

The identification phase consisted of visual recognition and male assault against females (n=155), which were engaged in activitiesintheirnestsorwereseizedwhileflyingoverthe nes-tingsite.Allapproachesrecordedwereaggressive,precedingthe attemptofimmobilization,corroboratingtheexistenceofcoercive copulation.Thesuccessin immobilizationoffemaleswas80.0% (n=124)amongallapproachattempts(Fig.2).In18.7%ofthecases themalescouldnotimmobilizethefemalesorwererejectedbefore anyattempt,asthefemaleswerealwaysaggressive.

The beginning of pre-copulation is characterized by males mountingfemales,followedbyintensivecommunication, culmi-natingintheextrusionoftheaedeagusbeforeitsintromissioninthe female’sgenitalopening.Insomecasesmalesrubbedtheaedeagus laterallyonthefemales’gasterbeforetheintromission,whereas femaleshinderedthecopulationbycurvingtheirgaster.

In the copulation phase, receptive females positioned their gasterparalleltothesubstrateforaedeagusintromission. Contrac-tionandbendingmovementsdirectedthegenitalclasptoassure reproductivesuccess.Femalesshowedself-cleaningbehavior dur-inggenitalclasping(Fig.3),andthenwerestimulatedtoadopta disengagementbehavior.

Inpost-copulation,malescleanedtheirgenitalsaftertheywere disengaged.Weobservedbothdispersalandpermanencebehavior innestingarenasafterdisengagementinthepost-copulationphase inmalesandfemales.Mostfemalesremainedinthenestingarena (84.8%)andonlyafewdispersed(15.1%),whereasmalesshowed theoppositebehaviorwithhigherdispersal(73.2%)than perma-nence(26.7%)innestingarenas.Weobservedamongmalesthat remainedinthenestingarenaaftereffectivecopulationadecrease inmotoractivitiesreflectedinlowantennamobilityandwing fan-ning,characterizingarecoveryperiodof124.10±39.30sbeforea newcopulationattempt.

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Table1

SexualbehaviorrecordedformaleandfemalediggerwaspsSphexingens(Smith1856)(Hymenoptera,Sphecidae).

Behavioralacts Abbreviation Description

Recognitionandassault REAS Malesrecognizevisuallyfemalesandmovetowardsthem.

Immobilization IMOB Malesassaultfemalesdirectlyforacopulationattempt.Malesusuallyimmobilize

femalesusingthefirstpairofappendages.

Aggressivedisplay1 DIS1 Behavioralactcharacterizedbypartiallyopenedmandiblesandverticalinclinationof

thebodyonthelastappendages.

Confrontation CONF BehavioralactassociatedwithDIS1,characterizedbyaggressivenessand

advancementoffemalesagainstmales.Itisusuallytriggeredbylateralorfrontal

immobilizationattempts.

Rejection REJE Behavioralactcharacterizedbytherefusalofthepartnerduringlateralorfrontal

immobilizationattempts.Thisactwasalsoobservedwhenamaleunderwentmany

unsuccessfulcopulationattempts.

Mount MOUN Recurrentbehavioralactafterasuccessfulimmobilization.Malesremainontopof

femalestobeginthepre-copulationsequence.

Extrusion EXTR Extrusionoftheaedeagusfortheintromissioninthegenitalsoffemales.

Rubbing RUBB Tolaterallyrubtheaedeagusonthefemale’sgasterbeforegenitalintromission.

Curvatureofthegaster CUGA Femalesbendtheirgasteringeneraltopreventtheaccessofmalestothefemale’s

genitalopening.

Antennation ANCO Antennacommunication.

Wingfanning WIFA Wingfanningcommunication.

Aedeagusintromission AEIN Aedeagusintromissioninthefemale’sgenitalopening.

Aggressivedisplay2 DIS2 Behavioralactcharacterizedbypartiallyopenedmandiblesandintenseantenna

vibration.

Swayingbodymovements SWAY Unsociablebehavioralactcharacterizedbyswayingbodymovementsintheattempt

todislodgethemale.

Drumming DRUM Consistsinknockingseveraltimesthefirstpairofappendagesagainstthesubstrate.

Connubium CONN Sexualactivitymarkedbycopulationdynamicscomposedofgastercontractionand

bendingmovements.

Unsuccessfulcopulation UNSU Nogenitalclaspingoccursafterconnubium,characterizinganunsuccessfulcopulation

attempt.

Permanenceofmount PEMO Permanenceofmalesinthemountpositiontobeginanewcopulationattempt.

Genitalcleaning GECL Malescleantheirgenitalsusingthethirdpairofappendages.

Genitalclasping SUCC Genitalclaspingcharacterizingthecopulationsuccessofthemale.Malesclasped

duringcopulationbendtheirbodiesverticallyonthelastpairofappendages,andmay

twisttheirgasterlaterallyormaintainthemselvesindorsaldecubitus.

Genitaldisengagement DISE Behavioralactsofreleaseaftergenitalclasping.Femalesshovemalesusingthethird

pairofambulatorialappendages,dragthemontheground,ormakeflightattempts.

Self-cleaning SECL Usuallyperformedbythefemaleduringthegenitalclasping,comprisingthecleaning

ofantennaeandfirstambulatorialpairofappendages.

Permanence PERM Malesremaininthenestingarena.

Dispersion DISP Malesflyawayfromthenestingarena.

Sexualbehavior:behavioraltrends

Theconditionalprobabilitiesoftransitiondifferedsignificantly

betweenthe Poisson distribution model and theMarkov chain

(Dmax=0.240,df=n−1,p<0.01:Kolmogorov–Smirnov),sothatthe

vectorsoflimitingprobabilitieswerebuiltaccordingtotheMarkov chain.ThepredictionsderivedfromtheMarkovchaincorroborated theobservationthatthebehaviorsexhibitedduringmating dif-feredbetweenmalesandfemalesintermsofobservedtransition ofbehavior.However,sexualbehaviorsrecordedinloco(observed behavior)infemales,suchaseyeandantennacleaningwiththeir firstpairofambulatoriallegsduringgenitalclasp,draggingonthe

ground,andtheattemptofflightwithclaspedmales,were consid-eredirrelevantand,hence,excludedfromtheanalysis.

TheresultsexpressedbythediagramoftheMarkovchain high-lightedthatthebehavioraltransitionsincommunicationincluding theantennation(7.9%)andwingfanning(21.4%)behaviorsduring pre-copulationandcopulationhaveweakinfluenceonthemating behaviorofS.ingens.

Thetransitionoftheagonisticbehaviorsdisplayedbyfemales

during the identification (aggressive display 1: 10.3%,

con-frontation: 33.3%, and rejection: 33.0%), and copulation phases

(aggressive display 2: 24.5%, swaying body movements: 31.1%,

drumming:64.3%,andrejection:45.9%)indicateastrongtrendto

Fig.2. Sequenceofthephaseofidentificationandpre-copulation:(A)immobilizationattemptsbymaleswhilethefemaleissupplyingitsnestwithprey,(B)efficient

immobilizationofthefemaleandmountinthenestingarea,(C)aedeagusextrusion.Femaleshowsamixedbehaviorofreceptiveness(lastpairsofappendagesup)and

aggressiveness(partiallyopenedmandibles).

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Fig.3. Sequenceofthecopulationphase:(A)beginningofaedeagusintromission.Copulationduringnestdigging–femalecarryingaclodofsand.(B)Connubium,gaster’s

contractionmovements.(C)Connubium,gaster’sbendingmovements.(D)Successfulcopulation–claspingofclaspingorgans.Malewiththebodyverticallyinclinedand

femaleself-cleaning.

Photoby:JonasPederassi.

selectmales.Anothertrendpointedoutbytheanalysiswasthe

attemptof malestoremainmounted onfemales (47.9%) when

copulationattemptswereunsuccessful(Fig.4). Discussion

InthediggerwaspS.ingens,eventhoughmalesand females showedcommonbehavioralactsduringmating,differencesinthe frequency and diversity of these acts indicate different energy investmentbetweensexes.Historically,thedescriptionofmating eventsinhymenopteransischaracterizedbydifferenteffortsand methods,whichhindercomparisons.

However, although a behavioral similarity among species betweencopulation and mating phaseshas beendescribed for some hymenopteran species, such as Mormoniella vitripennis Walker (Barrass, 1960, 1961), Campoletis sonorensis Cameron (Vinson,1976)BrachymeriaintermediaNees(LeonardandRingo, 1978),ApantelesglomeratusLinnaeus(Tagawaetal.,1985), Asco-gasterreticulatusWatanabe(Kainoh,1986),EdithamagnificaPerty (Martins, 1993), NasoniavitripennisWalker(AssemandWerren, 1994),andRubricanasutaChrist(PimentaandMartins,1999),the detailsofthebehaviorofS.ingens,aswellasthevariationin behav-ioralacts,theirsequence,time,andfrequencydifferfromthoseof otherwaspspecies.

TheconfrontationandrejectionbehaviorsrecordedinS.ingens werecommonandpresentinallmatingphasesbetweenmalesand females.AccordingtoCorderoandEberhard(2003)pre-copulatory confrontationsindicatetheexistenceofconflictsbetweensexes andsexualselection,whichfavorsmanipulativemalesincoercive copulations.Theresistanceoffemalestotheantagonisticbehavior ofmalesmayselectindividualsaccordingtotheircapacityof indi-vidualmanipulation(signalingvigorandfitness)inclaspingthe femaleasittriestogetridofthemale(AllenandSimmons,1996).

InS.ingenscoercivecopulationisanalternativestrategyofmales inresponsetotheconstantaggressivenessoffemales,asthelatter usethiscriteriontoselectpartners.

InS.ingensfemales,thelargernumberofcopulationattemptsin relationtothephaseofnestconstruction(diggingthetunnelor sup-plychamber)reflectsahighenergyinvestment,whichmakesthem moreevidentintheirrespectivearenasandnests,andjustifiesthe trendofremaininginthenestafteracopulationattempt, regard-lessoftheresult.Evansetal.(1976),Jangetal.(1996),andMelo (2000)consensuallyaffirmedthatmosttimeandenergyoffemales ofthefamilySphecidaeisinvestedinmaternalcareintheformof constructionandprovisionofnestsduringtheirreproductivelife.

MaleS.ingenswereabletocopulaterepeatedlywithfemales inthenestingsiteatanyphaseofnestbuilding.Thisresultsinan intensivedailycopulationactivitythatinvolvesarelevant invest-mentoftimeandinpartcorroboratesthestudiesbyGenaro(1998) onthespeciesSphexjamaicencisDrury.Inseveralinsectspeciesthe occurrenceofmultiplecopulationssuggeststheexistenceofcryptic femalechoice(Ebehard,1996),spermcompetition(Parker,1970), reductioninthefemale’sspermathecaorthatoneorfew copula-tionsarenotenoughforthefemalestoobtainenoughspermfora maximumproductionofoffspring(Ridley,1990),andeven physi-ologicaldeficienciesinthereproductivesystemofmales(Martins etal.,2004).

Severalstudiesreportedthatthecourtshipandcopulationof manyhymenopteransconsistofmovementsofwings,legs, anten-nae, and mouthparts of males (Barrass, 1960, 1961; Mathews, 1975;Vinson,1976;LeonardandRingo,1978;Tagawaetal.,1985; Kainoh,1986;Martins,1993;AssemandWerren,1994;Pimenta and Martins, 1999). The sequence of these movements varies accordinglybetweenspeciesandisrepeatedbyareceptivefemale (Mayr, 1973;Assem, 1986).Althoughthesestudies suggestthe existenceofvisualstimulithatprecedemount,wedidnotobserve

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1st phase: Identification REAS IMOB DYS1 CONF REJE MOUN EXTR RUBB CUGA ANCO DYS2 SWAY DRUM AIEN CONN UNSU SECL DISE PERM Symbols or <1% 1 ~ 5% 5 ~ 10% >10% <1% 1 ~ 10% 10 ~ 20% 20 ~ 30% 30 ~ 40% >40% DISP SUCC GECL PEMO WIFA 2nd phase: Pre-copulation 3rd phase: Copulation 4th phase: Pos-copulation

Fig.4.DiagramrepresentingtheMarkovchainforthesexualbehaviorrepertoireofthewaspSphexingensSmith1856(Hymenoptera,Sphecidae).Symbolsrepresentsexes. Symbolsizeandlinethicknessrepresentthefrequencyofoccurrenceofeachbehavior.Arrowheadsrepresentthetransitionfromonebehaviortothenextandarrowthickness representsthefrequencyclass.

anypre-copulationgesturalbehaviorinS.ingens.Thelackofthese behaviorsinS.ingensresultsfromtheinfluenceofthepromiscuous matingsystemandfromthewayfemalesselecttheirpartners.

Presumably,theenergyspentinintersexualcommunicationin S.ingensdoesnotsupportthatthisbehaviorinfluencescourtship, butwouldrepresenttheexchangeofstimuliusedinconspecific recognition,assuggestedbyMayr(1973),orgeneralexcitement signals.However,morespecifictestsontheperformanceof anten-nationanditsinfluenceonthesuccessfulandunsuccessfulmating couldclarifythefunctionofthisbehavior.Furthermore,itis possi-blethatinS.ingenspheromonesaretheonlyexpressionsoffemale receptivity,asweobservedmalestryingtocopulatewithpreyleft byfemalesattheentranceofnests.Thisbehaviorwasalsoobserved

instudieswithotherspeciescarriedoutinthelaboratory(Barrass, 1960,1961;Mathews,1975;Vinson,1976).

OtheraspectsofsexualbehaviorofS.ingens,thatwouldexpand theunderstandingofitsreproductivebehavior,refertothe adjust-ments,disputesandstrategiesadoptedbymalestoincreasetheir reproductive success. Apparently, preliminarytests on the col-lectedspecimenssuggestthattherearesizedifferencesbetween thetwosexes,aswellbetweenmaleswithterritorialandpatrol behavior.Therefore,differencesinsizeandbehaviorcould influ-enceindividualfitness,withconsequencestotheresultsofmating disputes,andinthefrequencyofthereproductivesuccess.

Ouranalysiscorroboratesthatthematingsystemandfemale aggressivenessresultinlowsexualselectivityandadecreasein

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courtshipeffortbymales,and,hence,favor themaintenance of coercivecopulation.Theyalsosuggestthattheabilityofmalesto manipulatethefemalesduringcopulationisthemainrequirement forasuccessfulcopulation.Hence,thedecreaseincourtshipeffort bymalesisanalternativestrategytoenergy-demandingstrategies basedonelaboratedcourtshipdisplays,consideringthewaythat copulationsoccur,numberof copulationattempts observedand constantconfrontationwithrivalmalesinthepresentstudy.The escalationoffemaleaggressivenessisanantagonisticsexual selec-tioncriteriondifferentfromclassicformsfoundintheliterature intermsofassessmentofattributesorcourtshiprites.Inaddition, althoughcoercivecopulationisnotanexclusivestrategyamong insects,itisrareinsolitarywasps,inparticularsphecids.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest. Acknowledgments

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