Sperm displacement ability in the damselfly Calopteryx haemorrhoidalis asturica Ocharan: no effect of male age, territorial status, copulation duration and syn-copulatory behaviour (Zygoptera: Calopterygidae)

6 Pages·2001·0.56 MB·English

by  Córdoba-Aguilar, A

Odonatologica30(4): 375-380 December I, 2001
Spermdisplacementabilityinthedamselfly
Calopteryx haemorrhoidalisasturica Ocharan:
noeffect ofmaleage, territorialstatus,
copulationdurationandsyn-copulatory behaviour
(Zygoptera: Calopterygidae)
A.Córdoba-Aguilar
CentrodeInvestigacionesBiológicas,Universidad Autónoma del Estado deHidalgo,
Apdo.P.69-1,Plaza Juárez,Pachuca,Hidalgo42001,México
[email protected]
Received June 19, 2000/Revised andAcceptedMarch 7, 2001
Duringcopulationandbeforespermtransfer,odon. 36 areabletomanipulaterivalsperm
storedinthe $ spermstorageorgans(usuallythebursacopulatrixandspermathecae).3 3 of
theterritorialC. h.asturicause2mechanisms forthis.Bursal spermisremovedphysically
whilstspermathecalspermisdisplacedviaaedeagalstimulation(throughaseriesofabdominal
flexions)ofthe$ sensorysystemthatcontrolsspermathecalspermejection.Mostbursalsperm
isremoved butthereisindividualvariationinspermathecalspermdisplacementPreviousresults
have foundthatthisvariationis relatedtoaedeagalwidth. Inthispaper4variablesthatmay
alsoexplainvariationinspermathecalspermdisplacementabilityareinvestigated:3age and
status(territorialandnonterritorial),durationofthespermdisplacementstageand thenumber
ofaedeagalstimulatoryflexions.Variationintheabilitytodisplacespermathecalsperm,however,
wasnotrelatedtothesevariables.Thissuggests thatvariationin thisabilityisreliant onlyon
3genitalicattributes,aedeagalwidth. Theseresultsarebrieflydiscussedin termsofcurrent
theoryofsexualselectionastheprocesspropellinggenitalicevolution.
INTRODUCTION
Animal genitalia show a greatdiversity in morphology in malesofintemally-
-fertilising species (EBERHARD, 1985, 1996)butthecauses ofthis are unclear.
Recent claimshave suggested thatsexual selection mightbe theoperating force
propelling genitalic evolution(EBERHARD, 1985, 1996; ARNQVIST, 1998).
During copulation, butpriorto spermtransfer,odonatemaleshavetheability to
manipulate thestoredspermofrivalsusingtheirspecialised genitalia(e.g. WAAGE,
1979;MILLER, 1987; CORDERO & MILLER, 1992).Thereis, however, little
376 A.Cordoba-Aguilar
evidence of male variation in sperm displacement ability, based on genital
morphology, tosuggestthatsexualselectionmightbeacting onthemalegenitalia.
Recently, however,experimentalevidencehassuggested thatsexualselectionisthe
process responsible forgenitalic evolutionin theterritorialdamselfly Calopteryx
haemorrhoidalisasturica (CORDOBA-AGUILAR, 1999).Malesofthis species
defendriverinespaces whichcontainresources thatfemalesuse duringoviposition
(CORDOBA-AGUILAR, 2000). Notall males areableto defendterritoriesand,
consequently, somemalesadoptanonterritorialbehaviour.However,anonterritorial
tacticdoesnotpreventamalefromobtainingcopulations (CORDOBA-AGUILAR,
2000).
Thebehaviouralprocessesthatoccurduringcopulation inC.h.asturicaare similar
to those ofotherodonates (e.g. MILLER& MILLER, 1981): males perform a
numberofabdominalflexions whicharerelated to the mechanisms that occur in
the femalegenitalia. During stageI (sensu MILLER& MILLER, 1981)males,
through aseriesof50.2±7.2abdominalflexions whichlasts 104.2± 10.2seconds
(CORDOBA-AGUILAR,2000), displace the spermstoredin thefemale’ssperm
storage organs (the bursacopulatrix andspermathecae). During stage II (sensu
MILLER& MILLER.1981) malestransfertheirspermtothespermstorageorgans
(CORDOBA-AGUILAR, 1999). Sperm displacement occurs via two different
mechanisms (CORDOBA-AGUILAR, 1999).Bursal spermisremovedphysically
whilstspermathecal spermis displaced viamaleaedeagal stimulation, mediatedby
theabdominalflexions, ofthefemalesensory system that controls spermejection
duringfertilisation.Mostbursalspermisdisplacedbutthereisconsiderablevariation
inspermathecal spermdisplacement. Themostlikelyexplanation forthisvariation
is that thereare individualdifferencesintheaedeagal morphology whichresultin
differencesinstimulation(CORDOBA-AGUILAR, 1999;forasimilarsuggestion
inanotherdamselfly species seeANDRES&CORDERO, 2000).
Variation in sperm displacement ability has been previously documented in
odonatesand thevariables that have beendemonstratedto havean effecton this
variationare malestatus (territorial or nonterritorial; S1VA-JOTHY& TSUBAKI,
1989;WOLFetal., 1989),maleageandcopulation duration(SIVA-JOTHY, 1987).
Anotherpotential sourceofvariationinspermdisplacement ability particular toC.
h. asturicamaybethenumberofstimulatory abdominalflexions occurring during
stageI.
Inthisstudy Iinvestigatetheeffectof malestatus(territorial andnonterritorial),
maleage,thedurationandnumberofflexionsduringthespermdisplacementstage
1 in C. h. asturica. My aimis to explore ifthesevariables couldalso explain the
observed variationin malesperm displacement ability.
MATERIALANDMETHODS
FieldworkwascarriedoutinanarrowstreaminSWSpain(seeCORDOBA-AGUILAR,2000foradescription
ofthefield site)in Julyand August, 19%, 1997 and 1998.Becausethis waspart ofalong-termstudy,most
SpermdisplacementinCalopteryxhaemorrhoidalis asturica 377
animalshadbeenindividuallymarked,usinganindelible inkpen, by thetimethemanipulationsweremade.
Twomaleagecategoriesweredefinedaccordingtothefollowingcriteria(seealsoJOHNSON,1973;PLAISTOW,
1997forarationaleofthisagingmethod):(a)“young”,individualswithfullydevelopedcolourationand“shiny”
or“glassy”wings;and(b)“young-old”,animalswithadustyappearanceofthethoraxandabdomenbutadegree
of“shininess” onthewings.
Femalesinthefieldhavevariablevolumesofspermathecalsperm(unpub.data).Forthelogicofthetreatments
describedbelow,however, itwasnecessary tohavefemales withfilledspermstorageorgansprevious to
manipulations.This wascarriedoutby inducingfemalestocompletecopulationsusingthe“hand-pairing”
technique(OPPENHEIMER& WAAGE, 1987).
EFFECTOFMALEAGEON SPERMDISPLACEMENT—Thevolumeofstoredspermwasmeasuredin
femalesthathadbeenpairedtoeithera“young”or“young-old”territorialmalerespectively(twodifferentsets).
Previousanalysesofcensusedindividuals hadsuggestedthatthedifferencein agebetween thesetwocategories
variedfromseventotendays(8.3±2.4days,N=53males).Sincemaleswereobserved for15-18days(from
thefirsttothelastobservationduringdailycensuses),adifferenceofsevendayswasthebestlogisticcompromise
totesttheeffectofage.Copulationswereinterruptedatthe50*abdominal flexion,since thisis thebehavioural
event atwhich maximum spermdisplacementoccurs(C6rDOBA-AGUILAR, 1999).Spermvolumewas
comparedforbothgroupsoffemales.
EFFECTOFMALETERRITORIALSTATUS(TERRITORIALOR NONTERRITORIAL)ONSPERM
DISPLACEMENT— Twogroupsoffemaleswerepairedtoasimilarnumberof“young-old”territorialand
“young-old”nontenritorialmalesrespectively. Copulationswereinterruptedatthe50* abdominal flexion.The
volumeofspermofbothgroups offemaleswas compared.
EFFECTOFDURATION OFSTAGEI ONSPERMDISPLACEMENT —Sixteen femaleswerepaired
andduration(insec)ofstageIwasrecorded.Oncetheflexionsthatcharacterisethisstage(foradetaileddescription
ofthisseeCORDOBA-AGUILAR,2000)werecompleted,pairingswereinterrupted.Thevolumeofsperm
wasmeasured and correlatedwiththedurationofthis stage.
EFFECTOFVARIATIONINTHE NUMBEROFABDOMINALFLEXIONSDURINGSTAGEION
SPERMDISPLACEMENT — Sixteenfemales werepairedand thenumberofabdominal flexionsoccurring
duringstageIwasrecorded. Thesepairingswereinterruptedsoonafterthey completedthis stage.The volume
ofspermwasmeasured and correlatedwithtirenumberofflexions.
Copulatingpairswerepreservedimmediatelyafterintemiptionin75%ethanol.Calculationofspermvolumes
(inmm3)wasasdescribedbyS1VA-JOTHY&HOOPER(1995).Onlyspermathecalspermvolumewasmeasured
sincethebursawasalwaysemptied(seealsoCORDOBA-AGUILAR, 1999).Tofulfilltheassumptionsofthe
parametricstatisticaltestsused,spermvolumesweretransformedusingtheformulalog(x+1).Means±standard
deviationsareprovided.
RESULTS
EFFECTOFMALEAGE — Femalespaired withthetwo groupsofmales(“young”
males,N = 8;“young-old”, N =7) showedno differencein storedspermvolumes
(females paired with “young” males = 0.050± 0.03 mm3; females paired with
“young-old” males= 0.047±0.03 mm3; t-test= -0.31,d.f. = 16,P =0.76).
EFFECTOFMALESTATUS(TERRITORIALANDNONTERRITORIAL) - Thevolumeof
spermoffemalespaired withterritorialmales (0.041 ±0.02mm3, N= 22) did not
differfromthatoffemalespaired withnonterritorialmales(0.048±0.02mm3,N=
22; t-test= -0.87,d.f. =39, P=0.39).
EFFECTOF DURATIONOFSTAGE I - Durationofstage I(98.1 ±9.7sec) was not
correlatedwithsperm volume(0.053±0.04mm3; N = 16, r =0.074,P>0.05).
EFFECTOF VARIATIONINTHENUMBEROFABDOMINALFLEXIONSDURING STAGEI
378 A.Cordoba-Aguilar
— No significantassociation was detectedbetweenthevolumeofsperm(0.05 ±
0.03mm3) andthenumberofstageIabdominalflexions (51.5 ± 7.8; N = 16,r =
-0.14,P> 0.05).
DISCUSSION
Inodonates, individualvariationin spermdisplacement ability hasbeenrelated
to several variables. Male age (SIVA-JOTHY, 1987), status (territorial or
nonterritorial;SIVA-JOTHY &TSUBAKI,1989;WOLF etal„ 1989)andcopulation
duration(SIVA-JOTHY, J987)appeartobeparticularly important. Inthesecases,
relatively old(SIVA-JOTHY, 1987)andnonterritorial(SIVA-JOTHY&TSUBAKI,
1989) males copulated for longer periods and displaced more stored sperm.
Experimental investigation ofthe roleofmaleage and status in C. h. asturica,
however,didnotexplain thevariationinstoredspermvolume.Thesamealsoapplies
forthedurationandthenumberofabdominalflexionsofthestageIofcopulation.
Therefore, independently ofwhetherholding aterritory, how old a maleis, how
long or how many abdominalflexions the stage I takes, spermathecal sperm
displacement ability doesnot change in individualmaleC. h. asturica.
MaleC. h. asturica displace spermathecal spermthrough genitalic stimulation
ofthefemalesensory system (CORDOBA-AGUILAR, 1999).Males perform a
seriesofapproximately 50abdominalflexions duringthespermdisplacementstage.
Theflexionsgeneratein-and-outaedeagal movements thatresultinstimulationof
the female sensory system that coordinates spermathecal sperm ejection.
Experimental evidencehasshownthatvariationinspermathecal spermdisplacement
isrelatedtothewidthoftheaedeagus (CORDOBA-AGUILAR.1999).According
totheresultspresented here,variationinsperm displacement ability seemsreliant
onlyonmaleaedeagal characteristicssinceotherpotential sourcesofvariationwere
discarded.
Spermathecal spermshows a reduction in volumealongside ofthenumberof
aedeagal flexions duringstageI(CORDOBA-AGUILAR,1999).Theresults show
thattherelatively variablenumberofflexionsattheendofstageI didnotaffectthe
volumeofspermathecal sperm displaced. Sincemaximumsperm displacement is
achieved at about 50 abdominal flexions, one explanation for this apparently
paradoxical pattern is that maleskeep performing stage Iflexions even though
maximumsperm displacement hasbeen already achieved.Theexceeding inmale
abdominalflexionswouldnot elicitanymoresperm displacement.This hypothesis
is being currently investigated.
Recentevidence supports thehypothesis thatanimal genitalia haveevolvedby
meansofsexual selection(EBERHARD, 1985, 1996;SIMMONS&SIVA-JOTHY,
1998; ARNQVIST, 1998).Ifthistrue, one prediction would bethat variationin
fertilisationsuccess willberelated to variationintheexpression ofthesexually-
-selectedgenitalictrait.Inthecaseofodonates,malegenitalia mighthaveevolved
SpermdisplacementinCalopteryxhaemorrhoidalisasturica 379
toreducethecompetition withothermales’ejaculates duringfertilisation(WAAGE,
1984):thosemaleswithahigherspermdisplacementabilitywouldachieveahigher
fertilisationsuccess. However,although variationinsperm displacementabilityhas
beendocumentedinodonates(SIVA-JOTHY, 1987;SIVA-JOTHY & TSUBAKI,
1989;WOLFetal., 1989),ithas not beenclearwhethersperm displacementability
was related to variationin male genital morphology. In fact, the most likely
explanation forthesecases is thatvariationinsperm displacement was dependent
oncopulation duration(however, seeANDRES &CORDERO, 2000fora case in
which,despitevariationinspermdisplacementability,therewas norelationbetween
copulationdurationandspermdisplacement). Theonlydocumentedcaseofvariation
insperm displacementrelated to variationingenital phenotypic expression is that
ofC.h.asturica(CORDOBA-AGUILAR, 1999):thewidertheaedeagus, themore
spermdisplaced. Isuggestmoreattentionhastobepaidtosimilarresearchavenues
inthe Odonatasinceitis unlikely thatthiswouldbe aunique case.
ACKNOWLEDGEMENTS
Iwanttoexpress my deepestacknowledgementtoM.T.SIVA-JOTHYforhis advicein allstagesofthis
study.A.CORDEROandJ.ANDRESprovidedinvaluable logisticsupport.A.Cordero andG.PRITCHARD
madecommentsthat significantlyimprovedthiswork. TotheDirection XeraldeMedioAmbiente(Xuntade
Galicia)forpermissionforthecollection ofanimals.Financialresourceswereobtained viaaPhDgrantbythe
ConsejoNacional deCienciayTecnologfa(CONACyT)oftheMexican government,the BritishCouncil, and
theSecretariadeEducacidn Publica(SEP-FOMES).
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