Behavioral Ecology Vol. 12 No. 4: 457–466
Social mating systems and extrapair
fertilizations in passerine birds
Dennis Hasselquist and Paul W. Sherman
Department of Neurobiology and Behavior, Seeley G. Mudd Hall, Cornell University, Ithaca, NY
14853-2702, USA
Two alternative hypotheses have been proposed to explain how social and genetic mating systems are interrelated in birds.
According to the first (male trade-off) hypothesis, social polygyny should increase extrapair fertilizations because when males
concentrate on attracting additional social mates, they cannot effectively protect females with whom they have already paired
from being sexually assaulted. According to the second (female choice) hypothesis, social polygyny should decrease extrapair
fertilizations because a substantial proportion of females can pair with the male of their choice, and males can effectively guard
each mate during her fertile period. To discriminate these alternatives, we comprehensively reviewed information on social
mating systems and extrapair fertilizations in temperate zone passerine birds. We found significant inverse relationships between
proportions of socially polygynous males and frequencies of extrapair young, whether each species was considered as an independent data point (using parametric statistics) or phylogenetically related species were treated as nonindependent (using
contrasts analyses). When social mating systems were dichotomized, extrapair chicks were twice as frequent in monogamous as
in polygynous species (0.23 vs. 0.11). We hypothesize that in socially polygynous species, (1) there is less incentive for females
and males to pursue extrapair matings and (2) females incur higher costs for sexual infidelity (e.g., due to physical retaliation
or reduction of paternal efforts) than in socially monogamous species. Key words: extrapair paternity, monogamy, passerine
birds, phylogenetic contrasts, polygyny, social mating system. [Behav Ecol 12:457–466 (2001)]
R
ecently it has become evident that the social and genetic
mating systems of many species are different. Social associations do not necessarily indicate exclusive mating relationships, particularly in birds. Extrapair copulations (EPCs)
have been observed in more than 150 species, and extrapair
fertilizations (EPFs) have been documented in about 75% of
the more than 100 species in which molecular genetic techniques have been used to infer paternity (reviewed by Birkhead and Møller, 1992, 1995; Møller and Ninni, 1997; Møller
and Cuervo, 2000; Westneat and Sherman, 1997; Westneat
and Webster, 1994; Westneat et al., 1990).
There is considerable variability among populations and
species in frequencies of EPCs and EPFs. To understand why,
we must consider the fitness costs and benefits of engaging in
extrapair sexual activities. For males, the obvious benefit of
EPCs is that they can enhance reproductive success (i.e., EPCs
result in EPFs). However, seeking EPCs may be costly if such
behavior reduces a male’s effectiveness in self-advertisement,
territorial defense, mate guarding, or parental care (e.g., Poston et al., 1998; Sherman and Morton, 1988; Westneat, 1988,
1993, 1994) or increases the male’s chances of contracting
parasites and diseases (Sheldon, 1993). For females, EPCs may
yield indirect benefits, such as ‘‘good genes’’ (Gowaty, 1996;
Hasselquist, 1994; Hasselquist et al., 1996; Kempenaers et al.,
1992), or direct benefits such as access to territories or other
resources (Gray, 1997; Hunter and Davies, 1998; Wolf, 1975),
assistance with parental care (Wagner, 1992), or insurance of
a fertile mating (Wetton and Parkin, 1991). Potential costs of
EPCs for females include contracting ectoparasites and sexually transmitted diseases and retaliation by their social mate.
For example, a male might respond to being cuckolded by
Address correspondence to D. Hasselquist, who is now at the Department of Animal Ecology, Lund University, Ecology Building, 223
62 Lund, Sweden. E-mail: [email protected].
Received 4 April 2000; revised 3 October 2000; accepted 15 October 2000.
2001 International Society for Behavioral Ecology
reducing nest defense (e.g., Weatherhead et al., 1994) or nestling provisioning (Dixon et al., 1994; Kokko, 1999; Møller and
Birkhead, 1993a; Møller and Cuervo, 2000; Westneat and Sargent, 1996; Wright, 1998), or by deserting the female (Cézilly
and Nager, 1995). Finally, females may sometimes be forced
to accept unsolicited EPCs when resistance to sexual harassment could result in physical injuries (e.g., Frederick, 1987;
Røskaft, 1983).
Increasingly investigators are taking advantage of the substantial comparative database that now exists to disentangle
the ecological and social factors underlying variations in EPCs
and EPFs. Two key variables, breeding density and synchrony,
have been foci of considerable interest and debate. Sometimes
extrapair activities increased with increasing density (e.g., Hoi
and Hoi-Leitner, 1997; Møller, 1987, 1991; Møller and Birkhead, 1991, 1993b) and synchrony (Chuang et al., 1999;
Stutchbury 1998a,b; Stutchbury and Morton, 1995), but in
other studies EPFs were not correlated with either density
(Westneat and Sherman, 1997) or synchrony (Saino et al.,
1999; Westneat and Gray, 1998; Yezerinac and Weatherhead,
1997). Some of this variability may be due to lumping of interand intrapopulational studies if differences in density and synchrony are more important within than among populations.
Regardless, effects of another key variable, the social mating
system, have yet to be adequately explored. This is the issue
addressed in this paper.
Two social mating systems characterize the majority of birds.
The most common is monogamy: in ⬎ 92% of species a male
and female form a pair bond and raise the young together
(Ford, 1983; Lack, 1968; Møller, 1986). Social polygyny is a
distant second: in about 5% of species ⬎ 5% of males form
pair bonds with multiple females. Two alternative hypotheses
have been proposed to explain how social mating systems
should affect extrapair sexual activities, and they make opposite critical predictions.
The male trade-off hypothesis
Social polygyny increases EPCs and EPFs, whereas social monogamy decreases both (Arak, 1984; Birkhead and Møller,
Behavioral Ecology Vol. 12 No. 4
458
1992; Dunn and Robertson, 1993). This hypothesis assumes
that in polygynous species there are trade-offs between attracting additional social mates and other breeding behaviors, especially mate guarding. When males concentrate on mate attraction, females with whom they have already paired receive
less attention, even though they may still be fertile (Arak,
1984; Hasselquist and Bensch, 1991; Westneat, 1993). On the
one hand, this frees females to seek matings with extrapair
males. On the other hand, unguarded females are more vulnerable to forced copulations by interloping extrapair suitors.
Both effects should increase the frequency of EPCs and EPFs
over their occurrence in socially monogamous species, among
which males do not have to trade off mate guarding for mate
attraction because there is no possibility of having another
social mate.
The female choice hypothesis
Social polygyny decreases EPCs and EPFs, whereas social monogamy increases both (Hasselquist, 1994; Hasselquist et al.,
1995a; Møller, 1992; Westneat et al., 1990). The enhanced
expression of male secondary sexual characters which occurs
in socially polygynous species facilitates female identification
of extremely attractive males (Gontard-Danek and Møller,
1999). Under the female choice hypothesis, EPCs are reduced
both because several females can form pair bonds with the
most attractive males and because females that are paired to
such males are unlikely to seek or accept EPC attempts by less
attractive individuals. In addition, EPCs may be reduced in
socially polygynous species if (1) males can simultaneously advertise themselves and guard against territorial intrusions by
extrapair suitors, (2) dominant, territory-holding males are
especially attractive to females and capable of physically
guarding them, or (3) dominant males are so occupied with
display and defense of their own territory that they do not
have the time or energy to pursue EPCs elsewhere. In contrast, in socially monogamous species a smaller proportion of
females in any population can associate socially and sexually
with the most attractive males, so a greater proportion of females may benefit from seeking or accepting EPCs with highquality suitors (Gowaty, 1996).
Birkhead and Møller (1992, 1996; Møller and Birkhead,
1993b) have already explored these ideas. They found no consistent relationship between the social mating system and frequencies of EPCs or EPFs. However, the issue bears reexamination because many new, high-quality genetic data have recently become available. Also, Birkhead and Møller included
all birds in their analyses, so their attempts to tease out effects
of the social mating system may have been diluted by ecological and evolutionary factors that influence life histories and
breeding behaviors in widely divergent taxonomic groups. For
example, Westneat and Sherman (1997) reported that EPFs
occur in a significantly greater proportion of passerine than
nonpasserine species and, among species exhibiting EPFs, at
significantly higher frequencies in passerines than nonpasserines.
To focus more directly on how differences in social mating
systems affect EPFs, we restricted our analyses to species of
passerine birds from temperate regions (predominantly North
America and Europe). These are related taxa that live under
comparable climatic and habitat conditions, yet there is considerable interspecific variation in frequencies of EPFs among
all families and genera. Moreover, temperate-region passerines typically pair with different social mates each breeding
season. This is important because lengths of social pair bonds
can influence frequencies of EPFs regardless of the social mating system (e.g., Birkhead and Møller, 1996). Here we explore
whether EPFs are randomly distributed among social mating
systems. We then consider, in light of the results, whether
comparative analyses of extrapair sexual activities should
henceforth include or can safely ignore species’ social mating
systems.
METHODS
Definitions
We define a ‘‘pair bond’’ as an extended social and sexual
association between a male and a female, lasting for days to
months or more, considerably longer than it takes to copulate
(Westneat et al., 1990). An ‘‘extrapair copulation’’ is a mating
by a female with a male other than her pair-bonded mate;
EPCs may result in extrapair fertilizations. Our definitions exclude birds that do not form pair bonds, especially lekking
species (Höglund and Alatalo, 1995) and species in which
males defend territories where groups (‘‘harems’’) of females
nest but the males only associate closely with each female to
copulate (e.g., montezuma oropendolas, Psarocolius montezuma: Webster, 1994; boat-tailed grackles, Quiscalus major: Poston et al., 1998; aquatic warblers, Acrocephalus agricola: Dyrcz
and Zdunek, 1993; Schulze-Hagen et al., 1993, 1995). Our
definitions also exclude matings between females and secondary males with whom they have had extensive social associations, such as in polyandrous and polygynandrous species
(e.g., dunnocks, Prunella modularis: Burke et al., 1989; alpine
accentors, Prunella collaris: Hartley et al., 1995; Smith’s longspurs, Calcarius pictus: Briskie, 1992) and in cooperatively
breeding groups (e.g., splendid fairy wrens, Malurus cyaneus:
Brooker et al. 1990; white-browed scrubwrens, Sericornis frontalis: Whittingham and Dunn, 1998).
We define ‘‘breeding density’’ as the number of individuals
breeding per unit area of suitable nesting habitat (Westneat
and Sherman, 1997). ‘‘Breeding synchrony’’ refers to simultaneity of female receptivity, which can be measured as the
average proportion of females that are fertile per day during
the breeding season (Kempenaers, 1993; Langefors et al.,
1998; Stutchbury and Morton, 1995).
Genetic and social mating systems
We compiled data from all field studies of passerine populations published through 1998 that (1) sampled ⬎ 40 chicks
and (2) presented an unambiguous estimate of the fraction
of chicks sired by extrapair males based on DNA fingerprinting (mini- or microsatellites; in total 50 studies; see Figure 1)
or on allozymes (four studies based on large data sets: Blakey,
1994; Bollinger and Gavin, 1991; Gowaty and Bridges,
1991a,b; Sherman and Morton, 1988). We used the fraction
of chicks sired by extrapair males (i.e., frequency of extrapair
young, EPY) rather than the proportion of broods with EPY
as the primary dependent variable in our analyses, because
frequencies of EPY yielded the larger sample size, and in our
data set these two measures were highly correlated (r ⫽ .93,
N ⫽ 36, p ⬍ .001). For each population from which EPY data
were available, we sought field studies of the social mating
system. Data on the proportion of socially polygynous males
(i.e., number of polygynous males/number of territorial
males) were extracted directly from the original source or
were calculated from information provided there or in another study of the same population. In the case of the pied flycatcher Ficedula hypoleuca, we used data reported by Lundberg and Alatalo (1992) to calculate the average proportion
of socially polygynous males in the two Scandinavian populations where paternity was investigated. We omitted a few studies because: (1) they were allozyme studies that estimated the
proportion of broods with mixed paternity without specifying
Hasselquist and Sherman • Mating systems and extrapair fertilizations
459
whether mismatched chicks resulted from extrapair matings
or intraspecific parasitism (McKitrick, 1990; Petter et al.,
1990), (2) they inferred rates of extrapair paternity from sexual differences in tarsus heritabilities (Alatalo and Lundberg,
1984, 1986; Alatalo et al., 1989; these were excluded because
the reliability of this method is questionable: Dhondt, 1991;
Gebhardt-Henrich and Nager, 1991; Hasselquist et al., 1995b;
Lifjeld and Slagsvold, 1989), or (3) they were conducted on
manipulated populations in which the procedures may have
confounded EPF rates (barn swallows, Hirundo rustica, with
manipulated tail feathers: Smith et al., 1991; dark-eyed juncos,
Junco hyemalis, with testosterone implants: Ketterson and Nolan, 1992). In total, 40 species met all criteria for inclusion in
our analyses (Figure 1).
ing tradition we made our results comparable to those of previous workers. And, in fact, the traditional cutoff corresponded to a natural break point in our data set, which was decidedly bimodal (Figures 1 and 2): in 29 of 40 species 0–5% of
males paired with ⬎1 social mate, and in the other 11 species
12–90% of males paired with ⬎1 social mate.
Rates of extrapair fertilizations differed between social mating systems. Frequencies of EPY were significantly higher in
socially monogamous species (mean ⫽ 0.233, SE ⫽ 0.025)
than in socially polygynous species (mean ⫽ 0.114, SE ⫽
0.025; ANOVA, F1,38 ⫽ 9.6, p ⫽ .004; Figure 2). Moreover,
frequencies of broods with EPY were significantly higher in
socially monogamous species (mean ⫽ 0.392, SE ⫽ 0.038)
than in socially polygynous species (mean ⫽ 0.261, SE ⫽
0.045; F1,34 ⫽ 4.7, p ⫽ .036).
When the social mating system was considered as a single,
continuous variable (Figure 3), there was a significant negative correlation between proportions of socially polygynous
males and frequencies of EPY (r ⫽ ⫺.32, p ⫽ .044). However,
this relationship might be spurious due to confounding effects of breeding synchrony and density. Therefore, we conducted a multiple regression analysis with the social mating
system, synchrony (data from Stutchbury, 1998b; Stutchbury
and Morton, 1995), and density (data from Westneat and
Sherman, 1997) as independent variables and frequencies of
EPY as the dependent variable. This halved our sample size
because information on all three factors was available for just
20 species. Among the factors, only the social mating system
predicted frequencies of EPY (p ⫽ .048); neither breeding
density (p ⫽ .40) nor synchrony (p ⫽ .82) was significantly
associated with EPY frequencies.
Comparative analyses
Many authors (e.g., Brooks and McLennan, 1991; Harvey and
Nee, 1997; Martins and Hansen, 1996) have argued that traits
of related species should not be regarded as independent in
statistical analyses. Others believe phylogenetic corrections
have been overemphasized (e.g., Reeve and Sherman, 2001;
Ricklefs and Starck, 1996). In light of these disagreements, we
analyzed the data both ways. In analyses that controlled for
phylogeny, we used independent contrasts (Felsenstein, 1985;
Garland et al., 1992, 1993; Harvey and Pagel, 1991), based
primarily on estimates of relationships derived from Sibley
and Ahlquist (1990). We followed Westneat and Sherman
(1997) in using the more recent phylogenetic studies of Sheldon et al. (1992) and Silkas et al. (1996) for the Paridae and
Sheldon and Winkler (1993) for the Hirundinidae; we used
the AOU checklist (American Ornithologists’ Union, 1983) to
resolve the location of the geospizine finches and the indigo
bunting (Passerina cyanea) within the Embirizinae.
Statistics
Standard, nonparametric statistical tests were conducted using
SYSTAT (SYSTAT Inc., Chicago). Proportions of EPY in populations were transformed (square-root arcsine) before analyses. For the phylogenetic contrasts, social mating systems
were characterized either continuously (proportions of males
per population with ⬎ 1 social mate) or dichotomously (monogamous ⫽ 0, polygynous ⫽ 1), and branch lengths were
inferred from genetic distances (Figure 1). We calculated contrasts from the difference between dyad species at each node
using the Phenotypic Diversity Analysis Program (PADP-3.0)
of Garland et al. (1993). Relationships between contrast values
and the standard deviation in branch lengths, calculated with
several different methods of transforming branch lengths,
were tested for internal biases in the data (e.g., a relationship
between the absolute values of contrasts and standard deviations of branch lengths; Garland et al., 1992). We analyzed
the association between standardized contrasts of social mating systems and EPFs with linear regression in PADP (Garland
et al., 1993).
RESULTS
Species as independent data points
Initially we categorized the social mating system of each of the
40 species in our sample as either socially polygynous or monogamous using the 5% criterion of Lack (1968), Møller
(1986), and Verner and Willson (1969). That is, we considered a species to be monogamous or polygynous depending,
respectively, on whether ⬍5% or ⬎5% of males paired with
multiple females. Although this cutoff is arbitrary, by accept-
Independent contrasts analyses
Frequencies of EPY were significantly higher in socially monogamous species, whether mating systems were categorized
dichotomously (r2 ⫽ .14, t ⫽ ⫺2.4, p ⬍ .05, df ⫽ 38) or continuously (r2 ⫽ .12, t ⫽ ⫺2.3, p ⬍ .05, df ⫽ 38). However,
there was a significant relationship between absolute values of
standardized contrasts and standard deviations of observed
branch lengths (r2 ⫽ .19, t ⫽ ⫺3.0, p ⬍ .01, df ⫽ 37), violating
an assumption of this analytical technique. We therefore converted observed branch lengths of social mating systems (i.e.,
the dependent variable) to a constant value (i.e., each branch
length was set at 1, as recommended by Garland et al., 1992,
1993). There was no significant association between standardized contrasts and standard deviations of constant branch
lengths (r2 ⫽ .05, t ⫽ ⫺1.4, p ⬎ .10, df ⫽ 37). Therefore, we
conducted the contrast analyses again, this time inferring constant branch lengths for the dependent variable. As before,
frequencies of EPY were significantly higher in more monogamous species, whether mating systems were categorized dichotomously (r2 ⫽ .26, t ⫽ ⫺3.7, p ⬍ .001, df ⫽ 38; Figure
4A) or continuously (r2 ⫽ .12, t ⫽ ⫺2.5, p ⫽ .02, df ⫽ 38;
Figure 4B).
DISCUSSION
In all our analyses, frequencies of extrapair young were significantly higher in socially monogamous than polygynous
passerine species (Figures 2–4). This outcome was evident
whether mating systems were considered as two categorical
variables or one continuous variable and whether species were
treated as independent data points or phylogeny was controlled for using independent contrasts. Of the alternative hypothesized relationships between social and genetic mating
systems, our results unequivocally supported the female
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Behavioral Ecology Vol. 12 No. 4
Hasselquist and Sherman • Mating systems and extrapair fertilizations
461
choice hypothesis (Hasselquist, 1994; Hasselquist et al., 1995a;
Møller, 1992; Westneat et al., 1990).
Of course, it is possible that low frequencies of EPY in socially polygynous species were due to confounding effects of
some other correlated variable(s). For example, EPFs might
be rarer in polygynous species because they breed more or
less synchronously or at higher or lower densities. Indeed,
Møller and Birkhead (1991, 1993b) reported a positive relationship between density and frequencies of EPCs, and Stutchbury (1998a,b) claimed that breeding synchrony best explains
variations in EPFs among species. However, our multiple regression analysis revealed no significant effects of density or
synchrony, and many other studies have found either no effects or inconsistent effects of breeding density or synchrony
on frequencies of EPY (e.g., Dunn et al., 1994; Kempenaers,
1997; Langefors et al., 1998; Perreault et al., 1997; Saino et
al., 1999; Weatherhead, 1997; Westneat and Gray, 1998; Westneat and Sherman, 1997; Yezerinac and Weatherhead, 1997).
We infer that confounding variables did not create or cloud
the relationship between social mating systems and EPY.
To understand why EPY are more common in socially monogamous species, it is useful to consider separately the reproductive interests of the paired male, the female, and the
extrapair male (Lifjeld et al., 1994). Advantages and disadvantages to each of these parties will shape outcomes of conflicts
over extrapair activities.
Females seek EPCs
Assume first that females seek EPCs, as has been observed in
several species (e.g., Ahnesjö et al., 1993; Kempenaers et al.,
1992; Otter et al., 1998; Smith, 1988). If so, frequencies of
EPY will be determined primarily by benefits and costs for the
female.
Benefits
In socially monogamous species, not all females can form pair
bonds with the highest quality males. Females arriving at the
breeding site earliest presumably have first choice. In addition, regardless of when they arrive, large, healthy, experienced females may be able to monopolize access to attractive
males by driving rival females away (Breiehagen and Slagsvold,
1988; Sandell and Smith, 1996, 1997; Yasukawa and Searcy,
1982). As a result, in socially monogamous populations the
majority of females will not be able to pair with the most attractive males.
A female can make the best of this situation by forming a
social pair bond with the most attractive male that is available
and also seeking extrapair matings with higher quality males
than her social mate when the opportunity arises (Gowaty,
1996). Females benefit by adopting this mixed reproductive
strategy if offspring sired by the most attractive males are predictably larger, healthier, more likely to survive, or more likely
to be chosen by other females (Hasselquist et al., 1996; Kem-
Figure 2
Frequency (⫹SE) of extrapair young in relation to the social mating
system (M ⫽ monogamy, P ⫽ polygyny) of 40 species of passerine
birds (see Figure 1; p ⫽ .004).
penaers et al., 1992; Møller, 1992; Otter et al., 1998; Sundberg
and Dixon, 1996; Yezerinac and Weatherhead, 1997). In socially polygynous species, in contrast, even late-arriving and
less competitive females potentially can pair with high-quality
males, at least until breeding territories of the most attractive
males are saturated (e.g., Bensch, 1996; Davies, 1989; Hasselquist et al., 1995a). Because a greater fraction of females can
pair with the male of their choice, fewer females should be
inclined to seek EPCs. The result is that EPFs and EPY should
be less common in socially polygynous than monogamous species.
Costs
If EPCs are more costly for females in socially polygynous species, their occurrence and thus the frequency of EPY may be
reduced relative to that in socially monogamous species.
There are two reasons that costs of EPCs might be greater in
socially polygynous species. First, risks of exposure to sexually
transmitted diseases (Sheldon, 1993) should be higher because many individuals have multiple sex partners. Moreover,
such sexually transmitted diseases may be more numerous and
virulent due to frequent horizontal transmission (Ewald,
1994). Second, in socially polygynous species, cuckolded
←
Figure 1
Phylogeny of 40 passerine species in which patterns of paternity have been investigated using genetic markers, and information on (1) proportions of young sired by extrapair males (EPY), (2) proportions of broods containing EPY, (3) proportions of males with ⬎1 social mate,
(4) social mating system category of the studied population (M ⫽ monogamous [⬍5% of males have ⬎1 social mate], P ⫽ polygynous [⬎5%
of males have ⬎1 social mate]), (5) degree of breeding synchrony (SI index), (6) nearest neighbor distance (NND), and (7) references for
the parentage studies (in most cases superscript letters indicate that more than one population of that species has been studied; data from
multiple studies of the same species were combined and averaged for analysis): aLifjeld et al. (1991), Gelter and Tegleström (1992); bGowaty
and Bridges (1991a,b); cSmith and von Schantz (1993); dStrohbach et al. (1998); eMøller and Tegelström (1997); fWhittingham and Lifjeld
(1995); gDale (1995); hDunn et al. (1994); iGyllensten et al. (1990), Bjørnstad and Lifjeld (1997); jBuchanan and Catchpole (unpublished
data); kHasslequist D et al. (unpublished data); lcited in Møller and Briskie (1995); mcited in Stutchbury and Morton (1995); ncited in Petrie
et al. (1998); oWestneat (1993), Gray (1996). Numbers in the phylogeny refer to branch lengths between species and groups of species.
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Behavioral Ecology Vol. 12 No. 4
Figure 3
Proportion of polygynous males in well studied populations of 40
species of passerine birds in relation to frequencies of extrapair
young in each population as determined using genetic markers.
males may be able to retaliate against mates that engage in
EPCs more effectively than in socially monogamous species.
Due to strong sexual selection, males in socially polygynous
species often are larger than females ( Jehl and Murray, 1986;
Webster, 1992). Physical attacks by larger males are more damaging (Clutton-Brock and Parker, 1995a,b) in these species
than in species in which the sexes are similar in size. Moreover, if a socially polygynous male observes one of his females
mating with another male, or infers that she did so, he may
either reduce his parental care to that brood in favor of
broods where his likelihood of paternity is greater or else ‘‘divorce’’ the unfaithful female (e.g., Cézilly and Nager, 1995).
Among many socially polygynous species males divide their
nestling provisioning efforts unequally among nests (e.g.,
Bensch and Hasselquist, 1994; Dyrcz, 1986; Johnson et al.,
1993; Patterson et al., 1980; Sejberg et al., 2000; Wittenberger,
1982). We believe that female extrapair mating activities underlie some of these asymmetries in paternal efforts (Westneat
and Sherman, 1993; Møller and Cuervo, 2000).
Retaliation may not be as effective a deterrent in socially
monogamous species. Although males sometimes attack unfaithful females (e.g., Barash, 1976), because the sexes are
about the same size such attacks are less likely to be physically
damaging. Moreover, retaliation by withholding parental care
from a brood may not yield much benefit for males. First,
males usually have no other reproductive options, such as
finding a new mate, by the time nestlings are being fed (Kokko, 1999). Second, some of the chicks in a mate’s nest usually
are the male’s own offspring (Westneat and Sherman, 1993;
Whittingham et al., 1992); a male that neglects the whole
brood thus risks starvation of his own progeny (there is no
evidence that males can discriminate their own offspring from
unrelated chicks in their nest; Kempenaers and Sheldon,
1996; Westneat et al., 1995). Third, females may use male
feeding effort as a cue for subsequent matings with that male,
and withholding care may result in divorce (Freeman-Gallant,
1996; Wagner et al., 1996). Fourth, benefits from reducing
parental efforts usually cannot be gained until the subsequent
breeding season, but there is no guarantee that withholding
Figure 4
Results of phylogenetic contrasts analyses relating contrasts in social
mating systems of well studied populations of 40 passerine bird
species to contrasts in their frequencies of extrapair young when
each species’ social mating system was set as (A) a categorical
variable (monogamous or polygynous), and (B) a continuous
variable (frequency of polygynous males in the studied population;
see Figure 1).
care will enable males to survive that long, or that, even if
males do survive, they will then be paired to a more faithful
female than their current mate (Westneat and Sherman,
1993).
These considerations help explain why paternal provisioning is independent of paternity in so many socially monogamous passerines (e.g., MacDougall-Shackleton and Robertson,
1998; Wagner et al., 1996; Whittingham and Lifjeld, 1995;
Whittingham et al., 1993; Yezerinac et al., 1996). However, in
some birds males do adjust nestling provisioning or nest-defense efforts to the whole brood according to their likelihood
of paternity (reviewed by Møller and Cuervo, 2000). Such ad-
Hasselquist and Sherman • Mating systems and extrapair fertilizations
463
justments have been documented in species in which males
have a reliable behavioral cue about certainty of paternity. For
example, in polygynous or polygynandrous mating systems,
males often use the time spent alone with the female when
she was receptive (i.e., the male’s perceived effectiveness at
mate guarding; Burke et al., 1989; Lifjeld et al., 1998; Sheldon
et al., 1997; Sheldon and Ellegren, 1998; Weatherhead et al.,
1994).
breeding synchrony, density, or female condition also may affect the frequency of extrapair activities (Gowaty, 1996; Møller
and Birkhead, 1993b; Stutchbury, 1998a,b). However, our results imply that social mating systems should henceforth be
included as an important variable in attempts to understand
the factors underlying differences in extrapair sexual activities
among populations and species of passerine birds.
Males seek EPCs
Now assume that males seek EPCs. If so, frequencies of extrapair activities will be affected by trade-offs with other reproductive behaviors and responses of females.
Trade-offs with other reproductive behaviors
In socially polygynous species, paired males can increase their
reproductive success by staying on their territory and advertising for additional social mates. This is not an option for
males in socially monogamous species: they can only increase
their mating success by leaving their territory to seek EPCs.
Thus males in socially polygynous species can potentially enhance their mating success while simultaneously maintaining
mate guarding efficacy, whereas males in socially monogamous species must sacrifice mate guarding for gallivanting (or
else wait until their mate is no longer fertile). The result is a
higher frequency of EPCs and EPY in socially monogamous
species.
Responses of females
When extrapair suitors appear, females may either accept or
physically resist their copulation attempts (e.g., by struggling
or fleeing; Westneat, 1987, 1990; Westneat et al., 1990). Resistance is more likely in socially polygynous than in monogamous species because a greater proportion of females can pair
with attractive (i.e., preferred) males. These females gain by
avoiding dilution of the sperm of their high-quality mate. In
addition, by protesting, females may attract the attention of
their social mate and receive his protection, as well as avoiding
retaliation for perceived infidelity. Finally, males in socially polygynous species may be large enough relative to females that
they can force intrapair copulations on females that have mated with other males (Møller and Birkhead, 1991). If these
retaliatory intrapair matings give the paired males’ sperm an
advantage, frequencies of EPY would be reduced despite frequent EPCs.
In socially monogamous species, in contrast, there is a greater chance that an extrapair suitor will be of higher quality
than a female’s social mate. If so, females should be less likely
to protest his sexual advances. Moreover, because males of
socially monogamous species are about the same size as their
mate, they are presumably less able to force retaliatory intrapair copulations and also less able to physically punish their
mate for copulating with other males.
Conclusion
Our analyses indicate that social mating systems of passerines
have important effects on their genetic mating systems. The
most likely explanation is that females control copulations and
sperm usage, and they choose to be more faithful to their pairbonded mate in socially polygynous than in monogamous species. This is probably because benefits of engaging in EPCs
are lower and costs are higher than in socially monogamous
species. Thus, the female choice hypothesis best explains the
relationship between social mating systems and EPY among
passerine species; however, the male trade-off hypothesis may
apply within some species (see Figure 3; Dunn and Robertson,
1993; Soukup and Thompson, 1997).
Of course, other environmental and social factors, such as
We thank David F. Westneat for help with the phylogenetic contrast
analyses and James F. Dale, Mark E. Hauber, David F. Westneat, Ronald C. Ydenberg, and two anonymous referees for constructive comments on previous manuscript drafts. Our research was supported by
grants from the Swedish Council for Forestry and Agricultural Research (SJFR), the Fulbright Commission, the Swedish Institute, the
Crafoord Foundation, the U.S. National Science Foundation, and
Cornell University.
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