Behavioral Ecology Vol. 12 No. 6: 666-673
© 2001 International Society for Behavioral Ecology
Genetic monogamy in the absence of paternity guards: the Capricorn silvereye, Zosterops lateralis chlorocephalus, on Heron Island
Department of Zoology and Entomology, The University of Queensland, Brisbane 4072 Queensland, Australia
Address correspondence to B.C. Robertson, who is now at Department of Zoology, University of Canterbury, Private Bag 4800, Christ-church, New Zealand. E-mail: b.robertson{at}zool.canterbury.ac.nz .
Received 13 July 2000; revised 15 November 2000; accepted 1 December 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We investigated the genetic mating system of a socially monogamous passerine bird, the Capricorn silvereye Zosterops lateralis chlorocephalus, on an island of the Great Barrier Reef. There were no cases of extrapair paternity (EPP) among 122 offspring from 53 broods detectable by minisatellite or microsatellite DNA fingerprinting. Behavioral observations of paired birds showed that this was not a consequence of efficacious paternity guards and that females did not engage in extrapair copulation (EPC). Frequency of intrapair copulations was also low, with only 14 cases observed during 199 hours of observations of the 11 focal pairs in the fertile periods of females, and this was consistent with anatomical features of the cloacal protuberance in males. In this population, young birds form life-time pair bonds soon after gaining independence but females are obviously not attempting EPC possibly to redress this early mate choice. This is despite the fact that they breed in high density with a synchronous start and asynchronous spread of laying in a protracted season and males do not positively exhibit mate guarding behavior when females are fertile. Our results support high fidelity of socially monogamous birds on islands and are consistent with the hypothesis that sexual selection is reduced where genetic variation in fitness is limited.
Key words: DNA fingerprinting, island birds, monogamy, parentage, paternity guards, white-eyes.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Extrapair paternity (EPP) is a feature common in the mating systems of many socially monogamous birds. Considerable variation exists within and between species in the frequency of EPP (Westneat and Sherman, 1997
), perhaps reflecting the outcome of intersexual
conflict (review in Petrie and Kempenaers,
1998). Females apparently have considerable control over
copulation success (Birkhead and
Møller, 1993) and, hence, the paternity of their eggs. For
monogamous females, then, particularly those in which mate selection for
life-time bonding occurs at an early age, EPP is a viable option to redress
early or limited choice in mate selection
(Møller, 1992). For
males, on the other hand, constraining their female's access to other males
and ensuring their own paternity should be paramount. Thus males of many bird
species employ strategies, such as mate guarding, frequent copulation, song
activity or territoriality, to counter female infidelity (reviewed in
Birkhead, 1998). The efficacy
of paternity guards, however, varies considerably across species (e.g.,
Hunter et al., 1992;
Kempenaers et al., 1995), and
may reflect female involvement in EPP
(Petrie and Kempenaers,
1998).
Here we present the results of our study of a socially monogamous species
of white-eye, the Capricorn silvereye Zosterops lateralis
chlorocephalus, on Heron Island, in the southern Great Barrier Reef.
Young Capricorn silvereyes often select mates soon after becoming independent
(Kikkawa and Wilson, 1983;
Kikkawa unpublished data) and the pair bond established then lasts for life.
Normally, they re-mate only when widowed and divorce is extremely rare
(Kikkawa, 1987). For female
silvereyes, EPP would be an obvious means to alter early life-time mate
choice.
Available evidence from this population suggests, however, that EPP may be
rare. This is despite silvereyes breeding in high density, e.g., local density
ranges from 11 to 30 pairs/ha near food sources
(Catterall et al., 1982), and
laying multiple broods (up to five) asynchronously in a protracted season
(August to April; Kikkawa,
1987); both factors are thought to increase opportunities for EPP
(Birkhead and Biggins, 1987;
Møller and Birkhead,
1993; but see Stutchbury and
Morton, 1995). Indeed, during daily observations of breeding birds
between 1979 and 1994, no extrapair copulation (EPC) was observed.
Furthermore, in a multilocus DNA fingerprinting study of six silvereye broods
(N = 14 offspring), no EPP was noted
(Degnan, 1993). Together these
results suggest that EPP is at least uncommon on Heron Island and imply that
either females are not engaging in EPP or that male strategies are successful
in constraining female choice.
In this study, we examine if EPP is used by female silvereyes to alter
early life-time mate choice and the role of male strategies in constraining
female choice. First, we made a thorough genetic analysis of a large number of
young to determine their parentage by means of DNA fingerprinting. Second, we
investigated behavior of paired birds to obtain evidence of paternity guards
which might influence opportunities for extrapair copulation. Third, because
rate of copulation can be difficult to measure and copulation behavior is
reflected in reproductive anatomy (reviewed in
Birkhead, 1998), we examined
the male cloacal protuberance in breeding birds as an indication of copulation
behavior and intensity of sperm competition.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study species and field methods
The Capricorn silvereye is a sexually monomorphic, passerine bird (14 g), endemic to the wooded cays of the southern Great Barrier Reef (Kikkawa, 1997a
), off the east
coast of Australia. On one of these cays (Heron Island, 16 ha in area) the
social behavior and population dynamics of the species have been studied for
over 30 years (Brook and Kikkawa,
1998). Almost all silvereyes on the island were individually
colorbanded at the beginning of each breeding season
(Kikkawa, 1997b) when the
population size varied between 225 and 445. For general field methods used in
this study, including population censusing and breeding season monitoring, see
details described in Kikkawa and Wilson
(1983).
Genetic analysis of parentage
Sample collection and DNA extraction
A total of 53 full clutches from 43 breeding pairs were sampled in the
1990-1991 breeding season (20 clutches/44 offspring) and the 1991-1992
breeding season (33 clutches/78 offspring). Six pairs were represented by two
clutches (one from each season in four of the pairs) and two pairs by three
clutches (all from the 1991-1992 season). Putative parentage was assigned to
established pairs and confirmed for each clutch by regular observations at
nests of the individuals involved in all phases of breeding (nest building to
provisioning of young). Blood samples were obtained non-destructively
(Degnan, 1993) from all
parents and from all nestlings at the time of banding, usually 7 or 8 days
after hatching. Blood (25-50 µL) was stored at -70°C in 1 x SSC
(150 mM NaCl, 15 mM sodium citrate), before total genomic DNA was extracted by
a standard phenol/chloroform method (Sambrook et al., 1989).
Minisatellite DNA fingerprinting
Minisatellite DNA fingerprints were generated for 25 (five clutches from
1990-1991 and 20 clutches from 1991-1992; 54 offspring in total) of the 53
broods using re-cloned versions (18.15 and 19.6 probes:
Carter et al., 1989) of the
33.15 and 33.6 minisatellite probes (Jeffreys et al.,
1985a,b).
Electrophoretic and hybridization conditions were similar to those of Degnan
(1993) with a few
modifications: we used Hybond Nfpt (Amersham) membranes, capillary blotting
(15 to 24 h in 20 x SSC) and UV cross-linking (50 mJ) of DNA to
membranes. We also 32P-random-prime labeled probes using a
multiprime labeling kit (Amersham) and hybridized at low stringency
(50°C), before exposing membranes to Amersham Hyperfilm-MP.
We scored minisatellite autoradiographs with the aid of
/HindIII size markers run on both sides of gels and only
scored bands greater than 3 kb following the criteria of Degnan
(1993). Pair-wise comparisons
of DNA fingerprints were limited to individuals separated by not more than two
lanes to ensure precise comparison of band mobility. The proportion of bands
shared between individuals was compared using a band-sharing coefficient
(Wetton et al., 1987).
Hybridization of the 18.15 and 19.6 probes to HaeIII-digested
silvereye DNA produced an average (mean ± SD) of 9.5 ± 3.4
(18.15 probe) and 13.7 ± 3.11 (19.6 probe) bands in presumptive
unrelated individuals (32 adults not related by direct descent and not sharing
any first-order relatives among themselves as determined by field
observations). Band-sharing coefficients between unrelated individuals were
similar for both probes (18.15 probe, D = 0.323 ± 0.100 and 19.6 probe,
D = 0.317 ± 0.121). Using these, we estimate the probability of two
randomly chosen silvereyes in this population having identical minisatellite
DNA fingerprints (see Jeffreys et al.,
1985a) to be 2.0 x 10-5 for the 18.15 probe and
1.7 x 10-7 for the 19.6 probe. As both probes reported
similar results with respect to resolving parentage and parentage exclusion
(i.e., no EPP or intra-specific brood parasitism: IBP), for simplicity, we
report the results for the 19.6 probe only.
DNA profiles were obtained for all adults and offspring of the 25 broods
hybridized to the 19.6 probe. From an analysis of segregation of maternal and
paternal bands (see Jeffreys et al.,
1986) in eight full siblings from three clutches (Robertson,
unpublished data), we concluded that the scored bands represent alleles of
stably inherited heterozygous loci that segregate in a Mendelian fashion.
Band-sharing values for unrelated individuals and for putative
parent-offspring (mean of 0.638 ± 0.07) dyads showed limited overlap
(Figure 1). We used two
criteria (e.g., Lifjeld et al.,
1993) for excluding parentage: (1) the presence of more than two
novel (i.e., not found in either parent) bands in an offspring's fingerprint,
and (2) a band-sharing coefficient of less than 0.5 with at least one putative
parent.
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Microsatellite DNA fingerprinting
Microsatellite DNA fingerprints were generated for all 53 broods (122
offspring) from the combined allelic variation at four microsatellite loci
(ZL12, ZL22, ZL35, and ZL38) previously isolated from a silvereye partial
genomic library (Degnan et al.,
1999). Allelic variation was assayed in 6.5 µl polymerase chain
reactions (PCR) following the protocol of Degnan et al.
(1999). Size of resolved
alleles was determined by comparison with a sequencing size ladder run at
regular intervals on all gels.
Population allele frequencies for each locus were calculated from the
genotype information obtained from putative parents only (see
Chakraborty, 1991). Linkage
disequilibrium and heterozygote excess and deficiency, the latter a potential
indicator of the presence of null alleles, were investigated using GENEPOP 3.1
(Raymond and Rousset, 1995).
The statistical power of the genotyping system for parentage analysis was
evaluated by calculating expected exclusion probabilities for paternity. We
have used the equations of Double et al.
(1997), which accounts for the
presence of close relatives among candidate fathers (using Monte Carlo
simulations), a social feature common to many birds
(Greenwood and Harvey,
1982).
For each of the four microsatellite loci, allele frequencies and
heterozygosity were estimated from a sample of 73 putatively unrelated adults
(Table 1). Allelic diversity
ranged from 10 alleles at locus ZL12 (heterozygosity 0.82) to four alleles at
locus ZL38 (heterozygosity 0.53) and allele frequencies were dominated by one
allele in three of the four loci (Table
1). Inheritance of alleles at each locus was independent of the
others and only locus ZL35 was deficient of observed heterozygotes compared to
Hardy-Weinberg expectations (p <.01). Autoradiographs of this
locus were re-examined for signs of null alleles (see
Primmer et al., 1996) or
misscored alleles, but neither were found. Consequently, allelic designations
were considered correct and all four loci were used in the parentage
analysis.
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Variation at each of the four microsatellite loci was assayed for the total
sample of 84 putative parents (43 pairs including two re-mated birds) and 122
offspring from 53 broods (including the 25 broods examined in the minisatelite
analysis). All alleles amplified in all offspring could be traced to either of
the putative parents, suggesting that these loci were behaving in a Mendelian
manner and that putative parents were indeed genetic parents. The complete
absence of mismatch of bands suggests that these loci are not subject to high
rates of mutation, hence the probability of parental exclusion via confusion
with mutation (Hanotte et al.,
1991) is negligible. The probability that two unrelated
individuals in this population share the same multilocus genotype (see
Hanotte et al., 1991) was 3.5
x 10-4.
Behavioral observations
Mate guarding involves males actively following their mates, primarily
during the fertile period of the female
(Birkhead and Møller,
1992). In doing so, males potentially exclude extrapair males from
copulation with their mates, thereby limiting their chances of losing
paternity. Silvereyes display strong pair association expressed as the
maintenance of pair bonds throughout the year and frequent allopreening
(Kikkawa and Wilson, 1983). To
determine if this behavior constitutes mate guarding, we examined the
relationship between pair association (i.e., proportion of an observation
period the pair were < 5 m apart) and female fertility. We also
investigated if males were actively following their fertile mates and, hence,
were responsible for the observed levels of pair association.
Over two consecutive breeding seasons, we spent 199 h observing 11 pairs of silvereyes during 12 nesting cycles (one pair was observed in both years). All breeding attempts were the first of the season. Four nesting attempts were observed in one breeding season (8 October to 23 November 1992), with the remaining eight observed in the following season (13 September to 31 October 1993). Nine of the 11 pairs were also observed during the non-breeding season (19 to 25 June 1993: winter observations). Focal pairs were watched for 30 min daily between 0530 and 1100 h EST (in a random order), from up to 45 days (mean ± SD, 27.3 ± 12.2, N = 12) before the first egg was laid until the start of incubation. Two of the pairs were also observed daily for 30 min between 1600 and 1800 h EST (up to 15 days before clutch initiation), to investigate diurnal differences in behavior. Winter observations were conducted using the same protocol as breeding season observations.
Focal observations were conducted in the immediate vicinity of the territory of the pair. Observations commenced when either individual was located and paused if neither bird could be observed. Every 30 seconds, we recorded the distance of separation of the pair as > 5 m or < 5 m and whether the individual(s) were involved in nest building (i.e., active nest construction or collecting nesting material). Site changes (any flight that resulted in the individuals of the pair being separated by more than 10 m), copulations and territorial interactions (which individual was involved and presence of mate) were recorded ad libitum. For each site change, we noted which bird initiated the move, and whether the mate followed.
Silvereyes sing at dawn throughout the breeding season
(Kikkawa, 1987) and silvereye
song has been suggested to function in territory defense
(Slater, 1993). If dawn song
functions as a paternity guard, we would expect song output to be greatest
during the fertile period of female silvereyes
(Møller, 1991; but see
Gil et al., 1999). We examined
if a relationship exists between dawn song and female fertility using the song
output of 11 male silvereyes (distinct from the 11 for which pair association
was observed). A total of 62 dawn songs were observed from 10 September to 16
November 1994 with each male being observed no more frequently than every
third day. Observations commenced at nautical twilight (sun 12° below
horizon) and ceased at the end of the dawn chorus (last bird heard singing).
From within the territory of the male, we recorded the cumulative duration of
the focal male's dawn song and the number of song bouts. Silvereye song is
typically a continuous warble made up of songs of approximately 6 s duration
(Slater, 1993). Inter-song
intervals vary and can be of considerable length. Only inter-song intervals of
greater than 10 s duration were omitted from the cumulative song in duration.
Although this results in an overestimation of actual vocalization time, this
measure still gives a good approximation of song output
(Cuthill and MacDonald,
1990).
We analyzed all behavioral data using non-parametric statistics (following
Siegel and Castellan, 1988)
because of sample sizes and the inability to correct non-normality in
proportions. We defined the fertile period of female silvereyes as the time
between 5 days before clutch initiation and the laying of the penultimate egg
(see Birkhead and Møller,
1992). Only one data set (1992) from the pair observed in both
years was included in the analysis. Similar data for pair association,
collected over 2 years, were not significantly different (mean pair
association for each pair, Mann-Whitney U test: U = 8.00,
N1 = 3, N2 = 8, P =.414) and
were pooled in all subsequent analyses. Mean values of pair association were
calculated for each period of the nesting cycle (i.e., winter, pre-fertile and
fertile) for each pair. All tests were two-tailed. Values are means ±
standard errors, unless otherwise stated. Sample sizes vary between tests
because not all variables could be collected for all pairs.
Structure of the male cloacal protuberance
To determine if the anatomy of the cloacal protuberance of males is
indicative of silvereyes being subject to intense sperm competition, we
examined 20 live male silvereyes at the peak of breeding during late October
1994. Each male was weighed (g), and the length (anterior/posterior), width
(left/right) and height (anterior) of the cloacal protuberance measured using
callipers (± 0.01 mm). Cloacal protuberance volume of males was
estimated following Briskie
(1993). Values are given as
means (± SE).
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RESULTS |
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Genetic analysis of parentage
The minisatellite DNA fingerprinting analysis found no evidence of band mismatches between offspring and putative parents indicating that parentage had been correctly assigned from field observations for all 53 nestlings from 25 broods. No nestlings shared less than 0.5 of their bands with either of their putative parents. We estimated the probability of falsely including an offspring resulting from EPP (see Jeffreys et al., 1985b
) to be 4.1 x 10-4 and the
probability of falsely including an offspring resulting from IBP (see
Burke et al., 1989) to be 2.0
x 10-4. Given this level of parentage exclusion, we conclude
that we found no evidence of EPP or IBP in our sample of the Heron Island
population of silvereyes.
When the four microsatellite loci were used to address paternity, under the
assumption that no first-order relatives were competing for paternity, we
could determine paternity with up to 92% certainty. If we assume that one
first-order relative was competing for paternity this certainty is reduced to
65%. In concordance with the minisatellite results, no cases of IBP were
detected by the microsatellite analysis. We estimate that maternity can be
determined from these four loci with up to 98.8% certainty (see
Gundel and Reetz, 1981).
Allelic variability at the silvereye-specific loci, therefore, supports the
finding that EPP and IBP are extremely rare events, if they occur at all, in
the Heron Island population.
Behavioral observations
Do male silvereyes guard their mates?
In general, silvereyes spent more than 50% of their time within five meters
of their mates during the nesting season. Patterns of pair association showed
little diurnal variation (Pair 1, AM: 0.39 ± 0.44, PM: 0.30 ±
0.46, both N = 15 from day -12; Pair 2, AM: 0.57 ± 0.46, PM:
0.61 ± 0.59, both N = 19 from day -16) and may vary little
between years within pairs (single pair in 1992: 0.41 ± 0.92, and 1993:
0.43 ± 0.71; both N = 10 from day -7).
Although pair association in the silvereye is suggestive of mate guarding
it is not positively related to female fertility. In fact, levels of pair
association decreased when females became fertile, which is contrary to what
is expected if males were guarding their mates. Comparison of the intensity of
pair association during the three periods (winter, prefertile, and fertile
periods) revealed significant differences in the proportion of time pairs
spent together (Figure 2: nine
pairs, Friedman test, 
2 = 12.67, df = 2, P =.002).
Post hoc comparisons indicated that pairs spent significantly less time
together when females were fertile compared with during the pre-fertile period
(Wilcoxon matched pairs test, z = -2.67, N = 9, p
<.008). Interestingly, this level of pair association was less than that
observed in winter period (Wilcoxon matched pairs test, z = -2.07,
N = 9, p <.038), a period when males should have no
reproductive interest in their mates.
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As both sexes build the nest when females are fertile, we examined if the presence of a nest, and consequently, nest-building activity, was responsible for the reduced level of pair association. Pair association was lower when a nest was present (nest absent, 0.70 ± 0.23 and nest present, 0.60 ± 0.25: Wilcoxon matched pairs test, z = -1.17, N = 10, p <.24, one pair already had a nest at the start of observations). Rate of nest building (i.e., collection of nesting material and nest building) also had a negative influence on the time pairs spent together. By testing the sign of Spearman rank-order correlation coefficients calculated for the relationship between rate of nest-building and pair association in each pair, we found that significantly more negative coefficients (eight of 11 pairs) were noted than was expected given the assumption of randomness (two-tailed, one sample sign test, p <.039). We conclude, therefore, that the lower levels of pair association noted during the fertile period are consistent with both sexes building the nest.
If males are mate guarding, then this should also be reflected in an increased tendency for males to follow female initiated movements when their females are fertile. Males silvereyes, though, showed the same following behavior during the fertile period as was noted in winter observations (Figure 3). Importantly, it appears that both sexes are responsible for maintaining the observed levels of pair association. Males and females initiated similar numbers of site changes during all three periods (Wilcoxon matched-pairs test, N = 9 pairs, all ns) and females displayed similar levels of following as males. The only exception was when females were fertile, they tended to follow their mates less (Figure 3).
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Copulation frequency
Only 14 intra-pair copulations were observed during 199 h of focal
observations of the 11 pairs. Not all pairs were observed to copulate during
morning observations (five of 11 pairs) and no copulations were noted for the
two pairs observed in the afternoon. All copulations occurred in the female's
fertile period, except one that occurred 13 days before the start of
laying.
Territory intrusions and defense
Despite silvereyes spending considerable time off their territories
foraging (Catterall et al.,
1982), territorial interactions in this population were
infrequent. We also found that rates of territorial interactions (number of
interactions with all birds per 30 min) were not related to female fertility
(prefertile period, 0.056 ± 0.013 and fertile period, 0.066 ±
0.014; Wilcoxon matched pairs test, z = 0.00, N = 11 pairs,
p = 1.0). Both males and females were observed to defend their
territories from intruders in the presence and absence of their mates
(Wilcoxon matched pairs test; male, z = 1.07, N = 11 pairs,
p <.28 and female, z = 1.61, N = 11 pairs, p
<.1).
Dawn song as a paternity guard?
Silvereye dawn song was not related to female fertility. For most males,
singing increased through the nesting cycle
(Figure 4a; Friedman test,
2 = 4.33, df = 2, p <.115) and was generally more
frequent during the post-fertile period (Wilcoxon matched pairs test, z =
1.36, N = 6, p <.17). Examination of singing activity in
relation to the presence of eggs revealed that males sang more after the start
of laying than before laying (Figure
4b; Wilcoxon matched pairs test, z = 2.20, N = 6,
p <.028). This period also coincides with when males start
roosting alone due to female nighttime incubation.
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Anatomy of the male cloacal protuberance
The dimensions of cloacal protuberances for the 20 live males averaged 6.4
± 0.1 mm in length, 6.0 ± 0.1 mm in width and 5.6 ± 0.1
mm in height. Male mass averaged 13.4 ± 0.2 g (n = 20). Using
these values, a volume of the cloacal protuberance was calculated as 169.1
mm2, which is similar to the value expected for a passerine of this
body mass (see Briskie,
1993).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Our genetic analyses show that Capricorn silvereyes are among the few passerine species that are known to be both socially and genetically monogamous. We found no evidence of extrapair paternity or intra-specific brood parasitism in the Heron Island population. Since the genetic analysis involved 53 broods over two successive breeding seasons, if EPP did occur in this population it would be a very rare event. This finding indicates three important points. First, that demographic and behavioral characteristics of our population have little, if any, influence on the occurrence of EPP. Second, that female silvereyes do not attempt to alter their initial mate choice via EPP, even though lasting sexual pairs are formed long before their first breeding season. Third, that in this population, parent-offspring relations determined by behavioral observations permit genetic analysis of traits (Kikkawa et al., 1986
).
Reliability of the paternity analysis
Since paternity determined by minisatellite DNA fingerprinting has a high
level of certainty (only four EPP offspring out of 10,000 would remain
undetected in our study), this molecular method is not likely to fail to
detect EPP (Burke et al.,
1991). A slightly lower certainty of paternity was attained using
the microsatellite markers, but this value was still high (up to 92%).
Estimations of probability could be compromised if there were a number of
close relatives potentially competing for paternity.
The potential for such competition would be high if a number of related
males were occupying neighboring territories. This is possible on islands
where natal dispersal is limited, and on Heron Island young establish their
first nesting territories 5 to 7 territories away from their natal territory
(Kikkawa, 1987). Although
males tend to be more philopatric than females, the chances of sons or male
siblings breeding in neighboring territories are small because of the high
mortality of young (e.g., 79% from the nestling stage to age 1 in the
1990-1991 season). Thus, the potential competition for paternity among related
males is limited, suggesting that our results are not likely to have been
biased by undetected EPP involving closely related males.
Why no EPP in the Silvereye?
Strict genetic monogamy has been reported in very few passerine birds and
explained in even fewer. For example, in two socially monogamous species,
genetic monogamy is suggested to be the result of mate guarding in the case of
the palila Loxioides bailleui
(Fleischer et al., 1994) and
territorial aggression in the case of the New Zealand robin Petroica
australis (Ardern et al.,
1997), which interestingly are also characteristics of species
displaying high levels of EPP in other species (e.g., the blue tit Parus
caeruleus, Kempenaers et al.,
1992; the bull-headed shrike Lanius bucephalus,
Yamagishi et al., 1992).
Clearly, as EPP is now known to be the norm among passerine birds
(Griffith, 2000), the absence
rather than the presence of EPP demands explanation.
It has been recognized in recent years that females control the success of
copulations in many birds (Birkhead and
Møller, 1993). If this is true, then the costs and benefits
of monogamy and EPP to females, and the constraints placed on female mate
choice, may be the keys to understanding the dynamics of EPP as a mating
strategy (Petrie and Kempenaers,
1998). A number of constraints on female mate choice have been
suggested including inability to reliably assess relative male quality,
principally due to low breeding synchrony
(Stutchbury and Morton, 1995),
male behavior (i.e., paternity guards) and female behavior
(Gowaty, 1996). Nonetheless,
none of these constraints adequately explains the absence of EPP from the
mating system of the silvereye.
Because silvereyes on Heron Island breed asynchronously they appear to fit
the hypothesis that low breeding synchrony restricts EPP opportunities
(Stutchbury, 1998;
Stutchbury and Morton, 1995).
Low breeding synchrony, however, is not a satisfactory explanation for the
absence of EPP in our population for two reasons. First, a peak of breeding at
the beginning of the season (Catterall et
al., 1982; Kikkawa and Wilson,
1983) could result in females being able to reliably assess male
quality; a key assumption of the hypothesis
(Stutchbury, 1998). Second,
low breeding synchrony alone does not exclude EPP, as shown by the mangrove
swallow Tachycineta albilinea which displays a moderate level of EPP
despite having a synchrony index of only 8%
(Moore et al., 1999).
The behavior of silvereyes suggests that there is no threat of EPP to the
territory holders. Silvereyes show strong pair association, spending about 75%
of their time together during the breeding season, but this behavior is not
due to mate guarding by the male and certainly is not related to female
fertility. Interestingly, mates of fertile females put considerable effort
into nest building and, consequently, pair association dropped to a level
below that observed in winter. Following behavior, which for males and females
was always less than 50% (i.e., a chance event) regardless of female
fertility, also indicates that males are not guarding their partners. Levels
of female following also exclude the possibility that females are guarding
their males (Creighton,
2000).
Contrary to what is predicted from the literature
(Birkhead and Møller,
1992), silvereyes do not employ frequent copulation, as a
paternity guard, in the absence of mate guarding. Our observations of
copulation behavior are corroborated by the fact that silvereyes possess
cloacal protuberances typical of a passerine of this size. This suggests that
silvereyes are not producing and storing large volumes of sperm and probably
not subject to intense sperm competition
(Robertson, 1997). We also
found that dawn song is not related to female fertility, and hence does not
appear to function as a paternity guard despite its presumed function in
territory defense.
Silvereyes showed vigorous territorial defense, although the number of
territorial interactions recorded was low. Such territoriality could be either
a male or female behavior constraint to female mate choice. Indeed, such
behavior has been suggested to function successfully as a paternity guard in
the New Zealand robin (Ardern et al.,
1997), but not in the bull-headed shrike
(Yamagishi et al., 1992). As
is the case for all paternity guards, however, the efficacy of territorial
behavior as a paternity guard may well rest with whether females actively
pursue EPP.
A number of benefits of EPP to females have been proposed
(Birkhead and Møller,
1992), but the main focus has been on "good genes"
(Sheldon, 1994). Specifically,
it is suggested that females improve offspring quality by mating with males of
better quality than their own mates
(Møller, 1988a).
Extrapair paternity is assumed to be greatest in species that show
considerable variation in male quality, because relatively few good males are
available as mates. Consequently, females mated to poor-quality males would
benefit from seeking EPP from good-quality males
(Møller, 1992). As
Heron Island silvereyes form sexual pairs early in life (Kikkawa, unpublished
data; Kikkawa and Wilson,
1983), presumably long before any indicators of male quality for
reproduction would become noticeable to females, EPP is an obvious means of
altering early mate choice. The fact that EPP rarely, if ever, occurs in this
population and birds mate monogamously for life, suggests strong selection
against this reproductive strategy.
Low frequencies of EPP might also reflect the costs associated with EPP
(Birkhead and Møller,
1992), the most important of which is considered to be the
adjustment of male parental care in relation to male certainty of paternity.
This cost may be of little significance, if females alone can raise young
(Westneat and Sargent, 1996;
Westneat and Sherman, 1993) as
they could in silvereyes when nestlings start taking fruit in the diet
(Robertson, 1997;
Wilson and Kikkawa, 1988).
Given that passerine males do not usually desert young following EPC but
provide some parental care (Møller,
1988b; Wright and Cotton,
1994), the risk of reduced male parental care should not be
important to female silvereyes.
Recently, it has been shown that island-dwelling passerines are
characterized by lower levels of EPP than mainland populations
(Griffith, 2000). One
potential factor that appears to be ubiquitous to insular populations of birds
is low levels of genetic variation
(Frankham, 1997). Our
population is no exception; the degree of genetic variation is comparable to
that of other small island vertebrates, and is significantly less than that
observed in mainland silvereye populations
(Degnan, 1993). Levels of
genetic variation have been shown to be positively related to levels of EPP,
which lends support to indirect benefit models of female choice
(Petrie et al., 1998). Thus,
our results are consistent with the hypothesis that sexual selection is
reduced where genetic variation in fitness is limited.
In our population of silvereyes pairing of siblings is positively avoided
in early mate choice (Kikkawa, unpublished data), but other mechanisms to
maintain heterozygosity in offspring
(Brown, 1997) are not known. It
is unlikely that females could benefit from EPP if variation in genetic
quality of males is limited and not readily perceived by females, even if the
associated costs of EPP to females are low.
|
ACKNOWLEDGEMENTS |
|---|
This study was supported by research grants of the University of Queensland and the Australian Research Council (ARC) under permits of the Australian Bird and Bat Banding Scheme (ABBBS) and the Queensland Department of the Environment with approval of the University of Queensland Animal Experiment Ethics Committee. The Heron Island Resort and Queensland National Parks permitted field-work on their premises and provided support. We thank Ceinwen Edwards for help with monitoring of the breeding population, Peter Douglas for maintaining the computer file, Mike Double for use of the program to compute paternity exclusions, and many helpers in the field, in particular, Amanda Cornellison, Paul Fisk, Uwe Rascher, Fiona Robertson, Helen Sneath, Boyd Simpson, Rose Wolf, and the staff of the Heron Island Research Station 1991-1995. We are grateful to Tim Birkhead, Andrew Cockburn, Anne Goldizen, Ian Owens, Bart Kempenaers, and two anonymous reviewers for commenting on earlier drafts.
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