Sexual selection as the possible underlying force in calopterygid wing pigmentation: comparative evidence with Hetaerina and Calopteryx (Zygoptera: Calopterygidae)

2008·1.3 MB·English

by  Serrano-Meneses, M A

Odunatologica37(3):221-233 September1,2008
Sexualselectionas thepossibleunderlying
forcein calopterygid wingpigmentation:
comparative evidence
with Hetaerina andCalopteryx
(Zygoptera: Calopterygidae)
M.A.Serrano-Meneses¹,G.Sánchez-Rojas² andA.Córdoba-Aguilar³*
1DepartmentofBiologyand Biochemistry,University ofBath,Claverton Down,
Bath BA2 7AY, United Kingdom
2Centro deInvestigacionesBiologicas,Universidad Autonoma del Estado deHidalgo,
ApartadoPostal69-1,Pachuca,MX-42001 Hidalgo,Mexico
3DepartamentodeEcologiaEvolutiva,InstitutedeEcologia,Universidad Nacional Autonoma
deMexico,Apdo.Postal 70-275,MX-04510 Mexico,D.F.,Mexico
[email protected]
ReceivedMarch3,2006/ RevisedandAcceptedJanuary18,2008
Fivehypothesesfortheevolutionofconspicuous6 wingpigmentationhave been
proposed: sexual selection,differential niche utilisation,predatorwarning,social
badgeandecologicalcharacterdisplacement.Here,thesexualselection and ecologi-
calcharacterdisplacementhypothesesarecompared.First,thecoefficients ofvaria-
tion(CVs)ofpigmentationwerecomparedagainsttheCVsofaselected set ofother
animals'traitsthatareknown tobe maintainedbyeithernatural orsexualselection.
Hetaerina americana,H. vulnerata,Calopteryxaequabilis,C. haemorrhoidalis andC.
xanthostomawereused inordertocompare CVs.Second, it waspredictedthatpig-
mentation should not differin spp. whose populationsarein sympatry (compared
toallopatry)ifsexual selectionisdrivingtheevolution ofpigmentation(compared,
forexample,toanecologicalcharacterdisplacementhypothesisinwhichpigmenta-
tion between spp. should differ).Here,thepigmentationofsympatricand allopatric
populationsofH.americana and H.vulnerala werecompared.The studyproduced
2main results. First, the CVsof pigmentationwerenot different fromthe CVsof
sexuallyselected traitsinotheranimals;nevertheless,theyweredifferent fromthose
ofnaturallyselected traits.Second,thepigmentationofthe2spp. insympatry did
notdiffersignificantly.Thesamewastrueforallopatricpopulations.Taken together,
these resultssuggestthatsexualselection isthemain mechanism ofmaintenance of
*Correspondingauthor
222 M.A.Serrano-Meneses,G.Sanchez-Rojas&A.Cordoba-Aguilar
pigmentationin theseanimals.Otheralternative hypothesesfortheevolution ofpig-
mentation (differencesinhabitat useinboth sexes,warningtopredatorsby 66 and
ecologicalcharacterdisplacement)arediscussed inthe lightofthese results.
INTRODUCTION
Fivehypotheses havebeenadvancedtoexplaintheevolutionofexaggerated traits,
(i)Sexualselectionhypothesis. Thisis themostwidelyaccepted andwasoriginally
proposed by DARWIN(1871)to explainthedifferencesinmorphology, physiol-
ogy andbehaviourbetweenthesexes. Thesedifferencesare frequently observed
as exaggerated traitsexpressed by males. According to sexual selectiontheory,
two processes havepropelled the evolutionofmaleexaggerated traits:(1) male-
malecompetition oversexualaccess to femalesand(2) femaleschoosingamong
malesto fertilisetheireggs.
(ii)Differentialnicheutilisationhypothesis. Thesexes differin habitatuseand
hence this may have produced particular adaptations to certainenvironments
(ANDERSSON, 1994).Thismaybethecase, forexample,ifboth sexes differin
the places where they forage and haveevolved differenttraitsto copewithdis-
tinct needs(TEMELES etah, 2000).
(iii)Predatorwarninghypothesis. Thishypothesis suggeststhatmalesmaycom-
municateto theirpredators thatthey are difficulttargets viaconspicuous traits
thatpredators areable torecognise (BAKER &PARKER, 1979).
(iv) Socialbadge hypothesis. Ithasbeensuggested thatconspicuous traits(e.g.
colour) mayactas badges thatcommunicateanindividual’ssocialstatus to con-
specifics (ANDERSSON, 1994).Thesebadges wouldprevent unnecessary,po-
tentiallycostlyescalatedcontestsover theaccess toresourcesnotrelatedtosexual
reproduction or to females(reviewed by ANDERSSON, 1994).
(v) Ecological characterdisplacement hypothesis. Thisassumesthatexaggerated
traitsare species-specific traitsevolvedto distinguish membersofotherspecies
to prevent interspecific matings in zoneswhere the distributionoftwo or more
species overlap (BROWN& WILSON, 1956).
Sexualselectionhas been studied ingreat detailin Odonata, particularly the
Calopterygidae (reviewed by CORDOBA-AGUILAR &CORDERO RIVERA,
2005). Malesof mostspecies in this family develop specific wing pigmentation
patterns soon afteremergence(SILSBY, 2000). These patterns differfrom one
species toanother(forexample, aredbasalcolourationinHetaerinaandmetallic
black in Calopteryx)and they makemalesappearconspicuous. Once wingpig-
mentationhasbeendeveloped, malesestablishterritorieswherefemalesarriveat
forcopulation andoviposition (CORBET, 1999).Itis while defendingtheseter-
ritoriesthatwing pigmentation is apparently shownto conspecifics: (i)to males
during theflyingcontests fortheacquisition ordefenceof aterritory(suggested
by KOSKIMAKI et ah, 2004; RUPPELL et ah, 2005; CONTRERAS-GAR-
DUNOet ah, 2006), and(ii) to females during the pre-copulatory flyingcourt-
Sexualselection andwingpigmentationin Calopterygidae 223
ship(which isthecaseofCalopteryxonly; reviewedbyCORDOBA-AGUILAR
& CORDERO RIVERA,2005).
SeveralsourcesofevidenceinthegeneraCalopteryx(e.g. SIVA-JOTHY, 1999,
2000;CORDOBA-AGUILAR,2002;CORDOBA-AGUILAR etal.,2003; RAN-
TALAet al., 2000; ROLFF& SIVA-JOTHY, 2004; SVENSSON et al., 2004),
Hetaerina(GRETHER 1996a, 1996b;CONTRERAS-GARDUNOetal.,2006)
and Mnais (PLAISTOW& TSUBAKI,2000; TSUBAK1 & HOOPER, 2004)
strongly suggest thatmalewing pigmentation is sexually selected. Studieshave
shown thathighly pigmentedmales are usually the onesthatdefendaterritory
(e.g. GRETHER, 1996a, 1996b;SIVA-JOTHY,2000;CORDOBA-AGUILAR,
2002) andthey do it for longerperiods (e.g. GRETHER, 1996a, 1996b; COR-
DOBA-AGUILAR, 2002) compared to less pigmented males. The underlying
reason is thathighly pigmented malesusually have moremuscularthoracic fat
(CONTRERAS-GARDUNO etah,2006) andfewerintestinalparasites (SIVA-
JOTHY,2000;CORDOBA-AGUILAR,2002).Anumberofstudieshaveshown
that both variables are important in territorialcompetition. In termsoffat re-
serves,they providethenecessaryenergetic inputduringterritorialaerialcontests
(MARDEN & WAAGE, 1990;PLAISTOW& SIVA-JOTHY, 1996);inthecase
of parasites, they havea negative impact onfitness by affecting theelaboration
offatreserves, thereforereducing malelongevity (SIVA-JOTHY&PLAISTOW,
1999).Malepigmentationhasbeenalsoassociatedtofemalechoicesince indiffer-
ent Calopteryx species femalesprefer to matewithmalesthatexhibithigh levels
of pigmentation (S1VA-JOTHY, 2000;CORDOBA-AGUILAR,2002). Highly
pigmented malesactually end up having a higher lifetimemating success com-
paredto less pigmented males(CORDOBA-AGUILAR, 2002).
Sexualselection, however,maynotbethesoleexplanation forwingpigmenta-
tion in calopterygids. For instance, it is reasonableto accept thatadultfemales
andmales oftendifferin habitatuse(differential niche utilisationhypothesis).
Females, forexample, perch on trees or forage away fromthewater whilemales
staycloseto thewater,mainly todefendorto competeforaterritory(CORBET,
1999). Feeding canalso occur indistinctplacesbetweenthesexes. Thepredator
warning hypothesis may also apply given thatmales exhibit themselves during
territory defenceand alsobecause territoriesare usually openspaces whereac-
tivepredators, such as birds, canenter(e.g. KREBS &AVERY, 1984).Thesocial
badge hypothesis mayapply only ifmalesestablishcomplex socialgroupswhose
membersrespect the owners of otherterritories (TRIVERS, 1985). However,
this is unlikely to occur in calopterygids sinceterritory ownership follows des-
perado rules: non-territorial males obtainanextremely small numberof copu-
lations; thereforemaleswill fightuntilexhaustionifterritoriesare notavailable
(PLAISTOW&SIVA-JOTHY, 1996).Under thissystem, only thosemalesthat
havemorefatreserves willbe theonlyonesabletodefendaterritory(MARDEN
& WAAGE, 1990;PLAISTOW&SIVA-JOTHY, 1996). Fat reserves are corre-
224 M.A.Serrano-Meneses,G.Sanchez-Rojas&A.Cordoba-Aguilar
latedwithwingpigmentation, therefore, itispossible thatpigmentation commu-
nicatestheamountoffatreserves ofa givenmale(CONTRERAS-GARDUNO
etah, 2006). Finally, theecological characterdisplacement mayalso explain the
evolutionof wing pigmentation, sinceinterspecific matings and hybrids of dif-
ferentcalopterygid species havebeenobservedinnature (DUMONT etah, 1987;
LINDEBOOM, 1993).
Inthispaperweexaminethepotential ofsexualselectiontoexplain theevolu-
tionofpigmentation inthelightoftwopredictions. First,according to thesexual
selectiontheory, traitsthathaveevolvedviathisselectivepressure shouldexhibit
considerably large variationinexpression (whencompared tocharactersthathave
evolved via naturalselection, forinstance; ANDERSSON, 1994). Thispredic-
tion, unlikethepredictions ofthedifferentialnicheutilisationandtheecological
characterdisplacement hypotheses, assumes thattheproductionofpigmentation
is costly. This,however,is not thecaseforthepredator warninghypothesis, since
only malesin good condition wouldbeable toafford the production of costly
traitsto communicatetheirpredatorsabouttheirabilitytoescape(following the
handicap principle; ZAHAVI&ZAHAVI,1997).Thesecondpredictionisrelated
to theexpected patternofpigmentation differencesinallopatricversus sympatric
populations. Accordingto theecological characterdisplacement hypothesis,one
wouldexpect that populations (= pigmentation) of differentspecies should be
more differentwhen insympatry, sincethe risk ofinterspecific matingis higher
intheseplaces compared to allopatry (see anexample inWAAGE, 1975, 1979).
This difference, however, should not bethe case if sexualselection is operating
asmalesand femalesshould beabletorecognise non-conspecifics.
MATERIALAND METHODS
PIGMENTATIONMEASUREMENTSAND PHENOTYPICEXPRESSION PATTERNS -
Thefollowingspeciesandlocations wereused:C.aequabilisfromCanada in1999(N= 18),C.haem-
orrhoidalisfromSpainin 1998(N= 135),C. xanthostomafromSpainin 1998(N=28),H.americana
fromMexicoin2000 (N=30)and H.vulnerata fromMexico in 2000(N=24).Thefollowingcondi-
tionshadtobemetforthecollection: I) animalshadtobe sexuallymaturesothatpigmentationwas
already fully developed,and2) males had tocomefrom thesamepopulation,preferentially being
collected onthe samedayto avoid morphologicalvariation caused by seasonal differences(COR-
BET, 1999).Aftercapture, animals werestored in 70 %ethanol. Each individual wasthen placed
onapetri dish containingwaterfortwo hours fortissue rehydration.Waterwasremoved by plac-
ingevery individual onadrycloth atroom temperature.Wingswerecut offfromtheirinsertion to
thethorax,fixed onplasticacetates andsecured withtransparenttape.Drawingsofbothtotal wing
andpigmentedareaswereproducedforeveryindividual byusingastereomicroscopeequippedwith
adrawingtube(Zeissmicroscope, model Stemi SV6).Drawings weremademanuallyataconstant
distance onwaxed paper. The waxedcondition reduces variation in weightdue tohumidity.Cut
outsofthepigmentedandnon-pigmentedareaswereweighedusinganelectronicanalyticalbalance
(OHAUS, modelCT200;precision ±0.001 g).Thesedatawerelaterused to estimatethepercentage
wingpigmentationforeveryindividual. Asimilarmethodformeasuringpigmentationhasbeenused
inprevious studies andhas producedreliable results(seeCORDOBA-AGUILAR, 2002).Notethat
Sexual selection andwingpigmentationinCalopterygidae 225
this methodologyonlyusesdegreeofpigmentationbutotheraspects such ascolour intensity are
omitted.Thisapproachisvalidsinceitisknownthatthecolourintensityofthepigmentedpatchhas
nosexual function inthisspecies(CONTRERAS-GARDUNO etal.,2007).
We obtainedthecoefficient ofvariation (CV)forpigmentationareas.CVallows datatobecom-
paredasitisexpressed asapercentage (thelowerthe value ofCV,theless variation is exhibitedby
thedata,ZAR, 1999).WecomparedtheCVsofpigmentationwiththoseoftraits that haveevolved
bysexual and naturalselection fromother taxa. Thesedata weregatheredfrom different literature
sources(see Appendix 1and Appendix2 forafull list ofthese taxa and the traits used).We first
checkedforthedistribution shapeoftheCVsofnaturallyselectedtraits,which did not departfrom
normality(Kolmogorov-Smirnovtest, P =0.58).Usingthe meanand standard deviation ofthese
traits(p=4.51,<r= 1.87),wetransformed the CVsofpigmentationand those ofother traitsthat
have evolved bysexualselection inothertaxa,toastandard normal distribution (ZAR, 1999).With
thiscalculation we obtained Zscores (orunits ofstandard deviations) forthepigmentationCVs,
which allowedustotestwhether thesetransformedvalues,includingthoseofothersexuallyselected
traitsinother taxa (Fig, la),werelikelytobe found under thenormalcurveofnaturallyselected
traits(Fig. la).This wasdonebycheckingthecritical valuesoftheproportionofthenormalcurve
distribution instatistical tables (ZAR, 1999),which allowedusto obtaintheproportionofthenor-
malcurvethatliesbeyondagivenZscore.Forexample,ifthe P-valueofaZscoreofpigmentation
equalsorapproacheszero, itmeansthattheZscoreliesoutsidethenormal curve,thereforeexhibit-
ingavariation similartothatofsexuallyselectedtraits.
PIGMENTATIONVARIATIONIN ALLOPATRICANDSYMPATRICPOPULATIONS -
The followingspecimenswerecollected in 2000in Mexico: H. americana(N =20) fromJiutepec,
Morelos(allopatricpopulation),H.vulnerata (N =20)fromXalapa,Veracruz(allopatricpopulation),
H.americana(N=20) and H.vulnerata (N =20) from Jiutepec,Morelos (sympatricpopulations).
Thecollectingconditions werethesameasindicated above.Sincethemalesofallthesespeciesshare
similar patterns(aredbasal spotonthebasisofeach wing),theextentofpigmentationwasmeas-
uredasthe longitudinallengthofthe spot(fromthe wingbaseoutwards).The meanpigmentation
sizes ofallopatricandsympatricpopulationsweretestedusingt-tests.
Dataareprovidedasmeans±STDunlessstated otherwise.
RESULTS
PHENOTYPICEXPRESSION OFPIGMENTATION
TheCVsofpigmentation (C. aequabilis= 13.02%,C.haemorrhoidalis= 14.89%,
C. xanthostoma= 19.70%, H. americana= 14.44%, H. vulnerata= 13.06%) fell
outsidethecurve oftraitsshaped by naturalselection(Fig. lb), whichis similar
to thatwhichoccurs to sexually selected traitsin othertaxa(compare Figs la,
b).Thisexclusion was statistically significant inallspecies (Tab. I).
PIGMENTATIONINALLOPATRIC ANDSYMPATRICPOPULATIONS
Therewere no significant differencesbetween the lengths of the pigmented
patches inallopatric (f = -1.58, P=0.120) orsympatric populations (t =0.95,
38 3g
P =0.350).
226 M.A.Serrano-Meneses,G.Sanchez-Rojas&A.Cordoba-Aguilar
DISCUSSION
Our resultsindicatethatinaselectedsubset ofCalopteryxand Hetaerinaspe-
cies as representatives ofCalopterygidae, evidence supports a sexual selection
explanation forthe maintenanceof wing pigmentation, acommon traitshared
by mostmembersofthis family. Membersofthese two generahave beentradi-
tionally usedto testsexualselection assumptions and actually it ismainly from
Calopteryx whereevidenceforthistheory is stronger(reviewed inCORDOBA-
-AGUILAR & CORDERO RIVERA,2005). InCalopteryx andHetaerina, the
phenotypic expression of wingpigmentation ismoresimilarto theexpression of
thosetraitsthathavebeenshaped by sexualselection, ratherthanitis to theex-
pressionofthosetraitsshaped by naturalselectioninothertaxa.Notethatthelist
oftraitsweusedcame fromvery differentanimals(see Appendix 1 & 2).Given
this,andthelargesample ofspecies used, itisunlikely thatourresults are dueto
chance. Wealso testedwhetherpigmentation differedmorein sympatricthan in
Fig. la: Distribution of traits under natural and sexual selection in non-odonate species(see Ap-
pendix 1and 2respectively). The normalcurverepresentsthe distribution oftheCVs ofnaturally
selected traits andzerodenotesthemean.Numbersarestandard deviations.Note that upto 98%of
the valuesofthe CVsoftraitsundernatural selectionareincluded within + 3standard deviations.
Duetohighervariation,mostofthetraitsundersexual selection(invertedtriangles)falloutsidethe
normal distribution curveandmorethan 3standard deviations awayfromthemean(exceptforthe
extremevaluenoted byanasterisk). — Fig.lb:Normal distribution curveofthe CVsoftraitsunder
the influence ofnatural selection.Zero denotesthemean;numbersarestandard deviations. Inverted
trianglesrepresenttheZscoresoftheCVs ofpigmentation.
Sexualselection and wingpigmentationin Calopterygidae 227
allopatricpopulations. Weassumedthatinsympatricpopulations, theexpression
ofpigmentation shoulddifferconsiderably amongspecies ifaprocess ofecologi-
cal characterdisplacement was acting on the pigmentation patterns. Contrary
to this process, wefoundthatthepigmentation size inthetwo Hetaerinaspecies
didnot differinsympatric or allopatric populations. Thisclearly meansthat, if
ecological characterdisplacement isoperating, theselectedtraitthatmalesand/
or femaleswill recognise is not thepigmentation.
For ourfirst prediction (the phenotypic expression of wing pigmentation, see
Introduction), webelieve it is unlikely thatthe differentialniche utilisationhy-
pothesis provides anexplanation toourresults, mainlybecausetherewouldbeno
pointin producing amaletrait thatis very costly. Also, although mature males
andfemalesoftenoccupy differentareas, teneralandfullymaturenon-territorial
malesmayalso forage away fromterritories(KIRKTON& SCHULTZ,2001),
inareas wherefemalescanalso befoundforaging. Thepredator warning hypo-
thesis may apply as long as pigmentation has evolved to become an honest
characterthatnotallindividualsareabletoproduce, so thattheinformationpro-
videdtopredators is aguaranteethattheanimalisabletoescape ifchased. The
likely predators ofmost dragon-anddamselfliesarebirdsandother insectsthat
areactivelysearching forprey(reviewedby CORBET, 1999).Giventhatpigmenta-
tioncorrelateswithfatreserves (sothatmaleswithmorepigmentation candevote
moreenergyto flying (CONTRERAS-GARDUNO etah, 2006)), it ispossible
thatmorepigmented malesare better atevading a predator. This, however, has
notbeen tested.Thishypothesis assumes thatpredatorsforageonlywheremales
arepresent. Althoughthereisevidencethatsomebirdspecies specialize ineating
odonates(e.g. KENNEDY, 1950;BAGG, 1958),to ourknowledge, nostudy has
documentedamalebias in dragonfly predation by thesepredators.
Ourresultsare incompatible withtheecological characterdisplacement hypo-
thesis.Otherstudies inH.americanahavesuggested thatmalesuse thepigment-
edpatch when competing over territories.Thesestudieshave foundthatmales
withmorepigmentation aremorelikelytowinfights(KOSKIMAKI etah,2004;
TableI
Coefficients ofvariation ofwingpigmentation,Zscoresand theproportionofthe areathatlies
beyondthese scores.P values reflecthowlikely itisthattheexpression ofpigmentationvaluesfall
outsidethedistribution ofnatural selection characters
SSppeecciieess CCVVssooffWWPP ZZSSccoorree PP
CCaalloopptteerryyxxaaeeqquuaabbiilliiss 1133..0022 44..5533 PP<<00..000011
CCaalloopptteerryyxxhhaaeemmoorrrrhhooiiddaalliiss 1144..8899 55..5533 PP<<00..000011
CCaalloopptteerryyxxxxaanntthhoossttoommaa 1199..7700 88..0099 PP<<00..000011
HHeettaaeerriinnaaaammeerriiccaannaa 1144..4444 55..2299 PP<<00..000011
HHeettaaeerriinnaavvuullnneerraattaa 1133..0066 44..5555 PP<< 00..000011
228 M.A.Serrano-Meneses,G.Sanchez-Rojas&A.Cordoba-Aguilar
CONTRERAS-GARDUNO etal.,2006). Thispossibly meansthatcombatants
recogniseeachother’sfighting potential basedontheinformationtransmittedby
thepigmentation sizepatterns(seeSERRANO-MENESES etal.,2007). On the
otherhand(and contrary to thisrecognition idea),recent work on C. virgoand
C. splendens hasshown that,when insympatry, the formerspecies can bemore
aggressive towards the latter, oftendisplacing it (TYNKKYNEN etal., 2004).
Aggression ismoredirectedagainst C.splendens males,sincemalesofthisspecies
exhibitlargewingpigmentation spots thatresemblethepigmentation patternsof
C. virgo.This lack ofrecognition of heterospecifics issomehowsimilarto what
WAAGE(1975, 1979)has detectedin C. maculataand C. aequabilis.where fe-
malepigmentation was differentinsympatric situationscompared to allopatric
situations.Paradoxically, itis femalesand not males thathaveevolveddifferent
pigmentation patternstoavoidinterspecific matingssomaleswoulddiscriminate
among homo-and heterospecific females. Interestingly, evidence from C. xan-
thostomamalessuggests thatthey are ableto recognize femalemates from non
mates(HOOPER, 1995).In ©donates,in general, itis not clearwhether, andto
what extent,males canrecognize homo- andheterospecifics since itseems that
notall species havethisability(even in species withinthesame genus;reviewed
by CORBET, 1999). Given the potential costs of unnecessary fights by males
andof matings withfemales, this fielddeservesfurtherresearch. What seems a
reasonablesuggestion fortheoriginofpigmentation withrespect to theecologi-
cal characterdisplacementhypothesis, is thatpigmentation, given itsproduction
costs, arose viasexual selectionand possibly is nowbeing shaped by otherevo-
lutionary forcessuch as the interspecific male-maleaggression observed in Ca-
lopteryx (TYNKKYNENetal.. 2004,2005).
Finallyitshouldbenotedthatourpigmentationmeasurementshavebeenbased
on size only. However, given the factthat odonatescan seeultravioletpatterns
(CORBET. 1999), thepotential exists for using this as a mean forcommunica-
tionandthis deservesfurtherinvestigation.
ACKNOWLEDGEMENTS
ThanksareduetotheRoyalSocietyandAcademia Mexicana deCiencias foragrantprovidedto
AC-A, forashort visit totheUnited Kingdom.
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