Behavioral Ecology Vol. 12 No. 4: 496-500
© 2001 International Society for Behavioral Ecology
Survival of extrapair and within-pair young in tree swallows
Department of Biological Sciences, P.O. Box 413, University of Wisconsin-Milwaukee, Milwaukee, WI 53201, USA
Address correspondence to L.A. Whittingham. E-mail: whitting{at}uwm.edu .
Received 2 June 2000; revised 5 October 2000; accepted 13 November 2000.
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ABSTRACT |
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In monogamous species, it is generally accepted that males seek extrapair matings to increase their reproductive success without additional parental investment; however, the benefits of extrapair matings to females are much less clear. One possibility is that females obtain genes for enhanced offspring viability from the extrapair sires. If this is the case, then the increased viability of extrapair young may be evident throughout the period of embryonic development as well as later in life. Tree swallows (Tachycineta bicolor) have one of the highest known levels of extrapair mating in birds, and females have substantial control over the paternity of their offspring. We used molecular techniques to determine the parentage of nestlings and unhatched embryos to examine the possibility that female tree swallows gain viability benefits for their extrapair offspring. Although both extrapair paternity and mortality of embryos and nestlings were high (89% and 54% of broods respectively), we found no difference in the viability of within-pair and extrapair young prior to fledging. In addition, extrapair young were not more likely to be male. There was no bias in the sex of young at fledging, but unhatched embryos were more likely to be male. Our results do not support the idea that female tree swallows engage in extrapair mating to increase offspring viability, at least early in life.
Key words: embryonic survival, extrapair paternity, fertility insurance, good genes, viability.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Although most species of birds are socially monogamous, recent work has shown that extrapair matings occur in many of these species (reviewed in Petrie and Kempenaers, 1998
;
Westneat and Webster, 1994).
It is generally accepted that males seek extrapair fertilizations (EPF) to
increase their reproductive success without additional parental investment
(Trivers, 1972); however, the
benefits that females obtain through EPFs are much less clear. In socially
monogamous species, extrapair males usually do not assist females rearing the
young or provide other direct benefits to the female. Thus, it is often
suggested that females seek EPFs to improve the genotypes of their offspring
(i.e., indirect genetic benefits). These genetic benefit hypotheses predict
that young sired by extrapair males should show greater attractiveness or
viability (resulting from superior genetic quality) than young sired by the
female's social mate.
Evidence of female preferences for males providing genetic benefits has
been demonstrated in a few species of birds. For example, males with
exaggerated traits (e.g., tail length or forehead patch size) have greater EPF
success (Saino et al., 1997;
Sheldon et al., 1997)
suggesting that females gain more attractive male offspring from extrapair
matings. In other cases, extrapair young (EPY) are more likely to survive the
nestling or juvenile growth periods
(Kempenaers et al., 1997)
suggesting viability benefits for the female's extrapair offspring. The few
studies that have examined the relative viability of within-pair and extrapair
young have focused on survival of young during the nestling and juvenile
periods or their recruitment into the breeding population
(Kempenaers et al., 1997;
Krokene et al., 1998). If
females are gaining superior genes for their offspring through EPFs, then the
increased viability of EPY may be evident throughout the period of embryonic
development as well as later in life. Although mortality during embryonic
development can be substantial (e.g.,
Kempenaers et al., 1999), the
potential for differential survival of within-pair and extrapair young during
this period has received little attention.
Tree swallows (Tachycineta bicolor) offer an excellent opportunity
to examine the possibility that females gain viability benefits for their
extrapair offspring because: (1) extrapair paternity is very common, (2)
copulatory access is controlled by the female, suggesting that females benefit
from extrapair copulations, and (3) females do not gain any obvious help
rearing the offspring from extrapair males (e.g., feeding young). In addition,
a recent study of tree swallows showed that nests with EPY had higher hatching
success than nests without EPY (Kempenaers
et al., 1999). This correlation suggests that EPY were more likely
to proceed successfully through embryonic development; however, this idea was
not tested directly. In this study we determined the paternity of unhatched
embryos and young that died during the nestling period to examine whether EPY
were more viable early in development and whether female swallows gained
viability benefits for their offspring from extrapair matings. We also
determined the sex of within-pair and extrapair young to examine whether
paternity and mortality were associated with offspring sex.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study area and species
We studied tree swallows in 1997 and 1998 in a box-nesting population at the UWM Field Station near Saukville, Wisconsin, USA (43°23' N, 88°01' W). Tree swallows nested in two grids with 28-30 nest boxes each, in which nest-boxes were 40 m apart along a row and 28 m apart on the diagonal between rows. An additional 24 nest-boxes were distributed randomly in between the grids (these nest-boxes were 15-35 m apart). The density of nest-boxes at our study area was similar to natural tree swallow densities (Barber et al., 1996
) and to
densities in other box-nesting populations
(Robertson and Rendell,
1990).
All eggs, nestlings, and adults were marked for individual identification.
We identified the position in the laying sequence for each egg and nestling.
Eggs were numbered with felt-tip marker on the day that they were laid. Most
clutches hatch over 1-2 days and each egg takes 1-2 h to hatch
(Robertson et al., 1992). We
checked nests every 1.5-2 h between 0600 and 2000 h CDT to determine which
nestling hatched from which egg. Newly hatched nestlings were marked with a
unique color combination using nontoxic felt-tip markers until they were 4
days old at which time they were given a colored plastic leg band (see
Clotfelter et al., 2000 for
details). Eggs that did not hatch within 5 days of the first egg in the clutch
were collected and embryonic tissues were preserved in lysis buffer
(Seutin et al., 1991) or
frozen. During the nestling period, nests were checked everyday and dead
nestlings were removed and frozen to preserve tissues for DNA analyses. All
adults and 12-day-old nestlings were given a USFWS aluminum band. Adults were
also marked with nontoxic colors on the breast (felt-tip markers), wings or
tail (acrylic paint; Dunn et al.,
1994). Adult female swallows were classified as second-year (SY)
or after second-year (ASY) on the basis of plumage coloration
(Hussell, 1983). A small
(approximately 50 µl) blood sample was taken from all adults and 12 day old
nestlings for DNA analyses.
Paternity analyses
Paternity exclusions were made based on allelic variation at two highly
polymorphic microsatellite loci: HrU6 and HrU10 (Primmer et al.,
1995,
1996). Microsatellites were
amplified by polymerase chain reaction (PCR) in a total volume of 10 µl
with the following reaction conditions: 50 mM KCl, 10 mM Tris-HCl, 1.5 mM
MgCl2, 0.2 mM dNTPs, 0.5 µM of each primer, 0.35 U of
Taq polymerase and approximately 50 ng of genomic DNA. The forward
primer was end-labeled with 33-P dATP by incubating 0.15 pmol primer, 40mM
Tris-HCl, 10 mM MgCl2, 5mM DDT, and 0.375 U T4 Kinase at 37°C
for 30 min. PCR amplifications for HrU6 and HrU10 were performed under the
following thermal cycling conditions (conditions for HrU10 are given in
parentheses): an initial denaturing step at 94°C for 3 min followed by 35
cycles of 94°C for 30 (50) s, 63 (46)°C for 30 (60) s and 72°C for
45 (60) s. The program concluded with a final cycle of 72°C for 5 min. PCR
products were electrophoresed in a 6% polyacrylamide gel run at 55 W for 2-4.5
h depending on PCR product sizes. We ran a standard sequencing reaction of M13
mp18 DNA (labeled with 35-S) as a size reference on each polyacrylamide gel.
M13 sequencing reactions were performed using the Sequenase Version 2.0 DNA
Sequencing Kit (United States Biochemical US70770) following manufacturer's
directions. Following electrophoresis, the gel was dried and exposed to
autoradiography film for 1-3 days. We scored the size of microsatellite
alleles for each individual by comparing the band(s) to the reference M13
sequence.
Microsatellite loci used in paternity analyses were highly polymorphic
(Table 1). We calculated allele
frequencies from adults at 54 nests sampled in the breeding population during
1997 and 1998. Of 108 breeding adults, 19 (10 females and nine males) bred in
both years and, thus, we used 89 unique adults to determine the allele
frequencies at both loci. The frequency of each microsatellite allele
(xi), was used to calculate the expected frequency of
heterozygotes; he = 1 - 
(xi)2. The
observed heterozygosities (ho) were high and were similar to the
expected frequencies (Table 1).
Each locus used in this study had a high probability of paternity exclusion
(Pei; Table 1),
which is the probability that a randomly chosen male will not share the
paternal allele found in the young, given that the maternal allele is known
(Jamieson, 1994). The total
probability of exclusion in this study was 0.996 for both loci combined.
Extrapair young were identified as those that did not share an allele with
their social father at one of the two loci. For 11 young that mismatched at
just one locus we calculated the probability of chance inclusion, which is
based on the frequency of the matching allele in the population
(Jeffreys et al., 1992). This
probability was high for both HrU6 (range: 0.02 to 0.30) and HrU10 (range:
0.06 to 0.11). The probability of mutation was low (0.004 for HrU6;
Ellegren et al., 1997); thus,
we concluded that young with a mismatched allele at one locus were probably
due to extrapair paternity rather than mutation.
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Sex determination
In birds, females are the heterogametic sex and have one W and one Z
chromosome, where males are the homogametic sex and have two Z chromosomes. We
amplified an intron in the CHD-1 gene found on both the W and Z chromosomes
using Griffiths et al. (1998)
P8 and P2 primers (Whittingham and Dunn,
2000). PCR was carried out in a total volume of 10 µl with the
following reaction conditions: 50 mM KCl, 10 mM Tris-HCl pH 8.3, 1.5 mM
MgCl2, 200 µM of each dNTP, 0.5 µM of each primer, 0.25 U of
Taq polymerase and approximately 100 ng of genomic DNA. PCR
amplifications were performed under the following thermal cycling conditions:
an initial denaturing step at 94°C for 2 min followed by 30 cycles of
94°C for 30 s, 47°C for 45 s and 72°C for 45 s. The program
concluded with a final cycle of 48°C for 1 min and 72°C for 5 min. In
tree swallows the PCR products could not be distinguished on a standard
agarose gel so we digested PCR products with Hae III which cuts only
the CHD-Z fragment at one site
(Whittingham and Dunn, 2000).
Digested PCR products were separated by electrophoresis for 45-60 min at 10
V/cm in a 2% NuSieve 3:1 agarose (FMC Corporation) gel stained with ethidium
bromide. Digested PCR products were visualized under UV light and scored one
band as male and two bands as female. This method was completely accurate for
identifying known sex adult tree swallows
(Whittingham and Dunn,
2000).
Data analysis
Over the 2 years of this study, embryo or nestling mortality occurred in 29
of 55 nests. We were able to obtain DNA from all eggs that were laid except
one unhatched egg without visible embryonic development. Thus, we had 54
broods for which we had information about every egg that was laid. For these
nests clutch size varied from four to seven eggs (5.2 ± 0.1) and we
obtained genetic data for a total of 281 embryos and nestlings. Means are
reported ± SE unless noted otherwise.
To examine the survival of eggs or nestlings in each brood in relation to
paternity, we used generalized logistic models with binomial errors and logit
links (McCullagh and Nelder,
1983) as implemented in the Macintosh computer package GLMstat
(Beath, 1997). This analysis
used the number of eggs or nestlings that died in each brood as the dependent
(response) variable and clutch size as the binomial denominator. The
significance of predictor variables was tested by the change in deviance of
the model with and without the predictors
(McCullagh and Nelder, 1983).
To test for a random distribution of extrapair young among nests we used a
chisquare test in which the expected number of nests with 0-1, 2, 3, and 4-7
EPY was calculated from 1000 randomizations for each nest.
To examine the relationship between mortality and the position of the egg in the laying sequence we used two approaches. First, we used all nests in which the exact position in the laying sequence was known for every individual (n = 16 nests). Second, we had several nests in which more than one egg hatched simultaneously, so for these nests we categorized laying order as early and late (n = 35 nests). For clutches of four, the first two eggs were designated as early and the last two eggs were designated as late. For clutches of five, six, and seven, the first three eggs were designated as early and the remaining eggs were designated as late.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Similar to other populations of tree swallows, we found a high level of extrapair paternity and hatching failure. We found 43 broods (80%) with mixed paternity, six broods with no EPY and five broods that contained only EPY. EPY were not distributed randomly among broods (Figure 1;
2 =
10.7, 3 df, p <.025). There were more broods than expected with no
or one EPY and four or more EPY, and fewer than expected broods with two EPY.
The proportion of EPY per brood did not vary between years (F 1,52
= 0.46, p =.5) nor did the proportion of broods containing EPY
(2 = 0.24, 1 df, p =.63). Overall, we found 48.8%
(137/281) EPY in 88.9% (48/54) of broods (2.5 ± 0.21 EPY per brood).
Twenty-nine of 54 nests (53.7%) had at least one case of embryo or nestling
mortality. Overall, 20 nests had at least one unhatched egg (37.0%, 20 of 54
of nests) with an average of 1.4 (± 0.2) unhatched eggs per nest (range
1-3 eggs per nest). Although lower than the proportion of nests with hatching
failure in an Ontario population (51%;
Kempenaers et al., 1999), the
difference was not significant (Fisher's Exact Test, p =.17).
Overall, embryo mortality occurred in 10% (28/281) of all young. Mortality of
young during the nestling period was lower: 5.3% (15/281) of all nestlings in
16.7% (9/54) of nests. We examined mortality through embryonic development and
the nestling period in relation to paternity, sex of the young, position in
the laying sequence, and age of the female.
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If females gain viability benefits from extrapair males, then EPY should survive better than within-pair young (WPY); however, viability of embryos and nestlings was not related to paternity. Among all eggs laid, within-pair (81.9%, 118/144) and extrapair (87.6%, 120/137) young survived equally well to fledging (Fisher's Exact test, p =.25). Results were also non-significant when we examined mortality separately for the embryonic and nestling periods.
When we examined entire broods there was also no apparent advantage to
extrapair mating. For all broods, mortality of young (both embryos and
nestlings) was not related to whether extrapair young occurred in the brood
(change in deviance = 1.20, 1 df, p =.30), the number of extrapair
young in the brood (change in deviance = 0.16, 1 df, p =.69), or year
(change in deviance = 3.01, 1 df, p =.08) in bivariate analyses. When
we examined only nests with some mortality, again, we found no relationship
between any of these variables and the occurrence of embryo or nestling
mortality (all p >.32). Similarly, when we examined only nests
with embryo mortality, hatching failure was not related to whether EPY
occurred in the brood (2 = 0.85, 1 df, p =.59). We
also made a pairwise comparison of the mortality of extrapair and within-pair
young in the same nest, which controls for differences among nests
(Figure 2). If within-pair
young had greater mortality than extrapair young, then we would expect most of
the data points to lie below the 1:1 line (see
Figure 2); however, there was
no such trend (pairedt = 1.28, 42 df, p =.21;
Figure 2). Despite our
relatively large sample size of broods with mixed paternity (n = 43),
the power of this test was low (0.24) because the mean difference in mortality
was small (6.8%; 13.4% and 20.2% mortality for extrapair and within-pair
young, respectively).
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If females are choosing males based on traits that result in greater fitness of male young inheriting those traits, then we would expect a greater portion of extrapair young to be male. Again, we made a pairwise comparison of the sex of extrapair young in the same nest, which controls for differences among nests (and females). We found that broods containing extrapair young were not more likely to be biased toward males (median percentage of males in broods with at least one extrapair young = 47.5%, not significantly different from 50%; Wilcoxon signed-rank = 51.5, p =.12, n = 31 broods). Similarly, there was no bias toward males when we examined the overall percentage of extrapair young that were male (62/122, 50.8%; Fisher's Exact Test, p =.38). The only significant male bias occurred during embryonic development when males were more likely to die (22/28, 79%) than females (6/28, 21%; Fisher's Exact Test, p =.008). Mortality during the nestling period (six males and nine females died, n = 228 nestlings sexed; Fisher's Exact Test, p =.43) and, overall, was not sex biased (28 males and 15 females died, n = 256 embryos and nestlings sexed; Fisher's Exact Test, p =.13).
Viability of embryos and nestlings may be related to their order in the
laying sequence. Overall, young from eggs laid early were more likely to
survive to fledging than eggs laid late in the laying sequence (early versus
late: logistic regression 2 = 3.86, 1 df, p =.04,
n = 51 nests). We found a similar trend when we examined only nests
with exact hatching order (logistic regression 2 = 3.13, 1 df,
p =.07, n = 16 nests). The difference in the viability of
early versus late laid eggs was due to the reduced survival of nestlings
hatching from eggs laid late in the sequence rather than a difference in
embryo mortality. Embryo mortality did not vary in relation to position in the
laying sequence (early versus late: logistic regression 2 =
1.23, 1 df, p =.29; exact laying order: logistic regression
2 = 1.94, 1 df, p =.16).
Embryo or nestling mortality as well as the frequency of extrapair
paternity may be influenced by female age. In our sample of 54 females, 18
were second year (SY) and 36 were after second year (ASY) females. The
mortality of embryos and nestlings was not related to female age
(2 = 0.04, 1 df, p =.85), and we found no
relationship between female age and whether there were EPY in the brood
(2 = 0.11, 1 df, p =.75) or the number of EPY in the
brood (t = 0.99, 52 df, p =.33). In contrast, Kempenaers et
al. (1999) found that SY
females were less likely to have EPY in their brood.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Since mixed paternity is common and female tree swallows control copulation (Lifjeld and Robertson, 1992
),
it seems likely that females should benefit from having some of their
offspring sired by extrapair males. Our results do not support the hypothesis
that females are gaining viability benefits early in development for their
offspring from extrapair matings. Extrapair embryos and nestlings were not
more likely to survive embryonic development or the nestling period than
within-pair young. Our results are consistent with previous work on tree
swallows showing no difference in growth or survival between within-pair and
extrapair nestlings (Kempenaers et al.,
1999). Although these studies do not support the idea that females
are gaining viability benefits through EPY, they do not allow us to reject the
viability hypothesis completely. It is possible that EPY survive better after
fledging and are more likely to recruit into the breeding population. This
will be difficult to test as local recruitment is low in tree swallows
(Whittingham LA and Dunn PO, unpublished data).
In other species, there is some evidence of enhanced recruitment of EPY
(Kempenaers et al., 1997);
however, it is difficult to make generalizations as differences occur even
among populations of the same species (e.g., blue tits, Parus
caeruleus; Kempenaers et al.,
1997; Krokene et al.,
1998). Other possible types of benefits in tree swallows may
include genetic compatibility and fertility insurance.
Genetic incompatibility between mates may be expressed through embryo
mortality and, consequently, reduced hatching success. In support of this
idea, reduced hatching success was associated with genetic similarity between
mates in great reed warblers (Acrocephalus arundinaceus;
Bensch et al., 1994) and blue
tits (Kempenaers et al.,
1996). However, in great reed warblers it was not reported whether
unhatched eggs were infertile or the result of embryo mortality, and in blue
tits only 5% of unhatched eggs contained a visible embryo. In an Ontario
population of tree swallows, Kempenaers et al.
(1999) found that broods
containing at least one extrapair young hatched a greater proportion of eggs.
Based on this result, they suggested that females mate with extrapair males to
avoid the costs of genetic incompatibility. In this case we would expect a
greater proportion of embryos that died during development to be within-pair
young; however, Kempenaers et al.
(1999) did not report the
paternity of the eggs that did not hatch. In contrast, we did not find any
association between EPY in the brood (i.e., multiple mating) and greater
hatching success, nor were eggs or young that died before fledging more likely
to be sired by the within-pair male. Nevertheless, it is still possible that
female tree swallows may be gaining more compatible genes for their offspring
through extrapair matings, as the benefits of these genes may not be seen
until later in the life of offspring (i.e., after fledging).
Another possible benefit to female tree swallows from extrapair mating is
insurance that all of the eggs in a clutch are fertilized. Infertile eggs were
rare or absent in our population during the two year study. In another study,
many tree swallow eggs that appeared unfertilized due to the lack of embryonic
development were found to be fertilized upon investigation of the
perivitelline layers around the ovum
(Kempenaers et al., 1999).
Only one of our unhatched eggs (3%) showed no embryonic development and, thus,
could have been unfertilized. The near absence of unfertilized eggs in our
study suggests that avoidance of infertility is an unlikely reason why female
tree swallows engage in extrapair fertilizations, or alternatively, that the
high rate of extrapair paternity successfully allows females to avoid
unfertilized eggs. In either case, the high rate of EPP does not appear to be
associated with embryo viability, despite a relatively high frequency of
occurrence (37% of nests had at least one unhatched egg).
In summary, our results are consistent with a number of hypotheses,
including the fertility insurance hypothesis and various types of hypotheses
that propose genetic benefits. Correlations between the proportion of
unhatched eggs and extrapair paternity do not provide enough information to
differentiate among these hypotheses
(Lifjeld, 1994). Further
discrimination between these hypotheses may be possible with paternity
assignments of EPY (e.g., Dunn et al.,
1994; Kempenaers et al.,
1999) and investigation of both the fertility of unhatched eggs
and the genetic compatibility of mates.
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ACKNOWLEDGEMENTS |
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We thank Laura Stenzler and Mike Webster for advice on the nuances of microsatellite amplification and analysis, and Ethan Clotfelter, Mary Stapleton, Kevin Thusius, and the staff at the UWM Field Station for help in the field. We also thank Jan Lifjeld for assistance with the randomization test and for providing helpful comments on the manuscript. This research was conducted under UWM Animal Care and Use Committee permits 96-97#24 and 97-98#35. This work was supported in part by a UWM Graduate School Research Award and National Science Foundation grant IBN-98-05973.
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