Behavioral Ecology Vol. 12 No. 6: 746-752
© 2001 International Society for Behavioral Ecology
Sexual dimorphism, extrapair fertilizations, and operational sex ratio in great frigatebirds (Fregata minor)
Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, Columbus, OH 43210, USA
Address correspondence to D.C. Dearborn, who is now at the Department of Biology, Program in Animal Behavior, Bucknell University, Lewisburg, PA 17837. A.D. Anders is now at the Nature Conservancy, P.O. Box 5190, Fort Hood, TX 76544-0190. P.G. Parker is now at the Department of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, MO 63121, USA.
Received 3 May 2000; revised 14 December 2000; accepted 7 March 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Across taxa, the presence of sexual ornaments in one sex is usually correlated with disproportionately great parental effort by the other. Frigatebirds (Fregatidae) are sexually dimorphic, with males exhibiting morphological and behavioral ornaments, but males and females share in all aspects of parental effort. All other taxa in a clade of 237 species exhibit biparental care, but only frigatebirds exhibit pronounced sexual dimorphism. We tested for the presence of two factors that could contribute to the evolution of male ornaments in great frigatebirds: a high frequency of extrapair fertilizations and a male-biased operational sex ratio. In 92 families sampled over two breeding seasons, there was only one extrapair fertilization. However, in both seasons, there were more males than females available for mating, and the sex ratio among individuals actively engaged in mate-acquisition behavior was strongly male biased, with typically five or six males available per female. Our results suggest that extrapair fertilizations are not responsible for the exaggeration of sexual ornaments in male frigatebirds, and that operational sex ratio may be related to sexual dimorphism in this species. Further work is needed to determine whether the male-biased operational sex ratio creates the variance in male reproductive success that would be needed to drive the evolution of male ornaments.
Key words: extrapair fertilizations, Fregata minor, frigatebirds, operational sex ratio, ornaments, sexual dimorphism, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Across taxa, sexual selection theory predicts that the presence of exaggerated secondary sexual traits in one sex should correlate with mate choice and disproportionately great parental effort by the other sex (Andersson, 1994
). Thus, for
species in which males possess extravagant ornaments, females typically exert
mate choice and subsequently provide most or all of the parental care. In
contrast, species that lack sexual ornaments are often characterized by
balanced parental effort by males and females. Part of the explanation for
this relationship is that if males do not contribute to parental care, their
reproductive success becomes more heavily dependent on their mating success,
leading to more intense male—male competition or more selective female
choice; these pressures can, through a variety of mechanisms, lead to the
evolution of male sexual ornaments.
The positive relationship among male ornaments, female choice, and female
parental care holds true especially among birds
(Andersson, 1994). However,
frigatebirds (Fregatidae) depart from this pattern. Male frigatebirds exhibit
exaggerated secondary sexual traits not shared by females, including an
inflatable red throat pouch and an iridescent ruff of feathers. These traits
are highlighted by extravagant courtship displays, in which a male inflates
the throat pouch, erects his iridescent ruff, tilts and wags his head,
outstretches and trembles his wings, and vocalizes
(Nelson, 1975). These displays
are performed in large groups at which females can assess hundreds of
potential mates at once (Nelson,
1975). Despite this leklike mate choice, males and females form
social pair bonds, and males invest heavily in parental care. Males gather all
of the nest material (Nelson,
1975; Dearborn, unpublished data), they incubate for almost half
of the 57-day incubation period (Dearborn,
2001), they share in brooding the chick for 4-6 weeks
(Nelson, 1975; Dearborn and
Anders, unpublished data), and they contribute extensively to feeding the
chick for approximately 8 months (Nelson,
1975; Dearborn and Anders, unpublished data).
Because this combination of pronounced sexual dimorphism and balanced
parental effort by males and females is unusual from a life-history
standpoint, it is insightful to use a phylogenetic framework for considering
the presence of these traits in frigatebirds. By mapping sexual dimorphism and
balanced parental effort onto a phylogeny built with mitochondrial 12S-16S
rRNA and cytochrome B sequence data
(Siegel-Causey, 1997), one can
see that biparental care is a completely conserved ancestral trait in this
clade of more than 200 species but that pronounced sexual dimorphism is a
derived trait found only in the 5 species of frigatebirds
(Figure 1). This same result is
obtained by mapping these characters onto phylogenies based on morphology
(Cracraft, 1985),
mitochondrial rRNA sequence data (Hedges
and Sibley, 1994), DNA-DNA hybridizations
(Sibley and Ahlquist, 1990),
or a combination of behavioral and morphological traits
(Siegel-Causey, 1997). Thus,
when considering the unusual combination of male sexual ornaments and balanced
parental effort in frigatebirds, it seems most appropriate to ask why male
frigatebirds may have evolved sexual ornaments.
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One force that may have driven the evolution of male sexual ornaments in
frigatebirds is females' interest in, and ability to obtain, extrapair
fertilizations (i.e., fertilizations by males other than their social mates).
Over the past 15 years, researchers have come to realize that extrapair
fertilizations are prevalent in many species of birds
(Fleischer, 1996;
Gowaty, 1996;
Westneat and Sherman, 1997),
and this revelation has dramatically changed our view of avian mating systems
and sexual selection (Parker and Burley,
1998; Petrie and Kempenaers,
1998). Variation between species and between populations in the
frequency of extrapair fertilizations has been linked to a wide array of
ecological, behavioral, and morphological factors, including the degree of
breeding synchrony (Stutchbury and
Neudorf, 1998), the clustering of breeding territories or the
formation of colonies (Wagner,
1998), and the presence of bright male plumage
(Møller and Birkhead,
1994). The work by Møller and Birkhead
(1994) showed that, across
species, degree of male plumage brightness was positively correlated with
frequency of extrapair fertilizations. Extrapair fertilizations are generally
rare in seabirds (Austin and Parkin,
1996; Hunter et al.,
1992; Mauck et al.,
1995; Schwartz et al.,
1999; Swatschek et al.,
1994; but see Huyvaert et al.,
2000). Thus, the uniquely derived sexual dimorphism seen in
frigatebirds could be driven by an unusally high rate of extrapair
fertilizations.
A second possible driving force in the exaggeration of male traits in
frigatebirds is a male-biased operational sex ratio. At any given time, there
may be more males available for mating than there are females, leading to
female choosiness or male—male competition
(Kvarnemo and
Ahnesjö, 1996). A biased operational
sex ratio has been shown to drive sexual selection in many organisms,
including insects (Kvarnemo and Simmons,
1999), frogs (Wagner and
Sullivan, 1992), snakes
(Weatherhead et al., 1995),
fish (Kodric-Brown, 1988;
Balshine-Earn, 1996), and birds
(Colwell and Oring, 1988).
The mechanism linking male sexual ornaments to either a high rate of
extrapair fertilizations or a male-biased operational sex ratio is one of
heightened variance in male reproductive success and thus stronger sexual
selection on males (e.g., Yezerinac et
al., 1995). Under the extrapair fertilization hypothesis, variance
in male reproductive success would result from females preferring a subset of
males as fertilization partners; under the operational sex ratio hypothesis,
variance in male reproductive success would result from differential male
success at attracting a social mate. In this study, we determined whether a
high rate of extrapair fertilizations or a male-biased operational sex ratio
exists in a population of great frigatebirds, and thus whether either of these
factors has the potential to drive male variance in reproductive success in
this species.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study area and species
We conducted this study of great frigatebirds on Tern Island, French Frigate Shoals (23°45' N, 166°17' W), in the northwestern Hawaiian Islands. Tern Island is approximately 14 ha and is a breeding area for 15 species of seabirds totaling more than 200,000 individuals (see Amerson, 1971
, for more
details). Roughly 4000 adult frigatebirds come to Tern Island during the
breeding season (Dearborn et al., unpublished data). The nearest neighboring
colony of breeding frigatebirds occurs on Laysan Island, approximately 600 km
northwest of Tern Island. On Tern Island, male great frigatebirds begin performing courtship displays in January, and egg laying typically lasts from early February through late May. Groups of males display from perch sites in bushes (primarily Tournefortia spp.), and females fly above the colony, making initial inspections of males from the air. A female will then land beside a male to perform what appears to be a closer inspection, during which the male usually intensifies his display behavior. If the female accepts the male, they spend several days perched in close proximity to each other before they begin constructing the nest. The interval from initial pair formation to egg laying is typically 1-2 weeks. The total duration of parental care by frigatebirds is approximately 1 year and is among the longest for all species of birds. In addition, adult frigatebirds are very long-lived; there are individuals in our study population that are 37 years old (Dearborn et al., unpublished data).
Extrapair paternity
To measure the frequency of extrapair paternity, we collected blood samples
from 62 social families in 1998 and 30 families in 1999. In 1998, 21 of the 62
families were from nests that we were monitoring to collect detailed data on
parental effort (Dearborn,
2001); the remaining 41 families in 1998 were randomly chosen from
throughout the colony, and we spread our overall sample of nests across the
breeding season. Tern Island is elongated (roughly 1 km by 200 m), bisected
along its long axis by a sand runway, and marked with a short-axis grid every
10 m from 0 to 970 m. To choose a family from which to obtain blood samples,
we randomly selected the north or south side of the runway, randomly chose a
number from 0 to 970, and then chose the closest nest to that meter marker
that contained a chick old enough from which to obtain a blood sample. Due to
a shorter 1999 field season, in 1999 we sampled the 30 earliest nests of the
season that were successful long enough for us to obtain blood samples
(roughly 3 weeks after hatching). In both years, all blood samples were
collected when chicks were still being constantly brooded to ensure that
adults that we sampled were truly the social parents. We collected two
50-µl blood samples from each individual from the leg or foot, and samples
were stored in a lysis buffer (Longmire et
al., 1988).
To assess the frequency of extrapair fertilizations, we used multilocus
minisatellite fingerprinting, using the protocol of Parker et al.
(1994). Following extraction,
DNA was digested with HaeIII. The resulting fragments were separated
on agarose gels, blotted to nylon, and subsequently hybridized with Jeffreys's
probe 33.15 (Jeffreys et al.,
1985a,b).
Because a single egg is laid during a breeding attempt, each family group
consists of a male, a female, and a single chick. For each chick, we counted
the number of bands that were not attributable to either of its putative
parents. Second, we calculated a band-sharing index for dyads of chicks and
their putative parents. Band sharing was defined as 2S/(A +
B + 2S), where S = number of bands shared by the
pair of birds, A = number of bands unique to bird A, and B =
number of bands unique to bird B (Wetton
et al., 1987). Next, we assessed the extent of overlap in
band-sharing values between putative first-order relatives and putative
nonrelatives. To obtain dyads of nonrelated birds, we paired each chick's lane
with the lane of an adult from an adjacent family on the same gel. The sex of
the unrelated adult was chosen randomly. Birds paired in this way were usually
one or two lanes apart on the digestion gel. For comparison of the
distribution of the band-sharing scores of pairs of related and unrelated
birds, we restricted our parent—offspring dyads to those families in
which there were zero unattributable bands (n = 71), and we randomly
selected one of the parents for each chick. Thus, for this comparison each
chick was used once in a dyad with one of its parents and once in a dyad with
a nonparent from a nearby lane.
Using the resulting distribution of band-sharing values (Figure 2), we defined a cutoff of mean + 1.96 SD = 0.220 + 1.96 (0.090) = 0.398 as the upper limit for band-sharing values by unrelated birds. We marked this cutoff on a graph of band-sharing score versus number of unattributable bands, plotting separate points for chick-mother dyads and for chick—father dyads (Figure 3). Chicks falling below this band-sharing threshold and having more than two unattributable bands were classified as extrapair young.
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We calculated the mutation rate by counting the average number of novel fragments detected in all nonexcluded chicks and dividing this by the average number of fragments scored per chick. We used a one-sample Kolmogorov-Smirnov test to test whether the observed number of offspring having zero, one, or two novel fragments differed from the corresponding frequencies expected under a Poisson distribution.
Operational sex ratio
We used two different measures of operational sex ratio (OSR). We defined
the general OSR as the ratio of available males to females based on the number
of sexually mature adults that were at the breeding colony but were not
occupying nests. Data from hundreds of individually marked birds clearly
indicate that birds whose mates are incubating do not spend time at the
breeding colony while off the nest; rather, these birds fly away from the
island to forage, and when they return to the colony they go directly to the
nest to relieve their incubating mates. Thus, if a bird is at the colony but
is not currently occupying a nest, it does not have a nest that is being
tended by a mate.
In both 1998 and 1999, we measured the general OSR daily at 1730 h HST. At this time of day, birds in the colony are very active. Although some species of seabirds on Tern Island (e.g., red-footed boobies, Sula sula) exhibit pronounced diurnal variation in colony attendance, exploratory counts of frigatebirds conducted multiple times per day did not detect consistent variation in colony attendance over the course of the day.
Our counts of general OSR were made by taking the same route around the breeding colony each day, and our search path was never more than 50 m from the birds that we were counting. Frigatebirds are large animals (2-m wingspan) that perch on the tops of low bushes (generally 1 to 2 m high), and Tern Island is treeless and sparsely vegetated. Thus, detection of individuals during a count is not difficult. Daily counts were conducted by the same individual (D.C.D.) over both seasons. Because the number of birds that were flying during our counts was small relative to the total number of individuals being counted (6%), the likelihood of double counting a meaningful number of individuals over the 45 min that it took the observer to circle the colony is small.
In 1999, we included an additional measure of sex ratio, the immediate OSR. This was quantified by counting males that were currently performing mate-attraction behaviors and females that were currently involved in mate-searching or mate-evaluating behaviors. Male courtship display consists of many behavioral elements, including gular pouch inflation, head tilting, head wagging, wing fluttering, and vocalizations, but inflation of the gular pouch is the one component common to all levels of involvement in display behavior (Dearborn et al., unpublished data). Thus, a male was included in the immediate OSR if his gular pouch was partially or fully inflated. Mate choice by females primarily involves two stages: first, a female makes low flights over the colony making conspicuous visual inspections of displaying males below; second, a female lands and perches next to a male for further evaluation. Thus, a female was included in the immediate OSR if she was performing mate-inspection flights or if she was perched in physical contact with a male who was not on a nest. The immediate OSR was counted by a second observer (A.D.A.) at the same time as the general OSR and using the same route around the colony.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Extrapair paternity
The DNA fingerprints from 90 of 92 (97.8%) chicks had 0 or 1 bands that were unattributable to the chick's social parents. The frequency distribution of the number of unattributable bands did not differ from expected frequencies based on a Poisson distribution (Kolmogorov-Smirnov Z = 0.131, p = 1.00). The average number of novel bands per chick was 0.231, and the average number of bands scored per chick was 14.1, yielding a mutation rate of 0.0164 per locus per meiotic event, a value within the range of those found for minisatellite markers in other seabird species (0.008: Mauck et al., 1995
; 0.0145:
Schwartz et al., 1999; 0.017:
Hunter et al., 1992; 0.024:
Austin and Parkin, 1996). Based
on the Poisson distribution, the probability of a chick having three or more
unattributable bands from mutation alone is 0.0017. There was minimal overlap between the band-sharing scores for dyads of chicks with their putative parents and dyads of chicks with unrelated adults (Figure 2). Only one chick had a score below the 0.398 cutoff used to delineate the upper limit for band-sharing of unrelated birds, and this chick had four unattributable bands (Figure 3). Band-sharing between this chick and its mother was 0.594, whereas band-sharing with its father was 0.364, indicating that this chick was sired by a male other than its social father. To confirm this result, we extracted DNA from the backup blood samples for this family and repeated the genetic analysis; the male was still excluded as the sire of the chick. A chick from another family had two unattributable bands, but its band sharing was 0.609 with its mother and 0.500 with its father. The frequency of extrapair fertilizations in our sample was thus 1 in 92 (1.1%). Because frigatebirds lay a single egg, the rate per chick and rate per family are the same.
Operational sex ratio
In both years, the general OSR (based on the number of adults at the colony
that were not occupying nests) was male biased over the pair-formation and
egg-laying portion of the breeding season
(Figure 4). Typically, there
were two to three males available per female, and there was striking
similarity in the general OSR between years. As courtship displays tapered off
in April, the general OSR became balanced and, eventually, female biased. The
immediate OSR, measured during the pair-formation and egg-laying portion of
the 1999 season, was even more male-biased than the general
OSR—typically five or six displaying males for each female engaged in
mate evaluation. Unlike the general OSR, the immediate OSR did not exhibit a
seasonal decline (Figure
5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In this study, we found a low rate of extrapair fertilizations in a population of great frigatebirds, indicating that extrapair fertilizations likely do not play a role in driving the exaggeration of male sexual ornaments seen in this species. We did, however, find a strongly male-biased operational sex ratio. This male-biased sex ratio has the potential to select for male sexual ornaments, although a causal link between these factors remains to be established.
Extrapair paternity
Several observations during this study led us to anticipate a relatively
high frequency of extrapair fertilizations in great frigatebirds. First, of
the dozens of copulations that we witnessed, several were known to be
extrapair. Two of these extrapair copulations were conspecific and two
involved a female great frigatebird and a male lesser frigatebird (F.
ariel; Dearborn and Anders,
2000). It is unlikely that extrapair copulations (EPCs) frequently
involve lesser frigatebirds; rather, heterospecific extrapair copulations were
much more likely to be opportunistically noted by observers than were
conspecific EPCs because lesser frigatebirds were rare on Tern Island
(Dearborn and Anders, 2000)
and there were no mixed-species social pairs. Regardless of the relative
frequency of conspecific and heterospecific EPCs, it is clear that some female
great frigatebirds do engage in EPCs. Second, unlike many Passerines, male
frigatebirds cannot guard their mates during the female's fertile period
because unattended nests will be dismantled by other males competing for nest
material. Because a male could not follow his mate when she left the nest to
forage during her fertile period, the male could neither prevent EPCs nor
assess his likelihood of paternity. Third, within the 14-ha colony, hundreds
of males were potentially available as EPC partners. Fourth, male frigatebirds
have exaggerated secondary sex traits, and the presence of such ornaments is
often correlated with a high frequency of EPFs
(Møller and Birkhead,
1994). Although constraints on mate guarding are not unusual among
seabirds, the presence of sexual ornaments is unique to frigatebirds,
prompting our initial hypothesis that frequent extrapair fertilizations may
occur in frigatebirds.
In contrast to these expectations, we found a low frequency of extrapair
fertilizations in frigatebirds (1 chick out of 92; 1.1%). This result is
consistent with the predictions of a recent model
(Mauck et al., 1999) and with
most empirical studies of seabirds that lack the strong sexual dimorphism seen
in frigatebirds. Previous empirical work with seabirds has shown a low
frequency of extrapair fertilizations for northern fulmars, Fulmarus
glacialis (0%; Hunter et al.,
1992), short-tailed shearwaters, Puffinus tenuirostris
(9-13%; Austin and Parkin,
1996), Cory's shearwaters, Calonectris diomedea (0%;
Swatschek et al., 1994),
Leach's storm-petrels, Oceanodroma leucorhoa (0%;
Mauck et al., 1995), common
murres, Uria aalge (8%; Birkhead
et al., 2001), Humboldt penguins, Spheniscus humboldti
(0%; Schwartz et al., 1999),
royal penguins, Eudyptes schlegeli (4%;
St. Clair et al., 1995), and
chinstrap penguins, Pygoscelis antarctica (0%;
Moreno et al., 2000). Higher
frequencies of extrapair fertilizations have been noted in two seabirds, the
shag, Phalacrocorax aristotelis (18%;
Graves et al., 1992), and the
waved albatross, Phoebastria irrorata (25%;
Huyvaert et al., 2000).
Interestingly, northern fulmars (Hunter et
al., 1992) and Humboldt penguins
(Schwartz et al., 1999) both
exhibit low rates of extrapair fertilizations despite frequent EPCs. In
fulmars, males appear to prevent cuckoldry by performing frequent within-pair
copulations. In Humboldt penguins and also in razorbills (Alca
torda), many EPCs are solicited by females outside of their fertile
period (Schwartz et al., 1999;
Wagner, 1991), suggesting that
these copulations may serve to facilitate appraisal and acquisition of future
mates, as originally proposed by Colwell and Oring
(1989). In great frigatebirds,
the exact frequency and function of EPCs remains to be determined, but
extrapair fertilizations clearly are not common. Despite the apparent impact
of high extrapair fertilization rates on the evolutionary ecology of other
groups of birds (Fleischer,
1996; Gowaty,
1996; Møller and
Birkhead, 1994), sexual selection via extrapair paternity does not
appear to be a major force shaping the mating systems of seabirds in general
or frigatebirds in particular.
Operational sex ratio
The general OSR, defined by the number of unpaired adult males and females
at the breeding colony, was male biased over the mate-choice portion of the
breeding season in both years. The scale and pattern of the general OSR were
strikingly similar in the 2 years, suggesting that the presence and extent of
a male-biased OSR may be a general feature of this system. Limited data from
other populations suggest that a male-biased OSR may be widespread among great
frigatebirds (Diamond, 1975;
Reville, 1983). The decline in
general OSR late in the season was due primarily to an increase in the number
of females on the island. The status of these females (whether they were
nonbreeders, birds whose nests had already failed, etc.) was not known, making
it difficult to interpret the change in general OSR.
The more relevant measure of sex ratio, from the standpoint of sexual
selection, is the immediate OSR. The immediate OSR, defined as the ratio of
males to females currently participating in mate-acquisition behaviors, was
even more strongly male biased than was the general OSR. Moreover, the ratio
of displaying males to mate-seeking females remained strongly male biased over
the entire time that birds were seeking mates and starting nests. Such a skew
in the ratio of males and females that are ready to mate is often correlated
with other measures of intensity of sexual selection (e.g.,
Colwell and Oring, 1988).
An important next step in our system is to assess whether this male-biased OSR does indeed lead to large variance in male reproductive success. Such variance is most likely to arise via female choice, as males rarely compete overtly for display sites or nest sites, whereas females make careful physical inspections of males during mate choice. If the biased immediate OSR reflects an underlying skew in the numbers of males and females attempting to mate in a given season, variance in male pairing success might be a large component of male variance in overall reproductive success. In this case, males with more exaggerated sex traits would be expected to be more successful at attracting a mate. In contrast, if the immediate OSR reflects behavioral differences between males and females (rather than a skew in the number of birds trying to breed in a given season), variance in male reproductive success is more likely to be a result of variance in nesting success of mated males. This could occur in at least two ways: (1) males with more exaggerated traits might attract better quality or better condition females as mates, or (2) males with more exaggerated traits might attract a mate earlier in the season, with earlier mating being advantageous independent of mate quality. An alternative class of explanations is that the male-biased OSR is a behavioral consequence, rather than a cause, of strong sexual selection on males.
Understanding the relationship among OSR, sexual selection, and male
ornaments will require knowledge of the mechanism underlying the skewed OSR.
Demographic mechanisms, such as a skewed sex ratio at hatching or differential
male and female mortality, are possible. However, because the general OSR
declined over the season, while the immediate OSR remained constant and more
strongly male biased, a behavioral explanation is more likely. Behavioral
mechanisms could be of two types: there may be differences in time budgets of
the males and females that are trying to breed in the current year, or males
and females may differ in the frequency with which they attempt to breed. This
last possibility has been the subject of much speculation in the literature
over the past 30 years (Carmona et al.,
1995; Diamond,
1972,
1973;
Nelson, 1975;
Trivelpiece and Ferraris,
1987). Diamond
(1972) hypothesized that males
cease providing care for their chicks early enough to attempt to breed
annually, whereas females continue feeding chicks for a long enough time
period that they cannot attempt to breed during the year following a
successful nest. Of the five frigatebirds species, only magnificent
frigatebirds (Fregata magnificens) seem to exhibit this pattern of
early male abandonment (Osorno,
1999), but additional information on the duration of parental care
and on the frequency of breeding attempts by males and females is needed for
the four other species.
The overall adult sex ratio in birds is often slightly male biased
(typically 1.2 to 1.8 males/female among monogamous species;
Breitwisch, 1989), but
comparative data on OSR are generally scant. Measures of sex ratios in
Pelecaniformes and their allies are largely unavailable, because all other
members of this clade lack pronounced sexual dimorphism, and thus sex cannot
be determined by plumage. Among the few species for which adult sex ratio data
do exist, there is no evidence for a markedly male-biased sex ratio (brown
booby, Sula leucogaster: Gilardi,
1992, Tershy and Croll,
2000; Western grebe, Aechmophorus occidentalis:
Nuechterlein and Buitron,
1998; Buller's albatross, Dimomedea bulleri:
Stahl et al., 1998; Galapagos
cormorant, Compsohalieus harrisi:
Valle, 1995; great cormorant,
Phalacrocorax carbo: Van Eerden
and Munsterman, 1995). More detailed sex ratio data are needed for
this clade, and the recent advent of a broadly-applicable sex-specific
molecular marker (Griffiths et al.,
1998) will make such advances possible.
In summary, we found a low frequency of extrapair fertilizations, but a
strongly male-biased OSR, in this population of great frigatebirds. The
infrequency of extrapair fertilizations is unusual from the standpoint of male
ornaments and female opportunity but not from the standpoint of life history
traits. A strongly male-biased OSR has the potential to be a selective force
driving the unique derivation of male sexual ornaments in frigatebirds;
previous studies have demonstrated a positive relationship between skew in OSR
and strength of sexual selection (Kvarnemo
et al., 1995; Lawrence,
1986). Additional work is needed to determine whether the skewed
OSR in this system leads to variance in male reproductive success. Comparative
OSR data from other frigatebird species and from monomorphic Pelecaniformes
would also provide information on the relationship between a skewed OSR and
sexual dimorphism in these species.
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ACKNOWLEDGEMENTS |
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We thank the U.S. Fish and Wildlife Service, especially Beth Flint and Brian Allen, for logistical support and access to Tern Island. Assistance with blood collection was generously provided by Chris Hoeffer, Holly Ober, and Ram Papish. Two anonymous reviewers made helpful comments on the manuscript. Funding was provided by an Ohio State University Postdoctoral Fellowship to D.C.D. and a grant to D.C.D. from the American Philosophical Society. Additional support was provided by the Ohio State University and by the Parker lab, especially Nidia Arguedas, José Diaz, and Brad Worden.
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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