Behavioral Ecology Vol. 11 No.

2: 161–168

Male parental care, female reproductive

success, and extrapair paternity
Anders Pape Møller
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

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. [Behav Ecol 11:161–168 (2000)]

S perm competition plays an important role in sexual selec-

tion (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 sys-
tems and parental care, although the determinants of pater-
nity 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, im-
plying 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 re-
duction in the size of the spleen in adult male birds as com-
pared 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 poly-
morphic DNAs) as measures of genetic variability has dem-
onstrated that extrapair paternity in birds is more common
Address correspondence to A. P. Møller. E-mail: amoller@
hall.snv.jussieu.fr.
Received 12 November 1998; revised 22 July 1999; accepted 1 Au-
gust 1999.

2000 International Society for Behavioral Ecology
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 reflect-
ed by immunocompetence, and that females only rarely en-
gage in extrapair copulations in species in which females
choose mates based on direct fitness benefits such as signifi-
cant 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 Anders-
son, 1994; Møller, 1994). The relative roles of direct and in-
direct fitness benefits for female reproductive decisions re-
main 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 condi-
tions that promote particular kinds of fitness benefits from
mate choice by determining the factors that promote extra-
pair paternity over direct male investment in offspring provi-
sioning.
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 pheno-
type of their mate. The constraint on female mate choice im-
posed by social monogamy could thus be overcome by engag-
ing in copulations with more attractive males while still ac-
quiring 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 pop-
ulation (Møller, 1992).
162
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 be-
cause of ecological constraints or female–female aggression,
and (3) enforced monogamy by males monopolizing females.
Birkhead and Møller (1996) related the frequency of extra-
pair paternity to the importance of male care. Extrapair pa-
ternity was generally low in species where male care was es-
sential (Birkhead and Møller, 1996), although the criteria
used for determining essential male care were not indepen-
dently verified. Furthermore, the study did not control for
similarity among species due to common descent. It is impor-
tant 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 relation-
ships 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 evo-
lutionary responses by males, Kokko (1999) has shown that
two evolutionarily stable strategy equilibria exist: the tradition-
al social monogamy with varying degrees of extrapair pater-
nity, and polygamy with little or no male parental care. The
first system can only be stable if the initial cuckoldry frequen-
cy 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 to-
ward the second equilibrium (i.e., polygamy). These model
scenarios are interesting because they demonstrate that social
monogamy with considerable male care can be the evolution-
arily stable strategy if males cannot reliably assess the faithful-
ness 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 copula-
tions are large, if it is easy for females to compensate for losses
of male care, and if males cannot accurately assess female be-
havior.
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 re-
productive success has now been determined using male re-
moval 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 com-
pared directly with the estimate based on the proportion of
parental care provided by the male. Second, is extrapair pa-
ternity related to the importance of the male partner for suc-
cessful 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.
MATERIALS AND METHODS
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
Behavioral Ecology Vol. 11 No. 2
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 ex-
trapair 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 part-
ner 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 repro-
ductive cycle in different studies. I only used data from male
removal during laying, incubation, or the early nestling peri-
od; 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 pe-
riod. 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 off-
spring on parental care was also investigated using develop-
mental 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 per-
centage 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 vari-
ance 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 popu-
lation as that in which males were removed, whenever possi-
ble, with other estimates being excluded. If several estimates
were available for other populations, I always chose the esti-
mate 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 be-
tween mean male and female color score in the visual spec-
trum made by three independent scorers (Møller and Birk-
head, 1994). Such scores are highly repeatable among scorers,
and they correlated well with extrapair paternity in three oth-
er studies (Møller and Birkhead, 1994; Møller, 1997; Petrie et
Møller • Extrapair paternity and male parental care 163

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 val-
ues cannot be considered statistically independent. The statis-
tically 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 cal-
culations based on equal branch lengths, which mimic a mod-
el of punctuated evolution (Purvis and Rambaut, 1995), gave
qualitatively similar results. I used the phylogenetic relation-
ships among birds proposed by Sibley and Ahlquist (1990)
based on DNA–DNA hybridization combined with informa-
tion on emberizids from Patten and Fugate (1998). However,
the results reported here are independent of this particular
phylogenetic hypothesis becuase the use of a standard tax-
onomy of birds (Howard and Moore, 1991) provided similar
conclusions. Reduction in female reproductive success, rela-
tive male feeding rate, and extrapair paternity were square-
root–arcsine transformed before analysis.
I investigated the relationship between relative male feed-
ing rate and reduction in female reproductive success using
linear regression based on the standardized contrasts, with the Figure 1
regression line being forced through the origin as recom- Relative male feeding rate in relation to reduction in female
mended (Purvis and Rambaut, 1995). This procedure ensures reproductive success in the absence of a mate. Values are (a) mean
that cases of a consistent change in dependent and indepen- estimates for species and (b) statistically independent linear
dent variables are correctly identified as coevolution of two contrasts.
variables (Harvey and Pagel, 1991; Purvis and Rambaut,
1995). Similarly, I investigated the relationship between extra-
pair paternity and the reduction in female reproductive suc- correlated with the reduction in female reproductive success
cess in the absence of a male partner in a linear regression in the absence of a male partner when the relationship was
analysis. The potentially confounding effects of other variables investigated using species-specific values as data points (Figure
such as sexual dichromatism, which has been shown to covary 1a). Because values for species cannot be considered statisti-
positively with extrapair paternity and male parental care cally independent, the relationship was tested using statisti-
(Møller, 1997; Møller and Birkhead, 1993, 1994; Petrie et al., cally independent linear contrasts, and a strong positive re-
1998), and developmental mode, which covaries with amount lationship was found accounting for more than 30% of the
of male parental care (Lack, 1968), were controlled in step- variance in the data [Figure 1b; F ⫽ 13.99, df ⫽ 1,27, r2 ⫽
wise linear regression analyses, with the regression line forced .341, p ⫽ .0009, b (SE) ⫽ 0.426 (0.114)]. This conclusion did
through the origin. Analyses of reduction in reproductive suc- not depend on the extreme data point in Figure 1b, as a lin-
cess revealed a single extreme data point (see Results) that ear regression analysis of the ranked data for reduction in
potentially could cause bias in a linear regression analysis female reproductive success still gave a significant result [F ⫽
based on contrasts. This potential cause of bias was removed 7.25, df ⫽ 1,27, r2 ⫽ .212, p ⫽ .012, b (SE) ⫽ 0.004 (0.001)].
by ranking the variable and repeating the analysis. Ranked The potentially confounding effects of extrapair paternity and
data disregard the absolute difference between observations sexual dichromatism were entered as linear contrasts in a step-
and only consider the order of observations. The null hypoth- wise linear regression analysis with contrast in male contri-
esis of no relationship between contrasts of the dependent bution to feeding as the dependent variable and contrast in
and independent variables was tested using a linear regression the reduction in female reproductive success as an additional
analysis forced through the origin. If contrasts for the depen- independent variable. The only variable that entered the
dent and the independent variable tend to covary, the re- model was reduction in female reproductive success (with the
gression coefficient will significantly differ from zero. regression model remaining as stated above). Hence the pos-
itive relationship was not confounded by these variables.
An analysis excluding the species with complete breeding
RESULTS
failure in the absence of a male did not change the conclusion
The importance of male parental care measured as the re- from the analysis reported above [analysis of contrasts: F ⫽
duction in female reproductive success in the absence of male 17.70, df ⫽ 1,19, r2 ⫽ .482, p ⫽ .0005, b (SE) ⫽ 0.440 (0.105)].
parental care varied from no reduction to complete breeding Extrapair paternity was hypothesized to be more common
failure among bird species (see Appendix). The relative con- in species where male parental care was less essential for suc-
tribution of males to feeding offspring was strongly positively cessful reproduction, and values for species indicated such a
164
Figure 2
Extrapair paternity in relation to reduction in female reproductive
success in the absence of a mate. Values are (a) mean estimates for
species and (b) statistically independent linear contrasts.
negative relationship (Figure 2a). A statistical analysis of in-
dependent standardized linear contrasts confirmed that ex-
trapair 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 anal-
ysis of the ranked data for the reduction in female reproduc-
tive 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 con-
sideration; a stepwise regression analysis only entered the var-
iable representing the reduction in female reproductive suc-
cess in the absence of a male partner into the model (regres-
sion statistics as above). Hence, the importance of male pa-
rental care appeared to be the single most important variable
accounting for interspecific variation in extrapair paternity in
the present data set.
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 sig-
nificantly 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 con-
Behavioral Ecology Vol. 11 No. 2
trasts: F ⫽ 6.17, df ⫽ 1,19, r2 ⫽ .245, p ⫽ .0225, b (SE) ⫽
⫺0.585 (0.236)].
DISCUSSION
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 unat-
tended females may provide an estimate of differential paren-
tal investment by females. For example, it is possible that fe-
males may invest differentially in reproduction in the pres-
ence 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, fe-
males 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 de-
cisions. I found a positive correlation between the male share
of provisioning of offspring and the reduction of female suc-
cess due to the absence of the male partner (Figure 1). The
increasing importance of male parental care for female re-
productive success with increasing male share of food provi-
sioning 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 extra-
pair 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 pa-
ternity 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 part-
ner 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 spe-
cies with dramatic reductions in female reproductive success.
The alternative interpretation of the result in Figure 2 is that
Møller • Extrapair paternity and male parental care
Figure 3
Hypothetical causal relationships between genetic variation, indirect
and direct fitness benefits from sexual selection, and extrapair
paternity.
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 immedi-
ately after the end of the fertile period of their own mate
(review in Birkhead and Møller, 1992) and that extrapair mat-
ing 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 re-
sults of previous analyses demonstrating a negative relation-
ship 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 re-
lating 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). Extra-
pair copulations and extrapair paternity are generally infre-
quent in these species apparently because females may obtain
no or few indirect fitness benefits from extrapair copulations
(hence the negative relationship between direct fitness ben-
efits and extrapair paternity in Figure 3). A second category
of species is that in which attractive males with the most ex-
treme secondary sexual characters provide the least amount
of parental care, and these species appear to have more ge-
165
netic variation (Petrie et al., 1998; indicated by a positive re-
lationship between genetic variation and indirect fitness ben-
efits 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 re-
lationship between indirect fitness benefits and extrapair pa-
ternity (Figure 3). A high level of genetic variability may also
directly promote sexual selection and extrapair paternity be-
cause 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 ex-
trapair 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 as-
sistance, 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 ac-
quired 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).
Certain ecological conditions may allow females to rear off-
spring without much assistance from their male partners, and
males may in such circumstances evolve extravagant second-
ary sexual characters that reflect indirect fitness benefits.
Large variation in male phenotypic and genetic quality pro-
vides opportunities for females to acquire indirect fitness ben-
efits 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 spe-
cies 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 pa-
ternity tends to be low in this group of birds.
Three referees provided constructive criticism. E. Creighton, L. Gar-
amszegy, 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.
166 Behavioral Ecology Vol. 11 No. 2

APPENDIX
Reduction in female reproductive success in the absence of a mate, relative male feeding rate, extrapair paternity, sexual dichromatism, and
developmental mode of offspring for birds

Reduction in RS Male feeding

Species (%) Reference (%) Reference

Accipiter gentilis 100.0 Holstein, 1942 98.00 Holstein, 1942

Accipiter nisus 100.0 Newton, 1986 70.10 Møller and Birkhead, 1993
Agelaius phoeniceus 0.0 Shutler D, pc 4.92 Møller and Birkhead, 1993

Anser caerulescens 5.0 Martin et al., 1985 — Møller and Birkhead, 1993
Cardinalis cardinalis 54.0 Richmond, 1978 55.90 Ritchison et al., 1994
Columba livia 86.0 Burley, 1980 50.00 Johnson, 1992
Eudyptes schlegeli 100.0 Moreno J, pc 38.50 Marchant and Higgins, 1990
Falco sparverius 88.0 Bowman and Bird, 1987 53.10 Wiehn J, pc
Falco tinnunculus 100.0 Korpimäki E, pc 80.00 Cramp and Simmons, 1980
Ficedula albicollis 36.4 Garamszegy L, pc 53.00 Sheldon et al., 1997

Ficedula hypoleuca 34.0 Alatalo et al., 1982 44.00 Møller and Birkhead, 1993
Haematopus ostralegus 100.0 Heg and van Treuren, 1998 50.00 Møller and Birkhead, 1993
Hirundo rustica 8.3 Møller, 1988b 46.70 Møller and Birkhead, 1993
Junco hyemalis 14.0 Wolf et al., 1988 55.50 Wolf et al., 1990
Lagopus lagopus 9.0 Hannon, 1984, Martin, 1984 — Cramp and Simmons, 1980
Melospiza melodia 19.0 Smith et al., 1982 71.20 Møller and Birkhead, 1993
Nectarinia osea 60.0 Markman et al., 1996 32.97 Markman et al., 1996
Parus caeruleus 20.7 Sasvari, 1986 55.00 Kempenaers B, pc
Parus major 22.3 Sasvari, 1986 53.97 Verhulst, 1995
Passerculus sandwichensis 19.0 Weatherhead, 1979 30.00 Freeman-Gallant, 1996
Passerina cyanea 0.0 Payne and Payne, 1996 5.00 Møller and Birkhead, 1993
Phylloscopus trochilus 7.02 Bjørnstad and Lifjeld, 1996 36.43 Bjørnstad and Lifjeld, 1996
Pica pica 100.0 Dunn and Hannon, 1989 50.00 Parrott D, pc
Pygoscelis adeliae 100.0 Moreno J, pc 50.00 Marchant and Higgins, 1990
Sialia sialis 23.1 Gowaty, 1996 45.50 Møller and Birkhead, 1993
Spizella pusilla 0.0 Carey, 1990 50.00 Carey et al., 1994
Tachycineta bicolor 4.3 Dunn and Hannon, 1992 47.60 Møller and Birkhead, 1993
Tockus monteiri 100.0 Kemp, 1988 100.00 Kemp, 1988
Troglodytes aedon 26.5 Bart and Tornes, 1989 55.25 Johnson and Kermott, 1993
Turdus merula 75.4 Desrochers and Magrath, 1996 51.00 Hatchwell B, pc
Zonotrichia albicollis 0.0 Whillans and Falls, 1990 45.40 Falls and Kopachena, 1994

RS, reproductive success; EPP, extrapair paternity; SD, sexual dichromatism; DM, developmental mode (A, altricial; P, precocial); pc, personal
communication.

REFERENCES
Alatalo RV, Lundberg A, Ståhlbrandt K, 1982. Why do pied flycatcher
females mate with already-mated males? Anim Behav 30:585–593.
Andersson M, 1994. Sexual selection. Princeton, New Jersey: Prince-
ton University Press.
Bart J, Tornes A, 1989. Importance of monogamous male birds in
determining reproductive success: Evidence for house wrens and a
review of male-removal studies. Behav Ecol Sociobiol 24:109–116.
Birkhead TR, Møller AP, 1992. Sperm competition in birds. London:
Academic Press.
Birkhead TR, Møller AP, 1996. Monogamy and sperm competition in
birds. In: Partnerships in birds: The study of monogamy (Black JM,
ed). Oxford: Oxford University Press; 323–343.
Birkhead TR, Møller AP (eds), 1998. Sperm competition and sexual
selection. London: Academic Press.
Bjørnstad G, Lifjeld JT, 1996. Male parental care promotes early fledg-
ing in an open-nester, the willow warbler Phylloscopus trochilus. Ibis
138:229–235.
Bjørnstad G, Lifjeld JT, 1997. High frequency of extra-pair paternity
in a dense and synchronous population of willow warblers Phyllos-
copus trochilus. J Avian Biol 28:319–324.
Bowman R, Bird DM, 1987. Behavioral strategies of American kestrels
during mate replacement. Behav Ecol Sociobiol 20:129–135.
Brodsky LM, 1988. Mating tactics of male rock ptarmigan Lagopus
mutus: a conditional strategy. Anim Behav 36:335–342.
Burley N, 1980. Clutch overlap and clutch size: Alternative and com-
plementary reproductive strategies. Am Nat 115:223–246.
Burley N, 1986. Sexual selection for aesthetic traits in species with
biparental care. Am Nat 127:415–445.
Carey M, 1990. Effects of brood size and nestling age on parental care
by male field sparrows (Spizella pusilla). Auk 107:580–586.
Carey M, Burhans DE, Nelson DA, 1994. Tree sparrow (Spizella pus-
illa). In: The birds of North America, no. 103 (Poole A, Gill F, eds).
Washington, DC: The American Ornithologists’ Union.
Cramp S, Simmons KEL (eds), 1980. The birds of the Western Pale-
arctic, vol 2. Oxford: Oxford University Press.
Desrochers A, Magrath RD, 1996. Divorce in the European Blackbird:
seeking greener pastures? In: Partnerships in birds: The study of
monogamy (Black JM, ed). Oxford: Oxford University Press; 177–
191.
Dunn PO, Hannon SJ, 1989. Evidence for obligate male parental care
in black-billed magpies. Auk 106:635–644.
Dunn PO, Hannon SJ, 1992. Effects of food abundance and male
parental care on reproductive success and monogamy in tree swal-
lows. Auk 109:488–499.
Dunn PO, Whittingham LA, Lifjeld JT, Robertson RJ, Boag PT, 1994.
Effects of breeding density, synchrony, and experience on extrapair
paternity in tree swallows. Behav Ecol 5:123–129.
Falls JB, Kopachena JG, 1994. White-crowned sparrow (Zonotrichia
albicollis). In: The birds of North America, no. 128 (Poole A, Gill
F, eds). Washington, DC: The American Ornithologists’ Union.
Felsenstein J, 1985. Phylogenies and the comparative method. Am Nat
125:1-l5.
Freeland JR, Hannon SJ, Dobush G, Boag PT, 1995. Extra-pair pater-
nity in willow ptarmigan broods: measuring costs of polygyny to
males. Behav Ecol Sociobiol 36:349–355.
Freeman-Gallant CR, 1996. DNA fingerprinting reveals female pref-
erence for male parental care in Savannah sparrows. Proc R Soc
Lond B 263:157–160.
Møller • Extrapair paternity and male parental care 167

APPENDIX Heg D, van Treuren R, 1998. Female-female cooperation in polygy-

Extended nous oystercatchers. Nature 391:687–691.
Holstein V, 1942. Duehøgen. Copenhagen: Hirschsprung.
Houston AI, 1995. Parental effort and paternity. Anim Behav 50:1635–
EPP 1644.
Howard R, Moore A, 1991. A complete checklist of the birds of the
(%) Reference SD DM world, 2nd ed. London: Academic Press.
Johnson LS, Kermott LH, 1993. Why is reduced male parental assis-
3.2 Gavin et al., 1998 0.5 A tance detrimental to the reproductive success of secondary female
5.4 Newton I, and McGrady MI, pc 1.0 A house wrens? Anim Behav 46:1111–1120.
25.6 Gibbs et al., 1990; 2.5 A Johnson RF, 1992. Rock pigeon (Columba livia). In: The birds of
Weatherhead and Boag, 1995 North America, no. 13 (Poole A, Gill F, eds). Washington, DC: The
2.4 Lank et al., 1989 0.0 P American Ornithologists’Union.
13.5 Ritchison et al., 1994 2.0 A Kemp AC, 1988. Hornbills. In: The birds of Africa, vol. 3 (Fry CH,
1.0 Johnson, 1992 0.0 A Keith S, Urban EK, eds). London: Academic Press; 375–413.
4.0 St. Clair et al., 1995 0.0 A Kempenaers B, Verheyen GR, Broeck M v d, Burke T, Broeckhoven
11.2 Villarroel et al., 1998 1.0 A CV, Dhondt AA, 1992. Extra-pair paternity results from female pref-
1.9 Korpimäki et al., 1996 1.0 A erence for high-quality males in the blue tit. Nature 357:494–496.
18.2 Sheldon et al., 1997, 1.0 A Kempenaers B, Verheyen GR, Dhondt AA, 1995. Mate guarding and
Sheldon and Ellegren, 1999 copulation behaviour in monogamous and polygynous blue tits: do
23.7 Gelter and Tegelström, 1992 1.5 A males follow a best-of-a-bad-job strategy? Behav Ecol Sociobiol 36:
1.5 Heg et al., 1993 0.0 P 33–42.
28.0 Møller and Tegelström, 1997 1.0 A Kempenaers B, Verheyen GR, Dhondt AA, 1997. Extrapair paternity
28.3 Ketterson et al., 1997 0.0 A in the blue tit (Parus caeruleus): female choice, male characteristics,
9.4 Freeland et al., 1995 1.0 P and offspring quality. Behav Ecol 8:481–492.
0.0 Smith, 1991 0.0 A Ketterson ED, Parker PG, Raouf SA, Nolan Jr V, Ziegenfus C, Chan-
26.0 Zilberman R, pc 4.5 A dler CR, 1997. The relative impact of extra-pair fertilizations on
12.5 Kempenaers et al., 1992, 1995, 1997 0.0 A variation in male and female reproductive success in Dark-eyed Jun-
18.3 Lubjuhn et al., 1993 1.0 A cos (Junco hyemalis). Orn Monogr 49:81–101.
23.1 Freeman-Gallant, 1996, 1997 0.0 A Kokko H, 1999. Cuckoldry and the stability of biparental care. Ecol
36.7 Westneat, 1987 2.5 A Lett 2:247–255.
33.0 Bjørnstad and Lifjeld, 1997 0.0 A Korpimäki E, Lahti K, May CA, Parkin DT, Powell GB, Tolonen P,
5.2 Parrott, 1995 0.0 A Wetton JH, 1996. Copulatory behaviour and paternity determined
3.0 Hunter F, pc. 0.0 A by DNA fingerprinting in kestrels: effects of cyclic food abundance.
32.0 Gowaty and Bridges, 1991a,b 2.5 A Anim Behav 51:945–955.
15.1 Carey et al., 1994 0.0 A Lack D, 1968. Ecological adaptations for breeding in birds. London:
60.0 Dunn et al., 1994 0.0 A Chapman and Hall.
0.0 Stanback et al., 1999 0.0 A Lank DB, Mineau P, Rockwell RF, Cooke F, 1989. Intraspecific nest
8.4 Soukup and Thompson, 1997 0.0 A parasitism and extra-pair copulation in lesser snow geese. Anim Be-
14.0 Creighton E, pc 2.0 A hav 37:74–89.
12.8 Tuttle, 1993 0.0 A Lubjuhn T, Curio E, Muth SC, Brün J, Epplen JT, 1993. Influence of
extra-pair paternity on parental care in great tits (Parus major). In:
DNA fingerprinting: state of the science (Pena SDJ, Chakraborty R,
Epplen JT, Jeffreys AJ, eds). Basel: Birkhäuser; 379–385.
Freeman-Gallant CR, 1997. Extra-pair paternity in monogamous and Marchant S, Higgins PJ (eds), 1990. Handbook of Australian, New
polygynous savannah sparrows, Passerculus sandwichensis. Anim Be- Zealand and Antarctic birds, vol 1. Melbourne: Oxford University
hav 53:397–404. Press.
Gavin TA, Reynolds RT, Joy SM, Leslie D, May B, 1998. Genetic evi- Markman S, Yom-Tov Y, Wright J, 1996. The effect of male removal
dence for low frequency of extra-pair fertilizations in northern gos- on female parental care in the orange-tufted sunbird. Anim Behav
hawks. Condor 100:556–560. 52:437–444.
Gelter HP, Tegelström H, 1992. High frequency of extra-pair paternity Martin K, 1984. Reproductive defence priorities of male willow ptar-
in Swedish pied flycatchers revealed by allozyme electrophoresis migan (Lagopus lagopus): enhancing mate survival or extending
and DNA fingerprinting. Behav Ecol Sociobiol 31:1–7. paternity options? Behav Ecol Sociobiol 16:57–63.
Gibbs HL, Weatherhead PJ, Boag PT, White BN, Tabak LM, Hoysak Martin K, Cooch FG, Rockwell RF, Cooke F, 1985. Reproductive per-
DJ, 1990. Realized reproductive success of polygynous red-winged formance in lesser snow geese: are two parents essential? Behav
blackbirds revealed by DNA markers. Science 250:1394–1397. Ecol Sociobiol 17:257–263.
Gowaty PA, 1983. Male parental care and apparent monogamy among Møller AP, 1985. Mixed reproductive strategy and mate guarding in
eastern bluebirds (Sialia sialis). Am Nat 121:149–157. a semi-colonial passerine, the swallow Hirundo rustica. Behav Ecol
Gowaty PA, 1996. Battles of the sexes and origins of monogamy. In: Sociobiol 17:401–408.
Partnerships in birds: the study of monogamy (Black JM, ed). Ox- Møller AP, 1988a. Female choice selects for male sexual tail orna-
ford: Oxford University Press; 21–52. ments in the monogamous swallow. Nature 322:640–642.
Gowaty PA, Bridges WC, 1991a. Behavioral, demographic, and envi- Møller AP, 1988b. Infanticidal and anti-infanticidal strategies in the
ronmental correlates of extrapair fertilizations in eastern bluebirds swallow Hirundo rustica. Behav Ecol Sociobiol 22:365–371.
Sialia sialis. Behav Ecol 2:339–350. Møller AP, 1992. Frequency of female copulations with multiple males
Gowaty PA, Bridges WC, 1991b. Nest box availability affects extra-pair and sexual selection. Am Nat 139:1089–1101.
fertilizations and conspecific nest parasitism in eastern bluebirds, Møller AP, 1994. Sexual selection and the barn swallow. Oxford: Ox-
Sialia sialis. Anim Behav 41:661–675. ford University Press.
Gray EM, 1997. Female red-winged blackbirds accrue material bene- Møller AP, 1997. Immune defence, extra-pair paternity, and sexual
fits from copulation with extra-pair males. Anim Behav 53:625–639. selection in birds. Proc R Soc Lond B 264:561–566.
Hannon SJ, 1984. Factors limiting polygyny in willow ptarmigan. Anim Møller AP, 1998. Sperm competition and sexual selection. In: Sperm
Behav 32:153–161. competition and sexual selection (Birkhead TR, Møller AP, eds).
Harvey PH, Pagel M, 1991. The comparative method in evolutionary London: Academic Press; 51–89.
biology. Oxford: Oxford University Press. Møller AP, Birkhead TR, 1993. Certainty of paternity covaries with
Heg D, Ens BJ, Burke T, Jenkins L, Kruijt JP, 1993. Why does the paternal care in birds. Behav Ecol Sociobiol 33:361–368.
typically monogamous oystercatcher (Haematopus ostralegus) en- Møller AP, Birkhead TR, 1994. The evolution of plumage brightness
gage in extra-pair copulations? Behaviour 126:247–289. in birds is related to extra-pair paternity. Evolution 48:1089–1100.
168
Møller AP, Cuervo JJ, in press. The evolution of paternity and paternal
care in birds. Behav Ecol.
Møller AP, Sorci G, Erritzøe J, 1998. Sexual dimorphism in immune
defense. Am Nat 152:697–621.
Møller AP, Tegelström H, 1997. Extra-pair paternity and tail orna-
mentation in the barn swallow Hirundo rustica. Behav Ecol Socio-
biol 41:353–360.
Møller AP, Thornhill R, 1998. Male parental care, differential parental
investment by females, and sexual selection. Anim Behav 55:1507–
1515.
Newton I, 1986. The sparrowhawk. London: T & AD Poyser.
Parrott D, 1995. Social organisation and extra-pair behaviour in the
European black-billed magpie Pica pica (PhD thesis). Sheffield:
University of Sheffield.
Patten MA, Fugate M, 1998. Systematic relationship among the em-
berizid sparrows. Auk 115:412–424.
Payne RB, Payne LL, 1996. Dispersal, demography, and the persis-
tence of partnerships in Indigo Buntings. In: Partnerships in birds:
the study of monogamy (Black JM, ed). Oxford: Oxford University
Press; 305–320.
Petrie M, Kempenaers B, 1998. Why does the proportion of extra-pair
paternity in birds vary between species and between populations?
Trends Ecol Evol 13:52–58.
Petrie M, Doums C, Møller AP, 1998. The degree of extra-pair pater-
nity increases with genetic variation. Proc Natl Acad Sci USA 95:
9390–9395.
Purvis A, Rambaut A, 1995. Comparative analysis by independent con-
trasts (CAIC): an Apple Macintosh application for analysing com-
parative data. Computer Appl Biosci 11:247–251.
Richmond AW, 1978. An experimental study of advantages of monog-
amy in the cardinal (PhD thesis). Bloomington: Indiana University.
Ritchison G, Klatt PH, Westneat DF, 1994. Mate guarding and extra-
pair paternity in northern cardinals. Condor 96:1055–1063.
Saino N, Møller AP, 1995. Testosterone-induced depression of male
parental behavior in the barn swallow: Female compensation and
effects on seasonal fitness. Behav Ecol Sociobiol 36:151–157.
St. Clair CC, Waas JR, St Clair RC, Boag PT, 1995. Unfit mothers?
Maternal infanticide in royal penguins. Anim Behav 50:1177–1185.
Sasvari L, 1986. Reproductive effort of widowed birds. J Anim Ecol
55:553–564.
Sheldon BC, Ellegren H, 1999. Sexual selection resulting from extra-
pair paternity in collared flycatchers. Anim Behav 57:285–298.
Sheldon BC, Merilä J, Qvarnström A, Gustafsson L, Ellegren H, 1997.
Paternal genetic contribution to offspring condition predicted by
size of male secondary sexual character. Proc R Soc Lond B 264:
297–302.
Sibley CG, Ahlquist JE, 1990. Phylogeny and classification of birds: a
Behavioral Ecology Vol. 11 No. 2
study in molecular evolution. New Haven, Connecticut: Yale Uni-
versity Press.
Smith JNM, Yom-Tov Y, Moses R, 1982. Polygyny, male parental care,
and sex ratio in song sparrows: an experimental study. Auk 99:555–
564.
Smith JI, 1991. A behavioral and molecular analysis of monogamy in
two song sparrow (Melospiza melodia) populations. In: Abstracts of
the American Ornithologists’ Union Annual Conference, Montreal,
Canada.
Soukup SS, Thompson CF, 1997. Social mating system affects the fre-
quency of extra-pair paternity in house wrens. Anim Behav 54:
1089–1105.
Stanback M, Boix C, Richardson D, Mendelsohn J, 1999. Sperm stor-
age and pair bondage: Reproductive conflict in hornbills. Proc 22
Int Ornithol Congr 2657–2665.
Stutchbury BJM, 1998. Extra-pair mating effort of male hooded war-
blers, Wilsonia citrina. Anim Behav 55:553–561.
Tuttle EM, 1993. Mate choice and stable polymorphism in the white-
throated sparrow (PhD thesis). Albany: State University of New York
at Albany.
Verhulst S, 1995. Reproductive decisions in great tits: an optimality
approach (PhD thesis). Groningen: University of Groningen.
Villarroel M, Bird DM, Kuhnlein U, 1998. Copulatory behaviour and
paternity in the American kestrel: the adaptive significance of fre-
quent copulations. Anim Behav 56:289–299.
Weatherhead PJ, 1979. Ecological correlates of monogamy in tundra-
breeding Savannah sparrows. Auk 96:391–401.
Weatherhead PJ, Boag PT, 1995. Pair and extra-pair mating success
relative to male quality in red-winged blackbirds. Behav Ecol Socio-
biol 37:81–91.
Westneat DF, 1987. Extra-pair fertilizations in a predominantly mo-
nogamous bird: genetic evidence. Anim Behav 35:865–876.
Whillans KV, Falls JB, 1990. Effects of male removal on parental care
of female white-throated sparrows, Zonotrichia albicollis. Anim Be-
hav 39:869–878.
Wittenberger JL, Tilson RL, 1980. The evolution of monogamy: hy-
potheses and evidence. Annu Rev Ecol Syst 11:197–232.
Wolf L, Ketterson ED, Nolan Jr V, 1988. Paternal influence on growth
and survival of dark-eyed junco young: do parental males benefit?
Anim Behav 36:1601–1618.
Wolf L, Ketterson ED, Nolan Jr V, 1990. Behavioural response of fe-
male dark-eyed juncos to the experimental removal of their mates:
implications for the evolution of male parental care. Anim Behav
39:125–134.
Wright J, 1998. Paternity and paternal care. In: Sperm competition
and sexual selection (Birkhead TR, Møller AP, eds). London: Aca-
demic Press; 117–145.
Wright J, Cuthill I, 1989. Manipulation of sex differences in parental
care. Behav Ecol Sociobiol 25:171–181.