Received 7 May 2002 Accepted 8 July 2002 Publishedonline 25September 2002
Ageneralizedfemale biasfor long tailsin a short-tailedwidowbird Sarah R.Pryke * and Staffan Andersson AnimalEcology, Department of Zoology,Go ¨teborgUniversity, Box463, SE-405 30 Go ¨teborg,Sweden Tail elongation in thepolygynous widowbirds( Euplectes spp.)has evokedboth adaptive andnon-adaptive explanations. Female choicehas beenshown in thethree longest tailed species(20– 50 cm),whereas an agonistic functionwas proposed for amedium-tailed (10 cm)widowbird. To testthe generality anddirec- tionality ofsexual selectionon tail length in widowbirds,we experimentally investigated selectionin the relatively short-tailed (7cm)red-shouldered widowbirds ( E. axillaris ).Prior toterritory establishment, males wereassigned to four tail-treatment groups;control, short, long andsupernormal (similar toa sympatric long-tailed congener).No effects on male competition weredetected as the groups wereequally successfulin acquiring territories ofsimilar sizeand quality. However,mating successamong the92 territorial males wasstrongly skewedin favour ofsupernormal-tailed males (62% ofactive nests;5.2 ± 1.3 nestsper territory). Long-tailedmales also acquired more nests(1.9 ± 0.7) than control(0.7 ± 0.5) and short-tailed (0.5 ± 0.3) males,while thelatter twogroups didnot differ signi cantly. Theseresults support ageneral, open-endedfemale preferencefor long tails in widowbirdsand may representa receiver bias that aroseearly in their divergencefrom theshort-tailed weaverbirds (Ploceinae). Keywords: sexual selection;tail length; receiver bias; Euplectesaxillaris ;widowbirds
1. INTRODUCTION To differentiatebetween the debated functions of tail elongation, weexamined theselection pressures on tail The extreme variation in tail elongation among themale length in oneof the shortest-tailed species, the red- breeding plumages ofthe highly polygynous andecologi- shoulderedwidowbird (tail ca.7cm).Like other widow- cally similar African widowbirds Euplectes spp. (Craig birds,the male has pronouncedsexual andseasonal 1980; Andersson& Andersson1994) isa striking example dimorphism, andmoults from acryptic sparrow-brown ofenigmatic diversity in ornamentexpression. Male tail non-breedingplumage intoa black nuptial plumage with a length varies from therelatively shorttails (7cm) ofyel- shorttail andred carotenoid-based epaulettes (lesser wing low-rumped( E. capensis)andred-shouldered widowbirds coverts).During thebreeding season,these birds are terri- (E.axillaris )to50 cmin thelong-tailed widowbird torial andinhabit marsh andgrassland areas in central and E. progne.The functionof this signal has evokedboth southernAfrica. In ight display, themale has aslow, adaptive andnon-adaptive explanations (Savalli 1993, bouncy‘ rowing’action with exaggerated wing beatsand 1995; Andersson& Andersson1994; Craig &Villet afoldedtail. Ontheir territories, males build numerous 1998), butmany ofthe basic assumptionsremain incon- coarsenest frames (‘cock’s nests’), whichthe females line clusively tested.One of the main questionsconcerns the with nergrass, and then incubate and feed the nes- generality ofdirectional female preferencesfor elongated tlings alone. tails. Female choiceof long tails wasinitially demonstrated In this study,we experimentally manipulated male red- in long-tailed widowbirds(Andersson 1982) andhas sub- shoulderedwidowbird tails both within thenatural range sequentlybeen shown in thelekking Jackson’s widowbird (i.e.short, average andlong) andfar beyond,creating a E. jacksoni (Andersson1989, 1992 (tail 20 cm))and terri- supernormal tail similar in length tothat ofthesympatric torial red-collared widowbirds E. ardens (Pryke et al. 2001 red-collared widowbirds.As described by Tinbergen (tail 22 cm)).By contrast,tail length in themedium-tailed (1948) in early ethological literature, andrecently (10 cm) yellow-shoulderedwidowbird ( E.macrourus ) explored in articial neural networks(e.g. Enquist & Arak seemedto function in male competition for territories 1998), supernormal stimuli oftenelicit stronger receiver rather than female choice(Savalli 1994 a,b).Furthermore, responsesthan thenatural range ofstimuli towhich the other selectiveforces, such as stabilizing selection,may receiver is genetically or phenotypically adapted.For have contributedto the diverse tail variation among the example, if tail length is subjectto sexual selection,males widowbirds.For example, Savalli (1995) suggestedthat displaying supernormal tails may bemore dominantin tail length might beconstrained by speciesrecognition in male–male contestsor attract more females.Furthermore, areas ofsympatry with longer tailed congeners.However, if supernormal stimuli greatly exceed(by several s.d.)the only oneof the two investigated speciespairs showed natural range, astrong responseindicates that generalized character divergenceand only in apositive direction(i.e. preferencesand receiver biasesalone might besuf cient oneof the widowbirds had longer tails in sympatry than tocause and maintain signal exaggeration (e.g.Enquist & in allopatry). Arak 1998), i.e.without invoking Fisherian or ‘good genes’coevolution between the preference and signal. By contrast,females are also understrong selectionto *Authorfor correspondence ([email protected]). avoid heterospecic mating. If tail length is anessential
Proc.R. Soc.Lond. B (2002) 269, 2141–2146 2141 Ó 2002 TheRoyal Society DOI10.1098/ rspb.2002.2131 2142S. R.Prykeand S. Andersson Generalfemale bias for long tails
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manipulated tail length cm)
Figure 1. Theaverage ( ± s.d.) reproductive success of tail-manipulated malesthat established territories; the6 cm manipulations represent theshort-tailed ( n = 25), 7cm thecontrol-tailed ( n = 23), 8cm thelong-tailed ( n = 23) and 22 cm the supernormal-tailed ( n = 21) males. Theinner histogram showsthe natural distribution of breeding male tail length in the population ( n = 252), corresponding to theaxis of experimental tail lengths. componentof species recognition, and if ‘supernormal ’ (b) Colorimetrics tail length in onespecies is ‘normal’ toanother species Spectral re ectance(at 2nmresolution) from the redepaul- with which hybrid matings might occur,females should ettewas measuredwith an S2000spectrometer (Ocean Optics, avoid or at least beindifferent to asupernormal tail com- Dunedin,USA), using an HL2000halogen light sourceand a pared with trait values within orcloserto the conspeci c bre optic re ectanceprobe. The probe was heldperpendicu- variation. By simultaneously,and under natural signal larlyagainst the plumageand vescans fromthe centreof the conditions(i.e. a eldexperiment), exploring the epaulettewere taken and averaged for eachindividual. Using responsesto both ‘normal’ and ‘supernormal ’ tail the C-specsoftware (Ancal,Las Vegas, USA)re ectance was manipulations (resembling thesympatric red-collared measuredas the proportion of light re ectedin relationto aWS- widowbird),this studyprovides adirecttest of stabilizing 2white standard (morethan 98%re ectanceacross the measur- constraintsarising from speciesrecognition versusdirec- ing range). tional sexual selectionfor elaborate male tails. Objectiveindices of the threemain dimensions of colourper- ception(spectral intensity, location and purity)were computed fromthe raw spectralre ectancedata and then averaged for 2. METHODS eachindividual. ‘Brightness’ (spectralintensity) was estimated
(a) Morphologicalanalysis by R350–700,the sumof re ectancefrom 350 –700 nm. ‘Hue’
The experimentwas carriedout ona population of red- (spectralintensity) was estimatedas l(R50),the wavelength at shoulderedwidowbirds inthe Balgowan district,KwaZulu- which re ectanceis halfway betweenits minimum( Rmin) and
Natal, South Africa,between early December 2001 and March maximum (Rmax). ‘Chroma’ (spectralpurity) is based onseveral 2002.Males were captured with mistnets at night roosts and aspects, such as re ectanceslope height and steepness.To markedwith an aluminiumring and threeunique colour bands. incorporateboth of these spectralshape aspects, we useda seg- Measurementsof wing chord(to the nearest0.5 mm), culmen ment-based estimatethat comparesthe re ectanceabove and
(tothe nearest0.1 mm), tarsus (tothe nearest0.1 mm), tail below l(R50),dividedby Rav (average re ectance)to control length (tothe nearest0.1 mm) before and after manipulation, for brightness, i.e. C[R50] = (R[l(R50) – 700] – R[350 – l(R50)])/Rav. and mass (tothe nearest0.5 g) weretaken. Becausethe three Detailson further methods and analysis of re ectancedata are linearmeasures of body size(tarsus, culmenand wing) were providedin Pryke et al. (2001). intercorrelated,the rst componentsof aprincipalcomponents analysis,explaining 81.7% of the variance,were used to extract (c) Behaviouraland territory characteristics an independentmeasure of body size.An index of body con- Territorialmales were observed for 30minweekly over a ditionwas estimatedfrom the residualsof the linearregression 13weekperiod when the malesdefended their breeding territor- of log(body mass)on 3log(tarsus length) (S. Andersson1994). ies.Observationswere randomized and allactivities and their Epaulette sizewas calculated(to the nearest0.1 mm) as the durations werecontinuously recorded with the timegiven to the product of the maximumlength and the average of three nearest5 s.Data onthe timespent onthe territory(min 2 1) and maximumbreadth measures(perpendicular to the length)with display rates (min 2 1)wereextracted for analysis. the wing closed.The repeatabilityof eachmorphological measure- The territoriesof residentmales were mapped using the mini- mentwas testedin recapturedbirds and allof these werehighly mumconvex polygon method and updated every14 days. The signi cant (r = 0.86–0.97, F64,138 = 22.3–79.1, p , 0.001 malesdefended territories (mean ± s.d. = 0.17 ± 0.05 ha, n = 92) (Lessells& Boag 1987)). that wereeither isolated from one another orcontiguous with
Proc.R. Soc.Lond. B (2002) Generalfemale bias for long tails S.R.Prykeand S. Andersson 2143 other territorieswithin the grasslands (furtherdetails from S. R. (f ) Statisticalanalysis Prykeand S.Andersson,unpublished data). Multivariateanalyses of variance(MANOVA) were used to Although thereare a variety of territorycharacteristics that test whether malemorphology and territorialbehaviours differed have beenshown to in uencefemale mate choice (e.g. Eckert & among the fourtreatment groups. Scheffe` ’smultiplecomparison Weatherhead 1987;Aebischer et al. 1996),vegetation type isthe contrasts wereused to examinewhich speci ctreatments dif- most obvious and striking differencebetween the territoriesused feredfrom one another. As the residualswere normal with by red-shoulderedwidowbirds inthis study. Becausemales pro- homoscedasticvariances, no transformations wererequired. videfemales with nothing except nest framesand gametes,nest Nonparametrictests wereused when the assumptions of para- siteavailability is likely to bethe important territorycharacter- metrictests wereviolated. istic.The vegetation type, meandensity (on a rank scalefrom zeroto 10)and height (cm)within eachterritory were estimated 3. RESULTS as ameasureof habitat quality and nesting suitability.Veg- (a) Variationin male traits etation measurementswere taken fortnightly at xed sampling Asfemale choicedepends on there being suf cient points situated 20mapart on50 mtransects across the study intrapopulation variation for femalesto visually perceive areaand averaged for the nesting season. differencesbetween male characteristics, coef cients of Throughout the study, nests werecounted daily to register variation werecalculated. Body sizetraits exhibited coef- new cock’snests and activenests onthe territories.Nests were cientsof variation of3 –6%,typical for morphological then checkedevery third day to monitorprogress. characters that are notsexually selected(e.g. Alatalo et al. 1988; Evans& Barnard 1995), whereasterritory and (d) Tailmanipulations behavioural characteristics wereconsiderably more vari- Maletail lengths werealtered by cutting all12 rectrices able (9–30%). Tail length (mean ± s.d. = 70.3 ± 3.48 mm, through the shaft with ascalpelfour centimetres from the tail range = 59.4–81.1 mm), however,was relatively invariable base. Each apicalpiece was then replacedwith an appropriate (5%) in contrastto thefour previously studiedwidowbird feather length fromred-collared widowbird tails,by insertinga specieswith coef cientsof variation of5 –17% for tail minutienpin (FST, Vancouver, Canada) into the shaft of the length, ascompared with 2 –6% for body measurements two feather sectionsand gluingthem inplace with superglue (Andersson1982, 1993; Craig 1989; Savalli 1994 a; (YanlanProducts, Fuzhou, China). Treatments weresequen- Pryke et al. 2001). tiallyassigned to malesas they werecaptured (i.e. randomly assigned with respectto allother attributes) to produceshort, (b) Tailmanipulation andterritory and long,supernormal and control-tailedmales. Short-tailed males morphologicalcharacteristics (n = 30)had theirtails shortened to the lowerlimits of the Maleswere manipulated prior toestablishing territories natural population variation and approximately the samelength in thearea (whenmale competition is probably themost of immatureand non-breedingplumaged males (before: intense).There wasno difference between the tail- mean ± s.d. = 71.6 ± 2.4mm; after: 60 ± 1.1mm). Long-tailed manipulated groups in territory establishment,as 25 short, males (n = 30)had theirtails lengthened to the upper range of 23 control,23 long and21 supernormal-tailed males 2 the population (before:67.8 ± 2.9mm, after: 80 ± 0.4 mm). establishedbreeding territories in thearea ( x = 1.69, Supernormal-tailedmales ( n = 29)had theirtails lengthened d.f. = 3, p = 0.64). Similarly, therewas no differencein ter- similarto those of malered-collared widowbirds (before: ritorial characteristics betweenthe treatment groups 70.3 ± 2.1mm; after: 220 ± 0.9mm). To controlfor the effects (MANOVA,Wilks ’ l = 0.94, F1 8 ,2 3 5 = 0.37, p = 0.97; table of both tailmanipulation and adding red-collaredwidowbird tail 1). Neither didhabitat quality (vegetation type and feathers to red-shoulderedwidowbirds, the control-tailedmales density),production of cock ’snestsor territory size,differ (n = 30)had theirtails manipulated with red-collaredwidowbird among thegroups (table 1). Territory sizewas also unre- feathers to equalthat of the population mean(before: lated toterritory quality: thevegetation typesmost 68.7 ± 3.2mm, after: 70 ± 0.5mm). Pre-treatment tail lengths frequentlyused for feedingand nesting in, did not corre- didnot differamong the treatment groups (Kruskal –Wallistest, late with territory size(Spearman ’s rs , 0.1 for all comparisons). H30,30,29,30 = 3.74, p = 0.51). Overall male behaviour (time onterritory anddisplay rate) didnot differ among thegroups (table 1), however, (e) Male reproductive success therewas a signi cantinteraction betweendisplay rate The numberof nesting females(i.e. nests with eggs or andtreatment group ( F6 ,17 6 = 5.23, p = 0.04), with nestlings)on amale ’sterritorywas usedas ameasureof his supernormal-tailed males tendingto display lessthan reproductivesuccess, as maleswith moreactive nests ontheir males in theother groups (Scheffe`test, p , 0.01). territorieshad signi cantlymore nestlings (Spearman ’s rs = 0.82, Morphological characters may also affectterritory n = 159, p , 0.001) and edglings(Spearman ’s rs = 0.90, n = 44, establishmentand male reproductivesuccess. However, p , 0.001).Social mating successcould, however, becounter- male morphology (bodysize, initial tail length andbody actedby extra-pair (or ‘extra-harem ’)fertilizations(EPC). The condition)and epaulette size and colorimetrics weresimi- frequencyis unknown inthe red-shoulderedwidowbird, but it lar among all males (MANOVA,Wilks ’ l = 0.87, isrelatively low inthe redbishop ( E. orix),wherein addition, F2 1 ,3 1 4 = 0.62, p = 0.65; table 1). the numberof nestlingssired is strongly relatedto the number of nests onaterritory(Friedl & Klump1999). Furthermore, as (c) Tailmanipulation andmale reproductive femalesobtain littlemore than genesfrom their mates, it seems success unlikelythat EPCmatechoice criteria would be different from The experimental tail elongations had strong andposi- socialmate choice. tive effectson male mating success( gure 1), although
Proc.R. Soc.Lond. B (2002) 2144S. R.Prykeand S. Andersson Generalfemale bias for long tails
Table1. MANOVAof thedifferences in male morphology asegg patterns)were found on red-shouldered widow- and territorial characteristics among thefour tail-treatment bird territories. groups. The strong female preferencefor long tails in ashort- (Only signi cant interaction terms are reported ( p , 0.1).) tailed speciesindicates that thereis atail sizegeneraliz- ation (see gure 1) that may have arisen from ageneral F p female bias for longer tails. The evolutionof signal traits asexploitations ofreceiver biaseshas recentlyreceived a a morphological characteristics great deal ofattention (reviewed in Endler& Basolo initial tail length 0.41 0.71 1998). Preferencesfor heterospeci ctraits have been body size (PC1) 1.50 0.22 body condition 0.68 0.52 documentedin shes(Basolo 1990, 1995), frogs (Ryan & epaulet size 0.03 0.95 Rand1990, 1993) andarthropods (Proctor 1992; epaulet brightness 0.04 0.97 McClintock& Uetz1996), all suggesting somekind of epaulet hue 1.61 0.19 female pre-existing, sensoryor cognitive biases(Endler & epaulet chroma 0.51 0.68 Basolo 1998; Ryan 1998). Suchbiases can be hardwired territorial and behavioural characteristics b ‘sideeffects ’ ofthe cognitive architecture (e.g.Enquist & territory size 0.43 0.73 Arak 1993) or naturally selectedadaptations toother sen- cock’s nests 0.42 0.74 sory taskssuch as foraging or predator avoidance vegetation type 0.70 0.55 (Endler& Basolo 1998). Either way,demonstrating a vegetation density 0.05 0.98 receiver bias requiresevidence that (i) it phylogenetically time on territory 0.65 0.59 displayrate 1.93 0.10 predatesthe evolution of the trait, and(ii) it is generally displayrate ´ treatment group 5.23 0.04 presentin subsequentlyderived species in thetaxon. Among thewidowbirds, females in thethree longest tailed a Differences in male morphology among thefour tail- speciesprefer males with longer tails (Andersson1982, treatment groups (Wilks ’ l = 0.87, F21,314 = 0.62, p = 0.65). 1989, 1992; Pryke et al. 2001). In addition,a preliminary b Effectsof tail manipulations on territorial and behavioural phylogenetic analysis ofthe Euplectes (S.Anderssonand characteristics (Wilks ’ l = 0.94, F18,235 = 0.37, p = 0.97). A.Johansson,unpublished data) suggeststhat theshort- tailed red-shoulderedwidowbirds are ancestral tothe longer tailed widowbirds.Thus, the preference for long male display intensityhad noeffect on female visitation tails in thered-shouldered widowbird seems to support an ratesto the territories (either within orbetweentreatment ancientfemale bias that may have played acentral part in groups;Spearman ’s rs = 0.32–1.24, n = 21–92, p = 0.21– theevolution of elaborate tails in widowbirds. 0.74). Moststrikingly, anddespite their lowerdisplay rate During theevolution of costly sexually selectedsignals (seeabove), the supernormal-tailed males attracted 110 of andfemale preferencefor suchsignals, thereare several, the178 (62%) actively nestingfemales to their territories, notmutually exclusive,possible processes of evolutionary which wassigni cantly more than themales in theother change.Changes in signals andreceivers can be geneti- treatment groups (Kruskal –Wallis test, H2 5 ,2 3 ,2 3 ,2 1 = 46.72, cally correlated (e.g.runaway andgood genes models), p , 0.001; gure 1). Maleswith long tails (within the suchthat an evolutionary change in thetrait resultsin an natural range) attracted signi cantly fewerfemales than evolutionary adjustmentof the preference (M. Andersson thesupernormal-tailed males (Mann –Whitney U-test two- 1994). Alternatively, areceiver bias may arise beforethe tailed, z = 4.85, n = 21, p , 0.001), butmore than either signal that exploits it evolves(Basolo 1990; Enquist& thecontrol- ( z = 3.02, n = 23, p , 0.005) or short-tailed Arak 1993; Ryan 1998). While this explanation (similar (z = 3.68, n = 23, p , 0.005) males.However, there was tothe coevolutionary modelsof mate preference)is theor- no signi cantdifference between short- and control-tailed etically capable ofpromoting theevolution and mainte- (z = 1.29, n = 23, p = 0.19) males. nanceof costly ornamentation (Arak &Enquist1995; Enquist& Arak 1998), it seemslikely that thetwo pro- cessescomplement rather than excludeeach other. In the 4. DISCUSSION widowbirds,preset female biasesmay have beenrespon- Our resultsdemonstrate a natural andopen-ended sible for theinitial (andprobably notvery costlyand female preferencefor longer tails in thered-shouldered ‘honest’)elaboration oftail length, whichmay have simul- widowbird.Because the most attractive supernormal taneouslyor subsequentlybeen reinforced in somespecies manipulations (7s.d.of the natural variation) mimicked by adaptive mate choicethrough heritable attractiveness thetails ofthe sympatric red-collared widowbirds,and (Fisherian bene t),viability (goodgenes) or somecombi- evenused rectrices from this species,it seemsunlikely that nationof these that gives anet tnessgain tothe choosy speciesrecognition constrainsthe evolution of tail length. female (Kokko et al. 2002). This is also consistentwith theweak support for character In contrastto natural andsexual selectionpressures, displacementin sympatric widowbirdpopulations (Savalli geneticdrift has also beenproposed to explain theinter- 1995). Furthermore, if tail length wasa major cuein spec- speci cvariation in widowbirdtail ornamentation (Savalli iesrecognition, female red-collared widowbirds,which 1993; Craig &Villet 1998). Drift may have played apart werebreeding closeby, shouldat least occasionally be in thedivergence of graduated widowbirdtail lengths but attracted tothe supernormal-tailed red-shouldered it seemsunlikely that anatomical traits ofthis magnitude, widowbirds(displaying male red-collared widowbird with obviousproduction costs (S. Andersson 1994) and tails). However,no female red-collared widowbirdnests hampered locomotion(Balmford et al. 1993; Norberg (easily distinguishedby their differentnest shape as well 1995), couldresult from random processesalone. Sexual
Proc.R. Soc.Lond. B (2002) Generalfemale bias for long tails S.R.Prykeand S. Andersson 2145 selection,in oneform or another,is probably themain strain tail growth or maintenanceto almost noelongation selectiveforce behind tail elongation in widowbirds,with compared with thenon-breeding tail length. thedivergence resulting from differentbalances between In conclusion,the strong female preferencefor long tails sexual andnatural selectionin thedifferent species. in this short-tailed widowbirdindicates that directional Amajor questionthus raised from this studyis why red- female choice,unconstrained by speciesrecognition, is a shoulderedwidowbirds have notevolved along tail in general selectiveforce behind the evolution of tail orna- responseto this strong female preference.There are a mentsin thewidowbirds. Given that theminimal tail numberof potential explanations. First, thetail length of elongation ofthe red-shouldered widowbird is an ancestral red-shoulderedwidowbird males may have beenunre- rather than derivedcharacter state,the experimentally sponsiveto sexual selectionbecause of a lack ofheritable revealed preferencemight representa presetreceiver bias variation in tail length. This might bemanifested in the that has sequentially or simultaneouslybeen reinforced by lowphenotypic variability in tail length (coef cient of indirect Fisherian or goodgenes bene tsin several spec- variation = 5%) compared with that ofcongeners:6 –9.4% ies.The extreme diversity ofwidowbird tail elongation in thelong-tailed widowbird(Andersson 1982; Craig thusseems most likely toresult from differencesin con- 1989); 12.5% in Jackson ’swidowbird(Andersson 1993); straintssuch as energetic costs and predation, or trade- 5–8% in theyellow-shouldered widowbird (Savalli offswith investmentsin agonistic signalling. 1994a);and17% in thered-collared widowbird(Pryke et Specialthanks to themanagers and owners of Old Balgowan al. 2001). However,this ismore likely aresultof stronger Farm for permission towork on their land, and to two anony- conditiondependence and environmental variation of mous referees who provided helpful comments on themanu- longer tails, andthere is noreasonto suspectthat genetic script. Financial support in thisstudy wasprovided bythe variation is,or initially was,less of a constraintin these SwedishSTINT Foundation to S.P. and bythe Swedish speciesthan in red-shoulderedwidowbirds. Second, Science Council and Go¨teborgs Kungliga VetenskapsochVit- female choicemay target someother trait, directing atten- terhetssamha¨lle to S.A. tionaway from thenormally small (5%) variation in tail length. For example, mate choicecriteria in other Euplectes REFERENCES speciesinclude the number of male-built nestson terri- Aebischer, A., Perrin, N., Kreg, M., Studer, J.&Meyer, D.R. tories (E. orix (Friedl &Klump 1999); E.macrourus 1996 Therole of territory choice, matechoice and arrival (Savalli 1994 a)),which also seemsto in uencemating date on breeding success in theSavi ’s warbler Locustella successin this species(S. R. Pryke andS. Andersson, luscinioides . J.Avian Biol. 27, 143–152. unpublisheddata). In thelonger tailed speciesthe impor- Alatalo, R.V., Ho¨glund, J.&Lundberg, A.1988 Patterns of tancemay (for onereason or another) have shiftedfrom variation in tail ornament size in birds. Biol. J.Linn.Soc. 34, 363–374. suchterritory componentsto tail length asthe primary Andersson, M.1982 Female choice selects for extreme tail choicecue. Third, natural selectionagainst tail elongation length in awidowbird. Nature 299, 818–820. (from,for example, predation or energeticcosts) may have Andersson, M.1994 Sexual selection .Princeton University beenexceptionally strong in red-shoulderedwidowbirds. Press. Asregards predation,there were no observed predation Andersson, S.1989 Sexual selection and cues for femalechoice attempts onarti cially tail-lengthened males andnone of in leksof Jackson ’s widowbird Euplectes jacksoni . Behav. Ecol. them disappeared during theseason. Energetic con- Sociobiol. 25, 403–410. straints,however, might beparticularly high in red- Andersson, S.1992 Female preference for long tails in lekking shoulderedwidowbirds. Supernormal-tailed males had a Jackson’swidowbirds: experimental evidence. Anim.Behav. 43, 379–388. lowerdisplay rate andwere unstable in high winds(being Andersson, S.1993 Sexual dimorphism and modes of sexual twistedround by their tail whenit caught thewind), indi- selection in lekking Jackson ’swidowbirds Euplectes jacksoni . cating that thetail hampered locomotion.Increasing the Biol. J.Linn.Soc. 49, 1–17. long graduated tails ofmale widowbirdsis likely tobe Andersson, S.1994 Costsof sexual advertising in thelekking physiologically (inferredfrom thefrequent fault bars (S. Jackson’s widowbird Euplectes jacksoni . Auk 96, 1–10. Andersson1994)) andaerodynamically costly(Balmford Andersson, S.&Andersson, M.1994 Tailornamentation, size et al. 1993; Norberg 1995). Similarly, carotenoid-based dimorphism and wing length in thegenus Euplectes plumage (suchas that ofred epaulettes) has honest- (Ploceinae). Auk 111, 80–86. Andersson, S., Pryke, S.R., O ¨ rnborg, J., Lawes,M. J.& enforcingproduction costs due to the presumed costs of Andersson, M.2002 Multiple receivers, multiple ornaments foraging, parasite-inhibited uptakeand competing physio- and atrade-off between agonistic and epigamic signaling in logical functions(Olson & Owens1998). In red-collared awidowbird. Am. Nat.(In thepress.) widowbirds,a strong trade-offbetween carotenoid color- Arak, A.&Enquist, M.1995 Con ict, receiver biasand the ation (anagonistic signal) andtail length (anepigamic evolution of signals. Phil. Trans.R. Soc. Lond. B 349, 337– signal) indicatesan allocation con ict betweenthe two 344. costlyornaments (which are simultaneouslymaintained Balmford, A., Thomas,A. L.R.&Jones, I.L.1993 Aero- through multiple receivers(Andersson et al. 2002)). dynamics and theevolution of long tails in birds. Nature 316, Despitethe short tails ofred-shouldered widowbirds, 628–631. Basolo, A.L.1990 Female preference for male sword length in thereis asimilar trade-offbetween tail length andthe red thegreen swordtail, Xiphophorus helleri (Pisces, Poecilidae). epaulette,likewise used in male contestsignalling (S.R. Anim.Behav. 40, 332–338. Pryke andS. Andersson,unpublished data). It is thus Basolo, A.L.1995 Afurther examination of apre-existing bias possiblethat theinvestment in agonistic signalling andter- favouring asword in thegenus Xiphophorus . Anim.Behav. ritorial behaviour is strong enoughin this speciesto con- 50, 365–375.
Proc.R. Soc.Lond. B (2002) 2146S. R.Prykeand S. Andersson Generalfemale bias for long tails
Craig, A.J.F.K.1980 Behaviour and evolution in thegenus and wing shapeaffect the cost for ight in animals. Funct. Euplectes. J.Ornithol. 121, 144–161. Ecol. 9, 48–54. Craig, A.J.F.K.1989 Taillength and sexual selection in the Olson, V.A.&Owens, I.P.F.1998 Costly sexual signals: are polygynous longtailed widowbird ( Euplectes progne ): a cau- carotenoids rare, risky, or required? TrendsEcol. Evol. 13, tionary tale. S.Afr.J. Sci. 85, 523–524. 510–514. Craig, A.J.F.K.&Villet, M.H.1998 Sexual dimorphism and Proctor, H.C.1992 Sensory exploitation and theevolution of tail-length in widowbirds and bishopbirds (Ploceidae: male mating behaviour: acladistic testusing water mites Euplectes spp.): areassessment. Ibis 140, 137–143. (Acari: Parasitengona ). Anim.Behav. 44, 745–752. Eckert, C.G.&Weatherhead, P.J.1987 Competition for terri- Pryke, S.R., Andersson, S.&Lawes,M. J.2001 Sexual selec- tories in red-winged blackbirds: isresource-holding potential tion of multiple handicaps in thered-collared widowbird: realized. Behav. Ecol. Sociobiol. 20, 309–375. femalechoice of tail length but not carotenoid display. Endler, J.A.&Basolo, A.L.1998 Sensory ecology, receiver Evolution 55, 1452–1463. biasesand sexual selection. TrendsEcol. Evol. 13, 415–420. Ryan, M.J.1998 Sexual selection, receiver biases,and the Enquist, M.&Arak, A.1993 Selection of exaggerated male evolution of sexdifferences. Science 281, 1999–2003. traits byfemale aesthetic senses. Nature 361, 446–448. Ryan, M.J.&Rand, A.S.1990 Thesensory basisof sexual Enquist, M.&Arak, A.1998 Neural representation and the selection for complex calls in theTngara frog, Physalaemus evolution of signal form. In Cognitive ecology:the evolutionary pustulosus. Evolution 44, 305–314. ecology ofinformation (ed. R.Dukas),pp. 21 –79. Chicago Ryan, M.J.&Rand, A.S.1993 Sexual selection and signal University Press. evolution: theghost of biasespast. Phil. Trans.R. Soc. Evans,M. R.&Barnard, P.1995 Variable sexual ornaments Lond. B 340, 187–195. in scarlet-tufted malachitesunbirds ( Nectarinia johnstoni ) on Savalli, U.M.1993 An application of theneutral model to the Mount Kenya. Biol. J.Linn.Soc. 54, 371–381. evolution of tail length in thegenus Euplectes (Aves, Friedl, T.W.P.&Klump, G.M.1999 Determinants of male Ploceidae). Evolution 47, 696–699. mating success in thered bishop( Euplectes orix ). Behav. Ecol. Savalli, U.M.1994 a Matechoice in theyellow-shouldered Sociobiol. 46, 387–399. widowbird: correlates of male attractiveness. Behav. Ecol. Kokko, H., Brooks, R., McNamara,J. M.&Houston, A.I. Sociobiol. 35, 227–234. 2002 Thesexual selection continuum. Proc.R. Soc. Savalli, U.M.1994 b Taillength affectsterritory ownership in Lond. B 269, 1331–1340. (DOI10.1098/rspb.2002.2020.) theyellow-shouldered widowbird. Anim.Behav. 48, 105– Lessells, C.M.&Boag, P.T.1987 Unrepeatable repeatabilt- 111. ies: acommon mistake. Auk 104, 116–121. Savalli, U.M.1995 Theevolution of tail-length in widowbirds McClintock, W.J.&Uetz, G.W.1996 Female choice and pre- (Ploecidae): testsof alternatives tosexual selection. Ibis 37, existing bias: visual cues during courtship in two Schizocosa 389–395. wolf spiders (Araneae: Lycosidae). Anim.Behav. 52, 167–181. Tinbergen, N.1948 Social releasers and theexperimental Norberg, U.M.1995 How along tail and changesin mass method required for their study. Wilson Bull. 60, 6–51.
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