Signal function of wing colour in a polymorphic damselfly, Mnais costalis Selys (Zygoptera: Calopterygidae)

2006·1.3 MB·English

by  Hooper, R E

Odonatologica35(1):15-22 March I.2006
Signalfunctionof wingcolour
in apolymorphic damselfly, MnaiscostalisSelys
(Zygoptera: Calopterygidae)
R.E.Hooper¹S.J.Plaistow² andY.Tsubak*i
BiodiversityConservation ResearchGroup,National InstituteforEnvironmental Studies,
Tsukuba305-0053,Japan
1Nanoscale Function Group,SFIPhysics Department,TrinityCollege,Dublin 2,Ireland
2DepartmentofAnimal andPlant Sciences,UniversityofSheffield,Western Bank,
Sheffield S102TN, United Kingdom
ReceivedOctober21,2004 /RevisedandAcceptedAugust31,2005
Mnaiscostalis 33 exist in2formsspecialisedforthe demands of2 distinctstrat-
egies,territorial fighters andnon-territorial sneaks, which give approximatelyequal
fitnesspayoffs. Territorial 36 have orange wings,whereas typicalnon-territorial
33 areclear-winged.By simulatingagonisticencounters between 3 3 it is shown
that the2morphsshowed distinctresponses tothesignalfrom orangewings;territo-
rialorange-winged 3<5alwaystriedtoentercontests,whileclear-winged33always
avoidedthem.On theotherhand,the2morphsshowed similarresponses tothesig-
nalfromclearwings:bothmorphstriedtoattackmodels.Alsopresentedare‘painted
clearmodels’ which wereclear-winged33whose wingshad been paintedorange,
and bothmorphsrespondedasiftheywereorange-wingedmodels. These observa-
tions indicatethat 33 discriminate between fighterand sneakermorphsusingthe
colour ofwings, andshows differentstylesofagonisticresponses towardfighterand
sneaker morphs.Itislikely thatnon-territorial sneaks maygainanadvantagefrom
non-signallingbecause clearwingsincrease crypsis onanother 3 territory,increas-
ingtheirsuccessin stealingcopulations.No indication wasfound thatclear-winged
33 are9mimics,orthathavingclearwingsreducedthe levelofaggressiondirected
towardsthem byterritorial orange-winged3 3.
INTRODUCTION
Attempts to understandsignal function, andthe informationtransmittedby
a particular trait, ofteninvolvecorrelating variationin theexpression ofatrait
withotherknownfitnessparameters(e.g. QVARNSTROM etah, 2000). Exper-
*CorrespondingAuthor, e-mail:[email protected]
16 R.E.Hooper,S.J.Plaistow&Y.Tsubaki
imentalstudies havemanipulated the level ofexpression ofthe traitand then
recordedthe effect ofthe manipulation has on the reproductive success or fit-
ness of its bearer. An alternativeapproach is to study systems in which some
individualswithinthe population do not signal at all. Non-signallers may be
unableto pay the high social costs elicited by bearing a signal. Pigmented ar-
eas of plumage (‘badges of status’) are used to this effect in Harris’ sparrows
(Zonotrichia querula), enabling somemalestoavoidcostly aggression at feeding
sites (ROHWER, 1975). In these cases ‘non-signallers’ are likely to be inferior
individuals.However, in someother species not signalling maybe adaptive be-
cause it increasesthe success ofanalternative mating strategy. For example, in
crickets(Gryllus integer) signallingmalescallto attractfemales, andnon-signal-
ling malessilentlysearchforfemales(CADE, 1979).Ingenetically polymorphic
ruff Philomachuspugnax darkneckedresidentmales strongly repel otherdark
neckedmales,buttoleratethepaler submissivesatellitemales(LANK etah, 1995;
WIDEMO, 1998)whichenablessatellitemalesmoreopportunitytoobtainsneak
copulations.
Inthepolymorphic Mnaiscostalis (forlocalvariationofthepolymorphism, see
HAYASHI etah, 2004),malesecloseas oneoftwo morphs, whichwe call‘fight-
ers’ and‘sneaks’(TSUBAK1 etal., 1997).The development ofthetwo morphs
is genetically controlled(TSUBAKI, 2003). Fighters are territorial, defending
submerged pieces of deadwood intowhichfemalesoviposit, andpossess large
sexually selectedorangepatches ontheirwings andaredpterostigma atthewing
tip.Incontrast,sneakmalesarenon-territorialmales,havenoorangewingpatch
(although they do have the same red pterostigma), are smaller than territorial
malesTSUBAKI etal., 1997),andobtainmostoftheirreproductive success by
‘stealing copulations’ on othermales’territories.Females’wings are also clear,
butare distinguished from thoseof non-territorialmales by the presence ofa
whitepterostigma(HOOPERetal., 1999).Inadditionto thebehaviouraldiffer-
ences between the two morphs, previous studies havealso shownphysiological
differencesresulting froma selectivetrade-off:fighter males haveevolved spe-
cialisationstypically foundinterritorialodonatespecies, whilesneak maleshave
evolvedspecialisations typical ofnon-territorialodonatespecies (PLAISTOW&
TSUBAKI,2000). Theassociatedcostsandbenefitsofsuch differentspecialisa-
tionare likely to accountfordifferencesinreproductive lifespan,whichresultsin
thetwo strategies havingequal fitness (TSUBAKI etal., 1997).
Theorangewing colourin the territorial morph, unlikeinmost othercalop-
terygids (SIVA-JOTHY, 2000)varieswithnutrientlevelsandage,suggesting that
orangewings are costly to produce andmaintain(HOOPER etal., 1999).Thus
oneexplanation forwhy thesmaller clear-winged malesdo not produce theor-
angesignal is thatthey are avoiding theenergeticcostrequired to doso. Morph
fitnessis equal (TSUBAKI et al., 1997), and selection pressures are different
(PLAISTOW & TSUBAKI, 2000), suggesting that non-signalling may provide
Signalfunctioninapolymorphicdamselfly,Mnais costalis 17
additionalselectivebenefitsto clear-winged males.Therearethreewaysnon-terri-
torialsneaksmaygain anadvantage fromnon-signalling: (1) clearwings increase
crypsis on anothermales’territory, (2) clearwings enablenon-territorialmales
to mimicfemales, and/or (3) clear wings induceless aggression fromterritorial
orange-winged males.Thesehypotheses arenotmutually exclusive, howeverthey
can betestedseparately because they arerelated tothe aggressive responses oc-
curring atdifferentstagesofabehaviouralsequence:thefirst hypothesis iscon-
cernedwiththedetectionofconspecifics flying nearby, the secondis concerned
with morph recognition after detection,andthe thirdis a behaviouraldecision
madeaftermorph recognition. Inthisstudywemadefieldobservationsto assess
thefirst hypothesis, andwemeasuredtheresponseofthetwomorphs to control
andexperimental modelsofeach morph (orafemale), inorderto determinethe
functionoftheorange wing-spot andtestthesecondandthethirdhypotheses.
METHODS
STUDYSITEAND FIELDOBSERVATIONS. - Insectswereobservedatamountainwood-
land streamin Gozenyama,IbarakiPrefecture,Japan(36°33'N,140'17’E)in 1998. Inbothyearsall
adultspresentin,andentering,a20ra stretchwerecapturedandindividuallymarkedwith enamel
pens. Lefthind winglengthwastakenasameasureofbodysize.
BetweenMay24and July4 1998,wemadedailyfocal studies ofall individuals inthis stretchof
river,from 1200hrto 1500hr. Werecordedtheterritorial statusofeach male,andscored thenumber
ofcopulationseach secured.Individuals seenononlyonedaywereexcluded fromtheanalyses. Mat-
ingsuccessforeach individual ispresentedastheaverage number ofcopulationsobtainedperday.
MODELEXPERIMENTS.- Wegaugedtheresponse ofdifferentmorphstodifferent signalsby
artificiallyflyingdead malesmounted onwireinto orange-wingedmales’ territories,orintothe air-
spaceofperchedclear-wingedmales.Deadmales arehereafterreferred toas‘models’. Mountingthe
models onwiresallowed ustosimulatenatural flightpatternsbyvibratingthewire.In 1997,weused
three typesofmodel. ‘Realorange-wingedmodels’ weresimplydead orange-wingedmales mounted
onwire.‘Painted clear-wingedmodels’ wereclear-wingedmaleswhosewingshadbeenpaintedorange
with afelt-tippedartist’spen(Copic).The thirdtype,‘controlclear-wingedmodels’,weredeadclear-
wingedmales.We ‘flew’ themodels atthesubject male for30s andrecorded the amountoftime he
attacked themodel.Ifthesubjectmaleescalatedduringtheencounter, whichinM.costalisamounts
tosharpverticaljumps(NOMAKUCHIetal., 1984),wesimilarlyescalated the‘fight’ofthemodel.
Allmalesalongthe50mstretch ofriver weresubjectedto30s trialswitheachmodel,inarandom or-
der. Eachmalewassubjectedtothesamemodelonly oncebutwastestedwiththree differentmodels
unlessitdisappeared (afewclear-wingedmales disappearedafterthefirstorthesecond tests).We
allowedatleast 15minutesbetweensuccessivetrialsonthesamesubjectmale,andinthisexperiment
maleswereindividuallymarkedwith aseriesofcoloured dotsontheabdomen.
Anadditional experimentassessedtheresponse oforange-wingedmalesresidentonterritoriesto
adead female model,presentedmountedonwireinasimilarwaytothemale models.
18 R.E.Hooper,S.J.Plaistow&Y.Tsubaki
RESULTS
DAILY MATINGSUCCESS
Figure 1 shows the average
daily mating success of territo-
rial orange-winged males, non-
-territorialorange-winged males
andclear-winged males.Theav-
eragematingsuccess ofterrito-
rial males(2.27/day/male) was
higher than non-territorialor-
ange-winged males (0.28/day/
male) or clear-winged males
(1,25/day/male) (Tab. I). Non-
-territorial clear-winged males
Fig. 1. Average daily matingsuccessof territorial, showed higher mating success
non-territorial orange-wingedmales,andclear-winged than non-territorial orange-
male.
-winged males.
MODEL EXPERIMENTS
WeperformedanANOVAwithmodeltype(controlclear, painted clearandreal
orange)andmorph type(orange- orclear-winged male)as independent variables.
This enabledus to determinethe basis for the interaction.There was a highly
significant differenceinfight timewithrespect tomodeltype(Fig. 2):fighttimes
TableI
ResultofANOVA andFisher’sPLSD test fordailymatingsuccessofthree typesofmales (orange-
-wingedterritorial, orange-wingednonterritorial andclear-wingednonterritorial)
ANOVA
DF SS MS F P
Type 2 27.009 13.505 8.716 0.0007
Residual 42 65.073 1.549
Fisher’sPLSD
MeandifF. Critical diff. P
Clear,Nonterritorial orange 0.974 0.972 0.0496
Clear,Territorial orange -1.016 0.862 0.0220
Territorial,Nonterritorial orange -1,989 0.972 0.0002
Signalfunction inapolymorphicdamselfly,Mnaiscostalis 19
were longerwhen the
controlclear-winged
modelswere used(F,
= 12.65,/? <0.0001).
55
Therewas also a sig-
nificant differencein
fight time with re-
spect to morph type;
orange-winged males
fought more than
clear-winged males
(F, 55 = 8.11, p =
0.006). Andtherewas
a significant interac-
tion between model
typeandmorph type,
indicating differences
in fight timeof each Fig. 2.Time thatmales of each morphspentfightingeach ofthree
morph according to models that wereartificially flownatthem.There wasnosignificant
model type: clear- differenceinfighttimebyorange-wingedmaleswith respect tomodel
-winged males main- type,buttherewasforclear-wingedmales:clear-wingedmalesmainly
foughtagainstclear-wingedmodels.
ly fought the clear-
-winged model, whereas orange-winged males fought all model types (F =
2 55
5.75,p = 0.005).
Therewasnosignificant differenceinfighttimeaccording towhetherthemod-
elwas arealorange-winged male oraclear-winged malepainted orange(Fig. 2,
Orange male,paired ttest, t=0.124, df= 9,n.s.;Clearmale,l= 0.533, df= 18,
n.s.),suggesting thatthere was no perceived differencebetweenthe naturalor-
angecolourandthatof thepen,andthattheorangewingcolourwas thesignal
whichelicitedthefight response.
RESPONSE OFMALES TOFEMALEMODELS
In the experiment we conductedusing a deadfemale model, orange-winged
malesalwaysignored themodel(20/20times).
DISCUSSION
Therewas abehaviouraldifferencebetweenmales ofeach morph in theirre-
sponse to themodels: orange-winged males fought any modelbutclear-winged
malesonly fought modelsofclear-winged males.Clear-winged males invariably
fledwhenpresented withanorangemodel.Whenpresented toanorange-winged
20 R.E. Hooper,S.J.Plaistow& Y.Tsubaki
male,aclear-winged malemodelpainted orangeelicitedthesamefightresponse
as didareal orange-winged male. Display ofanorangewing probably signifies
‘I am afighter’ to conspecifics, whilst thegeneral appearanceofaclear-winged
male(the redpterostigma andthe bluebody colour) isaloneenough toelicitthe
fightresponse frombothmorphs. Theorangewing modifiesthe response(fight
or flight)oftheclear-winged morph.
Sinceorange-winged malestheyhaveresources to defenditisnot surprisingthat
they should fight morethan clear-winged males (NOMAKUCHI etal., 1984).
However, this does not explain why clear-winged maleswere prepared to fight
providing therewas noorangesignal. PLAISTOW&TSUBAKI(2000) showed
thatselectionfortraitsinfluencing flightability differsbetweenthetwo morphs:
compared to clear-winged males, orange-winged males have higher flightmus-
cleratiosand investmorein thebuild up ofmuscleandstoredfat. Thecurrent
study supports such a differentiationby experimentally confirming that they
show behaviouraldifferences to the same stimulus. A likely explanation, there-
fore, forthe divergent response ofthe morphs to a modelwithorangewings is
thattheorangewingsignals themale’s status as a territorial morph,andthator-
ange wings functionas anhonestindicatorofmalefighting ability (HOOPER
et al., 1999). Thetwo morphs haveevolved divergent adaptive behaviouralre-
sponses to this signal.
The adaptive significance of the non-territorialmorphs' 'flee' response to an
orangewing signal ofafighter maleis obvious, butitdoesnot explain why the
non-territorialmorph haslost, orneverevolved, orangewings. Since developing
andmaintaining anorangewing isenergetically costly (HOOPER etal., 1999),
it wouldaccrue no benefits to a malethatdoes not defendaterritoryand has
evolveda'non-fighting' strategy. Territorialorange-winged malesattackedclear-
-winged males, which suggests thatthe benefitclear-winged malesgetfromnot
signalling is notone ofavoiding aggression from orange-winged males.
Orange-winged males never attempted to engageclear-winged models in the
‘tandem’pre-copulatory grasp anddidnot showany interest infemalemodels,
suggesting thatthey do not confusethem forfemales.However orange-winged
males are occasionally seen in tandemwith clear-winged males in the field.In
naturalconditionsorange-winged malesdosometimesapparentlymistakeclear-
-winged males for females(WATANABE & TAGUCHI. 1990). Howeversuch
homosexualtandempairsoriginated usuallywhenmalesgrasped aclear-winged
male, whichhadalready in tandemwitha femaleon aperch. Thereseemslittle
confusionover sex whenthey are inair, suggesting thatthehypothesis of“mim-
icking females”is unlikely inthis species.
No directtestwas madeof thefemalemimicry andcrypsis hypotheses. How-
ever,weobservednon-territorialorange-winged malesoccasionally tryingtointer-
ceptfemalesarrivingatterritorialareas, butinmostcases they wereimmediately
chased away by residentmales. Incontrast, clear-winged malesoftensucceeded
Signalfunctioninapolymorphicdaraselfly, Mnaiscostalis 21
ingraspingfemalesbeforeterritorial malesfoundthem.Theloweraveragemat-
ing success ofnon-territorialorange-winged malescompared to that of clear-
winged males(Fig. 1) is probably due to theirconspicuous wing colour, which
maypreclude successful sneaky behaviouraround territories.
Thebenefitthatnon-territorialmalesgetfrom notdevelopinganorangewing
— asidefrom areduced energyexpenditure (HOOPER etal., 1999) — is prob-
ably derived fromincreasedcrypsis aroundorange-winged males’territories, or
inapproaching females.Thisidea is consistent withobservationsof thebehav-
iourofclear-winged malesonandaroundorange-winged males’territories(NO-
MAKUCH1 etal., 1984;TSUBAKI etal., 1997).
HOOPER etal.(1999)showedthataspectsofthepigmentationoforangewings
declinedwithmaleageandwereinfluencedbylevelsof nutrition,suggestingthat
orangewing pigmentation may honestly signal current condition.Costly traits
thathonestly signal anaspect of quality,such as condition, mayevolve andbe
maintainedby inter-sexual selection, intra-sexual selection, or amixtureofthe
two (ANDERSSON, 1994; BERGLUND et al., 1996).In territorialodonates
intrasexualselection is particularly important sincemale reproductive success
isoftendependent onobtaining aterritory (e.g., PLAISTOW&SIVA-JOTHY,
1996). Incalopterygids contests arebest describedas energetic wars ofattrition
inwhichthefattermalenormally wins(MARDEN& WAAGE, 1990;PLAIST-
OW&SIVA-JOTHY, 1996). Inthisstudy we foundthatterritorialmalesalways
engaged in aggressive interactions if they were challenged. In M. costalis also,
contestsbetweenorange-winged malesseems toberesolvedby energeticwars of
attrition, however, contests between orange-winged andclear-winged malesare
resolved by colour signalling: this signals works inanall-or-nothing mannerin
thissystem. Furtherwork willberequired todeterminewhetherany components
ofamale’swingpigmentation are usedincontests betweenfighter males.
ACKNOWLEDGEMENTS
YTwasfunded by agrant-in-aidfromthe JapaneseMinistryofEducation,Scienceand Culture
(no.08458168);REHbyanEUScienceandTechnologyFellowship;SJPby anAIRIESScienceand
TechnologyFellowship.
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