Behavioral Ecology Vol. 12 No. 4: 439-446
© 2001 International Society for Behavioral Ecology
Microsatellite identification of extrapair sires in a socially monogamous warbler
a Department of Biological Sciences, The University at Buffalo, 109 Cooke Hall, Buffalo, NY 14260, USA b Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA
Address correspondence to M. S. Webster, who is now at the School of Biological Sciences, Washington State University, P.O. Box 644236, Pullman, WA 99164-4236, USA. E-mail: mwebster{at}wsu.edu . H. C. Chuang-Dobbs is now at the Biology Department, Southern Utah University, Cedar City, UT 84720, USA.
Received 10 January 2000; revised 22 September 2000; accepted 8 October 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Few studies of avian mating systems have identified the sires of extrapair young, and hence it has been difficult to determine the scale at which reproductive interactions occur. For instance, females may be free to copulate with any male in the population (a "global" scale of interactions), or females may be restricted to copulating only with males on neighboring territories (a "local" scale). The scale of such interactions has important consequences for an understanding of the evolutionary causes and consequences of extrapair fertilizations. We used five hypervariable microsatellite loci and multilocus DNA fingerprinting to examine parentage of more than 400 nestling black-throated blue warblers (Dendroica caerulescens). Extrapair fertilizations were common, and the microsatellite markers allowed us to identify the sires for 89% of the young analyzed. Most identified extrapair sires were males on neighboring or nearby territories, and most nestlings for whom we could not identify a sire came from territories at the edge of the study plot. Thus, reproductive interactions appear to be more local than global in this population. Extrapair fertilizations contributed significantly to total variation in male reproductive success. However, the standardized variance in male reproductive success (0.68-0.74) was not substantially greater than that for females (0.53-0.60), and the contribution of extrapair fertilizations (9-14%) was much lower than the contribution of within-pair fertilizations (75-77%). This suggests that the local scale of reproductive interactions may limit variation in male reproductive success and hence the opportunity for selection.
Key words: black-throated blue warbler, Dendroica caerulescens, extrapair fertilization, microsatellites, opportunity for selection, socially monogamous mating systems.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Due to the large number of DNA fingerprinting studies conducted during the past 15 years (Westneat and Webster, 1994
), it is now clear that social monogamy does not imply genetic
monogamy: in many birds, females often copulate with males other than their
social partners. As a consequence, extrapair fertilizations (EPF) are a common
and widespread feature of avian mating systems. Now that this fact is firmly
established, attention has turned to identifying the social, genetic, and
ecological factors that may promote or hinder extrapair mating (e.g.,
Hoi-Leitner et al., 1999;
Johnsen et al., 1998;
Petrie et al., 1998;
Westneat and Gray, 1998), and
to the selective consequences of extrapair mating (reviewed in
Møller and Ninni,
1998).
An understanding of the causes and consequences of extrapair mating depends
critically on the scale at which extrapair interactions occur. For example, if
females of a territorial species interact and copulate only with males on
neighboring territories (a "local" scale of interaction), the
variance in male mating success and intensity of sexual selection generated by
EPF (Webster et al., 1995) are
likely to be relatively low. In contrast, if copulations can occur between
individuals from territories that are widely separated (a "global"
scale of interaction), then a very small number of males could potentially
monopolize mating success (e.g., Dunn and
Cockburn, 1998) and traits affecting the ability to obtain or
prevent EPF could be subject to very strong selection. Similarly, breeding
synchrony has been suggested as a factor having a strong influence on EPF
frequency (Stutchbury, 1998;
Stutchbury and Morton, 1995),
but it is not clear at what scale such synchrony should be measured: the
synchrony among all females in the population, or the synchrony only among
females on adjacent territories (Chuang et
al., 1999)?
The scale at which extrapair interactions occur can be determined by
identifying the sires of extrapair young: if local interactions are important,
then sires will come primarily from territories adjacent to the female's own.
Although some multilocus DNA fingerprinting studies have successfully
identified a number of extrapair sires
(Hasselquist et al., 1995;
Stutchbury et al., 1997;
Westneat, 1993;
Yezerinac et al., 1995), this
approach is laborious and the sires of many young are often not identified.
This is because it is difficult to compare each nestling to a large number of
potential sires using multilocus blotting techniques
(Webster and Westneat, 1998;
Westneat and Webster, 1994).
Single-locus markers, such as microsatellites, are much more powerful in
identifying extrapair sires, because each individual's genotype can be
catalogued and compared to all others
(Ellegren, 1992;
Primmer et al., 1995).
We have studied the social and genetic mating system of a population of a
migratory songbird, the black-throated blue warbler (Dendroica
caerulescens), breeding in New Hampshire, USA. Our multilocus DNA
fingerprinting studies (Chuang et al.,
1999) have shown that EPF are common in this population and that
the frequency of extrapair young is affected by local breeding synchrony
(i.e., the synchrony among females on adjacent territories) but not by
population breeding synchrony. This suggests that females interact and
copulate with males on nearby territories, but not with males from distant
territories. In this article we employ microsatellite markers to identify the
sires of extrapair young and directly test the importance of local
interactions. We used microsatellites to examine the parentage of 342
nestlings sampled from 97 broods (five to 28 females per season, 60 females
total) during the 1995-1998 breeding seasons, and verify the ability of
microsatellites to identify cases of EPF by comparison to results of our
earlier DNA fingerprinting analyses. Using the combined microsatellite and
multilocus results (413 nestlings from 117 broods), we describe general
patterns of EPF across the 4 years of this study, determine the locations of
extrapair sires relative to the young that they sire, and estimate the effects
of EPF on variance in male reproductive success. Finally, to determine whether
particular male traits affect a male's ability to obtain EPF, we present
preliminary comparisons of morphological traits of extrapair sires to traits
of the males that they cuckold.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Field methods
We monitored breeding on a 100 ha study plot at the Hubbard Brook Experimental Forest, West Thornton, New Hampshire, USA (see Holmes et al., 1992
) during
the years 1995 to 1998. All adults breeding on this plot (e.g., n =
75 in 1998) were color-banded for individual identification. At the time of
banding we measured the adults (tarsus and wing length, wing spot size,
measured from coverts to distal tip, and mass) and collected a small (ca. 20
µl) blood sample for genetic analyses. We also collected blood samples from
other adults captured incidentally near the main study plot each year. We
determined territory boundaries by mapping aggressive interactions among
males, as well as male singing behavior, and we found all warbler nests built
on these territories. We also recorded instances when we encountered an
individual outside of the area considered to be its territory. Each nest was
visited approximately once every 3 days. When nestlings reached 6 days of age, we banded them and collected a blood sample. We considered sampling young at an earlier age to be too risky. Therefore, our methods allow an estimate of the number of extrapair young that survive to fledging (about age 8-10 days; Holmes, 1994), rather than an estimate of the number of eggs fertilized by extrapair males. The mean ± SD brood size of sampled nests was 3.59 ± 0.73 (range 1 to 5), and we sampled 3.41 ± 0.84 nestlings per brood (range 1 to 5); the difference between these two figures was due to partial brood loss between hatching and day six (n = 16 nests). An additional 109 nests received eggs but were not sampled (97 failed, mostly due to predation, and 12 fledged before the young could be sampled).
Microsatellite methods
We used variation at five microsatellite loci to determine paternity of
nestlings (Table 1). Two of
these loci, Dpµ 01 and Dpµ 16, were isolated from the
genome of the yellow warbler (D. petechia) by Dawson et al.
(1997). The remaining three
loci, Dca 24, Dca 28, and Dca 32, were isolated from a
D. caerulescens genomic library enriched for simple sequence repeats
following the method of Hammond et al.
(1998).
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We determined the microsatellite genotypes of all adults and nestlings
captured on the study plot during the 1997 and 1998 breeding seasons.
Parentage had already been analyzed by multilocus DNA fingerprinting for the
1995 and 1996 family groups (Chuang et al.,
1999). In addition, we determined the microsatellite genotypes of
all males sampled in 1995 and 1996 as well as females and nestlings from most
(15 of 17) 1995 and 1996 family groups that showed mixed parentage in the
earlier study.
To score individual genotypes, we amplified genomic DNA from each
individual in a 10 µl PCR reaction that contained 100 µM dNTP (each),
0.25 µM primers (each), 1.5 µCi 33-P dATP (NENTM Life Science
Products), and our standard PCR reaction mix (1-3 units Taq DNA
polymerase, 3.0 mM MgCl2, 50 mM KCl, 10 mM Tris-HCl). This reaction
was subjected to 30 cycles of 94°C for 60 s, X°C for 60 s,
and 72°C for 45 s, where the annealing temperature (X) depended
on the primers used (Table 1).
PCR products were size-sorted via electrophoresis in a 6% denaturing
polyacrylamide gel containing 7 M urea at a constant temperature of 50°C
(see Strassmann et al., 1996).
We also ran a standard sequencing reaction of M13 DNA (also labeled with 33-P
dATP) as a size reference for each set of PCR reactions run on a gel. After
electrophoresis, the gel was dried and exposed to autoradiography film for 2-4
days.
We scored the size of PCR fragments for each individual by comparing its
band(s) to the reference M13 sequence. We calculated the frequency of each
allele (xi) from the total population of adults genotyped
(
xi = 1.00), and calculated the expected frequency
of heterozygotes (he) as:
 | (1) |
):
 | (2) |
Determination of parentage
In our previous DNA fingerprinting analyses
(Chuang et al., 1999), all 125
nestlings sampled (from 38 broods) showed high band-sharing with their social
mothers, indicating that intraspecific brood parasitism is rare in this
population. Therefore, for each nestling we assumed the social mother was the
biological mother, and used the microsatellite genotypes to identify the sire:
potential sires were the male or males who possessed the nestling's
nonmaternal allele at each locus. Thus, a female "matched" a
nestling at a particular locus if she possessed either of the nestling's
alleles, and a male "matched" the offspring if he possessed the
nestling's remaining nonmaternal allele.
We calculated the average probability of paternal exclusion
(Pej) for each polymorphic locus. This is the probability,
averaged over all alleles at the jth locus, that a randomly chosen
nonsire male will not possess the paternal allele found in an
offspring (i.e., will not match), given that the mother of the offspring is
known with certainty. This probability can be estimated as
(Jamieson, 1994):
 | (3) |
 | (4) |
We calculated the standardized variance (total variance divided by mean
squared, see Arnold and Wade,
1984) in female and male reproductive success. For males, we
calculated the standardized variance of both apparent reproductive success
(A), defined as the number of young produced on a male's territory,
and genetic reproductive success (T), defined as the number of young
sired. Following Webster et al.
(1995), we also broke down
male genetic reproductive success into three component parts:
 | (5) |
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Analyses of parentage
All five microsatellites used in this study proved highly variable, with 11 to 30 alleles, high levels of observed heterozygosity, and high probabilities of exclusion (Table 2). The combined probability that a nonsire would not match the paternal alleles of a nestling at all five loci was Pet
0.9998, and we were
able to identify extrapair young and their sires with high confidence. Two
loci, Dpµ 01 and Dca 24, showed a significant deficiency
of heterozygotes, suggesting a relatively high frequency of null alleles at
these loci (Table 2). This is
unlikely to have biased our results, as we accounted for possible null alleles
when scoring these loci (see Methods), and the total probability of exclusion
was high even when either locus was excluded (Pet
0.9985).
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Nestlings sampled during the 1995 and 1996 breeding seasons had been
previously analyzed by multilocus DNA fingerprinting
(Chuang et al., 1999). We
determined the microsatellite genotypes for 56 of these nestlings in the
present study. As expected, 55 of these nestlings matched their social mothers
at all five loci (the single exception was a nestling that matched at four of
five loci), regardless of whether DNA fingerprinting analyses indicated the
nestling was produced by EPF or not (Figure
1a,b). Similarly, of the 23 nestlings that matched their social
fathers in the DNA fingerprinting analyses, 20 matched their social fathers at
all five microsatellite loci and one matched at four of five loci
(Figure 1a). The remaining two
nestlings did not match their sires at three and four of the loci,
respectively. Both of these nestlings were "borderline" in the
fingerprinting analyses, in that each showed relatively high sharing with the
social male ( 50%) but had two novel fragments (nestlings showing three or
more novel fragments were considered to have resulted from EPF in the earlier
study). Of the 33 nestlings that did not match their sires in the DNA
fingerprinting analyses, 31 were mismatched at two or more microsatellite loci
(Figure 1b). The remaining two
nestlings matched their social fathers at four and five loci, respectively.
Thus, multilocus and microsatellite analyses agree with each other in large
part, but with a small number of discrepancies (see Discussion). These results
support the assumption that intraspecific brood parasitism is rare in this
population (but see next paragraph), and that most cases of microsatellite
mismatches between nestlings and their social parents will be due to extrapair
fertilizations.
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We determined the microsatellite genotypes of all individuals sampled during the 1997 and 1998 breeding seasons, and compared the genotypes of nestlings to those of their social parents (Figure 1c). In the vast majority (97.2%) of comparisons between nestlings and their presumed mothers (n = 283), the nestling matched the female (i.e., had an allele that matched one of the alleles present in the female) at all loci (Figure 1c). In an additional six cases the nestling matched its presumed mother at all but one locus. Five of these six cases (four from a single nest) were at locus Dca 28, and were situations in which both the female and nestling appeared homozygous for different alleles. This suggests that a null allele may have existed at this locus, although its frequency would have been very low (Table 2) and so would be unlikely to affect our analyses. The remaining case of a single mismatch likely represents a case of mutation or laboratory artifact. However, one nestling did not match its social mother at three loci, and another did not match at five loci. Both of these nestlings were from the same nest, and the other two nestlings from this nest did match the female at all loci. This suggests that a very low level of intraspecific brood parasitism may exist in this population, although the possibility of mislabeled samples cannot be ruled out. Even if present, a low level of parasitism is unlikely to affect the results given below.
Comparisons between the 1997 and 1998 nestlings and their social fathers (n = 280) yielded a somewhat different pattern (Figure 1c). In many comparisons the nestling matched its social father at all five loci (n = 216) or at four of the five loci (n = 3). In 61 comparisons, however, the nestling and its social sire were mismatched at two or more loci; two of these also matched poorly with the social mother (see above), where the remaining 59 represent cases of extrapair fertilization. At two additional nests (six nestlings total) we had a DNA sample for the nestlings and social father, but no sample for the social mother; in all six cases the male possessed an allele found in the nestling at all loci, indicating that the social father was the sire of each.
Identification of extrapair sires
We identified sires for 88.6% of the 413 nestlings analyzed, including the
sires for approximately half of the extrapair young
(Table 3). Our success at
identifying extrapair sires was highest in 1997 and 1998 (sires identified for
62.3% of 53 EPF offspring), when sampling efforts were most extensive. In all
but one case the extrapair sire possessed the nestling's paternal allele at
all loci scored. In the final case a male and nestling matched at four of five
loci and had alleles of very similar size at the fifth (Dca 24, 208
versus 210 bp); this male also matched two other extrapair young from the same
nest. Only one nestling matched two extrapair males at all loci; one of these
males also matched the second EPF offspring from the same nest, and this male
was therefore designated to be the sire. Three additional comparisons were
somewhat ambiguous, with an extrapair male matching a nestling at four of five
loci in each case. To be as conservative as possible, we did not assign these
nestlings to the extrapair males.
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In 68.0% of the cases in which we identified an extrapair sire (n = 25 males), the nestling was located on a territory adjacent to that of its extrapair sire, and in most of the remaining cases the sire was less than two territories away (Figures 2 and 3). Moreover, 70.2% of the young whose sires were not identified (n = 47) were produced on territories at the edge of the study plot, where some neighboring males had not been sampled. There were, however, four cases in which a male was separated from his extrapair young by two or more territories (e.g., male 352 in Figure 2), and another four cases in which young with an unidentified sire were found in a nest two or more territories from the edge of the study plot (e.g., territory of male 006 in Figure 2). Excluding territories at the edge of the study plot and limiting the analyses to 1997 and 1998 (when all males breeding on the plot were sampled), we identified the sires for 76.5% of all extrapair nestlings (n = 34). Thus, Figure 3 gives a general picture of the distribution of distances between extrapair offspring and their sires, but likely excludes a few cases in which the nestling and sire are separated by several territories. These results indicate that most, but not all, extrapair sires are males on nearby territories (usually adjacent neighbors), thus strongly supporting the role of local interactions in producing EPF.
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Patterns of extrapair paternity and variation in reproductive
success
The frequency of extrapair fertilizations was high in all years of this
study (Table 3), with nearly
1/4 of all sampled young having extrapair sires and over 1/3 of all sampled
nests containing such young. The frequency of EPF offspring was unaffected
(23.5%) by exclusion of the 16 nests showing partial brood loss. The frequency
of EPF offspring varied significantly among years (
2 = 7.88,
df = 3, p =.049), but post-hoc comparisons showed that the only
significant pairwise difference was between 1996 and 1997 (the years with the
highest and lowest frequency of EPF offspring, respectively; 2
= 7.43, df = 1, p =.006).
The proportion of extrapair young per nest varied from 0.0 to 1.0, with significantly more broods having many EPF than would be expected by chance (Figure 4). Of all broods analyzed, 16 contained a single extrapair nestling and 26 contained multiple extrapair nestlings. We identified the extrapair sires for 16 of the broods containing multiple EPF offspring—in all but one case a single male had sired all of the extrapair young in the brood. The one exception was a brood of four consisting of three nestlings sired by one extrapair male and a single nestling sired by a different extrapair male.
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Our sampling efforts were most complete in 1997 and 1998, when we obtained blood samples from nearly all nestlings that survived to an age of 6 days. This extensive sample allowed us to calculate variance in male reproductive success for both males and females (Table 4). The standardized variance in male genetic reproductive success (T) was approximately 45% greater than variance in apparent reproductive success (number of young per male territory, A). Moreover, success in siring extrapair offspring (E) contributed 9-14% of the total variance in T, and a positive covariance between within-pair success (W) and extrapair success (E) contributed a similar amount (correlation between W and E, 1997 and 1998 combined, r =.23, p =.06). Thus, EPF increased variance in male reproductive success. Nevertheless, variance in male reproductive success was only 23-29% greater than variance in female reproductive success in this socially monogamous population.
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Male characteristics and extrapair success
We were unable to identify any male characteristics that were associated
with EPF. First, male age class was not related to the probability of being
cuckolded (n = 47, log likelihood = -30.14, 2 = 2.56,
p =.917). Similarly, males who obtained EPF did not differ
significantly in age from the males that they cuckolded (paired sign test,
n = 25 comparisons, p >.999). Finally, none of the
morphological traits that we measured differed significantly between extrapair
sires and the males that they cuckolded
(Table 5).
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DISCUSSION |
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Effectiveness of identifying extrapair sires
Although many studies have used multilocus DNA fingerprinting to analyze parentage in birds, relatively few studies have used microsatellites (Webster and Westneat, 1998
),
and fewer still have assessed the degree of congruence between these two types
of genetic markers. We analyzed the parentage of 56 nestlings using both
techniques and found that they reached similar conclusions in all but four
cases. In three of these cases the nestling was near the cutoff for
classifying the nestling as resulting from EPF, and the fourth case may have
arisen because we used a conservative rule for determining whether bands
matched in the earlier fingerprinting study. Thus, although these results
corroborate the effectiveness of both techniques in identifying EPF offspring,
caution should be used in borderline cases.
With that caveat in mind, microsatellites nevertheless proved highly
effective in identifying both extrapair young and their sires. We were able to
identify the extrapair sires in over half of the cases of EPF, and in only one
case did more than one male match a nestling at all five loci. Moreover, when
nestlings produced on territories at the edge of the study plot were excluded
(because some of their potential sires had not been sampled), we were able to
assign sires to the majority of extrapair young. Thus, as suggested by earlier
studies (e.g., Ellegren, 1992;
Primmer et al., 1995),
microsatellite markers appear to be a highly effective approach to the
analysis of parentage in birds.
Locations of extrapair sires
In this study population, the majority of extrapair sires were males on
adjacent territories (i.e., neighboring males). Very few nestlings were sired
by males from distant territories, and the majority of nestlings with
unidentified sires were from territories at the edge of the study plot. Other
studies of socially monogamous birds have identified extrapair sires, and in
most (e.g., Hasselquist et al.,
1995; Kempenaers et al.,
1992; Sheldon and Ellegren,
1999; Stutchbury et al.,
1997; Yezerinac et al.,
1995) but not all (Dunn and
Cockburn, 1998; Dunn et al.,
1994) of these studies the identified sires were usually
neighboring males.
Thus, the emerging picture of mating systems in territorial passerines is
that most (but not all) extrapair sires come from neighboring territories.
This has two important implications for the study of avian mating systems.
First, because reproductive interactions appear to act on a local scale,
variance in total male reproductive success is likely to be lower than would
be the case if such interactions acted on a more global scale (see below). For
example, if females actively choose extrapair mates, any given female will
have a relatively limited pool of potential sires to choose among (i.e., her
neighbors). Second, studies attempting to identify the factors affecting
frequency of EPF should examine those factors at a local scale. For example,
in assessing the effects of breeding synchrony on EPF (e.g.,
Birkhead and Biggins, 1987;
Kempenaers, 1997;
Saino et al., 1999;
Stutchbury, 1998;
Weatherhead, 1997;
Westneat and Gray, 1998), the
synchrony among adjacent neighbors may be more important than the synchrony
among all females in the population (Chuang
et al., 1999).
Effects of EPF on variance in male reproductive success
The standardized variance in reproductive success measures the
"opportunity for selection," which is the maximum strength of
selection (Arnold and Wade,
1984). In populations with low variation in reproductive success,
the difference between successful and unsuccessful breeders will be slight,
and therefore selection on traits associated with success will be weak. In
contrast, in populations with high variation in reproductive success,
successful individuals will produce sub-stantially more offspring than
unsuccessful individuals, and traits that contribute to successful breeding
will be strongly favored by selection.
It is for this reason that sexual dimorphism in socially monogamous birds
has proved somewhat enigmatic. In a large number of species, males differ
substantially from females in morphology (e.g., in plumage coloration),
implying that sexual selection is acting strongly on male traits. However, in
monogamous species with a balanced adult sex ratio, variance in male mating
success should be very low, and variance in male reproductive success should
be almost identical to that of females. Under such conditions, how could
sexual selection be strong enough to affect male morphology so markedly?
Darwin (1871) proposed two
solutions to this problem. First, sexual selection may be generated by
variation in mate quality (i.e., some males may obtain mates that are much
more fecund than are the mates of other males). This proposal has received
theoretical (Kirkpatrick et al.,
1990) and some empirical (e.g., Møller,
1991,
1994) support, but requires
further study. Second, adult sex ratios may be male biased, such that some
males may not be able to obtain a mate. Consistent with this suggestion, adult
sex ratios of most monogamous birds appear to be male biased
(Breitwisch, 1989), and this
has been shown to generate selective pressures on male morphology (e.g.,
Price, 1984).
The recent discovery of extrapair fertilizations has suggested an
alternative explanation; if EPF are common, variation in male reproductive
success could be substantial even in socially monogamous species. Yet,
simulation studies (Webster et al.,
1995) have shown that EPF may have little effect on variation in
reproductive success, even when they are common. This could happen, for
example, if males who sire extrapair young are also cuckolded by other males.
In this case EPF would "cancel out" and there would be little
reproductive variation among males.
In this study, variance in male reproductive success was greater than
variation in number of young produced per territory (i.e., apparent
reproductive success), and variation in number of extrapair young sired
contributed significantly to total variation in male reproductive success.
This result is robust to sampling effort, because we obtained samples (and
hence genotypes) for nearly all territorial males on our study site, and
previous results indicate that there are few if any floaters in this
population (Marra and Holmes,
1997). Interestingly, a positive and fairly substantial covariance
existed between within-pair and extrapair success (see also
Ketterson et al., 1998). This
positive covariance indicates that males who sired many young on their own
territories were also successful in siring extrapair young on other
territories. Our preliminary analyses, though, have failed to identify any
male trait that might be associated with success in obtaining EPF
(Table 5). This result should
be accepted tentatively, however, because our sample sizes for these
comparisons are not large at this point, and we may have failed to measure
morphological traits important to female mate choice or intrasexual
competition.
Although the frequency and effects of EPF can vary substantially among
populations (e.g., Gyllensten et al.,
1990), our results suggest that EPF increase variation in
reproductive success among males, and hence the opportunity for selection, in
this dichromatic species. However, variation in male reproductive success was
only slightly greater than variation in female reproductive success even after
the effects of EPF had been factored in. This limited effect of EPF did not
occur because EPF gains and losses cancel each other out (the covariance
between W and E was positive). Rather, it appears to be due
to the fact that most EPF occurred on a local scale; that is, because males
sired young only on territories near their own, none sired a large number of
extrapair young. As a consequence, extrapair success was not biased strongly
toward a small subset of highly successful males in this population. Indeed,
most of the variation in male reproductive success was generated by variation
in within-pair success (Table
4; see also Webster et al.,
1995). This component of reproductive success is affected by
pairing success, mate quality, predation on nestlings, and numerous other
factors in addition to EPF (i.e., whether a male is cuckolded).
Although studies indicate that EPF increase the opportunity for sexual
selection in socially monogamous species (see
Møller, 1998;
Møller and Ninni,
1998), variance in male mating success is typically less than that
seen in polygynous species (e.g.,
Pruett-Jones and Pruett-Jones,
1990; Trail,
1985). Other studies of sexually dichromatic passerines have found
little effect of EPF on sexual selection (e.g.,
Hill et al., 1994;
Webster et al., 1995;
Westneat, 1993). Thus, it is
not yet clear whether EPF underlie the evolution of pronounced sexual
dimorphism (e.g., dichromatism) in socially monogamous birds
(Møller and Birkhead,
1994), or whether the mechanisms originally proposed by Darwin are
better explanations.
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ACKNOWLEDGEMENTS |
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We thank T.S. Sillett, J.J. Barg, and numerous assistants from the University at Buffalo and Dartmouth College for assistance in the field. H.L. Gibbs generously provided his preliminary results, including primer sequences. J. Feng, H.A. Murphy, and K.S. Phipps provided invaluable laboratory assistance. We thank M.A. Coffroth, H.R. Lasker, D.J. Taylor, and three anonymous referees for suggestions that improved this manuscript. Fieldwork was conducted in the Hubbard Brook Experimental Forest, which is administered by the U.S. Forest Service, Northeast Research Station, Radnor, Pennsylvania, USA. This study was supported by National Science Foundation grants to the State University of New York at Buffalo and to Dartmouth College.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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