Behavioral Ecology Vol. 12 No. 5: 633-639
© 2001 International Society for Behavioral Ecology
Extrapair paternity is influenced by breeding synchrony and density in the common yellowthroat
Department of Biological Sciences, University of Wisconsin—Milwaukee, PO Box 413, Milwaukee, WI 53201, USA
Address correspondence to P. Dunn. E-mail: pdunn{at}uwm.edu .
Received 16 August 2000; revised 6 December 2000; accepted 19 January 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The effects of breeding synchrony and density on levels of extrapair paternity in birds are controversial. We used multilocus DNA fingerprinting and microsatellite analysis to examine the effects of breeding synchrony and density on levels of extrapair paternity in the common yellowthroat (Geothlypis trichas). As in many Neotropical migrants, breeding synchrony was greatest at the beginning of the breeding season. Levels of extrapair paternity were higher after the peak in synchrony, leading to an overall negative relationship between extrapair paternity and breeding synchrony. However, there was a significant interaction between breeding synchrony and density, as levels of extrapair paternity were higher only for males breeding when both synchrony and density were low. We discuss several possible explanations for this interaction, including lower quality males or territories in low density areas and greater demands on mate guarding among males with larger territories. Most studies have not considered simultaneously the effects of breeding synchrony and density on extrapair paternity. Our results suggest that ecological correlates of paternity may be revealed only after testing for interactions in multivariate analyses.
Key words: breeding ecology, DNA fingerprinting, Geothlypis trichas, microsatellites, paternity, sexual selection, warblers.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The temporal and spatial distribution of mates, or the resources necessary to acquire mates, is predicted to influence mating systems (Emlen and Oring, 1977
). For
example, if mates or critical resources for reproduction are clumped
spatially, then the potential for one sex (usually males) to monopolize mates
increases. As a result, the variance in male mating success increases, which
leads to a greater potential for polygyny and more intense sexual selection.
In contrast, Emlen and Oring
(1977) suggested that greater
synchrony of breeding should leave little opportunity for individual males to
monopolize multiple mates. They assumed that when females breed in unison,
males have little time to seek additional mates once they have found, courted,
and mated with their first mate. Thus, Emlen and Oring
(1977) predicted that increases
in the synchrony of breeding would decrease the potential for polygyny and the
intensity of sexual selection, while increases in the spatial clumping of
resources would have the opposite effect.
Several studies in a variety of taxa, including invertebrates
(Goshima et al., 1996), fish
(Grant et al., 1995), mammals
(Ims, 1988), and birds
(Robinson, 1986), have
supported the above predictions. However, few studies have simultaneously
examined how spatial and temporal clumping of mates or resources interact to
influence mating systems. Results often vary among studies, possibly due to
the interaction of these two factors. Indeed, breeding synchrony and its
effects on extrapair mating in birds may be an example.
Early applications of Emlen and Oring's
(1977) ideas to extrapair
mating in birds led to the prediction that extrapair fertilizations would be
related negatively to breeding synchrony
(Birkhead and Biggins, 1987;
Westneat et al., 1990). This
prediction assumed that males initiate extrapair copulations and that greater
breeding synchrony reduces the ability of males to gain extrapair mates.
Breeding synchrony may reduce the rate of extrapair copulations in a
population simply because the ratio of fertilizable females to sexually active
males (the operational sex ratio; Emlen and
Oring, 1977) is closer to unity, whereas in asynchronous
populations there are relatively more sexually active males than females at
any given time (Westneat et al.,
1990). The ability of males to gain extrapair mates may also be
reduced as a consequence of conflicting demands faced by males during peak
periods of mating. For example, mate guarding could conflict with the pursuit
of extrapair copulations (Birkhead and
Biggins, 1987), but other activities (e.g., territorial defense or
foraging) may also limit males. Recently, however, it has been argued that
there should be a positive relationship between extrapair paternity and
breeding synchrony (Stutchbury and Morton,
1995). In this case it is assumed that females initiate and
control extrapair copulations and that greater breeding synchrony facilitates
extrapair mate choice by females. Greater synchrony may increase
male—male competition for extrapair mates and make it easier for females
to compare the quality of potential extrapair mates.
The spatial distribution of mates may also influence the rate of encounter
between potential extrapair mates. For example, at greater breeding density,
potential mates may be more accessible to the opposite sex and, as a
consequence, individuals may incur lower energetic costs searching for
extrapair mates (Birkhead and
Møller, 1992; Westneat
et al., 1990). At the same time, however, greater density may
impose some costs. For example, males may face an increase in the risk of
paternity loss at their own nest, while females may be subject to more
harassment by extrapair males. Thus, the influence of breeding density and
synchrony on extrapair paternity is the potentially complex outcome of which
sex initiates and controls extrapair matings and of how density and synchrony
affect the net benefits of pursuing extrapair copulations
(Dunn et al., 1994;
Westneat and Gray, 1998).
Field studies have rarely examined both density and synchrony, yet in many
birds it is likely that both factors interact to influence the level of
extrapair mating. For example, these factors may act in opposition if greater
breeding density increases the opportunity for males to gain extrapair
matings, whereas greater breeding synchrony reduces the opportunity.
In this study, we examined the interaction of breeding density and
synchrony on the frequency of extrapair matings in a socially monogamous bird,
the common yellowthroat (Geothlypis trichas). The common yellowthroat
is a neotropical migratory warbler that is similar in many respects to other
warblers whose patterns of extrapair fertilization have been related to
breeding synchrony (Chuang et al.,
1999; Stutchbury et al.,
1997). However, contrary to previous studies, we show that
extrapair paternity is more common in the nests of males breeding at both low
density and low synchrony. We provide some possible explanations for these
unusual results and suggest that future studies test for an interaction
between breeding density and synchrony.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Common yellowthroats winter throughout Middle America and the southern United States and migrate north in the spring to breeding grounds throughout most of the United States and southern Canada. Male common yellowthroats arrive on the breeding ground approximately 3-7 days before the females and immediately begin defending territories. Females pair with a male within a day of arriving and begin building their first nest within a few days. During the nest-building period males follow their mate, although they will also intrude onto neighboring territories when females are fertile and engage in extrapair copulations (Hofslund, 1959
;
Stewart, 1953). Breeding is
relatively synchronous among first broods; however, later broods are less
synchronous because of renesting after failures and second clutches
(Guzy and Ritchison, 1999;
Hofslund, 1959). Over the 2
years of this study, 41% of nests failed, mostly from predation, and 31%
(11/35) of females attempted a second brood after successfully fledging young
from the first brood. Females nested on or within a half meter of the ground
and produced clutches of two to five eggs. Females built the nest and
incubated alone, but both parents fed nestlings and fledglings. We studied common yellowthroats in wetland habitats at the University of Wisconsin—Milwaukee Field Station in Saukville, Wisconsin, USA (43°23' N, 88°01' W). During the breeding seasons of 1998 and 1999 there were 30 and 29 territories, respectively, on the study area (5.4 ha). Territories were contiguous and, except for the east side of the study area, isolated from other occupied habitat by upland fields and forest. Territories occurred in swamp (wooded wetland) and marsh (sedge and cattail wetland) habitats that were interspersed throughout the study area.
We surveyed the study area daily to determine arrival dates of males and
the date they gained a mate; thus our estimates of arrival and pairing are
accurate to within a day. Locations of males were plotted on maps to the
nearest 5 m using a 22.9-m (25-yard) grid system throughout the study area.
Nests were located by following females building nests or by following both
parents feeding nestlings. Adult birds were caught in mist nets and marked
with a unique combination of three colored leg bands and a U.S. Fish and
Wildlife Service band. We took measurements of the wing chord, tail length,
and tarsus to the nearest 1.0 mm and body mass to the nearest 0.1 g. We
estimated adult condition by the residuals from the regression of residual
body mass (adjusted for date) on tarsus length. Males have a black facial mask
that is absent in females. We measured the size of this mask by recording each
side of a male's face with a video camera and then tracing the outline of the
mask in an image analysis program (NIH Image V1.44) after scaling the image
with a ruler (see Thusius et al. in press;
Yezerinac and Weatherhead,
1997a). For paternity analysis, we collected blood samples (20-50
µl) from the brachial vein of each adult and nestling and placed them in 1
ml of Queen's lysis buffer (Seutin et al.,
1991). We considered unbanded males on our study area to be
inexperienced breeders because they were often less than 1 year old based on
plumage characteristics (Pyle,
1997). Overall, we analyzed 41 families with data on both
paternity and synchrony (17 and 24 from 1998 and 1999, respectively); an
additional five families from the eastern edge of the study area were not
included because we could not determine the breeding synchrony of their
neighbors outside the study area.
Breeding density and synchrony
Most (23 of 27) extrapair sires resided within two territories of the
female with whom they obtained an extrapair fertilization (Thusius et al., in
press). Thus, we measured local breeding density as the number of male
territories (both mated and unmated) within 90 m of the center of a male's
territory, which is twice the average territory diameter. This estimate
included territories that fell only partially within the 90-m radius. We
estimated territory diameter from the average of the maximum length and width
of each territory. For simplicity, we present breeding density as the number
of territories within 90 m of the center of a male's territory. We used a
breeding synchrony index to determine the proportion of females on the study
area that were fertile on a given day
(Kempenaers, 1993). We
estimated synchrony at both the population level (population synchrony) using
all available nests and at the local level (local synchrony) using nests
within two territories of the focal female. We estimated local synchrony to
examine the possibility that extrapair mating is influenced more strongly by
interactions with close neighbors (Chuang
et al., 1999).
Parentage analyses
Multilocus DNA fingerprinting was used initially for the analysis of all
1998 samples (n = 94). In 1999, microsatellite primers from other
species (see below) were optimized and used for subsequent analyses
(n = 136 individuals). We extracted DNA from the blood of parents and
offspring by salt extraction (Miller et
al., 1988). Detailed methods are presented in Thusius et al.
(in press) and in Peterson et
al. (in press).
Briefly, for DNA fingerprinting, we produced autoradiographs by digesting
genomic DNA with HaeIII and probing Southern blots with the
minisatellite probes per (Shin et
al., 1985) and 33.15 (Jeffreys
et al., 1985). Using these autoradiographs, we excluded young as
the direct descendants of putative parents if they had (1) more than two novel
bands, and (2) a band-sharing coefficient < 0.436 with each parent (Thusius
et al., in press; see also Westneat,
1990). In this study, the probability of two novel fragments
arising from mutation was <0.0001, and the lower 99% one-tailed confidence
interval for band-sharing between parents and their direct descendants
(mothers and their unexcluded young) was 0.436
(Peterson et al., in
press).
For microsatellite analysis of paternity, we used primers from yellow
warblers (Dendroica petechia, Dpu01, Dpu16;
Dawson et al., 1997) and
black-throated blue warblers (Dendroica caerulescens, Dca24, Dca28;
Webster et al., 2001). In
addition to multilocus DNA fingerprinting, all 1998 birds (n = 94)
were analyzed at one, two, or three microsatellite loci to verify the
microsatellite techniques. All 1999 birds (n = 136) were analyzed at
all four microsatellite loci. Details of the microsatellite paternity analyses
are given in Peterson et al. (in
press). Briefly, young that possessed a microsatellite allele that
did not match the putative father at two or more loci were considered
extrapair young. If a mismatch occurred at only one locus (n = 14
young), we used multilocus DNA fingerprinting to confirm paternity. The total
probability of exclusion (Jamieson,
1994) at all four loci was 0.999. For each excluded nestling, we
calculated the probability of chance inclusion, which is based on the
frequency of each allele in the population
(Jeffreys et al., 1992). The
mean (±SD) of these probabilities was 0.00298 ± 0.00347
(n = 31, range = 2.0 x 10-4-0.0117). Thus, the
probability that we would not detect extrapair paternity when it occurred was
very low. The genotypes of all offspring matched those of their putative
mother, so we concluded that there was no intraspecific brood parasitism.
We examined both the proportion of extrapair young in a male's own nest and
the presence or absence of extrapair young in the nest, as these may reflect
different processes. For example, a single extrapair copulation may result in
single or multiple fertilizations, and thus low or high proportions of
extrapair young. We analyzed the proportion of extrapair young in a male's own
nest using generalized linear models (GLM) with binomial errors and logit
links (GLMStat; Beath 1997).
This analysis used the number of extrapair young as the dependent (response)
variable and the total number of young as the binomial denominator. The
significance of predictor variables was tested by the change in deviance of
the model with and without these predictors, using a chi-square approximation.
We analyzed the presence (yes/no) of extrapair young in the nest using
logistic regression (SAS Institute,
1995). Of the 41 nests used in the analysis of extrapair
paternity, 11 were second broods of the same pair in the same year (30% of 23
males bred in both years). We considered each nest to be an independent data
point because there was no relationship between the proportion of extrapair
young (r2 =.008, n = 11, p =.79) or the
population level of breeding synchrony (r2 =.16,
n = 11, p =.23) in first and second broods when we conducted
a pairwise analysis. Nevertheless, we repeated our analyses after excluding
either first or second broods to avoid psuedoreplication within years. Means
are presented ±SE unless indicated otherwise.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Over both years, 22% (30/139) of young in 49% (20/41) of broods were sired by extrapair males. The proportion of broods that contained at least one extrapair young was higher in 1999 (67%, 16/24) than in 1998 (24%, 4/17; Fisher's Exact test, p =.01). Similarly, the overall proportion of extrapair young tended to be higher in 1999 (27%, 23/85) than in 1998 (13%, 7/54; Fisher's Exact test, p =.06).
Overall population synchrony during the 1998 and 1999 breeding seasons was 29.3 and 21.7%, respectively, and did not differ between years (F1,39 = 1.77, p =.19). Population synchrony decreased significantly as the breeding season progressed (both years, p <.001; Figure 1). Overall, mean breeding density was 5.9 ± 0.4 males within 90 m (range 2-10), and it did not differ between 1998 (5.9 ± 0.6) and 1999 (5.9 ± 0.5; t39 = 0.01, p =.99). However, breeding density was greater in swamp (6.7 ± 0.6 males) than in marsh (4.2 ± 0.5) habitats (t28 = 3.3, p = 0.003).
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= 1000); the line in the bottom panel is from a regression.
Numbers in circles indicate the number of overlapping data points. Sample size
was 41 nests in both panels.
In bivariate analyses, the proportion of extrapair young in the population
was smaller when population synchrony was greater (GLM,
21 = 10.8, p =.001;
Figure 1). Similarly, broods
were less likely to contain extrapair young as population synchrony increased
(logistic regression, 21 = 6.6, p =.01).
In contrast, breeding density was not related to the proportion (GLM,
21 = 0.5, p =.47) or presence of extrapair
young (logistic regression, 21 = 0.1, p
=.73) in bivariate analyses.
To control for correlations between variables, we performed multivariate analyses of extrapair paternity. We started with a general linear model containing the following predictors: year, laying date, habitat type (swamp or marsh), population and local synchrony, breeding density, breeding experience, and the interactions between both types of synchrony and breeding density and habitat type (Model I, Table 1). We included these interactions because synchrony and density may have different effects on paternity, and density varies with habitat type. Laying date was included to control for seasonal effects; adding brood number (first or second) to the model did not change the results qualitatively. Of the predictors above, only population and local breeding synchrony, breeding density, and their interactions approached significance (Table 1; overall model deviance = 26.7, df = 11, p =.005). To simplify our model, we excluded breeding experience, habitat type, and laying date. This smaller model revealed a nearly significant effect of year (p =.062) and significant interactions between both types of synchrony and density (model deviance = 23.0, df = 6, p <.001). These interactions were stronger for population (p =.006) than local (p =.07) synchrony, and local synchrony was correlated with population synchrony (r2 =.32, F1,39 = 18.1, p <.0001), so next we excluded local synchrony from the model. This reduced model (Model II, Table 1) indicated that extrapair paternity was influenced by year (p =.05), population synchrony (p =.003), breeding density (p =.03), and the interaction between population synchrony and density (p =.03, Table 1; overall model deviance = 19.3, df = 4, p <.001). Habitat type was not a better predictor of extrapair paternity than breeding density, as habitat type was not significant (p = 0.08) when we replaced breeding density with habitat type in this reduced model.
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To avoid pseudoreplication within years, we reanalyzed the reduced model (Model II, Table 1) using each male only once in a given year. We did this two ways: (1) using single broods and only the first brood of males with two broods (n = 30), and (2) using single broods and only the second brood of males with two broods (n = 30). The results of our analysis of single and first broods differed from the previous model including all broods (Model II, Table 1). Here only population synchrony and year were significant predictors. However, when we used single and second broods in the analysis, the results were qualitatively similar to the model including all broods (Model II, Table 1). Thus, the interaction between density and synchrony was due to a seasonal effect, as second broods were later in the season when synchrony was lower and extrapair paternity greater (Figure 1).
To better understand this interaction between synchrony and density, we
divided males into low and high density groups based on the mean breeding
density (6 males within 90 m). In the low-density group (2-6 males within 90
m, n = 23), the proportion of extrapair young decreased as population
synchrony increased (GLM, 21 = 8.5, p
=.004). In contrast, in the high-density group (7-10 males, n = 18),
there was no relationship between the proportion of extrapair young in a
male's nest and population synchrony (GLM, 21 =
2.3, p =.12). This interaction was most pronounced among the lowest
density males (2-3 males) when we divided the data into low-, medium- (4-6
males), and high-density (7-10 males) groups
(Figure 2). At low levels of
synchrony, which occurred late in the season, males in the medium- and
high-density groups had a lower proportion of extrapair young in their nest
than males in the low-density group (Figure
2).
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Based on these results, we examined several male characteristics to investigate whether males in lower density areas were poorer quality. There were tendencies for males in lower density areas to pair with a mate later in the season (p =.07) and to have shorter tarsi (p =.09, Table 2). However, there was no relationship between breeding density and male body condition, size of the male's facial mask, or date of arrival on the breeding grounds (Table 2). Males with breeding experience (5.7 ± 0.6 males, n = 20) and those without experience (6.0 ± 0.5, n = 21) also did not differ in breeding density (t39 = 0.5, p =.65). Thus, there was little evidence that males in low-density areas were poorer quality or less experienced breeders, although the power of these analyses was low (Table 2).
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Finally, we analyzed the presence or absence of extrapair young in a male's own nest using logistic regression. As above, we began with a complete model that included the following predictors: year, laying date, habitat type, population and local synchrony, breeding density, breeding experience, and the interactions between both types of synchrony and breeding density and habitat type (Model, I, Table 1). Population synchrony and its interaction with breeding density were the strongest predictors of extrapair paternity (Table 1). These variables remained significant predictors after we removed laying date, breeding experience, habitat type, and local synchrony from the initial model (Model II, Table 1). As before, we reanalyzed this reduced model after excluding either first or second broods to avoid pseudoreplication within years. This analysis revealed the same pattern of seasonal interaction as described above for the proportion of extrapair young. Thus, both presence of extrapair young and the proportion of extrapair young per nest were influenced by year, population-wide breeding synchrony, breeding density, and the interaction between synchrony and density.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In common yellowthroats, breeding was most synchronous at the beginning of the season, whereas extrapair paternity was greatest later in the season when breeding synchrony was low. Breeding synchrony declined over the season as a consequence of nest loss (41 % of nests), which occurred mostly from predation. Overall, we found a negative relationship between extrapair paternity and breeding synchrony. However, upon closer inspection, the negative relationship between extrapair paternity and synchrony depended on breeding density. The negative relationship was stronger for males breeding at low than at high density (Figure 2). Below we present some possible explanations for these results, and we suggest that similar interactions between density and synchrony may be important in understanding mating systems in other species.
A negative relationship may occur between extrapair paternity and breeding
synchrony if greater synchrony limits the ability of males to seek extrapair
fertilizations (Birkhead and Møller,
1992). This may occur if most males in the population are mate
guarding when breeding synchrony is high and mate guarding conflicts with
seeking extrapair fertilizations. We do not have quantitative data on mate
guarding in common yellowthroats, as the birds tended to stay in dense grass
and sedge cover <1 m above the ground. Nevertheless, males appeared to
follow their mates during the females' fertile period
(Stewart, 1953; Thusius et
al., personal observations). Thus, early in the season, when breeding
synchrony was highest, males may have had less time to seek extrapair
fertilizations. Another possibility is that fewer females were seeking (or
accepting) extrapair copulations early in the season because the net benefits
of extrapair mating were greater later in the season. For example, it may be
easier for females to gain extrapair copulations later in the season if their
mates are caring for fledglings from an earlier nest and, as a consequence,
are not guarding their fertile mates as closely. However, neither of these
explanations is complete, as they do not explain why low density males had
more extrapair young in their nest when synchrony was low.
To explain the density effect, we may also need to incorporate aspects of
the habitat or male quality. For example, it has been suggested that females
pairing later in the season are more likely to nest with poor quality mates or
in poor quality habitats, and, as a consequence, they should be more likely to
engage in extrapair copulations
(Møller, 1992).
Following this rationale, female common yellowthroats breeding at low density
and synchrony may have been in poorer breeding situations, and, as a
consequence, they may have solicited extrapair copulations to compensate for
the poorer quality of their mate or habitat. There is some evidence to support
this hypothesis, as we found a trend for males in low-density areas to gain a
mate later in the season (p =.09;
Table 2). Although no other
correlates of male quality were related to breeding density, the power of
these analyses was low (Table
2), so additional data are needed to examine this hypothesis.
Another hypothesis is that later in the season, males in low-density areas
are unable to guard their mates as well as males in high-density areas. This
could occur as a consequence of their larger territories or differences in
habitats combined with greater pursuit of extrapair copulations later in the
season. Habitat type was associated with density, but it was not a better
predictor of paternity in multivariate analyses. This suggests that density
per se, rather than habitat type, influenced levels of extrapair paternity in
this study. However, the ecological and behavioral factors that influence
breeding density are unknown, so it would be premature to rule out the
influence of habitat on paternity in common yellowthroats. Males breeding at
low density and synchrony may also have had other demands that conflicted with
mate guarding, such as parental care of fledglings from the first nest while
the female started a second nest (see also
Weatherhead and McRae, 1990).
As this was a correlational study, we cannot distinguish between these and
other potential hypotheses until we known more about the effectiveness of mate
guarding, which sex initiates extrapair copulations, and how the pursuit of
extrapair copulation varies with time of season, habitat, and male
quality.
Other studies have also found a negative relationship between extrapair
paternity and breeding synchrony. In great tits (Parus major,
Strohbach et al., 1998), snow
geese (Anser caerulescens; Dunn et
al., 1999), and barn swallows
(Saino et al., 1999),
extrapair paternity was related negatively to breeding synchrony. However,
several other studies have found no relationship between extrapair paternity
and breeding synchrony (Dunn et al.,
1994; Kempenaers,
1997; Perreault et al.,
1997; Weatherhead,
1997; Westneat and Gray,
1998). In contrast, a positive relationship between extrapair
paternity and breeding synchrony has been found in hooded warblers
(Wilsonia citrina; Stutchbury et
al., 1997) and in a comparison of two populations of willow
warblers (Phylloscopus trochilus,
Bjørnstad and Lifjeld,
1997). Comparative evidence also suggests a positive relationship
between the percentage of broods with extrapair young and breeding synchrony
(Stutchbury,
1998a,b),
but the interpretation of these data is controversial
(Weatherhead and Yezerinac,
1998).
Extrapair paternity has now been studied in a number of warbler species,
but even within this group, the effects of breeding synchrony on extrapair
paternity are mixed. In hooded warblers there was a positive relationship
between extrapair paternity and breeding synchrony
(Stutchbury et al., 1997).
Synchrony among neighboring birds (local synchrony) was also related
positively to extrapair paternity in black-throated blue warblers
(Chuang et al., 1999). However,
Chuang et al. (1999) found the
opposite trend (p =.06) when they examined synchrony at the
population level, similar to common yellowthroats. Both common yellowthroats
and black-throated blue warblers tended to have more extrapair fertilizations
later in the season, whereas extrapair fertilizations were more common early
in the season in hooded warblers. In American redstarts
(Perreault et al., 1997) and
yellow warblers (Yezerinac and
Weatherhead, 1997b) there was no relationship between breeding
synchrony and extrapair paternity within populations; however, in a comparison
of two populations of yellow warblers, the more synchronous, and also less
dense, population had a lower level of extrapair paternity
(Yezerinac et al., 1999).
Thus, even within the same family of birds, some studies have failed to find a
correlation between extrapair paternity and breeding synchrony, while other
studies have found positive or negative relationships.
Some of the variation among studies of breeding synchrony may be caused by the confounding effects of breeding density or habitat. In our study breeding density was not related to extrapair paternity in bivariate analyses (Table 2), but there was a significant interaction between density and synchrony when we conducted multivariate analyses (Figure 2, Table 1). Although several studies have examined the effects of both breeding density and synchrony on levels of extrapair paternity, they have generally conducted bivariate analyses and have not tested simultaneously for the effects of breeding density, synchrony, and their interaction. Our study indicates that multivariate analyses may be necessary to avoid incorrect conclusions. The same caution applies to comparative analyses, which are subject to the same confounding effects as intraspecific studies.
In summary, we found a negative relationship between extrapair paternity and breeding synchrony in common yellowthroats; however, this relationship only held for males with few neighbors (low density). Stated another way, extrapair paternity was more common in the nests of males breeding at low density, but this was only true when breeding was less synchronous. At present, we do not know why low breeding synchrony and density both favor higher levels of extrapair paternity. Nevertheless, our results indicate the need to analyze density and synchrony simultaneously. Future research that examines which sex initiates and controls extrapair copulations may help to explain these results, as well as the conflicting results of other studies.
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ACKNOWLEDGEMENTS |
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We thank Lisa Belli, Nicole Poirier, Mary Stapleton, Jocelyn Tank, Stacy Valkenaar, and the staff at the University of Wisconsin—Milwaukee Field Station for help in the field. We are also grateful to Jan Lifjeld, Bridget Stutchbury, Dave Westneat, and an anonymous reviewer for helpful comments on the manuscript and to H. Lisle Gibbs, Erica Leder, Mike Webster, and Chuck Wimpee for helpful advice on microsatellites. Mike Webster generously provided unpublished microsatellite primers for black-throated blue warblers. This work was conducted under UWM Animal Care and Use Committee permit 98-99#26. Funding was provided by the Wisconsin Society for Ornithology, the Animal Behaviour Society, Sigma Xi Grants-in-Aid of Research, and the James D. Anthony and Ruth Walker Scholarship Funds at University of Wisconsin—Milwaukee.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Beath KJ, 1997. GLMstat user manual, version 3.1. Available on the World Wide Web at: www.ozemail.com.au/
kjbeath/glmstat.html. Accessed 9
September 1998.Birkhead TR, Biggins JD, 1987. Reproductive synchrony and extrapair copulation in birds. Ethology 74: 320-334.[Web of Science]
Birkhead TR, Møller AP, 1992. Sperm competition in birds. Evolutionary causes and consequences. London: Academic Press.
Bjørnstad G, Lifjeld JT, 1997. High frequency of extra-pair paternity in a dense and synchronous population of willow warblers Phylloscopus trochilus. J Avian Biol 28: 319-324.
Chuang HC, MS Webster, Holmes RT, 1999. Extrapair paternity and local synchrony in the black-throated blue warbler. Auk 116: 726-736.[Web of Science]
Dawson RJG, Gibbs HL, Yezerinac SM, 1997. Isolation of microsatellite DNA markers from a passerine bird, Dendroica petechia (the yellow warbler), and their use in population studies. Heredity 79: 506-512.
Dunn PO, Afton AD, Gloutney ML, Alisaukas RT, 1999. Forced copulation results in few extrapair fertilizations in Ross's and lesser snow geese. Anim Behav 57: 1071-1081.[Web of Science][Medline]
Dunn PO, Whittingham LA, Lifjeld JT, Robertson RJ, Boag PT,
1994. Effects of breeding density, synchrony, and experience on
extrapair paternity in tree swallows. Behav Ecol
5: 123-129.
Emlen ST, Oring LW, 1977. Ecology, sexual selection,
and the evolution of mating systems. Science
197: 215-223.
Goshima S, Tsunenori K, Minoru M, 1996. Mate acceptance and guarding by male fiddler crabs Uca tetragonon (Herbst). J Exp Mar Biol Ecol 196: 131-143.
Grant JWA, Bryant MJ, Soos CE, 1995. Operational sex ratio, mediated by synchrony of female arrival, alters the variance of male mating success in Japanese medaka. Anim Behav 49: 367-375.
Guzy MJ, Ritchison G, 1999. Common yellowthroat (Geothlypis trichas). In: The birds of North America, no. 448 (Poole A, Gill F, eds). Philadelphia: The Birds of North America.
Hofslund PB, 1959. A life history study of the yellowthroat, Geothlypis trichas. Proc Minn Acad Sci 27: 144-174.
Ims RA, 1988. Spatial clumping of sexually receptive females induces space sharing among male voles. Nature 335: 541-543.[Medline]
Jamieson A, 1994. The effectiveness of using co-dominant polymorphic allelic series for (1) checking pedigrees and (2) distinguishing full-sib pair members. Anim Genetics 25: 37-44.
Jeffreys AJ, Allen M, Hagelberg E, Sonnberg A, 1992. Identification of the skeletal remains of Josef Mengele by DNA analysis. Forensic Sci Inter 56: 65-76.[Web of Science][Medline]
Jeffreys AJ, Wilson V, Thein SL, 1985. Hypervariable `minisatellite' regions in human DNA. Nature 314: 67-73.[Medline]
Kempenaers B, 1993. The use of a breeding synchrony index. Ornis Scand 24: 84.
Kempenaers B, 1997. Does reproductive synchrony limit male opportunities or enhance females choice for extra-pair paternity? Behaviour 134: 551-562.[Web of Science]
Miller S, Dykes D, Polesky H, 1988. A simple salting
out procedure for extracting DNA from human nucleated cells. Nucleic
Acids Res 16:
1215.
Møller AP, 1992. Frequency of female copulations with multiple males and sexual selection. Am Nat 139: 1089-1101.[Web of Science]
Perreault S, Lemon RE, Kuhnlein U, 1997. Patterns and
correlates of extrapair paternity in American redstarts (Setophaga
ruticilla). Behav Ecol 8:
612-621.
Peterson K, Thusius K, Whittingham LA, Dunn PO, in press. Allocation of male parental care in relation to paternity within and among broods of common yellowthroats. Ethology.
Pyle P, 1997. Identification guide to North American birds, Part I. Bolinas, California: Slate Creek Press.
Robinson S, 1986. The evolution of social behavior and mating systems in the blackbirds. (Icterinae). In: Ecological aspects of social evolution (Rubenstein D, Wrangham RW, eds). Princeton, New Jersey: Princeton University Press; 175-200.
Saino N, Primmer C, Ellegren H, Møller AP, 1999. Breeding synchrony and paternity in the barn swallow (Hirundo rustica). Behav Ecol Sociobiol 45: 211-218.[Web of Science]
SAS Institute, 1995. JMP statistics and graphics guide, version 3.1. Cary, North Carolina: SAS Institute, Inc.
Seutin G, White BN, Boag PT, 1991. Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69: 82-90.[Web of Science]
Shin H-S, Bargiello TA, Clark BT, Jackson FR, Young MW, 1985. An unusual coding sequence from a Drosophila clock gene is conserved in vertebrates. Nature 317: 445-448.[Medline]
Stewart RE, 1953. A life history study of the yellowthroat. Wilson Bull 65: 99-115.
Strohbach S, Curio E, Lubjuhn T, 1998. Extrapair
paternity in the great tit (Parus major): a test of the good genes
hypothesis. Behav Ecol 9:
388-396.
Stutchbury BJM, 1998a. Breeding synchrony best explains variation in extra-pair mating system among avian species. Behav Ecol Sociobiol 43: 221-222.[Web of Science]
Stutchbury BJM, 1998b. Female mate choice of extra-pair males: breeding synchrony is important. Behav Ecol Sociobiol 43: 213-215.[Web of Science]
Stutchbury BJM, Morton ES, 1995. The effect of breeding synchrony on extra-pair mating systems in songbirds. Behaviour 132: 675-690.[Web of Science]
Stutchbury BJM, Piper WH, Neudorf DL, Tarof SA, Rhymer JM, Fuller G, Fleischer RC, 1997. Correlates of extra-pair fertilization success in hooded warblers. Behav Ecol Sociobiol 40: 119-126.
Thusius KJ, Peterson KA, Dunn PO, Whittingham LA, in press. Male mask size is correlated with mating success in the common yellow-throat. Anim Behav.
Weatherhead PJ, 1997. Breeding synchrony and extra-pair mating in red-winged blackbirds. Behav Ecol Sociobiol 40: 151-158.
Weatherhead PJ, McRae SB, 1990. Brood care in American robins: Implications for mixed reproductive strategies by females. Anim Behav 39: 1179-1188.
Weatherhead PJ, Yezerinac SM, 1998. Breeding synchrony and extra-pair mating in birds. Behav Ecol Sociobiol 43: 217-219.[Web of Science]
Webster MS, Chuang-Dobbs HC, Holmes RT, 2001.
Microsatellite identification of extra-pair sires in a socially monogamous
warbler. Behav Ecol 12:
439-446.
Westneat DF, 1990. Genetic parentage in the indigo bunting: a study using DNA fingerprinting. Behav Ecol Sociobiol 27: 67-76.
Westneat DF, Gray EM, 1998. Breeding synchrony and
extrapair fertilizations in two populations of red-winged blackbirds.
Behav Ecol 9:
456-464.
Westneat DF, Noon WA, Reeve HK, Aquadro CF, 1988.
Improved hybridization conditions for DNA `fingerprints' probed with M13.
Nucleic Acids Res 16:
4161.
Westneat DF, Sherman PW, Morton ML, 1990. The ecology and evolution of extra-pair copulations in birds. Curr Ornithol 7: 331-369.
Yezerinac SM, Gibbs HL, Montgomerie R, 1999. Extrapair paternity in a far northern population of yellow warblers Dendroica petechia. J Avian Biol 30: 234-237.
Yezerinac SM, Weatherhead PJ, 1997a. Extra-pair
mating, male plumage coloration and sexual selection in yellow warblers
(Dendroica petechia). Proc R Soc Lond B
264: 527-532.
Yezerinac SM, Weatherhead PJ, 1997b. Reproductive synchrony and extra-pair mating strategy in a socially monogamous bird, Dendroica petechia. Anim Behav 54: 1393-1403.[Web of Science][Medline]
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