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Molecular Ecology (2002)
11
, 2195– 2212
© 2002 Blackwell Science Ltd
Blackwell Science, Ltd
INVITED REVIEW
EXTRA PAIR PATERNITY IN BIRDS
Extra pair paternity in birds: a review of interspecific
variation and adaptive function
SIMON C. GRIFFITH,
*
IAN P. F. OWENS
†
and KATHERINE A. THUMAN
‡
*
Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK,
†
Department of Biological Sciences and NERC Centre for
Population Biology, Imperial College London, Silwood Park, Ascot, Berkshire, SL5 7PY, UK,
‡
Department of Animal Ecology, EBC,
Uppsala University, 752 36 Uppsala, Sweden
Abstract
The application of molecular genetic techniques has revolutionized our view of avian mating
systems. Contrary to prior expectations, birds are only very rarely sexually monogamous,
with ‘extra-pair offspring’ found in approximately 90% of species. Even among socially
monogamous species, over 11% of offspring are, on average, the result of extra-pair paternity
(EPP). Based on over 150 molecular genetic studies of EPP in birds, we review two topical
areas: (i) ecological explanations for interspecific variation in the rate of EPP; and (ii) evid-
ence bearing on the adaptive function of EPP. We highlight the remaining challenges of
understanding the relative roles of genes and ecology in determining variation between
taxa in the rate of extra paternity, and testing for differences between extra-pair offspring
and those sired within-pair.
Keywords
:
avian breeding systems, extra-pair paternity, monogamy, polygyny
Received 7 March 2002; revision received 24 July 2002; accepted 24 July 2002
Introduction
‘Well over nine-tenths [93%] of all passerine subfamilies
are normally monogamous.… Polyandry is unknown’
(Lack 1968: 35)
The extent to which molecular tools have revolutionized
our view of avian mating patterns is apparent when we
consider that the application of such tools has revealed that
true genetic monogamy occurs in only 14% of surveyed
passerine species, and that genetic polyandry occurs regularly
in the remaining 86% of species (Appendix I and Fig. 1).
This is a spectacular (and almost exact), reversal of Lack’s
(1968) summary quoted above. Indeed, it has been argued
that the discovery of extra-pair paternity (EPP) via molecular
tools is the most important empirical discovery in avian
mating systems over the last 30 years (Bennett & Owens 2002).
The rate of extra-pair paternity (EPP) is defined as the
proportion of fertilizations resulting from copulations out-
side the social bonds recognized by the tradition mating
system classification (Møller 1986; Westneat
et al
. 1990;
Davies 1991). Hence, in socially monogamous species
extra-pair young are those sired by males other than the
single putative father, whereas in species displaying co-
operative polyandry extra-pair young are those sired by
males from outside the social group (Owens & Hartley
1998). Contrary to Lack’s (1968) view, it is now commonly
accepted that genetic mating systems cannot be predicted
by simply observing the pattern of social bonds. For
instance, a substantial proportion of socially monogamous
species have turned out to be sexually promiscuous, with
the average frequency of extra-pair offspring among
socially monogamous bird species being 11.1% of offspring
and 18.7% of broods. Indeed, levels of extra-pair patern-
ity below 5% of offspring are now considered worthy of
explanation (Petrie & Kempenaers 1998; Griffith
et al
.
1999a; Griffith 2000; Robertson
et al
. 2001). True genetic
monogamy (0% EPP) has been found in less than 25%
of the socially monogamous bird species studied to date
(Fig. 1). This raises the question of why there should be
such pronounced interspecific variation in the rate of
EPP even among socially monogamous species.
In addition to its widespread distribution across species,
levels of EPP are often remarkably high within particular
Correspondence: Simon C. Griffith. Fax: 01865 271168; E-mail:
simon.griffith@zoo.ox.ac.uk
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S. C. GRIFFITH, I. P. F. OWENS and K. A. THUMAN
© 2002 Blackwell Science Ltd,
Molecular Ecology
, 11, 2195– 2212
species, with a quarter of socially monogamous passerines
having rates of EPP in excess of 25%. Among socially
monogamous species, the most promiscuous bird detected
to date is the reed bunting
Emberiza schoeniclus
, in which a
recent study found that 55% of all offspring were fathered
by extra-pair males and 86% of broods contained at least
one chick fathered outside the pair bond (Dixon
et al
. 1994).
Indeed, in the cooperatively breeding superb fairy-wren
Malurus cyaneus
, it has been shown that 72% of offspring
may be fathered by males other than the putative father,
and 95% of broods contained extra-pair offspring (Mulder
et al
. 1994; Double & Cockburn 2000). Such high rates pro-
voke questions about the adaptive function of EPP.
The overall aim of this review is to review a series of
advances in the study of EPP in birds. We do not aim to
review in detail the molecular methods used to investigate
EPP, the entire fields of alternative reproductive tactics and
sperm competition in birds because all of these have been
the subject of excellent reviews (e.g. Burke 1989; Westneat
et al
. 1990; Birkhead & Møller 1992, 1996; Queller
et al
. 1993;
Birkhead 1998; Møller 1998; Petrie & Kempenaers 1998;
Ligon 1999). Instead, we have chosen two topics that we
feel are of current interest and that we have highlighted in
the preceding paragraphs: interspecific variation in the
rate of EPP; and the adaptive function of EPP.
We believe that a review of these topics is both timely
and important. With more than 150 published estimates
of the rate of EPP in birds (Appendix I), there now exists
a substantial interspecific database that is ripe for com-
parative analysis. However, several problems remain
associated with making comparisons between species
with respect to the incidence of EPP. As a result, our
understanding of interspecifc variation in the rate of EPP
is still based largely on statistically inadequate tests.
Moreover, it has become increasingly evident that EPP is
important, not only because it may influence the strength
of sexual selection (Møller & Ninni 1998; Sheldon &
Ellegren 1999), but also because it plays a fundamental
role in the evolution of many other aspects of life-history
strategies (Gowaty 1996; Slagsvold & Lifjeld 1997; Mauck
et al
. 1999; Møller & Cuervo 2000; Møller 2000). An under-
standing of the adaptive basis of EPP remains therefore
an important challenge for molecular and evolutionary
ecologists.
Variation between species and between
populations
EPP in birds has been investigated in over 150 studies,
encompassing approximately 130 species. This massive
empirical effort thus provides a potentially powerful
interspecific database for those seeking to understand both
the origin and the subsequent evolution of alternative
reproductive strategies (Trivers 1972). However, in order
to maximize the value of this database it is important to be
aware of the methodological and analytical limitations
of individual estimates of the rate of EPP in a particular
population or species. In this section, first we review briefly
the methodological problems of comparing estimates
of EPP; second, we compile a standardized database of
interspecific variation; third, we examine the phylogenetic
distribution of EPP; then finally we review a series of
adaptive explanations for interspecific variation in EPP.
Empirical investigation of EPP
Early studies of EPP in birds used a wide variety of tools,
including plumage colour polymorphism (e.g. Birkhead
et al
. 1988), polymorphic enzymes (e.g. Gowaty & Karlin
1984) and sex-differences in estimates of the heritability
of morphological traits (Alatalo
et al
. 1984). Although
each of these methods can be used to estimate the
likelihood that EPPs are present or absent in a population,
none of them provide sufficiently accurate estimates to
allow meaningful cross-species comparisons. The reasons
for this shortfall vary across the different types of marker
listed above. Plumage polymorphism, for instance, is
striking in a few bird species but is insufficiently
widespread to constitute a general approach. Allozyme
Fig. 1 Frequency histogram of the rate of extra-pair paternity
(EPP) in terms of the percentage of offspring that are fathered
outside the pair bond. Data from Appendix I.
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© 2002 Blackwell Science Ltd,
Molecular Ecology
, 11, 2195– 2212
variation, on the other hand, is widespread across species
but is insufficiently variable across individuals to provide
high statistical confidence of being able ‘exclude’ a male as
being the genetic father of a chick. Finally, heritability
estimates are both difficult to obtain for many intrinsically
interesting populations, and sex differences in heritability
estimates are prone to both wide statistical confidence
limits and alternative explanations (such as sex-specific
environmental effects). Because of these various short-
comings, the modern study of EPP is based almost exclus-
ively on estimates of the rate of EPP using ‘DNA-methods’,
namely multilocus minisatellite fingerprints, single-locus
minisatellite fingerprints, and microsatellite genotyping.
In total, DNA-methods have been used to investigate the
paternity of over 25 000 avian offspring (Appendix I). It is
indicative of the small scale of most studies, however, that
two single studies combined have contributed over 12% of
that total (Reyer
et al
. 1997; Lubjuhn
et al
. 1999). Published
sample sizes range from 15 to 2013 offspring (Fleischer
et al
. 1997; Lubjuhn
et al
. 1999), with more than half of pub-
lished studies being based on less than 100 offspring and
almost three quarters of studies being based on less than 50
broods (Appendix I). Perhaps not surprisingly, therefore,
the majority of studies have not reported the confidence
intervals around their estimates. To illustrate the potential
importance of the issue of sample size and the heterogene-
ity in the quality of existing data, we have calculated the
99% confidence intervals for the published estimates of
EPP (Fig. 2). This calculation uses the percentage of extra-
pair offspring reported and the sample size and assumes
that extra-pair offspring are distributed approximately
evenly in any sample of offspring. It gives the range inside
which an estimate would be found 99% of the times that
the level was estimated from a population with the
reported level of EPP and sample size. In the worst cases,
confidence intervals span over 35%, which means that for
these species the actual level could occur anywhere
between 5% and 40% (e.g. Morton
et al
. 1990; Morton
et al
.
1998; Stutchbury
et al
. 1998). This level of uncertainty
makes comparisons between populations extremely diffi-
cult. Such a high level of uncertainty is even more worry-
ing when we consider that levels of EPP are not normally
distributed across species and over three quarters of pub-
lished estimates fall between zero and 20% (see Fig. 1).
For illustrative purposes we have also plotted the mag-
nitude of the confidence intervals (difference between the
high and low interval), for a population with an actual
level of 15% EPP (an average level) based on different sam-
ple sizes (line on Fig. 2). The shape of this curve suggests
that at around 200 offspring a reasonable compromise is
reached between the costs of further sampling and the
potential reduction in error to be gained. For sample sizes
of between 10 and 150 offspring it is clear that great
improvements in the accuracy of the estimate can be
achieved by relatively minor increases in sample size. We
suggest, therefore, that 200 offspring is a good sample size
to aim for in future estimates of EPP. To date, less than
25% of published studies have achieved this sample size
(Appendix I).
The relationship between sample size and reliability of
the EPP estimate has stark implications for those wishing
to make comparisons between species. If the confidence
limits around any particular EPP estimate are very large,
then it may be impossible to draw any conclusions at all
from comparisons between species which differ little in
their estimates rate of EPP. This is especially true when
comparisons are based on only a pair of populations or
species, which are described typically as having ‘high’ and
‘low’ rates of EPP, despite the fact that the confidence limits
of their estimates overlap by up to 30% (e.g. Morton
et al
.
1998). Even in large-scale comparative analyses, where it is
often assumed that sampling errors are likely to balance
themselves out, better resolution may be gained by weigh-
ing estimates by sample size to minimize the statistical
noise associated with small sample sizes (e.g. Møller &
Ninni 1998; Griffith 2000).
An unambiguous database
As we have already stressed, the available literature on
interspecific variation in the level of EPP in different
species is a potentially powerful resource for comparat-
ive work. Published empirical studies of the rate of EPP
are, however, extremely heterogeneous with respect to
sampling strategy, the statistical methodology by which
EPP is estimated, the type of population under study and
the presence or absence of experimental treatments
0
10
20
30
40
50
60
0 200 400 600 800 1000
Sample size
% Error around estimate
Fig. 2 The magnitude of error around actual estimates of EPP
levels against the sample size of those studies. ‘% error’ on the
uertical axis refers to the magnitude of the difference between the
upper and lower 95% confidence intervals around an estimate.
The line plotted is this ‘% error’ for a hypothetical population with
a rate of 15% EPP across different sample sizes.
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S. C. GRIFFITH, I. P. F. OWENS and K. A. THUMAN
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Molecular Ecology
, 11, 2195– 2212
designed to influence the rate of EPP. To date, most
comparative studies have made little distinction between
these different sorts of empirical study and have tended to
lump all available data irrespective of source.
This lumping of data across sources has led to prob-
lems in interpreting comparative analyses. For example,
although a series of comparative study have cited (Wetton
& Parkin 1991) as the single source for the level of EPP in
the house sparrow,
Passer domesticus
, the level of EPP for
this species has variously been cited as 12.1% (Møller &
Birkhead 1993, 1994), 12.85% (Møller 1997), 13.6% (Møller
& Briskie 1995; Wink & Dyrcz 1999; Møller 2001), and
14.0% (Owens & Hartley 1998). Although the differences
between these estimates may appear trivial, these values
have all been derived from the same well-established
source indicating the difficulties involved in extracting a
single representative figure for a species.
Another general problem that hinders the interpretation
of comparative studies is the widespread use of unpub-
lished EPP estimates. Although it is difficult to evaluate
properly the total number of unpublished studies that have
contributed to recent comparative studies, they are often
responsible for substantial proportions of the data in sev-
eral analyses. For instance, in a series of recent large-scale
comparative studies the percentage of data points based
on unpublished sources has varied all the way from 0%
(Arnold & Owens 2002), through 13% (Owens & Hartley
1998; Hasselquist & Sherman 2001), 16% (Wink & Dyrcz
1999) and 21% (Møller 2001), up to a maxiumum of 55%
(Møller & Birkhead 1994; Møller & Briskie 1995). For many
of these unpublished sources of data it is impossible to dis-
cover the methodology, sample sizes or characteristics of
the population on which these estimates are based, and
estimates are vulnerable to being included or excluded
without full justification.
Given these general problems, we have attempted to col-
late a standardized database of EPP estimates (see Appen-
dix I). As far as we are aware, the set of data we have
compiled contains the entire set of studies reporting a spe-
cies level of EPP in the primary, peer-reviewed literature
before 1 January 2002, with the exception of those estimates
which have been excluded for one of the reasons below. It
is compiled by species, and where more than one popula-
tion of a species has been analysed, a mean (weighted by
sample size) has been calculated. It is important to note that
studies (or species estimates) that have been excluded are
not necessarily excluded because they are inherently poor
studies, but merely because we feel the results they rep-
resent are not particularly relevant to natural variation in
levels of EPP (see below and Appendix II). The database
shown in Appendix I was obtained from a complete search
of the following journals published prior to January 2002:
American Naturalist
,
Animal Behaviour
,
Auk
,
Behaviour
,
Behavioural Ecology
,
Behavioural Ecology and Sociobiology
,
Condor
,
Ethology
,
Evolution
,
Hereditas
,
Ibis
,
Journal of Avian
Biology
,
Journal of Heredity
,
Journal für Ornithologie
,
Molecu-
lar Ecology
,
Nature
,
Oikos
,
Proceedings of the Royal Society of
London Series B
and
Science.
Furthermore, we attempted to
find all literature, or sources given for EPP estimates in the
appendices of the following comparative analyses: Møller
& Birkhead (1993), Møller & Birkhead (1994), Møller & Briskie
(1995), Møller (1997), Westneat & Sherman (1997), Møller &
Ninni (1998), Owens & Hartley (1998), Wink & Dyrcz (1999),
Hasselquist & Sherman (2001) and Møller (2001).
It should be noted that some of the species estimates
in this database will be different from others found in the
literature and with which people may be familiar. The
values we present have been compiled directly from
primary sources and the most probable source of difference
will be due to the composition of species means (from
multiple studies) and the exclusion of whole studies and
parts of studies for the reasons given below.
Exclusion criteria for the database.
There are a number of
species estimates of EPP cited frequently in the literature
which we have excluded from the database shown in
Appendix I. Details of these excluded studies are given in
full in Appendix II. We will now review the reasons why
these studies were excluded from the database.
Unpublished studies.
We included only studies that were
published in primary, peer-reviewed journals and which
contained sufficient methodological details to establish how
paternity was excluded for putative fathers. We used these
criteria because we found that it was often extremely difficult
to evaluate the methodology and/or obtain unambiguous
estimates of EPP from studies published in other sources
other than the primary literature. As a result, estimates from
conference proceedings, theses, personal communications
and books and journals that have not been peer-reviewed
are all excluded. Equally, preliminary estimates given in
the primary literature but unsupported by sufficient
methods and/or analysis to establish how paternity of
putative fathers was excluded were also excluded.
Methodology.
For the reasons referred to above, we in-
cluded only studies based on DNA methodology (multilocus
minisatellites, single-locus minisatellites, microsatellite
genotyping). As a result, all estimates based on allozymes,
heritability estimates and polymorphic plumage markers
were excluded. We also excluded studies conducted on
offspring without samples from the putative fathers.
Captive populations.
We included only studies of free-living
populations. Studies of captive birds may be useful for invest-
igations of the mechanisms of sperm competition but are
unlikely to represent naturally occurring levels of EPP. Captive
populations included aviaries, zoos and wildlife parks.
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, 11, 2195– 2212
Manipulated individuals.
Some studies have manipulated
individuals experimentally with the aim, or the result, of
influencing the rate of EPP. Where such manipulations
were performed on all individuals for which EPP estimates
were available, we excluded the entire study. Where the
manipulations were restricted to a few individuals, we
excluded those manipulated individuals from the estim-
ates of the species specific rate of EPP.
Unrepresentative subsamples.
In some cases a study has been
carried out on a subsample of a population for which
there is a strong a priori expectation that such a subsample
may not show a level of EPP representative of the popula-
tion as a whole. For instance, in some species showing a
variable social mating system (i.e. some males are paired
monogamously whereas other males are paired poly-
gamously) a number of studies have reported the rate of
EPP in the broods of monogamously paired males only.
Such studies were excluded unless we were able to find a
published estimate of the rate of EPP among the rest of
the same study population.
For the studies that remained after these criteria were
applied we collated data on the rates of EPP both in terms
of the percentage of offspring that were fathered by a male
other than the pair male, and the percentage of broods con-
taining offspring not sired by the pair male. In cases where
there was more than one social male (such as those species
showing social polyandry or polygynandry), we classified
an EPP offspring as being one fathered by a male outside
the social group, and an EPP brood as being one that con-
tained at least one offspring fathered by a male outside the
social group (Westneat
et al
. 1990; Owens & Hartley 1998).
This is a different definition from that used in some other
studies, which counted any offspring not fathered by the
‘dominant’ or ‘alpha’ male in a group as being an EPP off-
spring even if that offspring was fathered by a male within
the social group. We avoided this latter definition because,
in our opinion, EPP offspring should be those that occur
outside the bonds described by the social mating system
(see Introduction).
Phylogenetic distribution of EPP
Many hypotheses have been put forward to explain inter-
specific variation in the level of EPP, but until recently there
has been relatively little success in identifying robust bio-
logical correlates of this interspecific variation (Birkhead
& Møller 1996; Ligon 1999; Bennett & Owens 2002). One
explanation for this paradox is that most attempts to
identify biological correlates of interspecific variation
in the rate of EPP have been based on the assumption
that the level of EPP shown by a species is determined
by contemporary ecological factors, such as breeding
density and/or breeding synchrony. However, phylogenetic
analysis of the EPP data has shown that estimates of
extra-pair paternity are not distributed randomly with
respect to phylogeny. In fact, over 50% of the interspecific
variation in the level of EPP occurs between families
or between orders, rather than among closely related
species (nested analysis of variance testing the effects of
‘taxonomic family’ nested within ‘taxonomic order’ using
data in Appendix I:
r
2
= 0.59,
F
35,69
= 2.82,
P
< 0.0001). This
suggests that many differences between species in terms
of EPP rate are likely to have been determined in the
ancient evolutionary history of avian lineages, and that
explanations based on contemporary ecology alone will
prove insufficient (Arnold & Owens 2002; Bennett &
Owens 2002). In the following section we will discuss the
potential implications of this finding when attempting
to identify robust ecological correlates.
Adaptive explanation for interspecific variation in EPP
EPP and breeding density.
Variation in breeding density is
one of the traditional ecological explanations for interspecific
variation in the rate of EPP. The relationship between
breeding density and EPP has been examined in four ways:
interspecific analysis across taxa; intraspecific comparisons
between populations; intraspecific comparisons between
different individuals within a single population; and meta-
analysis of species-specific studies. We will review briefly
each of these forms of evidence and demonstrate that, in
general, there is little evidence of a general interspecific
relationship between breeding density and the incidence of
EPP in birds. Instead, the importance of breeding density
appears limited to explaining differences between individuals
in the same population, and possibly variation between
different populations of the same species.
The hypothesis that interspecific variation in the rate of
EPP is linked to breeding density appears to have arisen
as an extrapolation from the observation that extra-pair
copulations are more common among colonially nesting
species than among species with more dispersed nests (e.g.
Møller & Birkhead 1993). Such an extrapolation assumes,
however, that the rate of EPP is closely correlated with the
rate of extra-pair copulation, that colonially nesting species
are typical of high nesting density species, and that raw
species data can be used as independent data points.
Subsequently, when these assumptions have been tested
using molecular data on the rate of EPP
per se
and a more soph-
isticated interspecific comparative analyses, no robust
evidence has been found for a relationship interspecific
variation in the rate of EPP and breeding density (Westneat
& Sherman 1997; Wink & Dyrcz 1999). There is therefore
no strong evidence for the role of breeding density in deter-
mining interspecific variation in the rate of EPP.
Similarly, intraspecific studies of variation between
populations have provided little evidence for a consistent
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Molecular Ecology
, 11, 2195– 2212
relationship between breeding density and the rate of EPP,
with positive relationships in three species [
Agelaius phoen-
iceus
(Gibbs
et al.
1990),
Ficedula hypoleuca
(Lifjeld
et al.
1991;
Gelter & Tegelström 1992),
Dendroica petechia
(Yezerinac
et al.
1999)] no detectable relationship in three species
[
Phylloscopus trochilus
(Gyllensten
et al.
1990; Bjørnstad &
Lifjeld 1997; Fridolfsson
et al.
1997),
Petroica australis
(Ardern
et al.
1997),
Passer domesticus
(Griffith
et al.
1999a)] and a
negative relationship in another species [
Acrocephalus
arundinaceus
(Hasselquist
et al.
1995; Leisler
et al.
2000)].
The lack of a consistent relationship between breeding
density and EPP in these intraspecific analyses does not
necessarily reflect the total absence of an underlying bio-
logical relationship, but more probably the poor design of
the tests. There are four common factors that undermine
the strength of published studies of population differences
in density and EPP: (i) the published studies have all been
observational rather than experimental; (ii) the published
studies have low statistical power due to the small number
of populations involved (usually between two and four);
(iii) there is usually very little variation between popula-
tions in both density and EPP; and (iv) the tests fail to
acknowledge the large standard error around the estimates
of EPP for any one population. So far, no published study
of between-population variation in EPP and breeding den-
sity has controlled for all these problems.
An alternative intraspecific approach is to make compar-
isons between individuals in the same population, such as
comparing the rate of EPP in pockets of the population
breeding at high density with the rate in pockets breeding
at low density. Using this approach, some workers have
found a positive relationship between breeding density
and EPP (e.g. Hill
et al.
1994; Hoi & Hoi-Leitner 1997;
Langefors
et al.
1998; Richardson & Burke 1999), while
others were unable to find a relationship between these
variables (e.g. Barber
et al.
1996; Sundberg & Dixon 1996;
Verboven & Mateman 1997; Tarof
et al.
1998; Chuang
et al.
1999; Moore
et al.
1999). Also, as part of their overall
comparative study of the link between breeding density
and the rate of EPP, Westneat & Sherman (1997) tested for
an overall relationship between populations of the same
species. While warning of a small sample size, they did
report that there was a general trend for high density
populations to have a higher rate of EPP than con-specific
populations at lower density. This is arguably the strongest
comparative evidence of a link between density and EPP,
albeit at the level of differences among populations rather
than differences among species. Of course, the weakness
of any such comparative approaches is that the density
at which individuals breed within a population will be
dependent on other factors which may also covary with
EPP. For example, low quality males may be forced to
breed at higher density than more aggressive high quality
males who defend a larger area around their nest. These
studies are unable therefore to provide diagnostic evidence
for a causal relationship between density and EPP, a fam-
iliar problem highlighting the need for experimental work.
To date only one study has investigated experimentally
a possible relationship between density and EPP and unfor-
tunately in this study paternity was determined using allozy-
mes. In their study, conducted on nest box-breeding eastern
bluebirds
Sialia sialis
, Gowaty & Bridges (1991) used nest
box-placement to manipulate the densities of breeding pairs.
This revealed a clear positive relationship between breeding
density and EPP and remains the best experimental evid-
ence of a link between density and EPP, albeit at the level
of variation within a single population. Even in this case,
however, it should be remembered that this experimental
study consisted of a single comparison between a ‘high’ den-
sity population and ‘low’ density population and this test is
equivalent to a sample size of one. More such studies are
required to establish whether this is a general phenomenon.
A final approach to testing for the role of breeding
density in determining the rate of extra-pair paternity is
to perform a meta-analysis across single-species studies.
Meta-analyses do not test for biological correlates of inter-
specific variation, but test whether there is evidence of a
consistent relationship between two (or more) variables
across a series of within-species studies (Rosenthal 1991).
This meta-analysis approach was recently employed by
Møller & Ninni (1998) to investigate a large range of factors
that have been suggested to be associated with intraspeci-
fic variation in the rate of EPP. As part of this study Møller
and Ninni found that, across studies, there was indeed con-
sistent evidence of a relationship between breeding density
and the rate of extra-pair paternity. This was true even
when Møller and Ninni used a multivariate approach to
control for the effect of variation in other factors, such as
the extent of sexual dimorphism. This suggests strongly
that breeding density is an important factor in determin-
ing variation in the rate of EPP between individuals or
between families in the same study population.
In summary, there is little evidence that interspecific
variation in the rate of EPP is due to variation in breeding
density. If there is a relationship across species between
breeding density and EPP then it is neither consistent
nor strong, and variation in breeding density explains very
little of the overall variation in EPP (see Westneat &
Sherman 1997). This agrees with the prediction from
phylogenetic analysis that much of the interspecific vari-
ation in the rate of EPP lies among ancient avian evolution-
ary lineages, which do not usually differ significantly from
one another in terms of overall breeding density (Owens
& Bennett 1997). There is good evidence, however, that
breeding density may be important in determining vari-
ation in the rate of EPP at lower taxonomic levels. The most
statistically robust evidence for this comes from Møller &
Ninni (1998) meta-analysis, which shows that breeding
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density is associated consistently with variation in the rate
of EPP among individuals in the same species. Westneat
& Sherman’s (1997) comparative studies also suggest that
breeding density may play a role in determining variation
in the rate of EPP between populations of the same species,
although further experimental work along the lines of
that pioneered by Gowaty & Bridges (1991) is required to
establish whether this relationship is causal.
EPP and breeding synchrony.
Variation in breeding synch-
rony is the other traditional ecological explanation for
interspecific variation in the rate of EPP. Here, breeding syn-
chrony refers to the proportion of females that are fertile
at any one moment in time, so that high synchrony refers
to a situation where many females are reproductively
active at the same time. The potential importance of
breeding synchrony as a determinate of interspecific
variation in the level of EPP was first championed by
Stutchbury & Morton (1995), who showed a positive
correlation between these two variables in a comparison
of 21 genera of passerines (later increased to 34 species;
Stutchbury 1998a) (see also Birkhead & Biggins 1987). Based
on this evidence Stutchbury and Morton suggested that in
a synchronously breeding population, females are better
able to compare between different males, facilitating their
choice of extra-pair partners. Unfortunately, however,
Stutchbury & Morton (1995) original analyses made no
attempt to control for two factors that may potentially
jeopardize the validity of the correlation: the phylogenetic
relationships between species in the analysis; and the
measurement error around the estimates of EPP. A sub-
sequent comparative analyses that controlled for phylo-
geny and explored potentially confounding factors found
no evidence of a relationship between EPP and breeding
synchrony (Westneat & Sherman 1997), albeit with a much
reduced sample size for breeding synchrony.
The difference in results between Stutchbury & Morton
(1995) original analyses and Westneat & Sherman’s (1997)
subsequent analyses led to an exchange of published
letters between Stutchbury (1998a,b) and Weatherhead &
Yezerinac (1998). In these articles Stutchbury provides
additional data of breeding synchrony and the rate of
extra-pair paternity (Stutchbury 1998a), performs a com-
parative analyses based on using species as independent
data points (Stutchbury 1998a), and then carries out two
types of analyses to control for phylogenetic noninde-
pendence: first a sister-taxa test on nine pairs of species
(Stutchbury 1998a) then a test based on 33 phylogenetic
independent contrasts (Stutchbury 1998b). All of these new
tests show a significant correlation between breeding
density and the rate of EPP, leading Stutchbury (1998a) to
claim that ‘the breeding synchrony hypothesis remains
the most viable explanation of the great variation in EPP
frequency among bird species world-wide’. Although we
regard this as being rather a strong claim considering the
relatively small size of the database available at that time
and the correlational nature of all comparative studies, we
would agree with Stutchbury (1998b) that the breeding
synchrony hypothesis has held up better in comparative
tests than has the breeding density hypothesis.
Despite Stutchbury’s (1998a,b) new phylogeny-based
comparative analyses, Weatherhead & Yezerinac (1998)
still had a major objection to the breeding synchrony
hypothesis: namely that the correlational evidence of com-
parative studies is not supported by the available empirical
tests. Weatherhead & Yezerinac (1998) argued that, if the
level of synchrony generally does drive variation in levels
of EPP between species, there should also be a relationship
between populations within a species or between ter-
ritories within a population. There is no such relationship
in the Eastern blue bird
Sialia sialis
(Meek
et al.
1994); tree
swallow
Tachycineta bicolor
(Dunn
et al.
1994); yellow warbler
Dendroica petechia
(Yezerinac & Weatherhead 1997); red-
winged blackbird
Agelaius caerulescens
(Weatherhead 1997);
blue tit
Parus caeruleus
(Kempenaers
et al.
1997); American
redstart
Setophaga ruticilla
(Perreault
et al.
1998); house
sparrow
Passer domesticus
(Griffith
et al.
1999a); sedge
warbler
Acrocephalus schoenobaenus
(Langefors
et al.
1998);
mangrove swallow
Tachycineta albilinea
(Moore
et al.
1999);
or serin
Serinus serinus
(Hoi-Leitner
et al.
1999). Indeed,
only two intraspecific studies have provided significant
support for such a relationship, both within a single popu-
lation. The most synchronous breeding families exhibited
higher levels of EPP in both the clay-coloured robin
Turdus
grayi
(Stutchbury
et al.
1998), and the hooded warbler
Wilsonia citrina
(Stutchbury
et al.
1997). This is, however,
relatively weak evidence for a causal relationship between
synchrony and rate of EPP due to the potential influence of
uncontrolled confounding variables and the small number
of independent comparisons. Also, negative relationships
between synchrony and EPP have been demonstrated in
the Eastern Phoebe
Sayornis phoebe
(Conrad
et al.
1998),
great tit
Parus major
(Strohbach
et al.
1998), and barn swal-
low (Saino
et al.
1999). The observational evidence on the
empirical link between breeding synchrony and EPP is at
best mixed, therefore.
To our knowledge only one published study has invest-
igated experimentally (albeit inadvertently) the relation-
ship between synchrony and EPP (Verboven & Mateman
1997). In a population of the great tit, the whole, or part, of
the first clutch was removed provoking a second, more
asynchronous breeding attempt. No difference was detect-
able in the levels of EPP in synchronous first broods and
asynchronous second broods although levels of EPP were
low throughout this whole population and the power of
this test is very weak (Verboven & Mateman 1997). The
only experimental evidence available does not, therefore,
support the breeding synchrony hypothesis.
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Overall, we suggest that, despite considerable empirical
effort and much heated debate, it remains difficult to assess
the role of variation in breeding synchrony in determin-
ing interspecific variation in EPP. Although Stutchbury
(1998a,b) comparative analyses appear to provide phylo-
genetically robust correlational evidence for a link between
these variables, it remains unclear whether this link is
causal. We say this for three reasons. First, the key sup-
portive comparative tests (Stutchbury 1998a,b) were per-
formed on relatively small databases and the relative
contribution of potentially confounding factors were not
examined in detail. Second, we know that over 50% of the
interspecific variation in EPP occurs among ancient avian
lineages, rather than among closely related species, mak-
ing it unlikely that a single ecological factor is going to
explain all the variation among species. Finally, the empir-
ical evidence for a causal link between breeding synchrony
is not straightforward. Although many empirical studies
have reported no association between the extent of breed-
ing synchrony and the rate of EPP, Møller and Ninni’s (1998)
recent meta-analysis did identify breeding synchrony as a
consistently important correlate. Given the lack of experi-
mental studies of the influence of breeding synchrony, this
contradiction is difficult to interpret biologically. We con-
clude that the breeding density hypothesis has not been
falsified and could plausibly play a role in determining
interspecific variation in EPP. To go further than this we
need further comparative tests on the
relative
role of breed-
ing density vs. other factors and experimental tests of
whether there is indeed a causal link between breeding
density and EPP. Without these forms of evidence we feel
it is too early to say that the breeding synchrony hypothesis
is either important or trivial.
EPP and genetic diversity.
The difficulties in finding sup-
port for the traditional ecological hypotheses based on
breeding density and breeding synchrony has led some
authors to suggest that the key factor in determining
interspecific variation in EPP may be genetic rather than
demographic. Although genetic benefits have often been
invoked to explain the reproductive behaviour of indi-
vidual males and females (see Andersson 1994), Petrie &
Lipsitch (1994) appear to have been the first to predict
explicitly that interspecific variation in the rate of polygyny
should be determined by the level of additive genetic
variation. Using a game theory approach, Petrie & Lipsitch
(1994) showed that, assuming that females suffered a cost
from seeking to mate with more than one male, females
should be more likely to mate with additional mates if
there was extensive additive genetic diversity among those
mates with respect to fitness. In terms of avian EPP, this
theory has been taken to predict that EPP should be most
common in those species with high genetic diversity
(Petrie & Kempenaers 1998). This ‘genetic diversity
hypothesis’ has been investigated both at the level of
variation between different species and at the level of
differences between populations of the same species.
As far as we are aware, the only published evidence of an
interspecific correlation between genetic diversity and rate
of EPP comes from two comparative studies combined
by Petrie
et al.
(1998). In the first of these Petrie
et al.
(1998)
collated data on the proportion of allozyme loci that were
polymorphic across 35 species of bird and then used a
phylogeny-based comparative approach to show that the
level of EPP was positively correlated with the allozyme
polymorphism. In a bivariate regression model based on
evolutionarily independent contrasts, the proportion of
polymorphic loci explained 22% of the variance in changes
in the rate of EPP, but a multivariate model incorporating
three other variables (level of sexual dichromatism, body
size and sample size) explained 85% of the variation in
EPP. In the second test the same authors identified seven
phylogenetically matched-pairs of species or populations
that differed significantly in terms of their rates of EPP,
then obtained genetic samples for all of these populations
and measured the proportion of polymorphism and gene
diversity (approximated to average heterozygosity) at a
series of random priming sites [random amplified poly-
morphic DNA (RAPD)]. In general the results supported
the genetic diversity hypothesis, although the results were
statistically significant only at the 10% level (in six of seven
of the matched-pairs the taxon with the higher rate of EPP
also had a higher rate of RAPD polymorphism (
P
= 0.06),
while in five of the seven pairs the taxon with the higher
EPP had a higher showed gene diversity (
P
= 0.08)). Never-
theless, when Petrie
et al.
(1998) used a combined prob-
ability test to maximize statistical power across both the
allozyme and RAPD based tests, they found an overall
effect of polymorphism significant at the 0.001% level.
Although it must be kept in mind that these comparative
tests are based on indices far removed from ‘additive
genetic variation in male fitness’, it is none the less remark-
able that such crude measures of genetic diversity can
explain such a high proportion of variation in EPP among
closely related taxa.
In addition to the matched-pairs test of Petrie
et al.
(1998), which includes a mixture of comparisons between
species (five comparisons) and within species (two com-
parisons), the role of genetic diversity in determining
variation in EPP among populations of the same species
has been addressed by comparing mainland and island
populations. Both Griffith
et al.
(1999a); Griffith (2000) and
Møller (2000) have suggested that the rate of EPP is often
unexpectedly low in island-dwelling populations. Thus,
if it is assumed that island populations are genetically
depauperate compared to their mainland counterparts,
this observation is consistent with the genetic diversity
hypothesis. Of course, for most of the species used in these
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island–mainland comparisons there is no quantitative evid-
ence that the insular population are indeed genetically
depauperate, but such an effect has been widely reported
in birds as well as other organisms (Frankham 1997).
Our main conclusion from these comparative studies is
that the genetic diversity hypothesis deserves more study.
Although the interspecific studies are difficult to inter-
pret because they are correlational and based on indirect
indices of additive genetic variation in male fitness, they
do show much stronger correlations than have ever been
demonstrated for either breeding density and breeding
synchrony. Ideally, the next stage of research would be to
experimentally manipulate the extent of genetic diversity
and then monitor both the short- and long-term effects on
the level of EPP. We predict that the greatest potential
of the genetic diversity hypothesis will be in explaining
differences in the level of EPP among very closely related
species and among populations of the same species.
EPP and the need for paternal care.
Another response to the
limited explanatory success of the two traditional ecological
explanations for interspecific variation in EPP (breeding
density and breeding synchrony) is the hypothesis that
high rates of EPP should be associated with little need for
paternal care. The idea that interspecific variation in the
rate of EPP may be determined, in part at least, by the need
for male care appears to have originated on at least three
independent occasions: by Mulder
et al.
(1994), Birkhead &
Møller (1996) and Gowaty (1996). The core prediction of
these hypotheses is that females should be more likely to
seek extra-pair copulations when they can rear offspring
with little help from their male partner, and can therefore
risk the cost of reduced parental care.
The general explanatory power of the hypothesis that
rates of EPP are determined by the need for paternal care
was first explored by Birkhead & Møller (1996), who used
a species-based comparative approach to show that, as pre-
dicted, EPP rates tended to be comparatively low in species
where male care was ‘essential’. Birkhead & Møller (1996)
stressed, however, that their analysis was only prelimin-
ary and cautioned that further studies were required to
improve scoring methods, and test for the effect of phylo-
genetic nonindependence (see Harvey & Pagel 1991).
Accordingly, both Møller (2000) and Arnold & Owens
(2002) performed a phylogeny-based comparative analysis
to test whether high rates of EPP really are associated with
little requirement for paternal care. As predicted, both
studies found that interspecific variation in the rate of EPP
was significantly negatively associated with variation in
the direct effect of paternal care in terms of reproductive
success (Fig. 3). Subsequently, the rate of EPP has also been
shown to be significantly negatively associated to other
indices of the role of paternal care, such as sex differences
in the provision of various types of care and the total dura-
tion of different components of care (see Møller & Cuervo
2000; Bennett & Owens 2002). Importantly, all these associ-
ations remain qualitatively unchanged, whether the ana-
lyses are based on raw species values or evolutionarily
independent contrasts (see Møller 2000; Arnold & Owens
2002; Bennett & Owens 2002), and in most cases they
remain significant when multivariate tests are used to
examine the importance of paternal care when controlling
for other variables (Arnold & Owens 2002; Bennett &
Owens 2002). Hence, interspecific variation in the extent of
female constraint appears to vary across the same phylo-
genetic levels as does interspecific variation in the level of
EPP (see Owens & Bennett 1997; Arnold & Owens 2002).
There is therefore strong correlative evidence from several
research groups for a link between interspecific variation
in the need for paternal care and interspecific variation in
the rate of EPP.
As far as we are aware, only a single empirical study has
investigated experimentally the link between the need for
paternal care and the incidence of EPP. In their study of
EPP in the serin, Hoi-Leitner
et al.
(1999) manipulated the
abundance of food around the nest during the fertile phase
of the female. As predicted by the paternal care hypothesis,
females breeding in areas of high food abundance (mani-
pulated and unmanipulated) were found to have a higher
Fig. 3 Association between interspecific variation in the rate of
extra-pair paternity (EPP) and interspecific variation in male
contribution to parental care. Extra-pair paternity is measured in
terms of the total percentage of young that were fathered by males
other than the social mates of the females (see Møller 2000 for
details). Male contribution to care is measured as the reduction in
reproductive success that females suffer when they care for a
b
rood alone, as a percentage of the full reproductive success that
females accrue when they care for a brood with the assistance of a
male (see Møller 2000 for details). Statistics and solid line refer to
log-linear regression using species as independent data points.
Redrawn from raw data in the Appendix of Møller (2000).
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incidence of extra-pair offspring in their broods (Hoi-
Lietner et al. 1999). Thus, although this is only a single
study, there is experimental support for a causal link between
differences in parental care can lead to differences in the
rate of EPP.
We conclude that there is relatively good evidence for a
link between the need for paternal care and the rate of EPP.
The correlational evidence is particularly strong, being
based on phylogenetically robust tests on large data sets
and controlling for several other factors, and is consistent
with the observation that much of the interspecific vari-
ation in both EPP and the form of parental care occurs at
high taxonomic levels. From this comparative evidence we
suggest that ancient changes in the form of parental care
may have influenced the large differences in EPP between
major lineages of birds. It is more difficult to know the role
that variation in parental care may play in explaining vari-
ation among more closely related species, or among popu-
lations of the same species, or even among individuals
within the same population. More experimental studies of
the type used by Hoi-Leitner et al. (1999) are required to test
for a general causal link at these levels.
EPP and the rate of adult mortality. Another variable that has
been suggested recently to explain interspecific variation
in the rate of EPP is the rate of adult mortality. Again, the
idea of a link between rates of mortality and EPP appears
to have arisen independently at least twice: by Mauck et al.
(1999) and Wink & Dyrcz (1999).
Based on a series of state-dynamic models, Mauck et al.
(1999) predicted that ‘because males of species with short
reproductive lifespans should tolerate higher EP[P] rates
than should males of species with long reproductive lives,
there should be greater range of EP[P] rates observed for
species with short than long reproductive life spans’ (Mauck
et al. 1999: 107). According to their model, for species with
short reproductive lifespans abandonment of a reproduct-
ive event is never adaptive even in the face of extreme
uncertainty of paternity because by that stage an altern-
ative reproductive event is unlikely (Mauck et al. 1999). In
consequence, high rates of EPP will only be evolutionarily
stable in species with short reproductive lifespans. As they
observed: ‘EP[P] rates observed in passerine birds range
from 0% … to > 70% … , whereas in long-lived birds such as
procellariiformes, EP[P] rates range from 0% to only 14%’
(Mauck et al. 1999: 107).
This prediction of an association between EPP and adult
mortality history was tested using a species-based com-
parative method by Wink & Dyrcz (1999) and Arnold &
Owens (2002), both of whom were able to confirm that vari-
ation in the rate of adult mortality explained nearly 50% of
the variation in the rate of EPP (see Fig. 4). Indeed, it is very
striking even from a visual inspection of the data in Fig. 4
that Mauck et al.′s (1999) verbal prediction is accurate. In
species with annual mortality rates of less than 30% the rate
of EPP very rarely rises above 20%, whereas in species
with a higher rate of mortality the rate ranges from 0% to
95% (albeit in over two-thirds of these high mortality
species the rate of EPP is above the 20% level). Also, the use of
phylogeny-based comparative methods has shown that
the association between EPP and adult mortality is intact
even when analyses are based on evolutionarily independ-
ent contrasts (Arnold & Owens 2002; Bennett & Owens
2002). When evolutionarily independent contrasts are used
to control for the effects of phylogeny, changes in the rate
of adult mortality still account for approximately 25% of
variation in changes in the rate of EPP (Arnold & Owens
2002), which agrees with the observation that both EPP
rates and life history traits show extensive variation at the
same ancient phylogenetic levels (Bennett & Owens 2002).
In the case of the mortality hypothesis, to our knowledge
there have been no attempts to test experimentally for a
causal relationship between the rate of mortality and the
rate of EPP. Indeed, because the logic of this argument is
based on changes over an evolutionary timespan, rather
than facultative changes within an individual, such tests
would not be straightforward. Other than by using long-
term selection experiments, it may not be possible to per-
form elegant manipulations of life histories that last over
tens of generations. We therefore conclude that, as with the
parental care hypothesis, there is strong correlative
evidence in support of of a link between adult mortality
Fig. 4 Association between interspecific variation in the rate of
extra-pair paternity (EPP) and interspecific variation in the rate of
adult mortality. Extra-pair paternity is measured in terms of the
total percentage of young that were fathered by males other than
the social mates of the females (see Wink & Dyrcz 1999 for details).
Annual rate of adult mortality is based on studies of uniquely
marked individuals (see Wink & Dyrcz 1999 for details). Statistics
and solid line refer to log-linear regression using populations as
independent data points. Redrawn from raw data in the Appendix
of Wink & Dyrcz (1999).
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and EPP but a lack of experimental evidence for the causal
nature of this relationship. Again, given that both adult
mortality and the rate of EPP vary most extensively among
ancient avian lineages, it seems most probable that changes
in adult mortality played a role in the ancient diversifica-
tion of sexual mating systems but that other factors may be
more important in determining contemporary variation
among populations and among individuals.
Hierarchical explanation for variation in EPP
We suggest that the major conclusion of our preceding
review of the various explanations for variation in the rate
of EPP is that there is no single explanation for this
phenomenon. For none of these hypotheses do we feel that
there is overwhelming evidence that the proposed factor
explains the majority of variation across all levels of
organization: that is, among major avian lineages, among
closely related species, among populations of the same
species and among individuals within a single population.
Instead, each factor appears to work best at one or two of
these levels. With respect to variation among major avian
lineages, for example, the recent comparative studies of
Wink & Dyrcz (1999), Møller (2000) and Arnold & Owens
(2002) suggest that such ancient patterns may be explained
most effectively by differences in fundamental life history
parameters, such as adult mortality rate and the form of
parental care. On the other hand, a combination of com-
parative, empirical and meta-analyses suggest that at the level
of differences among closely related species and between
populations of the same species, variation in EPP is more
likely to be influenced by contemporary ecological factors
such as breeding density (Gowaty & Bridges 1991; Westneat
& Sherman 1997; Møller & Ninni 1998), breeding synchrony
(Stutchbury 1998a,b; Møller & Ninni 1998) and the extent
of genetic variation (Petrie & Kempenaers 1998; Petrie et al.
1998; Griffith et al. 1999a; Griffith 2000; Møller 2000).
Taken together, we feel that these complex results sug-
gest a hierarchical explanation for variation in EPP, with
variation at different organizational levels determined
by different ecological, genetic and social correlates (see
Arnold & Owens 2002; Bennett & Owens 2002). Vari-
ation in the rate of EPP among major avian lineages
appears to be due to variation in the probable costs of extra-
pair behaviour in terms of the risks of retaliation, as deter-
mined by gross differences in the form of parental care (see
Mulder et al. 1994; Birkhead & Møller 1996; Gowaty 1996;
Møller & Cuervo 2000; Møller 2000) and reproductive
lifespan (see Mauck et al. 1999; Wink & Dyrcz 1999). Vari-
ation in the rate of EPP between populations of the same
species or between individuals in the same population, on
the other hand, are more likely to be determined by the
opportunities to indulge in alternative reproductive strat-
egies (see Westneat & Sherman 1997; Møller & Ninni 1998)
and/or the genetics benefits of so doing (see Houtman
1992; Hasselquist et al. 1996; Kempenaers et al. 1996; Petrie
& Kempenaers 1998; Petrie et al. 1998; Griffith et al. 1999a,b;
Griffith 2000; Møller 2000). This hierarchical explanation
for variation in the rate of EPP is consistent with previous
analyses of the ecological basis of interspecific variation in
avian mating systems (Owens & Bennett 1996, 1997; Arnold
& Owens 1998, 1999; Bennett & Owens 2002; Owens 2001).
The function of EPP
Hypotheses on the function of EPP
The question of why females should indulge in extra-
pair copulations, or seek to mate with more than one male,
has received much theoretical treatment and been re-
viewed thoroughly several times (e.g. Westneat et al. 1990;
Birkhead & Møller 1992; Birkhead 1998; Møller 1998;
Petrie & Kempenaers 1998; Ligon 1999). Here, therefore,
we will only review briefly the competing hypothesis and
concentrate instead on empirical tests of the predictions
arising from these hypotheses.
The main types of explanation for why females may seek
EPP for their offspring are summarized in Table 1 (from
Birkhead & Møller 1992; Møller 1998). In many respects
these explanations mirror the hypotheses that have been
proposed to explain the evolution of secondary sexual
ornaments in birds, with an early emphasis on fertility and
genetic diversity gradually being augmented by theories
on genetic quality and compatibility. Although some may
seem more probable than others, none of these explanations
can be excluded on logical grounds alone. Here, therefore,
we focus on the predictions that these hypotheses make
(Table 2) and the data required to test those predictions.
Evidence on the function of EPP
Despite the large number of theoretically plausible explana-
tions for EPP, there have been few direct empirical tests that
have provided unambiguous support for only one type of
explanation (even assuming that there will be a unitary
explanation). The reason for this shortfall is twofold: (1) failure
to gather sufficient types of data to differentiate between
different hypotheses; or (2) failure to use an experimental
approach to control for potentially confounding factors.
Table 2 shows the predictions that arise from the main
hypotheses for EPP in birds. It can be seen from this table
that three types of data are required to be able to confidently
distinguish between the main types of explanations: (i) the
distribution of EPPs among females; (ii) the distribution of
EPPs among males; and (iii) differences between extra-pair
offspring and their half-sibs resulting from within-pair
copulations. In the majority of studies that discuss the func-
tion of EPP, however, only one type of data is available.
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Most commonly, there are data on the distribution of EPP
among males and the ecological and phenotypic correlates
of intermale variation in reproductive success (Table 2), or
the distribution of EPP among females and the character-
istics of the females’ partners (Table 3). As Table 2 shows,
however, it is impossible to distinguish between hypo-
theses with only one type of data.
Even in those cases where all these types of data are avail-
able, it is usually impossible to tell whether the ecological
correlates are part of causal mechanism. Good examples of
Table 1 Hypotheses on the function of EPP in birds (adapted from Birkhead & Møller 1992; Møller 1998)
Hypothesis Description References
Fertility A Females seek EPP in order to guard against infertility in their own
social mate, but females have no way of assessing the fertility of males
Wetton & Parkin (1991)
Fertility B Females seek EPP in order to guard against infertility in their own
social mate, and females are able to assess male fertility through
phenotypic cues
Sheldon (1994)
Genetic diversity Females seek EPP to maximize genetic diversity among their offspring,
but females cannot assess the extent of genetic similarity between
themselves and males
Williams (1975);
Westneat et al. (1990)
Genetic compatibility Females seek EPP to maximize genetic compatibility between
themselves and the father of the offspring, and females can assess
the extent of genetic similarity between themselves and males
through phenotypic cues
Kempenaers et al. (1999);
Tregenza & Wedell (2000)
Good genes Females seek EPP to obtain ‘good genes’ for their offspring, and
females can assess the genetic quality of males through phenotypic
cues
Møller (1988); Hamilton
(1990); Westneat et al. (1990);
Birkhead & Møller (1992)
Direct benefit Females seek EPP to obtain (nongenetic) resources for their offspring,
and females can assess the resources held by males
Wolf (1975); Burke et al. (1989);
Colwell & Oring (1989)
Table 2 Predictions arising from hypotheses on the function of EPP in birds
Hypothesis
Predictions
Females Males Offspring
EPPs distributed
randomly
among females?
Which females
have more EPP?
EPPs distributed
randomly
among males?
Which males
have more EPP?
EPP offspring
different from
their half-sibs?
are EPP offspring
different from
their half-sibs?
Fertility A Yes Random No High fertility No None
Fertility B No Paired with low
fertility
No Attractive males No None
Genetic
diversity
Yes Random Yes Random No None
Genetic
compatibility
No Paired with
genetically
similar male
Yes/No Dependent on genetic
heterogeneity of
population and female
ability to discriminate
Yes EPP offspring
more
heterozygous
‘Good genes’ No Paired with male
with ‘poor genes’
No Most viable or
productive
Yes EPP offspring
fitter
‘Sexy son’ No Paired with
unattractive male
No Most attractive Yes EPP offspring
more attractive
Direct benefit No Paired with male
with poor resources
No Good resources No None
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this type of problem are the work conducted by Wetton &
Parkin (1991) and Gray (1997) on the fertility hypothesis,
where both studies found a relationship between the hatch-
ing success of a brood and the incidence of EPP within broods.
However, because of a lack of other types of evidence,
neither of these studies could rule out the possibility that
the relationships between EPP and hatchability were due to
confounding effects such as female quality. It is also useful
to note that 85% of house sparrow eggs that failed to hatch in
one study had a great deal of sperm present at the site of
fertilization and failed for other reasons (Birkhead et al. 1995).
In other cases the ecological or phenotypic correlates of rep-
roductive success are factors such as ‘age’ or ‘size’ (Table 3),
which are equally applicable to several competing hypo-
theses. Age, for instance, is clearly an important determinant
of paternity, an observation consistent with the idea that
females use EPP to gain viability genes for their offspring,
as older males have ‘proven’ their viability. However, only
one of these studies was experimental (Saino et al. 1997),
and in general the results may be confounded by factors
such as an increased ability of older males to display or seek
EPCs, their ability to protect their own paternity or provide
more direct benefits to females willing to participate in EPCs.
The biggest shortfall in empirical studies of the function
of EPP is the lack of data on differences between offspring
resulting from EPP and their half-sibs resulting from
within-pair copulations. Although many studies have
used correlations between reproductive success and age,
size or showiness to infer cryptic female choice for ‘good
genes’ (refs in Table 3), Table 2 shows that a key diagnostic
piece of information is whether extra-pair offspring are
fitter than within-pair offspring. Data on this question are
extremely limited. The simplest way to obtain unambiguous
data on potential genetic differences between within- and
extra-pair offspring is by direct comparison of maternal
half-siblings from the same brood (e.g. Kempenaers et al.
1997; Sheldon et al. 1997). For instance, in the blue tit
Kempenaers et al. (1997) found that in broods with partial
Table 3 Phenotypic correlates of variation between males in the number of extra-pair offspring they suffer in their own brood, and the
number of extra-pair offspring they sire in other broods. The table shows those species in which a significant association has been
demonstrated for each phenotypic variable in turn
Phenotypic factor Which males lose paternity? Which males gain paternity?
Age Bobolink1Red-winged blackbird10
Bullock’s oriole2Bullock’s oriole2
Indigo bunting4Superb fairy-wren3
Purple martin5Yellowhammer11
American redstart6Blue tit12
Eastern bluebird7Purple martin5
White-crowned sparrow8American redstart6
Eastern bluebird7
White-crowned sparrow8
House sparrow13
Size and condition Yellow warbler14 Blue tit12
Purple martin15
Willow warbler16
Crested tit17
Dominance Black-capped chickadee9
Sexual ornamentation and song Collared flycatcher18 Collared flycatcher18
Barn swallow19 Barn swallow19
Blue tit12 Great reed warbler20
Common yellowthroat21 Yellow warbler14
Bluethroat22 Yellowhammer11
Dusky warbler23 Superb fairy-wren3
Common yellowthroat21
Bluethroat22
Dusky warbler23
References: 1Bollinger & Gavin (1991); 2Richardson & Burke (1999); 3Dunn & Cockburn (1999); 4Westneat (1990); 5Wagner et al. (1996);
6Perreault et al. (1998); 7Gowaty & Bridges (1991); 8Sherman & Morton (1988); 9Otter et al. (1998); 10Weatherhead & Boag (1995); 11Sundberg
& Dixon (1996); 12Kempenaers et al. (1997); 13Wetton et al. (1995); 14Yezerinac & Weatherhead (1997); 15Morton et al. (1990); 16Bjørnstad &
Lifjeld (1997); 17Lens et al. (1997); 18Sheldon & Ellegren (1999); 19Smith et al. (1991), Møller & Tegelström (1997), Saino et al. (1997), Møller
et al. (1998); 20Hasselquist et al. (1996); 21Thusius et al. (2001); 22Johnsen et al. (2001); 23Forstmeier et al. (2002).
mec_1613.fm Page 2207 Tuesday, October 22, 2002 5:37 PM
2208 S. C. GRIFFITH, I. P. F. OWENS and K . A . THUMAN
© 2002 Blackwell Science Ltd, Molecular Ecology, 11, 2195– 2212
mortality, extra-pair offspring were more likely to survive
than their within-pair half-siblings. Similarly, in the col-
lared flycatcher Sheldon et al. (1997), revealed that extra-
pair offspring fledge in better condition than their maternal
half-siblings, the difference in quality being related to the
difference in the expression of a sexually selected trait of
their fathers. Most recently, in the bluethroat Luscinia svecica
Johnsen et al. (2000) discovered that extra-pair offspring had
a higher immune response than their within-pair maternal
half-siblings. In addition the extra-pair offspring were also
more immunocompetent than their paternal half-siblings,
suggesting an additional effect of maternal genotype. They
concluded that their results are consistent with the idea
that females engage in extra-pair copulations to obtain com-
patible viability genes, rather than ‘good genes’ per se (Johnsen
et al. 2000). By contrast, three studies of two populations of
the great tit found no significant morphological differences
between within-pair and extra-pair offspring (Krokene
et al. 1998; Strohbach et al. 1998; Lubjuhn et al. 1999).
The interpretation of all of the studies mentioned above
is problematic for three reasons. First, given that ‘good
genes’ effects are generally small, explaining an average of
just 2% of the variation in offspring viability (Møller & Alatalo
1999), very large sample sizes are required for sufficient
statistical power. Second, although it is commonly assumed
that ‘good genes’ effects must be equated with survivor-
ship, it is often equally plausible that such genes may show
their effect through an alternative mechanism, such as high
fecundity, whereby individuals could have a high fitness and
yet live for a relatively short time. Therefore a lack of ‘good
genes’ effects may simply reflect a lack of investigations
into a more diverse and complete set of fitness measures.
A final, more basic methodological problem is that addit-
ive genetic differences between half-siblings, even within
the same nest, may be confounded by parentally derived
environmental effects (Mousseau & Fox 1998). For example,
females have been shown to invest differentially in eggs by
either their sex (e.g. Cordero et al. 2000) or paternal pheno-
type (e.g. Cunningham & Russell 2000). As pointed out by
Sheldon (2000), however, differential investment by females,
based on offspring paternity, would be adaptive only if there
were differences in paternal genetic contributions to off-
spring fitness. Differential allocation of resources by either
parent during chick-feeding could also contribute environ-
mentally derived variation (e.g. Griffith et al. 1999b) to dif-
ferences between within- and extra-pair offspring, a problem
which can be removed by cross-fostering broods so that they
are not reared by their own parents. To date, no empirical
study has dealt with all these problems simultaneously.
Conclusions
Molecular techniques have revolutionized our view of
avian mating systems, with sexual monogamy now known
to be restricted to a minority of bird species, rather than
over 90% of species as assumed by Lack (1968). Explaining
interspecific variation in the extent of extra-pair paternity
has proved difficult, but an appreciation of the problems
of small sample sizes, and an ever-increasing compar-
ative database, have led to several recent advances. It now
seems probable that differences between species in the rate
of EPP are due to a combination of differences in life his-
tory, pattern of parental care and local opportunities for
promiscuity. Revealing the function of EPP, however,
remains the most conspicuous ongoing challenge. Here,
the most urgently required data is that on whether there
are systematic differences between maternal half-sibs
resulting from partial-brood EPP. So far, only five studies
have obtained this type of information, and three have
found consistent differences between within- and extra-
pair offspring. Thus far, therefore, only the ‘good genes’
and ‘genetic compatibility’ hypotheses have received
robust empirical support. It remains to be shown whether
these are the general explanation for EPP in birds.
Acknowledgements
We thank Kate Arnold, Tim Birkhead, Peter Bennett, Terry Burke,
Andrew Cockburn, Ian Hartley, Bart Kempenaers, Ben Sheldon,
David Westneat and two anonymous referees for discussion and/
or comments on the manuscript. This work was supported by
a NERC (UK) fellowship (GT 99/5/TS/11) to SCG, a Swedish
Natural Sciences Research Council grant to Ben Sheldon (SCG),
and an Australian Research Council grant to IPFO.
Supplementary material
The following material is availiable from
http://www.blackwellpublishing.com/products/journals/
suppmat/MEC/MEC1613/MEC1613sm.htm
Appendix I
Table A1. Species-specific estimates of the rate of extra-pair
paternity at both the individual offspring level (% EPP offspring)
and the percentage of broods that contain at least one extra-pair
chick (% EPP broods).
Appendix II
Table A2. Species estimates reported in the literature that have
been excluded from the unambiguous database (Appendix I) for
the reasons given.
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Simon Griffith is a NERC research follow based at Oxford
University currently working on sexual selection, and ornamental
signaling in birds, particularly in monogamous mating systems.
Ian Owens is based at Imperial College (Silwood Park) and is
interested in diversification and speciation in birds. Katherine
Thuman is a PhD student in the Department of Animal Ecology at
Uppsala University, Sweden. Her work focuses primarily on
understanding sexual selection in highly polygynous lok-mating
systems.
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