Extrapair paternity in the blue tit (Parus caeruleus): female choice ...

Behavioral Ecology Vol. 8 No. 5: 481-492

Extrapair paternity in the blue tit(Parus caeruleus): female choice, malecharacteristics, and offspring qualityBart Kempenaers,*^ Geert R- Verheyen,* and Andre A- Dhondt**•Department of Biology, University of Antwerp, U.I A., B-2610 Wilrijk, Belgium, bAustrian Academy ofSciences, Konrad Lorenz-Institute for Comparative Ethology (KLIW), Savoyenstrasse la, A-1160Vienna, Austria, and "KHornell Laboratory of Ornithology, 159 Sapsuckcr Woods Road, Ithaca, NY14850, USA

Extrapair paternity is common in many birds, and it is now generally accepted that female choice plays an important role.However, die benefits that females obtain from extrapair paternity are much less dear. To test the hypothesis that females obtainindirect fitness benefits, we studied paternity in a blue tit population over 4 years. Extrapair paternity occurred in 31-47% ofall nests and accounted for 11-14% of all offspring. Most males that fathered extrapair young did not lose paternity themselves,males never "exchanged" paternity, and within nests the extrapair offspring were usually fathered by a single male. Comparisonsbetween males that did and did not lose paternity and pairwise comparisons between the extrapair male(s) and the withln-pairmale showed that successful males had longer tarsi and sang on average longer strophes during the dawn chorus. Successfulmales weighed less (relative to their size) during the nettling stage, but neverthalen they survived better. Male age did notinfluence their likelihood of losing paternity, but extrapair males were usually older than the witbin-pair male they cuckolded.Within nests with mixed paternity, extrapair young were more likely to survive than within-pair young in cases of partial broodmortality. Our data also suggest that extrapair offspring were more likely to be males. Because extrapair males were usuallyclose neighbors, male quality should be considered relative to the quality of the neighbors. Despite this, we found consistencyin female choice over years. Our observations provide support for the hypothesis that female blue tits engage in extrapaircopuladons to obtain good genes for their offspring. Key words: good genes, mate choice, Parus carruleus, sperm competition,song, survival. [BAav Eeol 8:481-492 (1997)]

Sperm competition is widespread among birds because inmany species females engage in extrapair copulations

and these copulations often lead to multiple paternity (Birk-head and Metier, 1992). Although sperm competition can beconsidered as the ultimate form of male-male competition, itis now widely accepted that female choice plays an importantrole as welL Active female choice for a copulation partner,other than the social mate, has been clearly documented insome species (e.g., Gray, 1996; Houtman, 1992; Metier, 1990;Smith, 1988; Wagner, 1992). Even in species where behavioralevidence for choice is lacking, it is likely that females have atleast some control over paternity (Iifjeld and Robertson,1992). This is because (1) in most species males do not havean intromittent organ, and female cooperation may thus benecessary for successful insemination (Fitch and Shugart,1984), and (2) female choice of paternity may not only workvia behavioral control of copulations, but it may also involvea postcopulatory control over which sperm fertilizes the eggs("cryptic choice"; Adkiiu-Regan, 1995; Birkhead and Metier,1993).

To optimize their reproductive success, female birds shouldbe choosy: they should prefer to breed with a male that de-fends high-quality resources (e.g., territory, nest site, food),that is likely to invest a lot in parental care, and that is of highgenetic quality. However, the ability of females to choose isprobably restricted because (1) the quality of a male as a par-

Addreu correspondence to B. Kempenaen, KLIW, Savoyenstnssela, A-1160 Vienna, Austria.

Received 18 June 1996; revised 8 August 1996; accepted 21 Novem-ber 1996.1045-2249/97/J5.00 C 1997 International Society for Behavioral Ecology

ent, his genetic quality, and the quality of the resources hedefends are not necessarily positively correlated, (2) femalesmust compete with other females for the best breeding situ-ation (Slagsvold and Iifjeld, 1994) and (3) females must beable to assess the quality of the resources, the male's parentalabilities, and his genetic constitution. It is still poorly under-stood how the choice process works and what cues femalesuse to assess males, but choice for particular traits such asplumage characteristics (e.g., color, tail length) or behavioraltraits (e.g., song, display) has been well documented in manyspecies (Andersson, 1994; Johnstone, 1995). Extrapair pater-nity can be considered as a way in which females can escapesome of the limitations on their choice; i.e., females can firstchoose a social partner and then choose another male as fa-ther for (part of) their offspring (Mailer, 1992).

One of the most controversial issues in the study of femalechoice in general, but particularly in the context of extrapairpaternity and in lekking species, is what benefits females gainfrom their choice (Andersson, 1994; Johnstone, 1995; Kellerand Reeve, 1995; Kirkpatrick and Ryan, 1991; Sheldon, 1994).Females should obtain substantial benefits because beingchoosy is likely to be costly (Reynolds and Gross, 1990; seealso Sheldon, 1993). If females engage in extrapair copula-tions to escape some of the limitations on their choice, thechoice of a social mate could be based more on direct benefits(resources, parental abilities), while the choice of a father ofthe offspring could be based on indirect benefits (geneticquality). However, evaluating the relative importance of directand indirect benefits is difficult (Andersson, 1994; Metier,1994c). In the case of female choice for extrapair paternity,different direct and indirect benefits have been postulated(Birkhead and Metier, 1992; Westneat et aL, 1990). Although

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482 Behavioral Ecology Vol. 8 No. 5

many studies have suggested that females obtain genetic ben-efits in the form of "attractiveness genes" or "good genes"for their offspring (e.g., Freeman-Gallant, 1996; Graves et aL,1993; Hasselquist et aL, 1996; Houtman, 1992), the debate iscontinuing (e.g., Birkhead and Fletcher, 1995; Sheldon,1994). The suggestion that genetic benefits are important infemale choice for extrapair paternity is often based on theabsence of any dear direct benefit* (but see Sheldon, 1994),but the critical test is still missing. Convincing evidence forthe "good genes" hypothesis would be to show that extrapairoffspring have higher fitness than witbin-pair offspring (e.g.,because they survive better or because they, in turn, attractmore females; Kempenaers and Dhondt, 1993). So far, thisevidence is lacking because data on offspring performanceare hard to collect

The aim of this study was to investigate whether femalechoice for extrapair paternity in the blue tit {Pans carruleus)can be explained by females seeking to improve the geneticquality of their offspring. The rationale behind this study isas follows: (1) Extrapair paternity is common in the blue tit(Kempenaers et aL, 1992, 1995). (2) Evidence for behavioralcontrol of paternity by females is strong because females ac-tively seek extrapair copulations during their fertile period,often by visiting neighboring males in their territory (Kem-penaers et al., 1992) and mate-guarding intensity and copu-lation frequency do not explain differences in extrapair pa-ternity between males, while female cooperation in mateguarding does (Kempenaers et aL, 1995). (3) It is unlikelythat females gain any direct benefits from their choice. Fe-males did not receive any resources from the extrapair malesand they did not forage during their extraterritorial visits, nordid extrapair males provide any help in feeding or defendingthe offspring (Kempenaers B, personal observation). Further-more, it is unlikely that females engage in extrapair copula-tions to remate with a better male ("mate sampling hypoth-esis"; Heg et al., 1993). In our blue tit population divorce wasextremely rare (Dhondt and Adriaensen, 1994) and femalesnever remated with an extrapair male during the next breed-ing season (Kempenaers B, unpublished data). Finally, fe-males are unlikely to gain benefits through an increased prob-ability of having their eggs fertilized (see Kempenaers et aL,1996). (4) We concluded earlier that females choose high-quality males as extrapair partners because we observed thatmales that lost paternity had a lower chance to survive andwere smaller (in tarsus length) than males that did not losepaternity. This conclusion was based on data from only onebreeding season (1990). Here, we use data on extrapair pa-ternity from four breeding seasons (1990-1993), and we as-signed paternity for the 1990-1992 seasons, allowing a directcomparison of characteristics of the within-pair and extrapairmales.

The paper is organized as follows. First, we investigatedwhether die patterns of extrapair paternity are in accordancewith the idea that females choose particular males (see Kem-penaers and Dhondt, 1993). We also investigated whether fe-male choice is consistent (i.e., whether male fertilization suc-cess is repeatable). We therefore compared the males' successin fathering offspring over different years. Second, we inves-tigated which males are preferred by females by relating dif-ferent characteristics of males (song output, morphology, age,survival), wiffi their success in avoiding loss of paternityand/or obtaining extrapair offspring. Third, we comparedcharacteristics (morphology, sex, survival) of extrapair andwithin-pair offspring, and we discuss here whether and howthese characteristics can influence female fitness.

METHODS

General

We studied a blue tit population from 1990 to 1993 in the17-ha wooded part of die private estate Calixbergen (51*15'N, 4°28' E), in Schoten, north of Antwerp, Belgium. One hun-dred small-holed nest-boxes have been present since 1979,and each year about 40-60 pairs breed in these boxes. Allindividuals were captured and marked with a unique combi-nation of color bands during the «""""" and winter (Novem-ber-March). Nest-boxes were checked at least weekly, and allnests were closely followed from the start of nest building untilfledging of the young. In total we followed 188 nesting at-tempts in nest-boxes over 4 years. Of these, 144 (77%) suc-cessfully produced at least one fledgling. Young were bandedand measured when 15 days old. From most adults and nest-lings, blood samples (10-100 jil) were taken for DNA finger-printing. Nestlings were bled when 14 days old. In addition,we collected dead nestlings found in the nest before takingblood and extracted DNA from the brain. For more detailson die study area and general methods, see Kempenaers(1994b).

" '«y and alignment

Details on the fingerprinting methods can be found in Kem-penaers et al. (1992,1996) and Verheyen et aL (1994). Briefly,to exclude paternity we carried out multilocus DNA finger-printing for adults and nestlings from 1990 to 1993. We fin-gerprinted 165 nests (out of a total of 173 nests where at leastone nestling was born and including all nests with at least onefledgling). We used HinU restriction enzyme and Jeffrey'sprobe 33.15.

For all nests from 1990 to 1992 we used four hypervariableminisatellite single-locus probes (SLPs; cPcaMSl, 3, 11, and14) and one hypervariable double-locus probe (DLP; c-PcaMS8) to assign paternity (i.e., to find the genetic father ofthe extrapair offspring). Details on die isolation and initialcharacterization of these blue tit specific markers and on dietechniques used during the processing of blood samples tosingle-locus profiles can be found in Verheyen et al. (1994,1995). In short, high molecular weight DNA was digested withHinQ restriction enzyme. Fragments were separated overnightby electrophoresis in 0.6% agarose gels. The DNA was subse-quendy transferred onto nylon membranes by Soudiern blot-ting. SLPs were [o-JtP]dCTP (deoxycyddine 5'-trlphosphate)-labeled and hybridized overnight to die nylon membranes at68°C, followed by several high stringency washes. After auto-radiography (overnight at — 70°C), the patterns were ana-lyzed.

The limited resolution of the agarose gel electrophoresistechnique, combined with die hypervariability of the detectedminisatellite loci, make it impossible to score die alleles dis-cretely, resulting in quasi-continuous allele distributions (Bu-dowle et aL, 1991). Therefore, allele classes have to be con-structed before analysis can take place. In a previous analysis(Verheyen et aL, 1995), we estimated the allele sizes by com-paring die migration distance of die fragments to the migra-tion distance of length markers (Duggleby et aL, 1981). Thealleles were then grouped in 100 base pair (bp) classes, andeach class was considered as an allele.

We checked relatedness between die young in die nest anddie parents at die nest primarily using the multilocus DNAfingerprinting technique. However, the results were doublechecked using die SLPs and the DLP. The exclusion proba-bility (Weir, 1990; based on die 100 bp classes) for each mark-er separately ranges from 0.71 up to 0.90. For die combina-tion of all markers this probability exceeds 0.999 (details not


Kempenaen et aL • Female choice for extrapair paternity 483

Table 1

Variable measured

Wing lengthTunis lengthAvenge strophe lengthAvenge pause lengthProportion of time singingAverage number of notes per strophe

xisttes

F

18.039.89.46

19.83.125.95

df

140.148129,207

19.2319,2319,2321,25

T

.89

.94

.80

.89JO.70

P

<.0001<.0001•C0001<.0001<.01<.0001

See text for further explanation.

shown). The markers therefore are extremely useful in par-entage exclusion.

To identify the biological fathers, we stored the genotypesof all adult individuals in a genetic database. For each extra-pair young, we determined the size of the paternal allele forat least three markers. By comparing the genotypes of indi-viduals analyzed more than once on separate gels, we ob-served that alleles differed by an average of 0.75% (procen-tual deviation) from their mean size. We added and subtract-ed at least three procentual deviations from the paternal allelein the extrapair offspring, and we then identified all individ-uals in the database with an allele within this range. We ap-plied this strategy for four SLPs for the 1990 data (MSI, 3,11, and 14) and for three SLPs (MSI, 3, and 14) and one DLP(MS8) for die 1991-1992 data. Using this strategy, no or onecandidate biological father was identified. The probability ofpaternity (W, Weir, 1990) was then calculated for these fa-thers. In these calculations all allele frequencies within 2 pro-centual deviations of the paternal allele of the extrapair youngwere combined (Baird et aL, 1986). The mean Wwas 99.6%(range: 96.900-99.997%; details not shown).

Morphological measurement!

For most adults we measured tarsus length (mm), wing length(mm), and body mass (g). Similarly, we measured the tarsuslength and body mass of all nejtlingi at age 15 days. The wingwas measured to the nearest 0.5 mm using a ruler and ac-cording to Svensson's (1992:20-21) "maximum length" meth-od. For individuals measured more than once during oneyear, we used average values in our analyses. Measurementsfrom different years could not be averaged because winglength increases with age (data for n — 15 individuals thatbred as juvenile and adult; first yean 65.03 ± 0.94 SD, secondyear 67.08 ± 1.10 SD; paired t test: I = 7.65, df = 14, p<.001). To control for age effects, we standardized (mean = 0,SD " 1) wing length within age classes.

We measured the tarsus with calipers to the nearest 0.1 mm.In 1990, the tarsus was measured from the notch on die backof the intertarsal joint to the lower edge of die last completescale before the toes diverge (see Svensson, 1992:27). From1991 onward, measurements were taken up to the last but onescale. From 34 individuals measured in 1990 and later, wecalculated that the average difference using die two methodswas 1.0 mm. Therefore, we subtracted 1.0 mm from all the1990 measurements to make diem comparable with thosetaken later. Since tarsus length does not change over the lifeof the bird, we used average values for individuals measuredmore than once both within and between years.

Birds were weighed (estimate to die nearest 0.1 g) using a30-g Pesola spring balance. Because of substantial seasonaland daily fluctuations, body mass is not a useful measure tocompare individuals, unless all measurements are takenaround die same time. Therefore, we used body mass mea-

surements taken in die morning from adults feeding their8-day-oki offspring. We used die residuals of die regression ofIn (body mass) on m (tarsus length) as a measure of condition.

Because we caught and measured many individuals multipletimes, we could calculate repeatabilities for most measure-ments, allowing us to assess their reliability (Lessells and Boag,1987). Table 1 shows that all repeatabilities are highly signif-icant Tarsus length is die most reliable of die measured traits.

Song recording and analyst!

In 1990 and 1991 one of us (B.K.) recorded song during diedawn chorus using a UHER CR 1601 cassette recorder con-nected to an UHER M646 microphone, mounted in die focusof a Sony (pbrSSO) parabolic sound reflector. In 1990, diesong of 18 males was recorded between 13 March and 18April, hi 1991, 44 males were recorded between 4 April and3 May. Recordings were made between 0500 and 0720 h (Bel-gian standard time) on mornings widiout rain or strongwinds. We recorded each male for about 10-30 min, so diatone to three males could be recorded during one morning.We limited our analyses to include only those males recordedduring die presumed fertile period of their mate (i.e., from5 days before die first egg was laid until die morning thepenultimate egg was bid). Five males were recorded in bodiyears, but to avoid pseudo-replication we used only die longestrecording for each of these males.

Tapes were analyzed using a Unigon 4600 Spectrum ana-lyzer (Uniscan). Blue tits sing different song types (see Bijnensand Dhondt, 1984). For our analyses, we only used die mostcommon song types sung during die dawn chorus (types SI,S2, S3, and S9 according to Bijnens and Dhondt, 1984; seealso Bijnens, 1988). For each strophe, we measured die totalnumber of notes, die total duration of die strophe (strophelength), and die duration of die following pause (pauselength). Song rate was defined as die proportion of die totaltime die bird is actually singing and was calculated as die sumof all die strophe lengths divided by die total recording time(=» die sum of all strophe lengths plus die sum of all pauselengths). These measurements were only used in our analysesif a minimum of 50 strophes were recorded during a contin-uous song bout. We were able to use data from 25 differentmales. We did not have enough multiple recordings of diesame male to calculate repeatabilities. However, to get someidea of die relevance of our measurements, we calculated re-peatabilities for different song types sung by die same male(usually, but not necessarily, during die same morning). Allsong characteristics showed highly significant repeatabilities(Table 1), which justifies combining measurements from diedifferent song types.

Our analysis of song characteristics is limited in that we didnot measure repertoire size, nor did we measure die totalduration of die dawn chorus or die number of song typessung during one dawn chorus. However, strophe length is


484 Behavioral Ecology VoL 8 No. 5

Table 2apair paternity data £n i a blue tit population (plot C, 1990-1993)

1990 1991 1992 1993 Total

% of nests with extnpair young(total number of nesti fingerprinted)

% of males that lost paternity(total number of males)

% of extrapair offspring(total number of offspring)

% of extrapair offspring per nest(mean ± SD)

% of nests with >1 extrapair father(number of nests with extrapair young)

% (number) of nests with extrapairoffspring where biological fatherwas successfully determined

% (number) of extrapair young thatcould be assigned to a male

30.6(36)34.4

(32)10.5

(314)

42 ± 2927.3

(11)81.8(9)

72.7(24)

44.7(47)47.5

(40)14.1

(384)

35 + 259.5

(21)71.4

(15)

70.4(38)

42.1(38)45.5

(33)12.4

(331)

35 ± 256 J

(16)87.3

(14)

80.5(S3)

47.7(44)52.5

(40)11.6

(414)

27+190.0

(21)

41.8(165)

45.5(145)

12.5(144S)

33 ± 248.7

(69)__

If more than two paternal alleles were found with the single-locus probes and double-locus probes (see Methods), we concluded that therewas more than one extrapair father.

probably a good measure of male quality in the blue tit be-cause Bijnens (1988) found a relation between average stro-phe length and survival.

Ddmiiliilng age ana sac

Age of breeding birds was determined according to Svensson(1992) to distinguish between juveniles (born during the pre-vious season) and adults (more than one year old). Based onthe known history of marked birds, we could determine theexact age (for individuals ringed as nestling or as juvenile) orthe minimum age (for individuals ringed as adults, we as-sumed they were 2 years old when ringed).

Nestlings were sexed based on the intensity of the blue col-or on the newly developed wing and tail feathers. Based onthe known sex of individuals that survived and reproduced inthe population (local recruits), we correctly sexed 86% of thenestlings (n - 57 local recruits) from the 1990-1992 breedingseasons. Males were more likely to be sexed correctly as nest-lings (92% of 39) than females (72% of 18; Fisher's Exact test,p - .0493).

Definitions and data analyse*

An adult bird that bred in year Xwas considered as survivinguntil the next breeding season if it was observed in year X+lat least until the start of the breeding season (nest building).Offspring were considered local recruits if they started a min-imum of one breeding attempt (at least egg laying) within thestudy area.

Data were analyzed using the statistical packages SPSS/PC+, GUM, and StatXact-Turbo with standard techniques(Crawley, 1993; Sokal and Rohlf, 1981; StatXact, 1992). Alltests are two-tailed unless stated otherwise. For multiple 2 X2 contingency tables, we calculated a common odds ratio andtested the null hypothesis that this ratio is equal to one (Man-tel-Haenszel inference; StatXact, 1992).

We investigated which male characteristics females choosein two ways. First, we tested whether, in a given year, malesthat lost-paternity are different from those that did not losepaternity. In all analyses, each male was only used once (i.e.,for porygynous males, we calculated the proportion extrapairyoung on the total number of of&pring in all their nests).

Second, we compared the extrapair male(s) with the social

male they cuckolded with pairwise tests. This is the strongesttest because it directly reflects female choice. For this test, wecombined the data over all years where paternity was assigned(1990-1992). In some nests, young were fathered by two ex-trapair ™ l w In such a case, we calculated mean values forthe two extrapair males. Some males fathered extrapair youngin different nests, but each case (nest) can be considered anindependent event of female choice.

The correlation matrix with all male characteristics showedno significant correlations between any of the morphologicalmeasurements (all p > .05). Average strophe length wasstrongly correlated with average number of notes sung (r =.92, n = 25, p < .001), and average pause length was corre-lated with the proportion of time singing (r m - .75, n «= 25,p < .001). Therefore, we only used two song variables (aver-age song length and average pause length) in further analyses.

RESULTS

Fkwjoency and patterns of extnpair paternity

We studied extrapair paternity in 4 years for a total of 165nests and 1443 of&pring. Each year, we found extrapair pa-ternity in 31-47% of the nests, and 11-14% of all offspringwere fathered by an extrapair male (see Table 2). Extrapairyoung were not distributed randomly over the nests (Figure1). More nests than expected contained either no or manyextrapair young.

We assigned paternity, Le., found the biological father ofthe extrapair offspring, in most, but not all cases (Table 2).We do not believe that floater males fathered of&pring be-cause it is highly unlikely that such males were present in thepopulation (Kempenaers, 1994a). Moreover, many males thatwere caught in winter but later disappeared were included inour genetic analysis, and none of them turned out to be acandidate father. It is more likely that the other extrapairmales were males breeding in the study area (in natural cav-ities) or just outside the study area for which we did not havea blood sample.

In 87% of 46 nests with more than one extrapair young, all -the extrapair young were fathered by a single male, while inthe other six nests (13%), two different males fathered extra-pair young. Most males that lost paternity did not gain pater-nity in other nests (73% of 11 males in 1990, 85% of 20 males


Kempenaers et s i • Female choice for extrapair paternity 485

0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9

Proportion extra-pair young in the nest1.0

figure iDistribution of extrapair roung over the nests (data from 1990-1993). We used a logEnear model, controlling for the number of young pernest, to analyze whether the distribution differed from expectation under a binomial distribution. This was the case for all years (1990: j * —111.29. n - 36 nests, p < .001; 1991: *» - 144^3, n - 47 nests, p < .001; 1992: *» - 113.56. n - 38 nests, p < .001; 1993: f - 115.04, »- 44 nests, p < .001).

30 -

1 2 3 4 5

Distance in number of territoriesFigure 2Frequency distribution of the distance (in number of territories)that extrapair males bred from the territory where they fatheredoffspring (1 • nearest neighbor).

in 1991, and 73% of 15 males in 1992). Males never "ex-changed" paternity—i.e., fathered offspring in each other'snests. The extrapair male(s) were usually the nearest neigh-bors, although in a few cases they bred as far as four to fiveterritories away from the territory where they fathered off-spring (Figure 2).

For 28 males breeding in different years (2-3) with thesame (8 males) or with a different (20 males) female, therewas a significant repeatability in the proportion of young theyfathered in their own nest ( f^ , - 3.18, r = .51, p < .005).From 20 males that bred in different years with different fe-males, 9 males (45%) either never lost paternity or lost pa-ternity in each breeding season, while 10 males (50%) onlylost paternity in the last year they were present. Only 1 male(5%) lost paternity in the first year, but not in the second(Table 3). Of the eight males that bred with the same femalein different years, six never lost paternity (Table 4). Thus,males that bred with different females in subsequent yearswere more likely to lose paternity (75%, n •* 20) than malesthat bred with the same female (25%, n = 8, p •* .0299, Fish-er's Exact test). Unlike males, females that bred in differentyears with different males often had extrapair young in theirnest in the first year, but not in the next (or vice versa). Table5 suggests that females engage in extrapair copulations de-pending on the male with which they are paired. Femalesbreeding with a different male were also more likely to engagein extrapair copulations (85%, n = 20) than females breedingwith the same male (25%, n °» 8, p - .0048).



Table 3of

t yea

Male lostpaternity inyear X

a l a binding with dlfleieul females (a • 20

NoYes

Male lost paternity inyearX + 1

No Yes

105

Data are from 1990 to 1993 unless otherwise indicated. Individualsthat bred in 3 yean are entered twice.

lableSPatterns of filiii»ali paternity for males and females breeding mdifferent years females breeding with different males (* - »females)

Femaleengaged inEPCilnyear X

NoYes

Female engaged inEPCsinyearX+ 1

No Yes

EPCs, extrapsir copulations.

Most males breeding in different yean either did or did notfather cxtrapair offspring in all years they were present (69%of 26 males). Only one male (4%) fathered extrapair off-spring in the first year, but not in the next (Table 6).

rterffMaled

We found no significant effect of male age on the likelihoodof losing paternity (Table 7). In 1 year out of 4, males thatlost paternity had significantly smaller tarsi than nudes thatdid not lose paternity (Figure 3), and males did not differ inwing length (Table 8). In 1 year out of 3, males that lost pa-ternity were in better condition (body mass/tarsus length)than males that did not lose paternity (Table 8). Males thatlost paternity were less likely to survive than males that didnot lose paternity, while there was no difference in the sur-vival of their mates (Figure 4). Males that lost paternity hadshorter average strophe lengths (1.3 s ± 0.5 SD, n - 9) thanmales that did not lose paternity (1.8 s ± 0.2 SD, n = 16; t— 3.37, df - 19.23, p < .005), but the average pause lengthdid not differ (extrapair-voung males: 3.9 s ± 4.4 SD, n •» 9;no extrapair-young males: 3.6 s ± l.S SD, n •» 16; r - 0.15,df •• 8.77, p > .5). A logistic regression with proportion ofextrapair young as the dependent variable and male tarsuslength, average strophe length, and average pause length asthe explanatory variables showed only a significant effect ofaverage strophe length (Figure 5).

The extrapair males, when compared with the males theycuckolded, had larger tarsi and a lower condition and theysang longer strophes with longer pauses between strophes.Extrapair and within-pair males did not differ in standardizedwing length (Table 9). Extrapair males were also older onaverage than within-pair males: of 37 pairwise comparisons,only 5 extrapair males were younger, 14 were the same age,and 18 were older (sign test: p < .05).

Offspring characteristics and extrapair paternity

Males that lost paternity were less likely to recruit their ownoffspring in the population than males that did not lose pa-

Table 4Patterns of t apair paternity for males and females breeding mduTaent years: pairs biceding together in different years (a • 8)

Extrapairyoung innest iny e a r * •

NoYes

Extrapair young in nestin year X + 1

No

70

Yes

11

ternity (only males that produced at least one fledgling areincluded; 1990: 20% of 10 males versus 32% of 19 males, 1991:0% of 14 males versus 16% of 19 males, 1992: 33% of 12 malesversus 41% of 17 males), but the difference is not significant(common odds ratio for three 2 X 2 contingency tables "2.14, p m .18). Moreover, males that lost paternity fatheredfewer fledglings, and a loglinear model (GLIM), controllingfor the number of fledglings, showed no differences in theprobability of recruiting an offspring between males that didor did not lose paternity (all p > .10).

In 10 nests with <mixed paternity where part of the brooddied between day 14 and fledging (possibly due to starvation),the extrapair young were more likely to survive than the with-in-pair young (61% ± 28 SD of within-pair young versus 80%± 36 SD of extrapair young survived; common odds ratio forten 2 X 2 contingency tables - 7.918, p - .046).

Offspring sex ratios (proportion of males) did not differbetween nests with extrapair young (0.52 ± 0.12 SD, n - 60)and nests without extrapair young (0.51 ± 0.11 SD, n • 81;Mann-Whitney Utest, U, •• 2709.5, p > .2). However, in nestswith mixed paternity, the extrapair young were more likely tobe males than the within pair young (extrapair young: 0.61 ±0.37 SD, within-pair young: 0.50 ± 0.17 SD, n = 57, sign test:p < .025).

In nests with mixed paternity, the extrapair young did nothave significantly longer tarsi than the within-pair young (ex-trapair young: 14.73 ± 0.53 SD, within-pair young: 14.65 ±0.42 SD, paired Meat t = 1.38, df = 56, p > .10). However,extrapair young were significantly heavier than within-pairyoung (extrapair young: 10.44 ± 0.91, within-pair young:10.26 ± 0.83, t - 2.43, df = 56, p< .025). Since extrapairyoung are more likely to be males, this result could be foundif male offspring are, on average, larger and heavier than fe-male offspring at age 15 days, which is indeed the case (bothwhen comparing male and female within-pair young and maleand female extrapair young within nests, males are larger andheavier than females, all p < .01, data not shown). Male ex-trapair young were not larger, nor heavier, than male within-

Table 6Patterns of extrapair paternity for ««•!*• and females breeding indifferent years: males breeding in different years over 1990-1992 (a« 2 6 )

Fatheredextrapairyoung inyear X

NoYes

Fathered extrapairyoung in year X + 1

No

151

Yes

87


Kempenaers et aL • Female choice for extrapair paternity 487

Table7Proportion of male* (ample rixe) mat kwt paleiultj in relation totheir age

Age (yean)

Year 1 4+ b

1990199119921993Total

0.56 (14)0.41 (27)0.46 (13)0.44 (25)0.42 (79)

0.40 (10)0.50(6)0.62 (13)0.50(8)0.51 (37)

0.25 (4)1.00 (3)0.00 (4)0.86(7)0.56 (18)

0.25 (4)0.50(4)0.33(3)— (0)0.36(11)

1.00.38.21.17

• p value from Fisher's Exact probability test.b Males 4 years or older were grouped in one category.

pair young, and the same is true for female offspring (pairedt tests, all p> .25).

There is no evidence that extrapair young are more likelyto survive locally until the next breeding season than within-pair young from the same nest, but the sample size is smalLYoung were recruited from 17 (28%) of 60 nests with extra-pair young. From those nests, on average, 15% (± 9 SD) ofthe within-pair young were recruited and 17% (± 30 SD) ofthe extrapair young. A GLIM model for the 17 mixed pater-nity nests with recruits using recruitment as the binary re-sponse variable and nest and status of the offspring (extrapairor within-pair) as factors showed no effect of nest (jf = 3.91,df •• 16, p > 3), nor of status (jf - 0.09, df - 1, p > £).

drapafa- paternity: do females choose particular

DISCUSSION

Patterns of imales?

In all 4 yean, extrapair paternity was common in our blue titpopulation. Because there were no cases of mate switchingduring nest building or egg laying, die possibility that mixedpaternity was caused by rapid mate switching could be ruledout (see, e.g., Pinxten et aL, 1993). The strongest evidencefor female choice for extrapair paternity is the behavioral ev-idence reported earlier (1) females actively seek extrapaircopulations from particular males often by intruding in theterritory of this male (Kempenaers et aL, 1992), and (2) whenthe resident male was experimentally removed, females re-fused to copulate with most of die intruding males (Kempen-aers et aL, 1995). Data on the patterns of extrapair paternityreported here are consistent with these behavioral observa-tions (see Kempenaers and Dhondt, 1993): (1) more oftenthan expected under a random distribution, nests contained

20 11 20 19 18 15 16 19

p< .10

1990 1991 1992 1993

YearFigure 3Tarsus length (+ SE) of males that did (shaded bars) or did not(open bars) lose paternity In their nests. Numbers at the top of thegraph indicate sample sizes. Differences between the two group* ofmales tested with / tests: 1990, ( - 3.17, df - 29, p < .005; 1991, (- -0.94, df - 37, p > J; 1992, / - 1.83, df - 31, .05 < p< .10;1993. t - 0.64, df - 33, p > J ) .

either no or many extrapair offspring, (2) in most cases allthe extrapair young in one nest were fathered by die tamemale, (3) extrapair paternity was never reciprocal, and (4) alldie extrapair fathers that could be determined were residentmales breeding in die population and usually they werenear(est) neighbor(s). These patterns are similar to thosefound in many other socially monogamous or polygynous pas-serines (e.g., Gibbs et aL, 1990; Gray, 1996; Hasselquist et al.,1996; Stutchbury et aL, 1994; Westneat, 1992, 1993;~Wetton etaL, 1995; Whittingham and Lifjeld, 1995; Yezerinac et aL,1995). A notable exception is die tree swallow Tadtycmeta bi-colcrr. extrapair offspring in the same nest are often fatheredby different males, males do exchange extrapair young, andmost of die extrapair fathers are not found on die tame nest-box grid (Dunn et aL, 1994). Also, in the yellow warbler Dtn-droica ptUchia, extrapair males were sometimes nonresidentmales, and one case of reciprocal cuckoldry was found (Yez-erinac et aL, 1995). Wetton et aL (1995) also found one caseof reciprocal cuckoldry in die house sparrow Passer domtsti-cus. Under die "good genes" hypothesis, it seems unlikelythat females would choose to copulate with unpaired males

Table8

Yfear EPY

wing leuglli and condition of —•!»? ***•* did and did not l o t paternity in their nesti

Standardized wing length Condition'

Mean £ SE n t p Mean ± SE

-0.0093 i0.0093 i

-0.0169 10.0261 i0.0082 =

-0.0082 2

i 0.014: 0.010t 0.014t 0.013: 0.011: 0.013

n

161617111616

1900

1991

1992

1993

NoYesNoYesNo

. YesNoYes

-0.14-0.36-0.03

0.14-0.03

0.24

-0.13

0.210570.170.280.210.320.18

0.27 i. 030

2011201918151718

0.64

-0.52

-0.74

-1.18

>*>

-1.06

-2.12

0.97

<.05

(see Methods).



21 11

/>•» .0006

21 19 19 16 (a)

p - .06 p - JOOS

24 11 25 20

l JO

22 16

(b)

Figure 4Survival to the next breeding i e u o n for (a) males and (b) femalesthat d id (shaded bars) or did not (open bars) have extrapair youngin their nests. Numbers at top of each graph indicate ample sizes.The Rvalues are from Fisher's Exact probability test.

or floaters because such males are likely to be of lower quality(they were unable to get a territory or a mate) and becausefemales can probably better assess male quality of knownneighbors than of passing floaters. Also, reciprocal cuckoldryis not expected unless females differ in their preferences.

Which m*i» traits do fenisles choose *TT^ how ***** *K#ybenefit from their choice?

Our earlier finding (data from 1990) that males that lost pa-ternity were smaller (in tarsus length) than males that did not

0.0 -

1.0 1.5 Z0 2.5

Mean strophe length (s)

3.0

Figure 5Relation between the proportion of extrapair young in the nest andthe average strophe length (s) sang by the male during the dawnchorus (data for 25 males from 1990 and 1991). The curved line bbased on the parameter estimates of a logistic regression withequation p « «***/(l + «•**•) where p « proportion of extrapairyoung, x - average strophe length, a - 5.674 (1.635 SE) and ft - -5.496 (1.273 SE). The model yvp1»in. 39% of the total variation inproportion of extrapair young <j? m 16.75, df ~ 1, p > .001).

lose paternity (Kempenaers et aL, 1992) was only partly con-firmed (a similar trend in 1992). However, a pairwise com-parison of the social male and the extrapair male(s) that fa-thered offspring in his nest confirmed that extrapair maleshad longer tarsi. Tarsus length in blue tits is heritable(Dhondt, 1982), and a within-nest comparison of within-pairand extrapair young showed that the extrapair young on av-erage had longer tarsi, but the difference was not significantdespite a reasonable sample size. It is unclear how the off-spring would benefit from having longer tarsi If tarsus lengthis a measure of overall size, then larger individuals may bebetter able to compete over resources such as food, roosting,or nesting sites, but this remains to be shown. Wing length isalso a measure of size, which increases with age. However,standardized wing length (controlled for age) did not differbetween males that were or were not successful in protectingtheir paternity or in gaining extrapair offspring. In a similarstudy on red-winged blackbirds (Agdatus photnicrus), Weath-erhead and Boag (1995) showed that larger males were moresuccessful in siring young (on their own territory and extra-

Table 9Pali w i t comparisons of chaneteriadca of »«n»|»»ii males and hin-pair

CharacterWi thin-pairmales*

Extrapairmales*

ales fathering young in the same nest (data from 1990 to 1992)

n t p

Tarsus lengthStandardized wing lengthCondition*Average strophe length (s)Average pause length (s)

14.62 ± 0.530.07 • 1.12

0.024 ± 0.0381.29 • 0.23235 * 0.75

15.01 ± 0J10.22 • 0.92

-0.033 • 0.0531.77 ± 0.253.77 ± 1.18

35321866

-2.82-0.56-3.28-3.02-3.11

<.0O5<.O5<.O5

• Means * SD.• Residuals (see Methods).



pair young) and that male body size was positively correlatedwith survival.

Remarkably, we found that males that lost paternity were inbetter condition (Le., heavier relative to their size) than malesthat did not lose paternity (significant in 1 year out of 3), andextrapair males had a significandy lower condition than thewithin-pair males they cuckolded. There are several possible,not mutually exclusive, explanations for this finding. Sincebody man was measured during the nestling stage, it is pos-sible that the successful males invested more in their offspringeither because they had larger broods or more than onebrood or because cuckolded males responded by feeding less.Successful males might also invest more in mating display(e.g., song) and in sperm production because they are likelyto copulate more frequently or over a longer period. It seems,however, that successful males are able to invest more becausetheir lower condition did not result in a lower probability ofsurvival. An alternative explanation is that high-quality malesare able to reduce the costs associated with fat storage (Witterand Cuthifl, 1993), for example, because they are better for-agers or have better resources available, while low-qualitymales may have to insure against uncertain foraging successby carrying larger fat reserves. Whether this is the case duringthe breeding season is unknown, but at least in wintering tits,dominant individuals carry less fat than subordinates (e.g.,Ekman and IilliendahL 1993).

Within nests, die extrapair young were significantly heavierthan the within-pair young, but we also found that extrapairyoung were more likely to be males. When analyzed separatelyfor each sex, within-pair young and extrapair young did notdiffer in tarsus length, nor in body mass. These data are dif-ficult to interpret because our method of sexing is based onplumage characteristics (intensity of the blue color) andtherefore probably not independent of die size of die chick(Le., a chick that develops more slowly and is thus smaller orweighs less at age 15 days is more likely to be scored as afemale). Ideally, we would want to determine sex of die nest-lings using a molecular marker. On die other hand, recap-tures of local recruits showed that our method was quite re-liable (see Methods).

We did not find a difference in sex ratio between nests withand without extrapair young, but our (preliminary) findingthat extrapair young are more likely to be males supports diehypothesis that females manipulate die sex ratio in relationto male quality or attractiveness (e.g., Burley, 1981). Othersupport for this hypothesis comes from a study of blue tits bySvensson and Nilsson (1996), who showed that females matedto males diat survived until die next season produced broodswidi male-biased sex ratios. Females might benefit from pro-ducing extrapair sons if, in nests with mixed paternity, dieextrapair offspring might become more attractive or betterable to compete, which would affect the future reproductivesuccess of sons more than that of daughters.

The probability of losing paternity did not depend on dieage of die male (Le., males of all ages were equally likely tolose paternity). However, die extrapair males were on averageolder than die within-pair males they cuckolded. This has alsobeen found in die purple martin Progru subis (Morton et aL,1990), die red-winged blackbird (Weadierhead and Boag,1995), and die house sparrow (Wetton et aL, 1995), and itsupports die hypothesis that females acquire "good genes"for their offspring because it is likely that older individuals inthe population are of higher genetic quality than average(Trivers, 1972). The above results, together widi die obser-vation that males are more likely to lose paternity in die sec-ond of two breeding seasons (Tables 3-6), may seem contra-dictory. A possible explanation is that when males get older,some become very attractive (e.g., those in good condition),

while othen become less attractive (e.g., diose in bad condi-tion).

Cuckolded males were less likely to survive than males diatdid not lose paternity (significant in 2 years out of S), butthere was no difference in female survival, which suggests diatdie difference in male survival is caused by differences in malequality rather dian in territory quality. Moreover, we founddiat in multiple paternity nests widi partial brood mortality,die extrapair young were more likely to survive dian die wid>in-pair young. These findings strongly suggest diat females ob-tain indirect fitness benefits from their choice of extrapairfadiers. However, die results from die nests widi partial broodmortality should be interpreted cautiously for die followingreasons. First, die sample size is limited to 10 nests and diedifference is only marginally significant Second, in case ofharrhing asynchrony, it is likely diat young nestlings suffermore mortality dian die older ones in die brood. If hashingasynchrony occurred and if die extrapair young are more like-ly to be die older nestlings, we would indeed find diat extra-pair young survived better, but diis may have nodiing to dowidi good genes. Unfortunately, we have no data on die exactchick age (hatching asynchrony) nor on die pattern of extra-pair paternity in relation to die order of egg laying (or hatch-ing). Third, die differential survival of extrapair and within-pair chicks might result from sex-biased mortality (becauseextrapair young are also more likely to be males). Our meth-od of sexing nestlings (based on plumage characteristics) isnot suitable to check whether mortality is sex biased becauseit is not independent of die age or condition of die chick (seeabove).

The data on longer term survival (recruitment) of offspringshowed diat males diat lost paternity were not less likely tolocally recruit offspring when controlling for die number offledglings they fathered. There is no evidence diat extrapairyoung have a higher chance to recruit dian within-pair youngfrom die same nest. Akhough they would potentially providedie strongest evidence for die good genes hypothesis, dieproblems widi this type of data are diat local recruitment isnot the same as total recruitment and die effect may be toosmall to detect given die low numbers of local recruits.

It is difficult to find out which cue(s) females use to assessthe quality of their social mate and diat of potential extrapairfadiers. Nevertheless, we determined at least one cue diat fe-male blue tits can use: die average length of strophes sungduring die dawn chorus. Since most extrapair copulations inblue tits were observed early in die morning just after diefemale left die nest-box (Kempenaers, 1994b) and since ex-trapair males are usually close neighbors, it is not unlikely diatfemales choose males based on their dawn chorus perfor-mance. Song characteristics have been shown to be importantcues for mate choice in many passerines (e.g., Catchpole etal., 1986; Collins et aL, 1994; Eens et aL, 1991; Lampe andSartre, 1995), and a recent study on die great reed warblerAcroaphahu arundinacrus showed diat females obtained ex-trapair young from males widi larger song repertoires (Has-selquist et aL, 1996).

The function of die dawn chorus has been subject of muchspeculation and study. Based on observations diat in manypasserines die intensity of die dawn chorus is positively relatedto female fertility (e.g., Cudull and Macdonald, 1990; Greig-Smith, 1982; Mace, 1987; Meller, 1988; Welling et al., 1995;but see Part, 1991; Rodrigues, 1996), it was hypothesized diatdie dawn song of paired males functions as a paternity pro-tection mechanism (mate guarding), as courtship behavior'stimulating their own mate to solicit copulations, or as a strat-egy to obtain extrapair copulations (Greig-Smith, 1982; Mail-er, 1991b, see also Slagsvold et aL, 1994). However, die ideadiat dawn singing functions to repel potential cuckolders is



not supported by the data (e.g., Part, 1991; Slagivold et aL,1994). This study strongly suggests that females choose malesas extrapair copulation partners based on a characteristic oftheir dawn chorus song (strophe length). Our data thus sup-port Mailer's (1991b) hypothesis that dawn singing is a strat-egy to obtain extrapair copulations, although as Slagsvold etaL (1994) pointed out, this is unlikely to be the only expla-nation for the existence of the dawn chorus.

Consistency and Hmh«Ht»M of female choice

If females choose to engage in extrapair copulations with par-ticular males to obtain genetic benefits, we would expect themto be consistent in their choice (M#Uer, 1994b); Le., we wouldexpect that male success in avoiding cuckoldry or gaining ex-trapair offspring in different breeding attempts is repeatable.This was indeed the case: the proportion of young fatheredby males breeding in different years was highly repeatable.However, a detailed look at individual males showed a morecomplex pattern. If the attractiveness of a male is reflected bythe fact that he does or does not lose paternity, we found thatfrom one year to the next males rarely increased, but oftendecreased, in attractiveness (Tables S, 5). This may seem tocontradict the good genes hypothesis. However, it is importantto realize that male quality or attractiveness should be consid-ered relative to the quality or attractiveness of the group ofmales from which the female can choose (Le., the close neigh-bors). Therefore, male quality does not necessarily have tostay the same in different years, and we should not expectthat all males who father extrapair young do not lose paternitydiemserves. Another reason males might decrease in attrac-tiveness (measured as loss of paternity) is that in their finalbreeding season, some males may already be in a bad condi-tion, which may be reflected in a cue their female uses todetermine his quality (e.g., song). Data on changes in songoutput of individual males in relation to their subsequent sur-vival would provide a test of this hypothesis. Males that bredwith the same female rarely changed in attractiveness (mea-sured as loss of paternity), which suggests consistency of fe-male choice. There is no evidence that particular females aremore likely to engage in extrapair copulations (Table 5) in-dependent of their mate's attractiveness. There was also someconsistency in the probability that a male will father extrapairyoung. Most males either never fathered extrapair young, orthey fathered extrapair young in all die years they were pres-ent (Table 6). Moreover, males that did not father extrapairyoung in their first breeding season could often father youngin later seasons, but the reverse was rare.

Female blue tits are restricted in their choice for a breedingmate (Kempenaers, 1994a), but it seems that they can modifytheir choice for a father for their offspring. If females benefitfrom having their offspring fathered by a male other than thesocial male, then why is extrapair paternity not more com-mon? And why do not all females mate with the most attrac-tive male of die population? dearly, there are also severalconstraints on this type of choice. First, females are probablyunable to select any male from the population as father fortheir offspring; extrapair fathers are usually (close) neighbors.This may be because females cannot assess die quality of malesthat are breeding farther away or because they cannot getcopulations with those males. Either die female or die malehas to leave die territory and travel a long distance to copu-late, aad this seems unlikely to happen because of die risk ofdetectidn by other territorial birds, resulting in aggressive en-counters. Thus, females can only choose from those malesbreeding in die vicinity (see also Meller, 1994a, for choice ofa breeding partner). Second, extrapair paternity is die resultof a conflict of interest between die social male, die extrapair

male, and die female (Iifjeld et aL, 1994), and it is highlyunlikely that die female would always win. Females often cop-ulate widi their social partner during die fertile period (Kem-penaen et aL, 1995), which may be necessary to receive malehelp in raising die brood (e.g., Davies et aL, 1996). Also, malesdo guard their females, and although diey are often not en-tirely successful (see Kempenaers et aL, 1995), it is likely thatguarding does help to some extent to protect their paternity.Because male parental care is often so important for repro-ductive success, females might have to walk a tightrope be-tween evading die guarding male and assuring his confidenceof paternity. Finally, females must be able to assess male ge-netic quality via one or several behavioral or morphologicalcues reflecting quality, which might cost considerable time.

General conclusion

Our data provide farther evidence for die hypothesis thatblue tit females seek extrapair paternity to obtain good genesfor their offspring. This study thus adds to a growing body ofevidence that females can obtain indirect genetic benefitsfrom their choice (e.g., Alatalo et aL, 1991; Hasselquist et aL,1996; MoUer, 1991a, 1994a; Petrie, 1994). In many other birdspecies, die available data on extrapair paternity are generallyconsistent with die good genes hypothecs. However, detailedstudies on die performance of extrapair versus within-pair off-spring are still needed to critically test die good genes hy-pothesis. The next step will be to formulate and test hypoth-eses ^plaining the variation in die level of extrapair paternity,both among species and among populations of die same spe-cies.

We are grateful to Frank Adriaensen, Fran* Fierens, and WernerPkunpen for their help in the field. We thank the Bncht family forkindly allowing ui to work on their beautiful estate, Marleen van denBroeck for her good DNA cooking capabilities, Christine van Broeck-hoven for providing laboratory ipace, Frank Adriaensen and FrantFierens for their help with retrieving data from the riarahaw, Stefanvan Dongen for statistical advice, and Luc Bijneru and Marcel Ecrufor their help with the song analyses. Marcel Ecus, Herbert Hoi, Ri-anne Pinxten, Tore Slagsvold, Michael Tabonky and an anonymousreferee provided constructive comments. BJL was supported ai a re-tearch assistant of the Belgian National Fund for Scientific Researchand by the Austrian Academy of Sciences.

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Extrapair paternity in the blue tit (Parus caeruleus): female choice ...

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