Maintenance of polymorphism in the orb weaving spider species Agalenatea redii (Araneae, Araneidae)

2012·5.4 MB·English

by  Catherine Geay

ArachnologischeMitteilungen43:51-57 Nuremberg,July2012
Maintenance of polymorphism in the orb weaving spider species Agalenatearedii
(Araneae,Araneidae)
CatherineGeay,Raymond Leborgne,Olivier Francois&Alain Pasquet
doi:10.5431/aramit4310
AbstractiThemaintenanceofpolymorphismwithinpopulationsmaybetheconsequenceofseveralelementsof
specieslifehistorysuchasuseofspace,activityrhythms,predation,parasitismandreproduction.Thepresentstudy
focusesonthelatteraspectusinganorbweavingsp\der,Agalenatearedii,whichpresentsfivedifferentmorphsof
theopisthosomapatternintheadultstage.Overthecourseoffouryears,from2008to2011,adultspiders(males,
femalesandpairs)wereobservedatdifferentsites.In2011,wealsoconductedasix-weeksurveyofasinglepopu-
lation,observingthe numberofspidersofeach morph andthe morph ofpaired spiders.Wecollectedfield data
onthespatial andtemporal distribution ofspiders based on theirsexand morph.Using a distanceanalysis,we
comparedthefielddistributionwithasimulatedoneinwhichpairswereassociatedatrandom.Theresultsshowed
thatalthoughtherewerechangesovertimeand spaceintheproportionsoffemalesofthedifferentmorphs,as
wellas intheproportion ofthepairassociations,pairing accordingto morphs probablyoccursatrandom.
Keywords:colourpattern,fielddata,mating,orbweaver
HUXLEY (1955) defined polymorphism as the dependedonaninteractionbetweenhabitatstructure
existence of at least two different phenotypes in a andpredatorpressure.Theimportanceofpredationin
population whose rarest form is too frequent to be favouring the rarer morphs has also repeatedlybeen
solely a consequence ofrecurrent mutations (GRAY shown,forexample inLutianusgriseus(REIGHARD
&MCKINNON2007).Polymorphismcanbefound 1908)orin Cepaeahortensis(CLARKE1962).Another
inmanyspecies such as the mollusc Cepaeanemoralis factoris linked to differences in reproductive behav-
(COOK2007),theanuranBufocanorus(HOFFMAN iourandmatechoice,whichmaintainpolymorphisms
& BLOUIN 2000), the spider Enoplognatha ovata {Cepaeanemoralis, CAIN &SHEPPARD 1950, 1954;
(HIPPA &OKSALA 1981) and in females ofmany guppies Poecilia reticulate, GRAY & MCKINNON
damselfly species (ROBERTSON 1985, CORDERO 2006) often consisting of morphological variation,
1992, CORDERO etal. 1998,ANDRES etal.2000). for example in colouration (ANDERSSON 1994).
The number of morphs can be limited, such as in One ofthegreat,persistingissues in ecologyand
melanic moths (MAJERUS 1998) or large, as in the evolution are the numerous cases ofpolymorphism
meadow spittlebug, Philaenus spumarius (HALKKA linked with colour morphs. Indeed, many natural
&HALKKA 1990); aphenomenon called exuberant colourpolymorphismshavebeenshowntobecaused
polymorphism (OXFORD 2009). by non-selective processes such as migration and
Many theories have been put forward to explain dispersal (DEARN 1984, KING &LAWSON 1995,
&
theevolutionandmaintenanceofpolymorphism.For REILLO WISE 1988), or genetic drift and local
instance, spatial and temporal habitat heterogeneity population bottlenecks (BRAKEFIELD 1990).
has long been known to promote phenotypic and Our study was conducted on the spider species
genetic variations (FULLER et al. 2005). BOND & Agalenatearedii,whichpresentsfivedifferentmorphs:
KAMIL (2006) used digital moths preyed upon by a,Y,Ö, 8 and^(Fig. 1) inboth sexes.The aim ofthis
realbirdstoshowthattheevolutionofpolymorphism studywas to evaluate over several years the mainte-
nance and stabilityofthe polymorphism in different
CatherineGEAY,RaymondLEBORGNE,AlainPASQUET,Universite spider populations using their temporal and spatial
deLorraine,FacultedesSciencesetTechnologies,Laboratoire distribution. First, a multi-annual studywas carried
«ExpressionetEvolutiondesComportements».B.P.239-54506 out on different sites to test if polymorphism was
VandoeuvrelesNancyCedex-France
OlivierFRANC^iOIS,UniversitedeLorraine,FacultedesScienceset maintained across space and time. Afterwards, the
Technologies,lECN,UMRCNRS7502.B.P.239-54506Vandoeuvre study ofa breeding season was carried out to deter-
lesNancyCedex-France mine whether there was a differential emergence of
Correspondence:[email protected]
morphs during a season limiting the possibility of
submitted:6.12.2011,accepted: 19.4.2012;onlineearly:31.7.2012 morphpairing.Finally,adetailed studyofthe spatial
52 C.Geoy,R.Leborgne,A.Pasquet&O.Francois
distribution ofindividuals at a single site was done Dynamics ofthe population
to test whether aggregation could contribute to an Multi-annualstudy
increase in the probability of meeting and repro- Datafrom severalpopulations oiAgalenatea redii
duction ofthe different morphs. We calculated the studied from 2008 to 2010 at different sites in the
frequency ofpaired individuals according to morph areaofNancy(Meurthe-et-Moselle,France,48°41’N,
and sexin the different experiments.We also looked 6°17’E,272 m a.s.l.)were compiled.These dataena-
at pair composition (homomorph or heteromorph) bled us to characterize dynamics ofthe population
andwe testedwhether or not the frequencyofthese according to the sexes, morphs and pairs (by distin-
pairsfittedarandomtheoreticaldistributionofspider guishing homomorph from heteromorph pairs). For
pairs. these studies,two spiders (one male andone female)
were considered as forming a pair when they were
Materialandmethods both present at the same time on the same stem and
Biological model less than 3 cm apart,which is the mean distance be-
Agalenatea redii is an orb-weaving spider, whose tween a male and a female (there was no direct link
geographical distribution extends across the whole with potential fertilization) (personal observations).
ofEurope (JONES 1990).This specieshasanannual In2008 foursiteswere surveyed (numberofspiders;
biologicalcyclewithpost-embryologicaldevelopment N1 = 207). In 2010 three sites were surveyed (N2
spread over the entire year: eggs are protected in co- = 399). In 2011 only one site was examined (N3 =
coons,theyarelaidattheendofspringandtheyoung 551). Visual hunting was the method employed to
spidersremainintheeggsacsatjuvenilestages(often spotandidentifyspiders,whilebeingcarefulofallthe
mm
sub-adult) during winter. The adults (5.5 to 7 supports (drystems ofvegetation) usedbyspider.At
for females and 3.5 to 4.5 mm for males, ROBERTS thebeginningofspringthegreenvegetationhad not
1996) have a short appearance time that generally yetgrownandonlythedrystemsofthepreviousyear
starts at the beginning ofspring with reproduction, remained,whichallowedustosearchexhaustivelyfor
andends earlyinthe summerwhenthe eggs arelaid. spiders.
This spider is characterized by a polymorphism of
the dorsal pattern on the opisthosoma. Five morphs Singlebreedingseasonstudy
are present in both males and females (a, Y> Ö, 8, Q For this study, we surveyed one site during the
(Jones 1990) (Fig. l). reproductive period (from March 28^^ to May 6^^,
Fig.1:Schematicrepresentationofmorphsobservedinthespec\esAgalenatearedii{from Deom 1996).
Polymorphisminanorb-weavingspider 53
2011).Twotransects(26and28m,respectively)were ofmorphxamongthemales atlocationzandperiod
performed in the field using a string to mark them. tandthefrequencyofallfemales (pairedoralone) of
The spiders were located on vegetation in a strip of morphyamongthe females atlocationzand period
one meter on either side ofthe transectlines. t.The theoretical number (N^j^xyz morphxand
y pairs, at location z and period t, was estimated by
Spatial distribution ofthe spiders theproductoftheirfrequency(f^^xyz total
On the site ofthe 2011 survey, a positional map numberofpairs atlocationz and period t.
of)the spiders was constructed on March 22nd for a According to this calculation, the theoretical
rectangular area (10 m * 26 m), divided into units of number is the null hypothesis and is the
one square meter. Spiders were located and morph number ofmale morph x and female morph y pairs
andsexwerenoted.Thepositionofeachindividualor among the males at location z and period t. The
eachpairwasenteredintothecomputertodetermine test was done using a distance calculation with two
the spatialdistancesbetween the individuals and the methods: the firstbycalculatingthe square distance:
type ofdistribution.To do this, a dispersion index I
(basedontheindexofFISHER 1922)was calculated (1) ^4= 2x,y,z,t (NobsX,y,z- Nthx,y,z,t)^
based on the map distances: and the second by calculating the absolute value of
us^x distance:
(1)
(2 X=S(i,„^)X/n, (^ 2^)ad=-2^x,y,z,tJIN.obsx,y,z-N,thx,y,z,tIi.
wherex- is the numberofindividuals ofmorphi and One hundred thousands simulations were carried
s is the numberofdifferentmorphs in allthe nunits out on each distance. For each simulation in every
ofthe surveyed area, locationz,ateveryperiodt,the males andfemalesof
locationzandperiodtmatedrandomly.Wecalculated
(3) the number N ofsimulations in which the distance
A
test of threshold significance was performed (at
a=5%) and compared to the Chi-square table:
(p=0.05,df=59)=77.93and2C(p=0.95,df=59)=42.34).
Two conditions were then checked: T(number of
units (n) -1)>2^ if the distribution is aggregative
and T(numberofunits (n) -1)<A^ ifthe distribution
is uniform. The type of distribution can provide a
clue to the pairing. Ifthe distribution is uniform it
means thatpairingis random,but ifthe distribution
is aggregativeitsuggeststhatpairingmaynotbe due
to chance.
Statistical analysis
The relationship between the various morph pro-
portions for males, females and pairs were analyzed
based on the 2008/2010/2011 data. The temporal
follow up ofa 2011 population was evaluated using
a Monte Carlo method (METROPOLIS &ULAM
1949)specificallyprogrammedforthisstudy.ThenuU
hypothesiswas:ateachperiodandeverylocation,the
male morph is independent ofhis female partner’s
morph. The statistical test employed looks like the
Chi-square test ofindependence. It differs from the
latter in the following points. The theoretical fre-
pqauiersn,cayt(lfo^^ca^tioPnzofamnadlpeermioordpthwaxsanesdtfiemmaatleedmwiotrhpthhye Fia(gBc.)c2om:roCdrhipanhgnsgteo(sftrhionemtytheheaerplroefoftpootbrostetirhovenartoiifgohfnte:m(manolurempb(hAe)sra(onafd,cyam,paöt,lueer,ed
productoftheentiremalefrequency(pairedoralone) spidersonthegraph).
54 CGeay,R.Leborgne,A.Pasquet&O.Francois
between the random distribution ofthe simulation
and the theoretical distributionwas greaterthan the
distance between the real distributions observed in
the wild and the theoretical distribution. The test’s
levelofsignificancewasthenN/lOOOOO.Thedifferent
frequencieswere comparedwith a Chi-square test.
Results
Multi-annual study
Ratioofmalesandfemalesofdifferentmorphs
The distribution of morphs over the years ap-
peared to be the same for the males (Chi-square
test,JP=9.66; df=8; p=0.29) but not for the females,
Fig.3:Frequenciesofhomomorphand heteromorph pairs(%) which varied everyyear (Chi-square test,J\^=41.14;
observedovertheperiod2008-2011 (numberofspiderpairs df=8; p<0.01). Indeed the ratio ofmorphs amongst
onthegraph). females fluctuated between 2008-2010 (Chi-square
test, 2C=14.57; df=4; p<0.01), 2010 -2011 (Chi-
squaretest,2(^=32.17;df=4;p<0.01),and2008-2011
(Chi-square test, 10.28; df=4; p<0.05) (Fig. 2).
Proportionofheteromorphandhomomorphpairs
ofspiders
Over the three years (from 2008 to 2010), the
divisionbetweenhomomorphandheteromorphpairs
didnotdiffer(Chi-squaretest,J\^=4.22;df=2;p=0.12)
(Fig. 3). Furthermore, the Monte Carlo simulations
showedthattherewas no significantdifference from
a random association ofthe two morphs, based on
theirfrequencies in the population (N=100000 runs,
square distance (sq): p=0.61; absolute distance (ad):
p=0.72).
Single breeding season study
Proportionofmalesandfemalesofdifferentmorphs
The ratios ofmorphs amongthe females did not
vary according to the observation dates (Chi-square
test, 2C=19.34; df=28; p=0.89). The same pattern
was witnessed among the males (Chi-square test,
^=22.56; df=28; p=0.75) (Fig. 4).
Proportionofheteromorphandhomomorphpairs
Fig.4:Changesovertimeintheproportionoffemale(A)and ofspiders
male(B) morphs(numberofspidersonthegraph)duringa The distribution ofthe heteromorph and homo-
reproductiveseasonsurveyin2011. morphpairswasindependentofthedate,andthusof
Tab.1:Resultsofthesimulationsbydateforthepairsobservedonfieldtransectsandaccordingtotheproportionofeach
morph ineach pair.
Date ofobservation in 2011
probability 28/03 01/04 06/04 11/04 15/04 20/04
square distance (sq) 0.36 0.48 0.57 0.81 0.094 0.11
absolute distance (ad) 0.36 0.34 0.37 0.72 0.32 0.14
Polymorphisminanorb-weavingspider 55
A
3 1 (from 2008 to 2010). similar resultwas found for
the damselflies Ischnuragraellsii (CORDERO 1992),
Ceriagrion tenellum (ANDRES et al. 2002), and for
Ischnura ramburi (ROBERTSON 1985), where it was
observed that males matedwith females atrandom.
InAgalenatearedii,malesremainedwithsub-adult
or adult females before mating and also some days
after (personal observations), as in Zygiella x-notata
&
(BEL-VENNER VENNER2006).Ourstudyofmale
distribution(allmorphstogether)showedanaggrega-
tive distribution.This male distributioncouldreflect
thepresenceofafemalesignal(pheromones,dragline
Fig.5:Proportionofhomomorphand heteromorph pairs(%) cues)usedtolocatethem.However,iftheencounters
observed in2011 withthenumberofspidersonthegraph. were at random, these signals would not be specific
to morphs.
the timewithin the reproductive period (Chi-square Severalhypotheseshavebeenproposedinthelit-
test, X^=6.65; df=7; p=0.51) (Fig. 5). Moreover, the eratureto explainthemaintenance ofpolymorphism
simulationshowedthattheobservedpairdistribution indifferentspecies.Itcouldbegenetic,suchasinthe
accordingtotheproportionofspidersdidnotdiverge spidersEnoplognathaovata(OXFORD 1983,2009)or
from a random distribution for all dates (N=100000 Pityohyphantesphrygianus (GUNNARSSON 1987). In
runs, square distance (sq): p=0.44; absolute distance this case the preservation ofmorphs that showed a
(ad): p=0.28) or for each observation dates (p>0.05) low frequency in the population could be due to an
(Tab. 1). effect ofgenetic drift (OXFORD 2005).This did not
seem to be the case inAgalenatea redii, because dif-
Spatial distribution ofspiders at a site ferentmorphswere maintained overtime and space.
The spatial distribution ofall individuals (males Non-selective processes, such as dispersal and
and females all morphs together) in the sample site migration (FORD 1975, KIMURA 1983), maycause
appeared aggregative (I*(n-1)=85.7). The same was polymorphism. Our studywas conducted on differ-
true for the spatial distribution ofthe males (F(n- ent populations separated by several km from each
1)=91.7) although that ofthe females appears to be other.Theywerenotisolatedpopulations.Therewas
random (F(n-l)=71.7). a continuum between the different populations, so
exchange ofindividuals between study populations
Discussion by emigration/immigration processes was possible.
This studycarried out a spatio-temporal description However, there is no reason to expect that morphs
ofpolymorphismintheorbweavingspider,Agalenatea havedifferentdispersalproperties,andsodifferential
redii.Thefirstresultwasthatmorphswerenotequally emigrationisnotlikelytoexplainthemaintenanceof
probablewithin apopulation. Indeed one morph (a) polymorphism inAgalenatea redii.
predominatedinbothmalesandfemales.Thesecond Another hypothesis is the preference for a male
result revealed that morph distribution was stable morph as in the ladybird Harmonia axyridis where
over time for males and females, at least during one females showamale morphpreference in relation to
reproductive season. The difference of distribution the season (UenO et al. 1998).Therefore, polymor-
between the female morphs observed during these phismwouldbetheconsequencesofdirectionalsexual
three years could be due to the absence in 2010 of selection that would change with time. In our case
particular low frequency morphs. This information the frequencies ofthe morphs remained stable over
supported, however, the idea ofthe maintenance of thereproductiveseason,whichmakesthishypothesis
polymorphism in this species. unlikely.
Thecomparisonsoffielddataonmorphfrequen- Polymorphism may be part ofan alternative re-
cies with random morph associations showed that productive strategy. Forexample, one morph maybe
pair distributions depending on available morphs less attractive-butmore competitive-thananother
did not differ from field distributions either during (Kingstonetal.2003).FinCKE(1994)suggestedthe
a reproductive period (2011) or over several years hypothesisthatpolymorphismcouldbemaintainedby
56 C.Geay,R.Leborgne,A.Pasquet&0.Francois
amechanismofnegativefrequency-dependentselec- BrAKEFIELD pm. (1990): Genetic drift and patterns of
tionandthiswastestedbyFITZPATRICKetal.(2007). diversity among colour-polymorphic populations of
Thishypothesisimplies thattherarermorphshave a thehomopteranPhilaenusspumariusinanislandarchi-
higherphenotypicaptitudebyavoiding,forexample, pelago.-BiologicalJournalofthe Linnean Society39:
t1h9e99c)o.stIsnoofthaerlownogrdcso,puallaetsisopnre(vVaAilNinGgOmoSrSpUhMcaent bale. Cai2pno1l9y-A.m2Jo3.r7p&-hidcPoiMl:a.n1d0S.s1hn1ae1ipl1p/Cjae.rplad0e9a(51-n98e53m0o1)r2:a.l1iS9se.9l0e-.cttHbie0orn0e5di1in3t.ytxh4e:
less appealing, but more reproductively competitive 275-294-doi: 10.1038/hdy.1950.22
and consequently have higher reproductive success
(COOK et al. 1994, KINGSTON et al. 2003), and CaiCnepAa.eJa..&-PG.eMne.tiSchse3p9p:a8r9d-1(116954):Naturalselectionin
polymorphisminapopulationcanbestableonlyifall Clarke B. (1962): Balanced polymorphism and the
t(hFeIpNrCesKeEnt1m9o9r4,phBsIsZuEpp&orRtOeUquLalIsNel2ec0t0i7v)e.advantages Tdiavxerosnitoymoyfasnydmpagteroigcrasppheyc.iesS.ysItn:emNatiiCcHsOALsSsoDc.ia(teido.n)
To conclude, our results did not allow us to elu- Publication, Oxford. Pp. 47-70
cidatemechanismsbywhichpolymorphismismain- Cook L.M. (2007): Heterosis in Cepaea. - Biologi-
tainedmAgalenatearediipopulationsandhypotheses cal Journal of the Linnean Society 90: 49-53 - doi:
remain to be tested. Thus, we have to study the 10.1111/j.l095-8312.2007.00710.x
behaviour andperformance ofthe males ofdifferent CookS.E.,J.G.Vernon,M.Bateson&T.Guilford
morphs based on their pairing with homomorph or (1994): Mate choice in thepolymorphicAfrican swal-
heteromorph females. lowtail butterfly, Papilio dardanus: male-like females
may avoid sexual harassment.-Animal Behaviour 47:
Acknowledgements 389-397-doi: 10.1006/anbe.l994.1053
This study was carried out with the financial support of Cordero A. (1992): Density-dependent mating success
the University ofLorraine. We thank Ms. Karen Muller and colour polymorphism in females ofthe damselfly
who helps us during the field collection ofthe data. We Ischnuragraellsii(Odonata: Coenagrionidae).-Journal
also thank Dr. Nicolas Chaline for his helpful comments ofAnimalEcology61: 769-780
onthe textandforthe Englishtranslation. CorderoA.,S.S.Carbone&C.Utzeri(1998):Mating
opportunities and mating costs are reduced in andro-
References chrome female damselflies, Ischnura elegans. - Animal
AnDERSSON M. (1994): Sexual selection. Princeton, NJ: Behaviour55: 185-187-doi: 10.1006/anbe.l997.0603
PrincetonUniversityPress. 624pp. DeARN J.M. (1984): Colour pattern polymorphism in
Andres A.,R.A.Sänchez-Guillen&A.Cordero the grasshopperPhaulacridium vittatum I. Geographic
RiverJa. (2000): Molecular evidence for selection on variation in Victoria and evidence ofhabitat associa-
female color polymorphism in the damselfly Ischnura tion.-AustralianJournalofZoology32:239-249-doi:
graellsit. - Evolution 54: 2156—2161 - doi: 10.1111/ 10.1071/Z09840239
j.0014-3820.2000.tb01258.x DEOMP.(1996):Lepetitguidedesaraigneesätoilesgeo-
Andres A.,R.A.Sänchez-Guillen&A.Cordero metriques, lerepartie.-LaHulotte 73: 1-35
J.
Rivera (2002): Evolution offemale colour polymor- FINCKE O.M. (1994): Female colour polymorphism
phism in damselflies: testingthe hypotheses.-Animal in damselflies: failure to reject the null hypothesis.
Behaviour63:677-685-doi: 10.1006/anbe.2001.1948 - Animal Behaviour 47: 1249-1266 - doi: 10.1006/
BEL-VeNNERM.C.&S.VENNER(2006):Mate-guarding anbe.1994.1174
strategies and male competitive ability: results from a Fisher R.A. (1922): On the mathematical foundations
fieldstudyinanorb-weavingspider.-AnimalBehaviour oftheoretical statistics. - Philosophical Transactions
71: 1315-1322-doi: 10.1016/j.anbehav.2005.08.010 ofthe Royal SocietyofLondonA222: 309-368-doi:
BizcEolPo.u&r-pao.lyRmOoUrLpIhiNc(s2p0e0c7i)e:s:Seaxrueavliseewleocftieoxnpienrigmeennettailc Fit1z0p.a10t9r8i/crkstMa..Jl.9,22E..00F09eder, L. Rowe & M.B. So-
studies andperspectives.-JournalofEthology25: 99- KOLOWSKI (2007): Maintainingabehaviourpolymor-
105-doi: 10.1007/sl0164-006-0006-z phism by frequency-dependent selection on a single
BondA.B.&A.C. Kamil (2006): Spatialheterogeneity, gene.-Nature447:210-213-doi:10.1038/nature05764
predatorcognition,andtheevolutionofcolorpolymor- Ford E.B. (1975): Ecologicalgenetics,4th ed. Chapman
phism in virtual prey. - Proceedings ofthe National andHall,London.464pp.
AcademyofSciences ofthe United States ofAmerica FullerR.C.,K.L.Carleton,J.M.Fadool,T.C.Spady
103: 3214-3219-doi: 10.1073/pnas.0509963103 &J.Travis (2005): Genetic and environmentalvaria-
Polymorphisminanorb-weavingspider 57
tion in thevisualproperties ofbluefin killifishLucania MAJERUS M.E.N. (1998): Melanism evolution in action.
goodei. -Journal ofEvolutionary Biology 18: 516-523 OxfordUniversityPress,Oxford.338 pp.
-doi: 10.1111/j.l420-9101.2005.00886.x Metropolis N. & S. ULAM (1949): The Monte Carlo
Gray S.M. &J.S. McKinnon (2006): A comparative method. -Journal ofthe American StatisticalAssoci-
descriptionofmatingbehaviourintheendemictelma- ation44: 335-341
therinid fishes ofSulawesi’s Malili Lakes. - Environ- OxfordG.S.(1983):Geneticsofcolouranditsregulation
mental BiologyofFishes 75: 471-482 - doi: 10.1007/ during development in the spider Enoplognatha ovata
S10641-006-0037-X (Clerck) (Araneae: Theridiidae). - Heredity 51: 621-
Gray S.M. &J.S. McKinnon (2007): Linking color 634-doi: 10.1038/hdy.l983.74
polymorphism maintenance and speciation. - Trends Oxford G.S. (2005): Genetic drift within a protected
in Ecology & Evolution 22: 71-79 - doi: 10.1016/j. polymorphism: enigmatic variation in color-morph
tree.2006.10.005 frequencies in the candy-stripe, Enoplognatha ovata.
GUNNARSSONB.(1987):MelanisminthespiderPityohy- - Evolution 59: 2170-2184 - doi: 10.1111/j.0014-
phantesphrygianus: the genetics and the occurrence of 3820.2005.tb00926.x
different colour phenotypes in a natural population. - Oxford G.S. (2009): An exuberant, undescribed colour
Heredity59:55-61 -doi: 10.1038/hdy.l987.96 polymorphismin Theridioncalifornicum(Araneae,The-
HALKKAO.&cL.HALKKA(1990):Populationgeneticsof ridiidae):implicationsforatheridiidpatterngroundplan
thepolymorphicmeadowspittlebug,Philaenusspumarius andthe convergentevolution ofvisible morphs.-Bio-
(L.).-EvolutionaryBiology24: 149-191 logicalJournalofthe Linnean Society96:23-34-doi:
HIPPA H. & I. OKSALA (1981): Polymorphism and re- 10.1111/j.l095-8312.2008.01117.x
productive strategies ofEnoplognatha ovata (Araneae: REIGHARDJ. (1908):An experimentalheldstudyofwar-
Theridiidae) innorthernEurope.-Annales Zoologicii ning coloration in coral-reefAshes. - Publications of
Fennici 18: 179-190 the CarnegieInstitutionofWashington 103:257-325
Hoffman E.A. & M.S. BlOUIN (2000): A review of REILLO PR.&.D.H.Wise (1988):Anexperimentaleva-
colourandpatternpolymorphismsinanurans.-Biolo- luationofselectiononcolormorphsofthepolymorphic
gicalJournaloftheLinnean Society70:633-665-doi: spider Enoplognatha ovata (Araneae: Theridiidae). -
10.1006/bijl.l999.0421 Evolution42: 1172-1189
HuxleyJ.(1955):Morphisminbirds.-ActaCongressus Roberts M.J. (1996): Spiders ofBritain and Northern
Internationalis Ornithologici 11: 309-328 Europe. Collins Field Guide,London. 384pp.
JonesD.,J.-.CLEDOUX&M.EMERIT(1990):Guidedes RobertsonH.M.(1985):Femaledimorphismandmating
araigneesetdesopilionsd’Europe.DelachauxetNiestle, behaviourin adamselfly,Ischfturaramburi:females mi-
Lonay(CH).383 pp. mickingmales.-AnimalBehaviour33: 805-809-doi:
KimuRAM. (1983):The neutraltheoryofmolecularevo- 10.1016/S0003-3472(85)80013-0
lution.CambridgeUniversityPress,Cambridge.384pp. UenoH.,Y.SatoScK.TsUCHIDA(1998):Colour-asso-
King R.B.&R.Lawson (1995):Colorpatternvariation ciatedmatingsuccessinapolymorphicladybirdbeetle,
inLakeEriewatersnakes:theroleofgeneflow.-Evo- Harmonia axyridis. - Functional Ecology 12: 757-761
lution47: 1819-1833 -doi: 10.1046/J.1365-2435.1998.00245.x
Kingston J.J., G.G. Rosenthal &J.R. Michael VAN&GOSSUM H., R. Stoks, E. Matthysen, F. Valck
(2003): The role ofsexual selection in maintaining a L.DEBruyn (1999):Malechoiceforfemalecolour
colour polymorphism in the pygmy swordtail, Xipho- morphsinIschnuraelegans(Odonata,Coenagrionidae):
phoruspygmaeus.-AnimalBehaviour65:735-743-doi: testing the hypotheses.-Animal Behaviour 57: 1229-
10.1006/anbe.2003.2110 1232-doi: 10.1006/anbe.l999.1100