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Behavioral Ecology Vol. 11 No. 2: 161-168
© 2000 International Society for Behavioral Ecology
Male parental care, female reproductive success, and extrapair paternity
Laboratoire d'Ecologie, CNRS UMR 7625, Université Pierre et Marie Curie, Bât. A, 7ème étage, 7 quai St. Bernard, Case 237, F-75252 Paris, Cedex 05, France
Address correspondence to A. P. Møller. E-mail: amoller{at}hall.snv.jussieu.fr .
Received 12 November 1998; revised 22 July 1999; accepted 1 August 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Birds differ considerably in the degree of male parental care, and it has been suggested that interspecific variation in extrapair paternity is determined by the relative importance of benefits to females from male parental care and good genes from extrapair sires. I estimated the relationship between extrapair paternity and the importance of male parental care for female reproductive success mainly based on male removal studies, using a comparative approach. The reduction in female reproductive success caused by the absence of a male mate was positively correlated with the male contribution to feeding offspring. The frequency of extrapair paternity was negatively related to the reduction in female reproductive success caused by the absence of a mate. This was also the case when potentially confounding variables such as developmental mode of offspring and sexual dichromatism were considered. A high frequency of extrapair paternity occurs particularly in bird species in which males play a minor role in offspring provisioning and in which attractive males provide relatively little parental care. Bird species with frequent extrapair paternity thus appear to be those in which direct fitness benefits from male care are small, females can readily compensate for the absence of male care, and indirect fitness benefits from extrapair sires are important.
Key words: comparative analysis, direct fitness benefits, indirect fitness benefits, paternal care, sexual selection, sperm competition.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Sperm competition plays an important role in sexual selection (Birkhead and Møller, 1992
,
1998). For example, bird
species show considerable variation in extrapair paternity, with some species
having virtually none and others having more than 70% extrapair paternity
(reviews in Møller,
1998; Petrie and Kempenaers,
1998). This remarkable variation has important consequences for
the evolution of social mating systems and parental care, although the
determinants of paternity remain relatively unexplored. First, sexual
dichromatism in birds reflecting differences in the phenotypes of the two
sexes has been demonstrated to be positively correlated with the frequency of
extrapair paternity in two studies controlling for similarity due to common
descent (Møller, 1997;
Møller and Birkhead,
1994). Second, males provide relatively little food for their
offspring in bird species with a high frequency of extrapair paternity,
whereas interspecific variation in male nest building, courtship feeding, and
incubation is unrelated to extrapair paternity as determined by a comparative
analysis controlling for similarity due to common descent
(Møller and Birkhead,
1993). Third, the correlation coefficient between male
attractiveness and male contribution to provisioning of offspring is also
negatively related to extrapair paternity, implying that extrapair paternity
is common in species where attractive males provide relatively little care
(Møller and Thornhill,
1998). Fourth, immune function measured as the relative size of
the spleen is positively related to the frequency of extrapair paternity in a
comparative study controlling for similarity due to common descent
(Møller, 1997), and the
reduction in the size of the spleen in adult male birds as compared to
juvenile males is greater in species with high levels of extrapair paternity
(Møller et al., 1998).
Finally, a study using allozyme markers and RAPDs (randomly amplified
polymorphic DNAs) as measures of genetic variability has demonstrated that
extrapair paternity in birds is more common in species with a high degree of
genetic variation (Petrie et al.,
1998). The conclusion arising from these comparative studies is
that the frequency of extrapair paternity appears to be determined by indirect
fitness benefits, perhaps as reflected by immunocompetence, and that females
only rarely engage in extrapair copulations in species in which females choose
mates based on direct fitness benefits such as significant male contributions
to parental care.
Sexual selection may arise from female choice that provides individuals of
the choosy sex with direct or indirect fitness benefits or from male-male
competition (review in Andersson,
1994; Møller,
1994). The relative roles of direct and indirect fitness benefits
for female reproductive decisions remain largely unknown. If female engagement
in extrapair copulations is determined by the net benefits that females may
obtain, we can begin to investigate the ecological conditions that promote
particular kinds of fitness benefits from mate choice by determining the
factors that promote extrapair paternity over direct male investment in
offspring provisioning.
If female decisions concerning engagement in extrapair copulations and
ultimately extrapair paternity are determined by the costs and benefits of
this reproductive strategy, females may be more severely affected by male
behavior if males play an essential role in rearing of offspring. Females have
to achieve the delicate balance between cooperation of a mate and acquisition
of indirect fitness benefits from a potential extrapair partner. Not all
females are able to choose the most preferred male in a socially monogamous
mating system (and also to some extent in other mating systems) because only
the first female to make a choice will have access to that male. This point
was illustrated in an experiment
(Møller, 1988a) showing
that female barn swallows Hirundo rustica engaged in extrapair
copulations relative to the manipulated phenotype of their mate. The
constraint on female mate choice imposed by social monogamy could thus be
overcome by engaging in copulations with more attractive males while still
acquiring male parental care from the partner. This constraint on female
choice was suggested to be directly proportional to the magnitude of quality
differences among males in a population
(Møller, 1992).
If female decisions to engage in extrapair copulations are determined by
the costs and benefits of such behavior, we can expect that females are less
likely to participate in extrapair copulations if male parental care is
essential (Birkhead and Møller,
1996; Gowaty,
1996). This idea arises directly from the three hypotheses of the
evolution of monogamy described by Wittenberger and Tilson
(1980): (1) monogamy arising
from situations where male care is essential, (2) monogamous males being
failed polygynists rather than monogamists because of ecological constraints
or female-female aggression, and (3) enforced monogamy by males monopolizing
females. Birkhead and Møller
(1996) related the frequency of
extrapair paternity to the importance of male care. Extrapair paternity was
generally low in species where male care was essential
(Birkhead and Møller,
1996), although the criteria used for determining essential male
care were not independently verified. Furthermore, the study did not control
for similarity among species due to common descent. It is important to
distinguish between facultative and nonfacultative male responses in any
discussion of the relationship between extrapair paternity and paternal care
(review in Wright, 1998)
because, despite facultative responses showing weak relationships between
paternity and paternal care (Houston,
1995), a weak male response to paternity on an evolutionary scale
may render biparental care completely unstable
(Kokko, 1999).
In a series of models that incorporate ecological and evolutionary
responses by males, Kokko
(1999) has shown that two
evolutionarily stable strategy equilibria exist: the traditional social
monogamy with varying degrees of extrapair paternity, and polygamy with little
or no male parental care. The first system can only be stable if the initial
cuckoldry frequency is low, the intrinsic benefits of cuckoldry are not high,
males can accurately detect cuckoldry, and females are unable to compensate
for loss of male parental care (Kokko,
1999). Any deviation from these assumptions leads to evolution
toward the second equilibrium (i.e., polygamy). These model scenarios are
interesting because they demonstrate that social monogamy with considerable
male care can be the evolutionarily stable strategy if males cannot reliably
assess the faithfulness of their mates. Relatively high frequencies of
extrapair paternity are predicted by the models by Kokko
(1999) in the situation where
the benefits to females of extrapair copulations are large, if it is easy for
females to compensate for losses of male care, and if males cannot accurately
assess female behavior.
I tested two main questions in the present study. First, does the male share of parental care reflect the importance of the male partner for successful reproduction of a female? The importance of the presence of a male partner for female reproductive success has now been determined using male removal experiments in a large number of studies. The use of reproductive success in the absence of a male would provide an independent assessment of the role of the male partner in successful reproduction of a female because it can be compared directly with the estimate based on the proportion of parental care provided by the male. Second, is extrapair paternity related to the importance of the male partner for successful rearing of offspring? These questions were investigated in comparative studies based on female reproductive success in the presence and the absence of a partner, relative amount of male parental care, and extrapair paternity in birds.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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I searched the literature for information on the effects of male removal on female reproductive success for the 170 bird species for which there is information on the frequency of extrapair paternity. Such information was only available for 31 species, which formed the basis for the present study. Two studies with information on the effects of male removal on female reproductive success but with no information on extrapair paternity were excluded from the analyses to avoid any bias. However, none of the results reported here change by the inclusion of these species.
I estimated the importance of male parental care for female reproductive
success by determining the reduction in the number of fledged offspring for
females without a male partner in relation to male-assisted female success.
This reduction in female reproductive success caused by the absence of the
male was expressed as the proportional reduction in number of fledged
offspring (or number of offspring at the latest check of brood size before
fledging) compared to controls. Most of these studies were based on
experiments in which males were either removed or kept as controls. In some
cases, estimates of success in the absence of males were based on observations
of reproductive success for natural cases of male death. Males were removed at
different stages of the reproductive cycle in different studies. I only used
data from male removal during laying, incubation, or the early nestling
period; later removals were not considered (e.g., late removals in
Bjørnstad and Lifjeld,
1996). If more than a single study was available for a species, I
used the weighted mean estimate for the studies in the present analyses. The
sources are reported in the Appendix.
Relative male feeding rate was estimated as the proportion of all feedings provided by the male partner. I attempted to obtain estimates of relative male provisioning by searching for estimates based on observations during the entire nestling period. If estimates existed for different parts of the nestling period, the estimate of relative male parental care was the sum of all males' feeding rates divided by the sum of all male and female feeding rates combined. This method for estimating relative male parental care thus emphasizes the periods when the absolute male work load is the greatest. Estimates were obtained for the same population as that in which males were removed whenever possible. Males were assigned a missing value in the precocial species without male provisioning of offspring, although this effect of developmental mode of offspring on parental care was also investigated using developmental mode as an independent variable. The sources for the information on relative male feeding rate can be found in the Appendix.
I estimated the frequency of extrapair paternity as the percentage of
offspring sired by males other than the attending male based on molecular
studies and allozyme studies where the estimate was corrected for the
probability of detection of extrapair paternity. If estimates were available
for more than a single population, I used the mean estimate in the analyses.
Estimates of extrapair paternity in different populations are variable but
significantly repeatable: A recent analysis of variance based on 47 studies of
20 species of birds revealed a highly significant repeatability of 0.86
(Petrie et al., 1998), which
implies that most variation in extrapair paternity occurs among species.
Estimates were obtained for the same population as that in which males were
removed, whenever possible, with other estimates being excluded. If several
estimates were available for other populations, I always chose the estimate
from the closest population, based on the assumption that similarity will be
greater for neighboring populations. The sources for extrapair paternity are
given in the Appendix.
Sexual dichromatism was estimated as the difference between mean male and
female color score in the visual spectrum made by three independent scorers
(Møller and Birkhead,
1994). Such scores are highly repeatable among scorers, and they
correlated well with extrapair paternity in three other studies
(Møller and Birkhead,
1994; Møller,
1997; Petrie et al.,
1998, implying that scores estimate important features of color
signals related to sexual selection. Developmental mode of offspring is
closely associated with extensive male parental care, with altricial offspring
receiving extensive male parental care and often being fed by males. The
species were classified as either precocial or altricial. The entire data set
is reported in the Appendix.
The predictions under test were investigated using standard comparative
analyses that control for similarity in quantitative variables due to common
descent because species-specific values cannot be considered statistically
independent. The statistically independent standardized linear contrast method
was used to calculate standardized differences between values at the tips and
the nodes of a phylogeny (Felsenstein,
1985), using the CAIC software
(Purvis and Rambaut, 1995).
The analyses were based on a hypothesis of gradual evolution, with branch
lengths being proportional to the number of species that they contain
(Purvis and Rambaut, 1995),
although calculations based on equal branch lengths, which mimic a model of
punctuated evolution (Purvis and Rambaut,
1995), gave qualitatively similar results. I used the phylogenetic
relationships among birds proposed by Sibley and Ahlquist
(1990) based on DNA-DNA
hybridization combined with information on emberizids from Patten and Fugate
(1998). However, the results
reported here are independent of this particular phylogenetic hypothesis
because the use of a standard taxonomy of birds
(Howard and Moore, 1991)
provided similar conclusions. Reduction in female reproductive success,
relative male feeding rate, and extrapair paternity were squareroot-arcsine
transformed before analysis.
I investigated the relationship between relative male feeding rate and
reduction in female reproductive success using linear regression based on the
standardized contrasts, with the regression line being forced through the
origin as recommended (Purvis and Rambaut,
1995). This procedure ensures that cases of a consistent change in
dependent and independent variables are correctly identified as coevolution of
two variables (Harvey and Pagel,
1991; Purvis and Rambaut,
1995). Similarly, I investigated the relationship between
extrapair paternity and the reduction in female reproductive success in the
absence of a male partner in a linear regression analysis. The potentially
confounding effects of other variables such as sexual dichromatism, which has
been shown to covary positively with extrapair paternity and male parental
care (Møller, 1997;
Møller and Birkhead,
1993,
1994;
Petrie et al., 1998), and
developmental mode, which covaries with amount of male parental care
(Lack, 1968), were controlled
in stepwise linear regression analyses, with the regression line forced
through the origin. Analyses of reduction in reproductive success revealed a
single extreme data point (see Results) that potentially could cause bias in a
linear regression analysis based on contrasts. This potential cause of bias
was removed by ranking the variable and repeating the analysis. Ranked data
disregard the absolute difference between observations and only consider the
order of observations. The null hypothesis of no relationship between
contrasts of the dependent and independent variables was tested using a linear
regression analysis forced through the origin. If contrasts for the dependent
and the independent variable tend to covary, the regression coefficient will
significantly differ from zero.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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The importance of male parental care measured as the reduction in female reproductive success in the absence of male parental care varied from no reduction to complete breeding failure among bird species (see Appendix). The relative contribution of males to feeding offspring was strongly positively correlated with the reduction in female reproductive success in the absence of a male partner when the relationship was investigated using species-specific values as data points (Figure 1a). Because values for species cannot be considered statistically independent, the relationship was tested using statistically independent linear contrasts, and a strong positive relationship was found accounting for more than 30% of the variance in the data [Figure 1b; F = 13.99, df = 1,27, r2 =.341, p =.0009, b (SE) = 0.426 (0.114)]. This conclusion did not depend on the extreme data point in Figure 1b, as a linear regression analysis of the ranked data for reduction in female reproductive success still gave a significant result [F = 7.25, df = 1,27, r2 =.212, p =.012, b (SE) = 0.004 (0.001)]. The potentially confounding effects of extrapair paternity and sexual dichromatism were entered as linear contrasts in a stepwise linear regression analysis with contrast in male contribution to feeding as the dependent variable and contrast in the reduction in female reproductive success as an additional independent variable. The only variable that entered the model was reduction in female reproductive success (with the regression model remaining as stated above). Hence the positive relationship was not confounded by these variables.
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An analysis excluding the species with complete breeding failure in the absence of a male did not change the conclusion from the analysis reported above [analysis of contrasts: F = 17.70, df = 1,19, r2 =.482, p =.0005, b (SE) = 0.440 (0.105)].
Extrapair paternity was hypothesized to be more common in species where male parental care was less essential for successful reproduction, and values for species indicated such a negative relationship (Figure 2a). A statistical analysis of independent standardized linear contrasts confirmed that extrapair paternity was negatively related to the reduction in female reproductive success in the absence of a male partner, accounting for 30% of the variance in the data set [Figure 2b; F = 12.56, df = 1,29, r2 =.302, p =.0014, b (SE) = -0.272 (0.077)]. This relationship did not depend on the extreme data point to the right in Figure 2b because a regression analysis of the ranked data for the reduction in female reproductive success still was statistically significant [F = 9.96, df = 1,29, r2 =.256, p =.0037, b (SE) = -0.002 (0.001)]. This was also the case when the potentially confounding effects of sexual dichromatism and developmental mode were taken into consideration; a stepwise regression analysis only entered the variable representing the reduction in female reproductive success in the absence of a male partner into the model (regression statistics as above). Hence, the importance of male parental care appeared to be the single most important variable accounting for interspecific variation in extrapair paternity in the present data set.
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An analysis excluding the species with complete breeding failure in the absence of a male did not change the conclusion reported above [analysis of contrasts: F = 8.34, df = 1,19, r2 =.305, p =.0094, b (SE) = -0.296 (0.102)].
Finally, the male contribution to feeding offspring was significantly negatively related to extrapair paternity (F = 9.55, df = 1,27, r2 =.261, p =.0046, b (SE) = -0.737 (0.238)]. This was even the case when excluding species with complete breeding failure in the absence of a male (analysis of contrasts: F = 6.17, df = 1,19, r2 =.245, p =.0225, b (SE) = -0.585 (0.236)].
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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The reproductive success of monogamous females unassisted by their male partners has been used to assess the importance of male parental care for female reproduction (Gowaty, 1983
). Many of these studies have demonstrated a considerable
amount of interspecific variation in the relative importance of male parental
care for female reproductive success, ranging from no effect to complete
breeding failure (see Appendix). The difference in reproductive success of
females attended by their male partners and unattended females was assumed to
provide an estimate of the relative importance of male care. Alternatively,
the reduction in reproductive success of unattended females may provide an
estimate of differential parental investment by females. For example, it is
possible that females may invest differentially in reproduction in the
presence of a male partner, as shown in many different studies of birds (first
described by Burley, 1986;
review in Møller and Thornhill,
1998), whereas the absence of a partner reduces or eliminates any
reproductive value of offspring. Hence, females may not invest or reduce
investment in reproduction when the male is absent. However, we can
hypothesize that this reduction should be directly related to costs and
benefits experienced by females. We should expect females in either situation
to achieve a net benefit from their reproductive decisions. I found a positive
correlation between the male share of provisioning of offspring and the
reduction of female success due to the absence of the male partner
(Figure 1). The increasing
importance of male parental care for female reproductive success with
increasing male share of food provisioning was independent of developmental
mode because the two precocial species with no male feeding of offspring were
excluded. Females are known to compensate partially or fully for the absence
of male parental care by increasing feeding rate (e.g.,
Saino and Møller, 1995;
Wright and Cuthill, 1989), in
which case the value of male care to females may be an underestimate. The
present study assumes that the extent of female compensation is negatively
related to the importance of male care. This assumption is supported by
females being unable to compensate for the absence of male care in species
with large reductions in reproductive success or complete breeding failure.
The tests presented here suggest that the reduction in female reproductive
success in the absence of a male partner indeed reflects the importance of the
male for female reproductive success.
The second major finding was that the frequency of extrapair paternity was
inversely related to the reduction in female reproductive success in the
absence of a male partner (Figure
2). This relationship remained significant after controlling for
two potentially confounding variables (sexual dichromatism and developmental
mode of offspring). Hence, extrapair paternity appears to be particularly
common when males play a relatively small role in the successful rearing of
offspring. This result confirms the suggestion by Birkhead and Møller
(1996) that females generally
do not engage in extrapair copulations to adjust their choice of social mates
when male assistance is essential for the successful rearing of offspring. The
reduction in female reproductive success in the absence of a male partner was
solely estimated from the reduction in the number of fledged offspring. It is
likely that the presence of a parental male may also affect components of
reproductive success such as the quality of offspring. The effects reported in
the present study thus appear to be underestimates, in particular for species
with dramatic reductions in female reproductive success. The alternative
interpretation of the result in Figure
2 is that this trend arises as a consequence of a trade-off
between male care and pursuit of extrapair copulations (review in
Wright, 1998). This
explanation may not seem likely when considering that males particularly
pursue extrapair copulations immediately after the end of the fertile period
of their own mate (review in Birkhead and
Møller, 1992) and that extrapair mating effort consists of
a small fraction of the time budget of males (e.g.,
Brodsky, 1988;
Møller, 1985;
Stutchbury, 1998).
A final result of the comparative analyses was that males provided
relatively less parental care in species with a higher frequency of extrapair
paternity. This result confirms the results of previous analyses demonstrating
a negative relationship between extrapair paternity and male parental care
(Møller and Birkhead,
1993; Møller and
Cuervo, in press).
I can place the current study into a general framework relating sperm
competition to sexual selection for direct and indirect fitness benefits to
females (Figure 3). In some
species, females may choose mates for direct fitness benefits such as male
parental care, and the preferred males with the most extreme secondary sexual
characters generally provide the largest share of food provisioning to
offspring, as compared to less attractive males
(Møller and Thornhill,
1998). Extrapair copulations and extrapair paternity are generally
infrequent in these species apparently because females may obtain no or few
indirect fitness benefits from extrapair copulations (hence the negative
relationship between direct fitness benefits and extrapair paternity in
Figure 3). A second category of
species is that in which attractive males with the most extreme secondary
sexual characters provide the least amount of parental care, and these species
appear to have more genetic variation
(Petrie et al., 1998;
indicated by a positive relationship between genetic variation and indirect
fitness benefits in Figure 3)
and larger immune defense organs
(Møller, 1997), than
species in which females choose mates based on direct fitness benefits. Hence
the presence of indirect benefits promotes extrapair paternity as indicated by
the positive relationship between indirect fitness benefits and extrapair
paternity (Figure 3). A high
level of genetic variability may also directly promote sexual selection and
extrapair paternity because a high mutational input can maintain intense
sexual selection for longer than a low mutational input. Males of these
species appear to vary considerably in phenotypic and perhaps also genetic
quality, and females often engage in extrapair copulations. Hence, levels of
extrapair paternity often reach high levels in this group of species. Because
females are able to rear the offspring with no or relatively little male
assistance, this group is characterized by a weak influence of male parental
care on reproductive success of females. The reduction in female reproductive
success in the absence of a male partner is therefore small. This is the
situation in which females differentially invest in the offspring of
attractive males because the cost of parental care is relatively low and
because females stand to gain indirect fitness benefits from their mate
choice. The two different categories of species may represent two distinct
classes of species, as indicated by the negative interaction between direct
and indirect fitness benefits acquired by females through their mate choice
(Figure 3). This scenario has
similarities to the results of a series of models of the relationship among
male genetic quality, the importance of male parental care for female
reproductive success, and the ability of males to assess the probability of
cuckoldry (Kokko, 1999).
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Certain ecological conditions may allow females to rear offspring without
much assistance from their male partners, and males may in such circumstances
evolve extravagant secondary sexual characters that reflect indirect fitness
benefits. Large variation in male phenotypic and genetic quality provides
opportunities for females to acquire indirect fitness benefits from extrapair
copulations with attractive males. This group of species is thus characterized
by a high frequency of extrapair paternity. The alternative situation appears
in species where males signal their parenting ability and females choose mates
based on direct fitness benefits. Because such benefits only are acquired to a
small extent through extrapair copulations (e.g.,
Gray, 1997), the frequency of
extrapair paternity tends to be low in this group of birds.
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APPENDIX |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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ACKNOWLEDGEMENTS |
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Three referees provided constructive criticism. E. Creighton, L. Garamszegy, B. Hatchwell, F. Hunter, B. Kempenaers, E. Korpimäki, M. I. McGrady, J. Moreno, I. Newton, D. Parrott, D. Shutler, and J. Wiehn kindly provided unpublished information. A.P.M. was supported by an Atipe Blanche from CNRS.
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