Behavioral Ecology Vol. 8 No. 5: 481-492
Extrapair paternity in the blue tit
(Parus caeruleus): female choice, male
characteristics, and offspring quality
Bart Kempenaers,*^ Geert R- Verheyen,* and Andre A- Dhondt**
•Department of Biology, University of Antwerp, U.I A., B-2610 Wilrijk, Belgium, bAustrian Academy of
Sciences, Konrad Lorenz-Institute for Comparative Ethology (KLIW), Savoyenstrasse la, A-1160
Vienna, Austria, and "KHornell Laboratory of Ornithology, 159 Sapsuckcr Woods Road, Ithaca, NY
14850, 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 obtain
indirect fitness benefits, we studied paternity in a blue tit population over 4 years. Extrapair paternity occurred in 31-47% of
all 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. Comparisons
between males that did and did not lose paternity and pairwise comparisons between the extrapair male(s) and the withln-pair
male showed that successful males had longer tarsi and sang on average longer strophes during the dawn chorus. Successful
males weighed less (relative to their size) during the nettling stage, but neverthalen they survived better. Male age did not
influence 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 brood
mortality. Our data also suggest that extrapair offspring were more likely to be males. Because extrapair males were usually
close neighbors, male quality should be considered relative to the quality of the neighbors. Despite this, we found consistency
in female choice over years. Our observations provide support for the hypothesis that female blue tits engage in extrapair
copuladons 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)]
S
perm competition is widespread among birds because in
many species females engage in extrapair copulations
and these copulations often lead to multiple paternity (Birkhead and Metier, 1992). Although sperm competition can be
considered as the ultimate form of male-male competition, it
is now widely accepted that female choice plays an important
role as welL Active female choice for a copulation partner,
other than the social mate, has been clearly documented in
some species (e.g., Gray, 1996; Houtman, 1992; Metier, 1990;
Smith, 1988; Wagner, 1992). Even in species where behavioral
evidence for choice is lacking, it is likely that females have at
least some control over paternity (Iifjeld and Robertson,
1992). This is because (1) in most species males do not have
an intromittent organ, and female cooperation may thus be
necessary for successful insemination (Fitch and Shugart,
1984), and (2) female choice of paternity may not only work
via behavioral control of copulations, but it may also involve
a postcopulatory control over which sperm fertilizes the eggs
("cryptic choice"; Adkiiu-Regan, 1995; Birkhead and Metier,
1993).
To optimize their reproductive success, female birds should
be choosy: they should prefer to breed with a male that defends high-quality resources (e.g., territory, nest site, food),
that is likely to invest a lot in parental care, and that is of high
genetic quality. However, the ability of females to choose is
probably restricted because (1) the quality of a male as a parAddreu correspondence to B. Kempenaen, KLIW, Savoyenstnsse
la, A-1160 Vienna, Austria.
Received 18 June 1996; revised 8 August 1996; accepted 21 November 1996.
1045-2249/97/J5.00 C 1997 International Society for Behavioral Ecology
ent, his genetic quality, and the quality of the resources he
defends are not necessarily positively correlated, (2) females
must compete with other females for the best breeding situation (Slagsvold and Iifjeld, 1994) and (3) females must be
able to assess the quality of the resources, the male's parental
abilities, and his genetic constitution. It is still poorly understood how the choice process works and what cues females
use to assess males, but choice for particular traits such as
plumage characteristics (e.g., color, tail length) or behavioral
traits (e.g., song, display) has been well documented in many
species (Andersson, 1994; Johnstone, 1995). Extrapair paternity can be considered as a way in which females can escape
some of the limitations on their choice; i.e., females can first
choose a social partner and then choose another male as father for (part of) their offspring (Mailer, 1992).
One of the most controversial issues in the study of female
choice in general, but particularly in the context of extrapair
paternity and in lekking species, is what benefits females gain
from their choice (Andersson, 1994; Johnstone, 1995; Keller
and Reeve, 1995; Kirkpatrick and Ryan, 1991; Sheldon, 1994).
Females should obtain substantial benefits because being
choosy is likely to be costly (Reynolds and Gross, 1990; see
also Sheldon, 1993). If females engage in extrapair copulations to escape some of the limitations on their choice, the
choice of a social mate could be based more on direct benefits
(resources, parental abilities), while the choice of a father of
the offspring could be based on indirect benefits (genetic
quality). However, evaluating the relative importance of direct
and 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
Behavioral Ecology Vol. 8 No. 5
482
many studies have suggested that females obtain genetic benefits 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 is
continuing (e.g., Birkhead and Fletcher, 1995; Sheldon,
1994). The suggestion that genetic benefits are important in
female choice for extrapair paternity is often based on the
absence of any dear direct benefit* (but see Sheldon, 1994),
but the critical test is still missing. Convincing evidence for
the "good genes" hypothesis would be to show that extrapair
offspring have higher fitness than witbin-pair offspring (e.g.,
because they survive better or because they, in turn, attract
more females; Kempenaers and Dhondt, 1993). So far, this
evidence is lacking because data on offspring performance
are hard to collect
The aim of this study was to investigate whether female
choice for extrapair paternity in the blue tit {Pans carruleus)
can be explained by females seeking to improve the genetic
quality of their offspring. The rationale behind this study is
as follows: (1) Extrapair paternity is common in the blue tit
(Kempenaers et aL, 1992, 1995). (2) Evidence for behavioral
control of paternity by females is strong because females actively seek extrapair copulations during their fertile period,
often by visiting neighboring males in their territory (Kempenaers et al., 1992) and mate-guarding intensity and copulation frequency do not explain differences in extrapair paternity between males, while female cooperation in mate
guarding does (Kempenaers et aL, 1995). (3) It is unlikely
that females gain any direct benefits from their choice. Females did not receive any resources from the extrapair males
and they did not forage during their extraterritorial visits, nor
did extrapair males provide any help in feeding or defending
the offspring (Kempenaers B, personal observation). Furthermore, it is unlikely that females engage in extrapair copulations to remate with a better male ("mate sampling hypothesis"; Heg et al., 1993). In our blue tit population divorce was
extremely rare (Dhondt and Adriaensen, 1994) and females
never remated with an extrapair male during the next breeding season (Kempenaers B, unpublished data). Finally, females are unlikely to gain benefits through an increased probability of having their eggs fertilized (see Kempenaers et aL,
1996). (4) We concluded earlier that females choose highquality males as extrapair partners because we observed that
males that lost paternity had a lower chance to survive and
were smaller (in tarsus length) than males that did not lose
paternity. This conclusion was based on data from only one
breeding season (1990). Here, we use data on extrapair paternity from four breeding seasons (1990-1993), and we assigned paternity for the 1990-1992 seasons, allowing a direct
comparison of characteristics of the within-pair and extrapair
males.
The paper is organized as follows. First, we investigated
whether die patterns of extrapair paternity are in accordance
with the idea that females choose particular males (see Kempenaers and Dhondt, 1993). We also investigated whether female choice is consistent (i.e., whether male fertilization success is repeatable). We therefore compared the males' success
in fathering offspring over different years. Second, we investigated which males are preferred by females by relating different characteristics of males (song output, morphology, age,
survival), wiffi their success in avoiding loss of paternity
and/or obtaining extrapair offspring. Third, we compared
characteristics (morphology, sex, survival) of extrapair and
within-pair offspring, and we discuss here whether and how
these characteristics can influence female fitness.
METHODS
General
We studied a blue tit population from 1990 to 1993 in the
17-ha wooded part of die private estate Calixbergen (51*15'
N, 4°28' E), in Schoten, north of Antwerp, Belgium. One hundred small-holed nest-boxes have been present since 1979,
and each year about 40-60 pairs breed in these boxes. All
individuals were captured and marked with a unique combination of color bands during the «""""" and winter (November-March). Nest-boxes were checked at least weekly, and all
nests were closely followed from the start of nest building until
fledging of the young. In total we followed 188 nesting attempts in nest-boxes over 4 years. Of these, 144 (77%) successfully produced at least one fledgling. Young were banded
and measured when 15 days old. From most adults and nestlings, blood samples (10-100 jil) were taken for DNA fingerprinting. Nestlings were bled when 14 days old. In addition,
we collected dead nestlings found in the nest before taking
blood and extracted DNA from the brain. For more details
on die study area and general methods, see Kempenaers
(1994b).
"'«y
and alignment
Details on the fingerprinting methods can be found in Kempenaers et al. (1992,1996) and Verheyen et aL (1994). Briefly,
to exclude paternity we carried out multilocus DNA fingerprinting for adults and nestlings from 1990 to 1993. We fingerprinted 165 nests (out of a total of 173 nests where at least
one nestling was born and including all nests with at least one
fledgling). We used HinU restriction enzyme and Jeffrey's
probe 33.15.
For all nests from 1990 to 1992 we used four hypervariable
minisatellite single-locus probes (SLPs; cPcaMSl, 3, 11, and
14) and one hypervariable double-locus probe (DLP; cPcaMS8) to assign paternity (i.e., to find the genetic father of
the extrapair offspring). Details on die isolation and initial
characterization of these blue tit specific markers and on die
techniques used during the processing of blood samples to
single-locus profiles can be found in Verheyen et al. (1994,
1995). In short, high molecular weight DNA was digested with
HinQ restriction enzyme. Fragments were separated overnight
by electrophoresis in 0.6% agarose gels. The DNA was subsequendy transferred onto nylon membranes by Soudiern blotting. SLPs were [o-JtP]dCTP (deoxycyddine 5'-trlphosphate)labeled and hybridized overnight to die nylon membranes at
68°C, followed by several high stringency washes. After autoradiography (overnight at — 70°C), the patterns were analyzed.
The limited resolution of the agarose gel electrophoresis
technique, combined with die hypervariability of the detected
minisatellite loci, make it impossible to score die alleles discretely, resulting in quasi-continuous allele distributions (Budowle et aL, 1991). Therefore, allele classes have to be constructed before analysis can take place. In a previous analysis
(Verheyen et aL, 1995), we estimated the allele sizes by comparing die migration distance of die fragments to the migration distance of length markers (Duggleby et aL, 1981). The
alleles were then grouped in 100 base pair (bp) classes, and
each class was considered as an allele.
We checked relatedness between die young in die nest and
die parents at die nest primarily using the multilocus DNA
fingerprinting technique. However, the results were double
checked using die SLPs and the DLP. The exclusion probability (Weir, 1990; based on die 100 bp classes) for each marker separately ranges from 0.71 up to 0.90. For die combination of all markers this probability exceeds 0.999 (details not
Kempenaen et aL • Female choice for extrapair paternity
483
Table 1
xisttes
Variable measured
F
df
T
P
Wing length
Tunis length
Avenge strophe length
Avenge pause length
Proportion of time singing
Average number of notes per strophe
18.0
39.8
9.46
19.8
3.12
5.95
140.148
129,207
19.23
19,23
19,23
21,25
.89
.94
.80
.89
JO
.70
<.0001
<.0001
•C0001
<.0001
<.01
<.0001
See text for further explanation.
shown). The markers therefore are extremely useful in parentage exclusion.
To identify the biological fathers, we stored the genotypes
of all adult individuals in a genetic database. For each extrapair young, we determined the size of the paternal allele for
at least three markers. By comparing the genotypes of individuals analyzed more than once on separate gels, we observed that alleles differed by an average of 0.75% (procentual deviation) from their mean size. We added and subtracted at least three procentual deviations from the paternal allele
in the extrapair offspring, and we then identified all individuals in the database with an allele within this range. We applied 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 one
candidate biological father was identified. The probability of
paternity (W, Weir, 1990) was then calculated for these fathers. In these calculations all allele frequencies within 2 procentual deviations of the paternal allele of the extrapair young
were 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 tarsus
length and body mass of all nejtlingi at age 15 days. The wing
was measured to the nearest 0.5 mm using a ruler and according to Svensson's (1992:20-21) "maximum length" method. For individuals measured more than once during one
year, we used average values in our analyses. Measurements
from different years could not be averaged because wing
length increases with age (data for n — 15 individuals that
bred as juvenile and adult; first yean 65.03 ± 0.94 SD, second
year 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 back
of the intertarsal joint to the lower edge of die last complete
scale before the toes diverge (see Svensson, 1992:27). From
1991 onward, measurements were taken up to the last but one
scale. From 34 individuals measured in 1990 and later, we
calculated that the average difference using die two methods
was 1.0 mm. Therefore, we subtracted 1.0 mm from all the
1990 measurements to make diem comparable with those
taken later. Since tarsus length does not change over the life
of the bird, we used average values for individuals measured
more than once both within and between years.
Birds were weighed (estimate to die nearest 0.1 g) using a
30-g Pesola spring balance. Because of substantial seasonal
and daily fluctuations, body mass is not a useful measure to
compare individuals, unless all measurements are taken
around die same time. Therefore, we used body mass mea-
surements taken in die morning from adults feeding their
8-day-oki offspring. We used die residuals of die regression of
In (body mass) on m (tarsus length) as a measure of condition.
Because we caught and measured many individuals multiple
times, we could calculate repeatabilities for most measurements, allowing us to assess their reliability (Lessells and Boag,
1987). Table 1 shows that all repeatabilities are highly significant 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 die
dawn chorus using a UHER CR 1601 cassette recorder connected to an UHER M646 microphone, mounted in die focus
of a Sony (pbrSSO) parabolic sound reflector. In 1990, die
song of 18 males was recorded between 13 March and 18
April, hi 1991, 44 males were recorded between 4 April and
3 May. Recordings were made between 0500 and 0720 h (Belgian standard time) on mornings widiout rain or strong
winds. We recorded each male for about 10-30 min, so diat
one to three males could be recorded during one morning.
We limited our analyses to include only those males recorded
during die presumed fertile period of their mate (i.e., from
5 days before die first egg was laid until die morning the
penultimate egg was bid). Five males were recorded in bodi
years, but to avoid pseudo-replication we used only die longest
recording for each of these males.
Tapes were analyzed using a Unigon 4600 Spectrum analyzer (Uniscan). Blue tits sing different song types (see Bijnens
and Dhondt, 1984). For our analyses, we only used die most
common song types sung during die dawn chorus (types SI,
S2, S3, and S9 according to Bijnens and Dhondt, 1984; see
also Bijnens, 1988). For each strophe, we measured die total
number of notes, die total duration of die strophe (strophe
length), and die duration of die following pause (pause
length). Song rate was defined as die proportion of die total
time die bird is actually singing and was calculated as die sum
of all die strophe lengths divided by die total recording time
(=» die sum of all strophe lengths plus die sum of all pause
lengths). These measurements were only used in our analyses
if a minimum of 50 strophes were recorded during a continuous song bout. We were able to use data from 25 different
males. We did not have enough multiple recordings of die
same male to calculate repeatabilities. However, to get some
idea of die relevance of our measurements, we calculated repeatabilities for different song types sung by die same male
(usually, but not necessarily, during die same morning). All
song characteristics showed highly significant repeatabilities
(Table 1), which justifies combining measurements from die
different song types.
Our analysis of song characteristics is limited in that we did
not measure repertoire size, nor did we measure die total
duration of die dawn chorus or die number of song types
sung during one dawn chorus. However, strophe length is
Behavioral Ecology VoL 8 No. 5
484
Table 2
apair paternity data £n
% 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 extrapair
offspring where biological father
was successfully determined
% (number) of extrapair young that
could be assigned to a male
i a blue tit population (plot C, 1990-1993)
1990
1991
1992
30.6
(36)
34.4
(32)
10.5
(314)
44.7
(47)
47.5
(40)
14.1
(384)
42.1
(38)
45.5
(33)
12.4
(331)
42 ± 29
27.3
(11)
81.8
(9)
35 + 25
9.5
(21)
71.4
(15)
35 ± 25
6J
(16)
87.3
(14)
72.7
(24)
70.4
(38)
80.5
(S3)
1993
47.7
(44)
52.5
(40)
11.6
(414)
Total
41.8
(165)
45.5
(145)
12.5
(144S)
27+19
0.0
(21)
33 ± 24
8.7
(69)
__
If more than two paternal alleles were found with the single-locus probes and double-locus probes (see Methods), we concluded that there
was more than one extrapair father.
probably a good measure of male quality in the blue tit because Bijnens (1988) found a relation between average strophe length and survival.
Ddmiiliilng age ana sac
Age of breeding birds was determined according to Svensson
(1992) to distinguish between juveniles (born during the previous season) and adults (more than one year old). Based on
the known history of marked birds, we could determine the
exact age (for individuals ringed as nestling or as juvenile) or
the minimum age (for individuals ringed as adults, we assumed they were 2 years old when ringed).
Nestlings were sexed based on the intensity of the blue color on the newly developed wing and tail feathers. Based on
the known sex of individuals that survived and reproduced in
the population (local recruits), we correctly sexed 86% of the
nestlings (n - 57 local recruits) from the 1990-1992 breeding
seasons. Males were more likely to be sexed correctly as nestlings (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 surviving
until the next breeding season if it was observed in year X+l
at least until the start of the breeding season (nest building).
Offspring were considered local recruits if they started a minimum of one breeding attempt (at least egg laying) within the
study 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). All
tests are two-tailed unless stated otherwise. For multiple 2 X
2 contingency tables, we calculated a common odds ratio and
tested the null hypothesis that this ratio is equal to one (Mantel-Haenszel inference; StatXact, 1992).
We investigated which male characteristics females choose
in two ways. First, we tested whether, in a given year, males
that lost-paternity are different from those that did not lose
paternity. In all analyses, each male was only used once (i.e.,
for porygynous males, we calculated the proportion extrapair
young 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 strongest
test because it directly reflects female choice. For this test, we
combined the data over all years where paternity was assigned
(1990-1992). In some nests, young were fathered by two extrapair ™ l w In such a case, we calculated mean values for
the two extrapair males. Some males fathered extrapair young
in different nests, but each case (nest) can be considered an
independent event of female choice.
The correlation matrix with all male characteristics showed
no significant correlations between any of the morphological
measurements (all p > .05). Average strophe length was
strongly correlated with average number of notes sung (r =
.92, n = 25, p < .001), and average pause length was correlated with the proportion of time singing (r m -.75, n «= 25,
p < .001). Therefore, we only used two song variables (average 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 165
nests and 1443 of&pring. Each year, we found extrapair paternity in 31-47% of the nests, and 11-14% of all offspring
were fathered by an extrapair male (see Table 2). Extrapair
young were not distributed randomly over the nests (Figure
1). More nests than expected contained either no or many
extrapair young.
We assigned paternity, Le., found the biological father of
the extrapair offspring, in most, but not all cases (Table 2).
We do not believe that floater males fathered of&pring because it is highly unlikely that such males were present in the
population (Kempenaers, 1994a). Moreover, many males that
were caught in winter but later disappeared were included in
our genetic analysis, and none of them turned out to be a
candidate father. It is more likely that the other extrapair
males were males breeding in the study area (in natural cavities) or just outside the study area for which we did not have
a blood sample.
In 87% of 46 nests with more than one extrapair young, all the extrapair young were fathered by a single male, while in
the other six nests (13%), two different males fathered extrapair young. Most males that lost paternity did not gain paternity in other nests (73% of 11 males in 1990, 85% of 20 males
Kempenaers et s i • Female choice for extrapair paternity
0.0
0.1
0.2
0.3
485
0.4
0.5
0.6
0.7
0.8
0.9
1.0
Proportion extra-pair young in the nest
figure i
Distribution of extrapair roung over the nests (data from 1990-1993). We used a logEnear model, controlling for the number of young per
nest, 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 territories
Figure 2
Frequency distribution of the distance (in number of territories)
that extrapair males bred from the territory where they fathered
offspring (1 • nearest neighbor).
in 1991, and 73% of 15 males in 1992). Males never "exchanged" paternity—i.e., fathered offspring in each other's
nests. The extrapair male(s) were usually the nearest neighbors, although in a few cases they bred as far as four to five
territories away from the territory where they fathered offspring (Figure 2).
For 28 males breeding in different years (2-3) with the
same (8 males) or with a different (20 males) female, there
was a significant repeatability in the proportion of young they
fathered in their own nest ( f ^ , - 3.18, r = .51, p < .005).
From 20 males that bred in different years with different females, 9 males (45%) either never lost paternity or lost paternity in each breeding season, while 10 males (50%) only
lost 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 female
in different years, six never lost paternity (Table 4). Thus,
males that bred with different females in subsequent years
were more likely to lose paternity (75%, n •* 20) than males
that bred with the same female (25%, n = 8, p •* .0299, Fisher's Exact test). Unlike males, females that bred in different
years with different males often had extrapair young in their
nest in the first year, but not in the next (or vice versa). Table
5 suggests that females engage in extrapair copulations depending on the male with which they are paired. Females
breeding with a different male were also more likely to engage
in extrapair copulations (85%, n = 20) than females breeding
with the same male (25%, n °» 8, p - .0048).
Behavioral Ecology VoL 8 No. 5
486
Table 3
of
t yea
Male lost
paternity in
year X
a l a binding with dlfleieul females (a • 20
Male lost paternity in
yearX + 1
No
No
Yes
lableS
Patterns of filiii»ali paternity for males and females breeding m
different years females breeding with different males (* - »
females)
Yes
Female
engaged in
EPCiln
year X
10
5
No
Yes
Female engaged in
EPCsinyearX+ 1
No
Yes
Data are from 1990 to 1993 unless otherwise indicated. Individuals
that bred in 3 yean are entered twice.
EPCs, extrapsir copulations.
Most males breeding in different yean either did or did not
father cxtrapair offspring in all years they were present (69%
of 26 males). Only one male (4%) fathered extrapair offspring in the first year, but not in the next (Table 6).
ternity (only males that produced at least one fledgling are
included; 1990: 20% of 10 males versus 32% of 19 males, 1991:
0% of 14 males versus 16% of 19 males, 1992: 33% of 12 males
versus 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 fathered
fewer fledglings, and a loglinear model (GLIM), controlling
for the number of fledglings, showed no differences in the
probability of recruiting an offspring between males that did
or did not lose paternity (all p > .10).
In 10 nests with <mixed paternity where part of the brood
died between day 14 and fledging (possibly due to starvation),
the extrapair young were more likely to survive than the within-pair young (61% ± 28 SD of within-pair young versus 80%
± 36 SD of extrapair young survived; common odds ratio for
ten 2 X 2 contingency tables - 7.918, p - .046).
Offspring sex ratios (proportion of males) did not differ
between 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 nests
with mixed paternity, the extrapair young were more likely to
be 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 not
have significantly longer tarsi than the within-pair young (extrapair 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-pair
young (extrapair young: 10.44 ± 0.91, within-pair young:
10.26 ± 0.83, t - 2.43, df = 56, p< .025). Since extrapair
young are more likely to be males, this result could be found
if male offspring are, on average, larger and heavier than female offspring at age 15 days, which is indeed the case (both
when comparing male and female within-pair young and male
and female extrapair young within nests, males are larger and
heavier than females, all p < .01, data not shown). Male extrapair young were not larger, nor heavier, than male within-
Maled
rterff
We found no significant effect of male age on the likelihood
of losing paternity (Table 7). In 1 year out of 4, males that
lost paternity had significantly smaller tarsi than nudes that
did not lose paternity (Figure 3), and males did not differ in
wing length (Table 8). In 1 year out of 3, males that lost paternity were in better condition (body mass/tarsus length)
than males that did not lose paternity (Table 8). Males that
lost paternity were less likely to survive than males that did
not lose paternity, while there was no difference in the survival of their mates (Figure 4). Males that lost paternity had
shorter average strophe lengths (1.3 s ± 0.5 SD, n - 9) than
males 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 length
did 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 of
extrapair young as the dependent variable and male tarsus
length, average strophe length, and average pause length as
the explanatory variables showed only a significant effect of
average strophe length (Figure 5).
The extrapair males, when compared with the males they
cuckolded, had larger tarsi and a lower condition and they
sang longer strophes with longer pauses between strophes.
Extrapair and within-pair males did not differ in standardized
wing length (Table 9). Extrapair males were also older on
average 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 own
offspring in the population than males that did not lose paTable 4
apair paternity for males and females breeding m
Patterns of t
duTaent years: pairs biceding together in different years (a • 8)
Table 6
Patterns of extrapair paternity for ««•!*• and females breeding in
different years: males breeding in different years over 1990-1992 (a
«26)
Extrapair
young in
nest in
year* •
Fathered extrapair
young in year X + 1
No
Yes
Fathered
extrapair
young in
year X
No
Yes
No
Yes
7
0
1
1
No
Yes
15
1
8
7
Extrapair young in nest
in year X + 1
Kempenaers et aL • Female choice for extrapair paternity
487
20 11
Table7
Proportion of male* (ample rixe) mat kwt paleiultj in relation to
their age
20 19
18 15
16 19
p< .10
Age (yean)
Year
1
1990
1991
1992
1993
Total
0.56
0.41
0.46
0.44
0.42
4+b
(14)
(27)
(13)
(25)
(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)
1.00
.38
.21
.17
0.25 (4)
0.50(4)
0.33(3)
— (0)
0.36(11)
• p value from Fisher's Exact probability test.
Males 4 years or older were grouped in one category.
b
pair young, and the same is true for female offspring (paired
t tests, all p> .25).
There is no evidence that extrapair young are more likely
to survive locally until the next breeding season than withinpair young from the same nest, but the sample size is smalL
Young were recruited from 17 (28%) of 60 nests with extrapair young. From those nests, on average, 15% (± 9 SD) of
the within-pair young were recruited and 17% (± 30 SD) of
the extrapair young. A GLIM model for the 17 mixed paternity nests with recruits using recruitment as the binary response variable and nest and status of the offspring (extrapair
or 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 > £).
DISCUSSION
Patterns of i drapafa- paternity: do females choose particular
males?
In all 4 yean, extrapair paternity was common in our blue tit
population. Because there were no cases of mate switching
during nest building or egg laying, die possibility that mixed
paternity was caused by rapid mate switching could be ruled
out (see, e.g., Pinxten et aL, 1993). The strongest evidence
for female choice for extrapair paternity is the behavioral evidence reported earlier (1) females actively seek extrapair
copulations from particular males often by intruding in the
territory of this male (Kempenaers et aL, 1992), and (2) when
the resident male was experimentally removed, females refused to copulate with most of die intruding males (Kempenaers et aL, 1995). Data on the patterns of extrapair paternity
reported here are consistent with these behavioral observations (see Kempenaers and Dhondt, 1993): (1) more often
than expected under a random distribution, nests contained
1990
1991
1992
1993
Year
Figure 3
Tarsus length (+ SE) of males that did (shaded bars) or did not
(open bars) lose paternity In their nests. Numbers at the top of the
graph indicate sample sizes. Differences between the two group* of
males 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 all
the extrapair young in one nest were fathered by die tame
male, (3) extrapair paternity was never reciprocal, and (4) all
die extrapair fathers that could be determined were resident
males breeding in die population and usually they were
near(est) neighbor(s). These patterns are similar to those
found in many other socially monogamous or polygynous passerines (e.g., Gibbs et aL, 1990; Gray, 1996; Hasselquist et al.,
1996; Stutchbury et aL, 1994; Westneat, 1992, 1993;~Wetton et
aL, 1995; Whittingham and Lifjeld, 1995; Yezerinac et aL,
1995). A notable exception is die tree swallow Tadtycmeta bicolcrr. extrapair offspring in the same nest are often fathered
by different males, males do exchange extrapair young, and
most of die extrapair fathers are not found on die tame nestbox grid (Dunn et aL, 1994). Also, in the yellow warbler Dtndroica ptUchia, extrapair males were sometimes nonresident
males, and one case of reciprocal cuckoldry was found (Yezerinac et aL, 1995). Wetton et aL (1995) also found one case
of reciprocal cuckoldry in die house sparrow Passer domtsticus. Under die "good genes" hypothesis, it seems unlikely
that females would choose to copulate with unpaired males
Table8
wing leuglli and condition of —•!»? ***•* did and did not l o t paternity in their nesti
Standardized wing length
Yfear
1900
1991
1992
1993
EPY
No
Yes
No
Yes
No
. Yes
No
Yes
Mean £ SE
n
-0.14
-0.36
-0.03
0.14
-0.03
20
11
20
19
18
15
17
18
0.21
057
0.17
0.28
0.21
0.32
0.24
0.18
-0.13
0.27 i. 030
(see Methods).
Condition'
t
p
0.64
-0.52
-0.74
-1.18
Mean ± SE
n
>*>
-0.0093 ii
0.0093 i:
-0.0169 1t
0.0261 it
0.0082 =:
-0.0082 2:
0.014
0.010
0.014
0.013
0.011
0.013
16
16
17
11
16
16
-1.06
-2.12
0.97
<.05
488
Behavioral Ecology VoL 8 No. 5
21
11
21
19
/>•» .0006
p-
.06
24 11
19
16
(a)
p - JOOS
25 20
22
16
0.0 -
(b)
1.0
l JO
1.5
Z0
2.5
3.0
Mean strophe length (s)
Figure 5
Relation between the proportion of extrapair young in the nest and
the average strophe length (s) sang by the male during the dawn
chorus (data for 25 males from 1990 and 1991). The curved line b
based on the parameter estimates of a logistic regression with
equation p « «***/(l + «•**•) where p « proportion of extrapair
young, 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 in
proportion of extrapair young <j? m 16.75, df ~ 1, p > .001).
lose paternity (Kempenaers et aL, 1992) was only partly confirmed (a similar trend in 1992). However, a pairwise comparison of the social male and the extrapair male(s) that fathered offspring in his nest confirmed that extrapair males
had longer tarsi. Tarsus length in blue tits is heritable
(Dhondt, 1982), and a within-nest comparison of within-pair
and extrapair young showed that the extrapair young on average had longer tarsi, but the difference was not significant
despite a reasonable sample size. It is unclear how the offspring would benefit from having longer tarsi If tarsus length
is a measure of overall size, then larger individuals may be
better able to compete over resources such as food, roosting,
or nesting sites, but this remains to be shown. Wing length is
also a measure of size, which increases with age. However,
standardized wing length (controlled for age) did not differ
between males that were or were not successful in protecting
their paternity or in gaining extrapair offspring. In a similar
study on red-winged blackbirds (Agdatus photnicrus), Weatherhead and Boag (1995) showed that larger males were more
successful in siring young (on their own territory and extra-
Figure 4
Survival to the next breeding i e u o n for (a) males and (b) females
that d i d (shaded bars) or did not (open bars) have extrapair young
in their nests. Numbers at top of each graph indicate a m p l e 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 because
females can probably better assess male quality of known
neighbors than of passing floaters. Also, reciprocal cuckoldry
is not expected unless females differ in their preferences.
Which m *i» traits do fenisles choose *TT^ how ***** *K#y
benefit from their choice?
Our earlier finding (data from 1990) that males that lost paternity were smaller (in tarsus length) than males that did not
Table 9
Pali w i t comparisons of chaneteriadca of »«n»|»»ii males and
Character
Wi thin-pair
males*
Tarsus length
Standardized wing length
Condition*
Average strophe length (s)
Average pause length (s)
14.62
0.07
0.024
1.29
235
• Means * SD.
• Residuals (see Methods).
±
•
±
•
*
0.53
1.12
0.038
0.23
0.75
hin-pair
ales fathering young in the same nest (data from 1990 to 1992)
Extrapair
males*
15.01
0.22
-0.033
1.77
3.77
±
•
•
±
±
0J1
0.92
0.053
0.25
1.18
n
t
p
35
32
18
6
6
-2.82
-0.56
-3.28
-3.02
-3.11
<.0O5
<.O5
<.O5
Kempenaen et aL • Female choice for extrapair paternity
pair young) and that male body size was positively correlated
with survival.
Remarkably, we found that males that lost paternity were in
better condition (Le., heavier relative to their size) than males
that did not lose paternity (significant in 1 year out of 3), and
extrapair males had a significandy lower condition than the
within-pair males they cuckolded. There are several possible,
not mutually exclusive, explanations for this finding. Since
body man was measured during the nestling stage, it is possible that the successful males invested more in their offspring
either because they had larger broods or more than one
brood 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 likely
to copulate more frequently or over a longer period. It seems,
however, that successful males are able to invest more because
their lower condition did not result in a lower probability of
survival. An alternative explanation is that high-quality males
are able to reduce the costs associated with fat storage (Witter
and Cuthifl, 1993), for example, because they are better foragers or have better resources available, while low-quality
males may have to insure against uncertain foraging success
by carrying larger fat reserves. Whether this is the case during
the 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 heavier
than the within-pair young, but we also found that extrapair
young were more likely to be males. When analyzed separately
for each sex, within-pair young and extrapair young did not
differ in tarsus length, nor in body mass. These data are difficult to interpret because our method of sexing is based on
plumage characteristics (intensity of the blue color) and
therefore probably not independent of die size of die chick
(Le., a chick that develops more slowly and is thus smaller or
weighs less at age 15 days is more likely to be scored as a
female). Ideally, we would want to determine sex of die nestlings using a molecular marker. On die other hand, recaptures of local recruits showed that our method was quite reliable (see Methods).
We did not find a difference in sex ratio between nests with
and without extrapair young, but our (preliminary) finding
that extrapair young are more likely to be males supports die
hypothesis that females manipulate die sex ratio in relation
to male quality or attractiveness (e.g., Burley, 1981). Other
support for this hypothesis comes from a study of blue tits by
Svensson and Nilsson (1996), who showed that females mated
to males diat survived until die next season produced broods
widi male-biased sex ratios. Females might benefit from producing extrapair sons if, in nests with mixed paternity, die
extrapair offspring might become more attractive or better
able to compete, which would affect the future reproductive
success of sons more than that of daughters.
The probability of losing paternity did not depend on die
age of die male (Le., males of all ages were equally likely to
lose paternity). However, die extrapair males were on average
older than die within-pair males they cuckolded. This has also
been 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 it
supports die hypothesis that females acquire "good genes"
for their offspring because it is likely that older individuals in
the population are of higher genetic quality than average
(Trivers, 1972). The above results, together widi die observation that males are more likely to lose paternity in die second of two breeding seasons (Tables 3-6), may seem contradictory. A possible explanation is that when males get older,
some become very attractive (e.g., those in good condition),
489
while othen become less attractive (e.g., diose in bad condition).
Cuckolded males were less likely to survive than males diat
did not lose paternity (significant in 2 years out of S), but
there was no difference in female survival, which suggests diat
die difference in male survival is caused by differences in male
quality rather dian in territory quality. Moreover, we found
diat 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 obtain indirect fitness benefits from their choice of extrapair
fadiers. However, die results from die nests widi partial brood
mortality should be interpreted cautiously for die following
reasons. First, die sample size is limited to 10 nests and die
difference is only marginally significant Second, in case of
harrhing asynchrony, it is likely diat young nestlings suffer
more mortality dian die older ones in die brood. If hashing
asynchrony occurred and if die extrapair young are more likely to be die older nestlings, we would indeed find diat extrapair young survived better, but diis may have nodiing to do
widi good genes. Unfortunately, we have no data on die exact
chick age (hatching asynchrony) nor on die pattern of extrapair paternity in relation to die order of egg laying (or hatching). Third, die differential survival of extrapair and withinpair chicks might result from sex-biased mortality (because
extrapair young are also more likely to be males). Our method of sexing nestlings (based on plumage characteristics) is
not suitable to check whether mortality is sex biased because
it is not independent of die age or condition of die chick (see
above).
The data on longer term survival (recruitment) of offspring
showed diat males diat lost paternity were not less likely to
locally recruit offspring when controlling for die number of
fledglings they fathered. There is no evidence diat extrapair
young have a higher chance to recruit dian within-pair young
from die same nest. Akhough they would potentially provide
die strongest evidence for die good genes hypothesis, die
problems widi this type of data are diat local recruitment is
not the same as total recruitment and die effect may be too
small to detect given die low numbers of local recruits.
It is difficult to find out which cue(s) females use to assess
the quality of their social mate and diat of potential extrapair
fadiers. Nevertheless, we determined at least one cue diat female blue tits can use: die average length of strophes sung
during die dawn chorus. Since most extrapair copulations in
blue tits were observed early in die morning just after die
female left die nest-box (Kempenaers, 1994b) and since extrapair males are usually close neighbors, it is not unlikely diat
females choose males based on their dawn chorus performance. Song characteristics have been shown to be important
cues for mate choice in many passerines (e.g., Catchpole et
al., 1986; Collins et aL, 1994; Eens et aL, 1991; Lampe and
Sartre, 1995), and a recent study on die great reed warbler
Acroaphahu arundinacrus showed diat females obtained extrapair young from males widi larger song repertoires (Hasselquist et aL, 1996).
The function of die dawn chorus has been subject of much
speculation and study. Based on observations diat in many
passerines die intensity of die dawn chorus is positively related
to female fertility (e.g., Cudull and Macdonald, 1990; GreigSmith, 1982; Mace, 1987; Meller, 1988; Welling et al., 1995;
but see Part, 1991; Rodrigues, 1996), it was hypothesized diat
die dawn song of paired males functions as a paternity protection mechanism (mate guarding), as courtship behavior'
stimulating their own mate to solicit copulations, or as a strategy to obtain extrapair copulations (Greig-Smith, 1982; Mailer, 1991b, see also Slagsvold et aL, 1994). However, die idea
diat dawn singing functions to repel potential cuckolders is
Behavioral Ecology VoL 8 No. 5
490
not supported by the data (e.g., Part, 1991; Slagivold et aL,
1994). This study strongly suggests that females choose males
as extrapair copulation partners based on a characteristic of
their dawn chorus song (strophe length). Our data thus support Mailer's (1991b) hypothesis that dawn singing is a strategy to obtain extrapair copulations, although as Slagsvold et
aL (1994) pointed out, this is unlikely to be the only explanation for the existence of the dawn chorus.
Consistency and Hmh«Ht»M of female choice
If females choose to engage in extrapair copulations with particular males to obtain genetic benefits, we would expect them
to be consistent in their choice (M#Uer, 1994b); Le., we would
expect that male success in avoiding cuckoldry or gaining extrapair offspring in different breeding attempts is repeatable.
This was indeed the case: the proportion of young fathered
by males breeding in different years was highly repeatable.
However, a detailed look at individual males showed a more
complex pattern. If the attractiveness of a male is reflected by
the fact that he does or does not lose paternity, we found that
from one year to the next males rarely increased, but often
decreased, in attractiveness (Tables S, 5). This may seem to
contradict the good genes hypothesis. However, it is important
to realize that male quality or attractiveness should be considered relative to the quality or attractiveness of the group of
males from which the female can choose (Le., the close neighbors). Therefore, male quality does not necessarily have to
stay the same in different years, and we should not expect
that all males who father extrapair young do not lose paternity
diemserves. Another reason males might decrease in attractiveness (measured as loss of paternity) is that in their final
breeding season, some males may already be in a bad condition, which may be reflected in a cue their female uses to
determine his quality (e.g., song). Data on changes in song
output of individual males in relation to their subsequent survival would provide a test of this hypothesis. Males that bred
with the same female rarely changed in attractiveness (measured as loss of paternity), which suggests consistency of female choice. There is no evidence that particular females are
more likely to engage in extrapair copulations (Table 5) independent of their mate's attractiveness. There was also some
consistency in the probability that a male will father extrapair
young. Most males either never fathered extrapair young, or
they fathered extrapair young in all die years they were present (Table 6). Moreover, males that did not father extrapair
young in their first breeding season could often father young
in later seasons, but the reverse was rare.
Female blue tits are restricted in their choice for a breeding
mate (Kempenaers, 1994a), but it seems that they can modify
their choice for a father for their offspring. If females benefit
from having their offspring fathered by a male other than the
social male, then why is extrapair paternity not more common? And why do not all females mate with the most attractive male of die population? dearly, there are also several
constraints on this type of choice. First, females are probably
unable to select any male from the population as father for
their offspring; extrapair fathers are usually (close) neighbors.
This may be because females cannot assess die quality of males
that are breeding farther away or because they cannot get
copulations with those males. Either die female or die male
has to leave die territory and travel a long distance to copulate, aad this seems unlikely to happen because of die risk of
detectidn by other territorial birds, resulting in aggressive encounters. Thus, females can only choose from those males
breeding in die vicinity (see also Meller, 1994a, for choice of
a breeding partner). Second, extrapair paternity is die result
of a conflict of interest between die social male, die extrapair
male, and die female (Iifjeld et aL, 1994), and it is highly
unlikely that die female would always win. Females often copulate widi their social partner during die fertile period (Kempenaen et aL, 1995), which may be necessary to receive male
help in raising die brood (e.g., Davies et aL, 1996). Also, males
do guard their females, and although diey are often not entirely successful (see Kempenaers et aL, 1995), it is likely that
guarding does help to some extent to protect their paternity.
Because male parental care is often so important for reproductive success, females might have to walk a tightrope between evading die guarding male and assuring his confidence
of paternity. Finally, females must be able to assess male genetic quality via one or several behavioral or morphological
cues reflecting quality, which might cost considerable time.
General conclusion
Our data provide farther evidence for die hypothesis that
blue tit females seek extrapair paternity to obtain good genes
for their offspring. This study thus adds to a growing body of
evidence that females can obtain indirect genetic benefits
from their choice (e.g., Alatalo et aL, 1991; Hasselquist et aL,
1996; MoUer, 1991a, 1994a; Petrie, 1994). In many other bird
species, die available data on extrapair paternity are generally
consistent with die good genes hypothecs. However, detailed
studies on die performance of extrapair versus within-pair offspring are still needed to critically test die good genes hypothesis. The next step will be to formulate and test hypotheses ^plaining the variation in die level of extrapair paternity,
both among species and among populations of die same species.
We are grateful to Frank Adriaensen, Fran* Fierens, and Werner
Pkunpen for their help in the field. We thank the Bncht family for
kindly allowing ui to work on their beautiful estate, Marleen van den
Broeck for her good DNA cooking capabilities, Christine van Broeckhoven for providing laboratory ipace, Frank Adriaensen and Frant
Fierens for their help with retrieving data from the riarahaw, Stefan
van Dongen for statistical advice, and Luc Bijneru and Marcel Ecru
for their help with the song analyses. Marcel Ecus, Herbert Hoi, Rianne Pinxten, Tore Slagsvold, Michael Tabonky and an anonymous
referee provided constructive comments. BJL was supported ai a retearch assistant of the Belgian National Fund for Scientific Research
and by the Austrian Academy of Sciences.
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