Behavioral Ecology Vol. 12 No. 4: 457-466
© 2001 International Society for Behavioral Ecology
Social mating systems and extrapair fertilizations in passerine birds
Department of Neurobiology and Behavior, Seeley G. Mudd Hall, Cornell University, Ithaca, NY 14853-2702, USA
Address correspondence to D. Hasselquist, who is now at the Department of Animal Ecology, Lund University, Ecology Building, 223 62 Lund, Sweden. E-mail: dennis.hasselquist{at}zooekol.lu.se .
Received 4 April 2000; revised 3 October 2000; accepted 15 October 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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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.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Recently 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 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,
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
high-quality 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.
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METHODS |
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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
fly-catcher 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 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).
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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).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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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 accepting 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.
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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.
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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).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In all our analyses, frequencies of extrapair young were significantly higher in socially monogamous than polygynous passerine species (Figures 2,3,4). 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 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;
Kempenaers 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 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 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 adjustments 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).
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 pair-bonded 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 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.
|
ACKNOWLEDGEMENTS |
|---|
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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