Behavioral Ecology Vol. 10 No. 6: 626-635
© 1999 International Society for Behavioral Ecology
Sex ratios and sexual selection in socially monogamous zebra finches
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697-2525, USA
Address correspondence to N. Burley. E-mail: ntburley{at}uci.edu .
Received 2 October 1998; accepted 30 March 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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An experiment was performed in which adult sex ratios of zebra finches, Taeniopygyia guttata castanotis, were varied to test possible effects of adult population sex ratios on sexual selection intensity and mating system dynamics in species with biparental care. The possibility that sex ratio influences the success of social mating patterns (leading to polygyny when males are rare and polyandry when females are rare) was not supported. Results did support the prediction of the differential allocation hypothesis that individuals of the abundant sex would increase their relative parental expenditure (PE). Although total (male + female) PE did not vary between treatments, relative male PE was significantly higher in the male-biased treatment (MBT; sex ratio 64% male) than in the female-biased treatment (FBT; sex ratio 36% male). In both treatments, male PE contributions contributed to female reproductive rate. Results also supported the prediction of the differential access hypothesis that individuals of the abundant sex would experience greater intensity of selection on sexually selected attributes. Male beak color, a sexually selected trait, influenced male social parentage in the MBT but not in the FBT. Finally, broods in the FBT displayed higher hatching asynchrony and lower hatching success; we believe this was caused by early onset of incubation, a tactic used as a defense against intraspecific brood parasitism, which was much higher in the FBT. Population sex ratios may be an important factor affecting female ability to influence male parental investment patterns.
Key words: differential access, differential allocation, parental investment, sex ratio, sexual selection, social monogamy, zebra finches.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Researchers have long debated the relationship between adult sex ratio and population mating system. At the core of the debate is the question, do mating systems impact adult sex ratios (e.g., Koenig and Pitelka, 1981
;
Selander, 1965;
Willson, 1984;
Willson and Pianka, 1963;
Wittenberger, 1976), or do
adult population sex ratios cause mating patterns (e.g.,
Murray, 1984,
1985;
Rowley, 1965;
Wiley, 1974) ? Frankly
polygynous species (Johnson and Burley,
1997), for example, often display female-biased sex ratios. A
female-biased sex ratio may cause polygyny because "surplus"
females become willing to accept already-mated males as mates (as in song
sparrows; Smith et al., 1982).
In contrast, a female-biased sex ratio may result from polygyny because
polygynous males engage in mating investment that increases relative male
mortality rates (e.g., Berger,
1983; Lindstrom and Kokko,
1998; Selander,
1965). These two hypotheses (mating system affects sex ratio; sex
ratio affects mating system) are not necessarily mutually exclusive. Instead,
there may be feedback between the two processes.
Recent references to the idea that sex ratios impact mating systems
typically refer to operational sex ratios (OSRs)
(Emlen and Oring, 1977) rather
than population sex ratios. These two concepts are not synonymous. OSR refers
to the relative numbers of males and females in a population that are
available for pairing/copulation at any given time. OSRs are affected by adult
sex ratios (e.g., Clutton-Brock and
Parker, 1992), but they also reflect parental investment patterns
and tendencies toward extrapair matings. OSR is thus better viewed as a mating
system component than as an independent determinant thereof
(Burley and Parker, 1997).
Accordingly, we focus on adult sex ratios here.
To explore the role of sex ratios on mating system dynamics of species with
biparental care, we investigated possible consequences of changes in the
intensity of sexual selection resulting from sex ratio biases. Sex ratios may
affect patterns of social mating, resulting in frankly polygynous unions when
females are numerous or in polyandry when males outnumber females (e.g.,
Jouventin, 1982;
Maynard Smith and Ridpath,
1972; Smith et al.,
1982). Sex ratios may impact parental investment (PI) patterns
(Breitwisch et al., 1986;
Keenlyside, 1983). In species
with substantial biparental care and mate choice by both sexes, individuals of
the rarer sex have an advantage in mate choice by virtue of their short
supply. They may tactically prefer as social mates (individuals that share
offspring caregiving) those opposite-sex individuals that signal willingness
to incur relatively high PI ("differential allocation";
Burley, 1986b,
1988). Strategic choosers
benefit by reducing their PI, thereby increasing their residual reproductive
value.
The differential allocation hypothesis is based on the idea that individuals of both sexes can tactically respond to a situation, such as a locally skewed sex ratio, that impacts their mate-getting ability. This hypothesis thus predicts that the percent male contribution to offspring rearing (male PI/ total PI) should vary directly with the adult sex ratio (number of adult males) / (total number of adults). If males and females benefit equally from facultative adjustment of PI, one expects no net change in the total PI/brood, only changes in the percent male contribution. Alternatives include the possibility that only one sex facultatively adjusts PI; thus, females might have evolved set PI loads near their sustainable maximum, whereas males, with lower PI, might have greater capacity for tactical variation. If this were true, one would expect total PI/brood to vary with sex ratio. Another alternative, of course, is the null hypothesis; lack of responsiveness to population sex ratio might occur in species with large and fluid populations in which sex ratio imbalances have seldom occurred, or where constraints limit opportunity to retaliate against a social mate that fails to provide high PI (see Discussion below).
Finally, sex ratios may impact the relative intensity of sexual selection
via a direct effect on differential mate access
(Burley, 1977,
1983,
1986b). "Differential
access" means that preferred individuals have greater access to
potential mates, while nonpreferred individuals must mate with any willing
partner. When sex ratios are biased, effects of differential access are
weakened for the rare sex and increased for the common sex.
We tested the above hypotheses by establishing two captive populations of
zebra finches (Taeniopygia guttata castanotis) with complementary sex
ratios (64% versus 36% male; the typical tertiary sex ratio is about 52% male;
Burley et al., 1989). Zebra
finches are gregarious and nonterritorial socially monogamous estrildines.
They feed in flocks and nest in loose colonies
(Goodwin, 1982). Nonbreeders
intermingle with breeders (Burley et al.,
1989, unpublished data), such that information on local sex ratio
appears available to birds. Additional factors that make zebra finches
appropriate for this research include the following: (1) they display
substantial biparental care of young; (2) they demonstrate a capacity for
tactical variation in PI by both sexes
(Burley, 1986b,
1988); and (3) they readily
breed in captivity, tolerating a wide range of adult sex ratios. Domesticated
birds resemble wild birds closely in conformation and behavior and display
similar parental time budgets (Burley N, Solomon N, and Zann R, unpublished
data).
We expected that caregivers in the two treatments would experience different challenges to their genetic parentage: in the female-biased treatment (FBT), we expected intraspecific brood parasitism (IBP) to occur at an elevated rate; in the male-biased treatment (MBT), we expected extrapair fertilization (EPF) rates to be elevated. Accordingly, we collected data on possible tactics used to defend parentage.
One possible defense against IBP is close nest attendance (e.g.,
Lank et al., 1989) and onset
of incubation shortly after clutch initiation. Such behavior may physically
prevent laying of parasitic eggs. We thus expected greater hatching asynchrony
in the FBT than in the MBT. A competing hypothesis
(Slagsvold and Lifjeld, 1989)
is that females start incubation early to accelerate hatching and thus
increase their mate's share of PI. While this hypothesis was formulated for
species in which only females incubate, it could also apply to species, such
as the zebra finch, in which a male's share of incubation is typically lower
than his share of other parental activities. According to Slagsvold and
Lifjeld's hypothesis, we should see a positive correlation between hatching
asynchrony and male PI within treatments.
A limitation of this study is that we lacked resources to measure EPF rates
directly, although we could document a known correlate of such rates
("rapid renesting rate";
Burley et al., 1996). We were
able to identify eggs and young produced through IBP using techniques
previously developed (Fenske and Burley,
1995). Based on previous findings
(Burley and Parker, 1997;
Burley et al., 1996), we
expect that our measures of female social parentage correspond closely to
genetic parentage. For that reason, we focus several analyses on female
fitness.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Experiment initiation and husbandry protocol
Birds used in these experiments were young adults from two outcrossed populations ("A" and "B") of wild-type zebra finches maintained in the laboratory. In the FBT, females from population A and males from population B were used. In the MBT, males came from population A and females from population B.
The FBT was initiated 2 months after the MBT. Before the MBT began, we
created two pools of birds, one consisting of potential founders of the FBT
and the other for the MBT. At the time experiments began, birds were selected
so that the two experimental populations were similar with regard to several
traits. Distributions of these traits were controlled for the following
reasons: age may affect a bird's willingness to incurparental care, and beak
color is used in mate choice (Burley and
Coopersmith, 1987) and affects reproductive success of both sexes
(Price and Burley, 1994). With
the exception of male song rate (Balzer and
Williams, 1998; Houtman,
1992; but see Burley and
Coopersmith, in press), such effects have not been found for most
other phenotypic variables thus far investigated (Burley N, unpublished
data).
Finally, tail stripes of birds in candidate pools were scored because many birds were missing some fraction of striped tail coverts at the time the two experimental pools were selected. There was no difference in tail stripe scores between males or females assigned to the two treatments (t test, p >.20).
In the 2-month interval between the start of the MBT and start of the FBT, FBT candidates were held in unisexual flights. During this interval, FBT males grew additional tail stripes. Thus, at the time treatments began (but not when birds were assigned to treatments), FBT males had higher tail stripe scores than MBT males (mean ± SE: FBT, 0.91 ±.04; MBT, 0.55 ±.08; t = -3.27, 53 df, p =.002). No other significant population differences were present at the time of experiment initiation for phenotypic traits measured.
Before release into breeding aviaries, birds were randomly assigned
color-band combinations for individual recognition. Each bird wore two bands
per leg. Color band combinations used only colors previously shown to be of
neutral attractiveness to zebra finches
(Burley, 1985); moreover, the
two distal bands were of identical color to minimize phenotypic asymmetry and
its possible behavioral consequences
(Swaddle and Cuthill,
1994).
We established populations by simultaneously releasing adults into a breeding aviary. Initially, the treatments were to have reciprocal 2:1 sex ratios. Thus, the MBT was initiated using 40 males and 20 females as founders. Two weeks into the MBT, it became apparent that early nesting attempts of birds were being destroyed by conspecifics at an atypically high rate. Observations confirmed that this destruction was being performed by males lacking social mates; five such males were removed, after which pairs were better able to defend their nests. These five males are excluded from all analyses, as are two females that were accidentally released into the aviary about 4.5 months into the experiment. Thus, the sex ratio of this treatment was 63.6% male (35 males/55 total adults). Mean age (± SE) of male founders at the start of the MBT was 145 ± 6.4 days; that of females was 151 ± 8.7 days.
FBT founders included 20 males and 36 females. The sex ratio of this treatment was thus 35.7% male (20 males/56 total adults). Mean age of male founders was 139 ± 5.1 days, and that of female founders was 133 ± 5.0 days.
The experiment was conducted in large flights (approximately 50
m3) illuminated by Vitalights and standard flourescent bulbs and
under constant photoperiod (14 h light: 10 h dark). Husbandry procedures
closely adhered to those used previously
(Burley, 1986b). Most
resources (commercial finch seed mix, water, grit, cuttlebone, nestling food;
straw and grass for nest building) needed for reproduction were available
adlibitum. The remaining resources were added frequently (cotton batting for
nest lining; fresh food). Numerous nesting sites were available; each flight
contained 90 plastic nest cups set inside stainless-steel compartments.
At the end of the experiment, breeding was terminated by removing nest cups after young fledged. The duration of the FBT was 162 days; the duration of the MBT was 239 days.
Phenotype measurements
Birds were hand-held while they were measured for beak and tail traits. We
measured beak color using the Munsell Book of Color
(Burley and Coopersmith,
1987). For analysis purposes each bird's measurements (one each
for hue, value, and chroma) were transformed into a single composite numeral
(Burley et al., 1992). Beak
scores produced by this procedure correlate with fitness of birds in
experimental colonies (Price and Burley,
1994) in ways consistent with predictions of matechoice
experiments (Burley and Coopersmith,
1987, in press).
Thus, these scores appear to be meaningful representations of beak color as
perceived by zebra finches.
We measured tail stripe scores as the percentage of the rump area covered with stripes in a fully feathered bird that was actually covered in the bird being measured. Scores ranged from 0 (a bird missing all its striped coverts) to 1 (full feather coverage).
Reproductive variables
We determined social parentage of a clutch by scan sampling adult
attendants at active nests from a vantage point just outside the aviaries.
Attendants at each nest were identified multiple times over the 5-week nesting
cycle. We checked nests daily at midday and scored them for number of eggs and
offspring. Eggs were scored as deriving from IBP if they were different in
size or proportions from the rest of the clutch
(Fenske and Burley, 1995). A
deviant egg was often added on the same day as a native egg, which alerted us
to inspect egg proportions. Fates of IBP eggs were monitored by frequent nest
inspection at hatching time; hatchlings were marked with water-based colored
pens. We banded nestlings with numbered seamless aluminum bands about 11 days
after hatching. Juveniles were removed from aviaries at about 50 days of
age.
We standardized individual reproductive rates between treatments by dividing the number of young surviving to independence (2 weeks after fledging) produced by each social parent by the respective experimental intervals. Hatching asynchrony rate was calculated as the hatching span (in days) divided by the number of hatchlings for each nest. The mean hatching asynchrony of each social parent was calculated for all clutches with two or more hatchlings in which no IBP eggs were found. We also scored the hatching asychrony of each focal nest containing two or more hatchlings. Rapid renesting rate was the fraction of all clutch attempts of a social parent that were abandoned during or after egg laying and in which new clutches were initiated before the first possible hatch date of the abandoned clutch (12 days after the first egg date).
Behavioral measurements
Behavioral data were gathered by undergraduate researchers who were not
informed of the test hypothesis. Procedures were similar to those previously
reported (Burley, 1988).
Observers were trained to conduct focal nest sampling
(Altmann, 1974) of active
nests. Focal sampling involved monitoring the same nesting attempt throughout
the 5-week nesting cycle (except in four cases in which it was necessary, due
to sampling constraints, to combine prehatch days of one clutch with the
posthatch days of another for the same pair). Each day, 4-6 nests were
monitored, depending on observer availability; whenever possible, both a
morning and afternoon sample were collected for each focal nest (mean ±
SE of sample number per pair: FBT, 62.2 ± 1.7; MBT, 57.8 ± 1.6).
When one nest fledged, a new nest was selected for observation by locating a
recently initiated nesting attempt (containing two or more eggs) of a pair not
yet successfully observed.
Each focal nest sample lasted 15 min, during which observers recorded the arrival and departure of social parents and all of the activities engaged in by both parents in the immediate vicinity (within 0.5 m) of the nest. Activities were scored on a laptop computer, which recorded durations of timed events. Most activities were scored as timed events. Exceptions to these were agonistic activities whose typical durations were too short to be accurately scored. These activities were scored as "instantaneous" events, but observers ranked them for relative intensity and noted unusually long durations.
For purposes of analysis, parental activities were partitioned into four categories: active caregiving, or time spent nest building, nest inspecting, and feeding young; passive caregiving, time spent inside the nest in a position consistent with incubation/brooding; active defense, social interactions scored as "instantaneous"; and passive defense, time spent perching in the vicinity of the nest ("surveying") and time spent sitting high in the nest while "looking out" (see Table 1 for descriptions of behaviors). Both sexes of zebra finches typically participate in all four categories of activities.
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To minimize ambiguity in interpretation of results, data likely to reflect mating investment (expected to be higher in the MBT) or defense against intraspecific brood parasitism (IBP; expected to be higher in the FBT) were dropped before analysis. One ambiguous category of behavior is "incubation." In these experiments, warming of eggs/young was not ascertained but was inferred from the posture of the social parent. Parents, however, attend nests even before egg laying and also sometimes later in the developmental period when young no longer require brooding. Nest attendance at these times may be associated with mating investment (Enstrom D and Burley N, unpublished data) and/or defense against IBP. Thus, time spent in passive care is presented here only for the week immediately preceding hatching of the first egg (week 2: day —7 to day —1), and the week that includes first hatch date (week 3: day 0 to day 6). During weeks 2 and 3, eggs/young require incubation/brooding for development, and competing functions appear minimal. Similarly, data on active defense are excluded for those week 1 days (day —14 to day —8) during which egg laying occurred, as defense activities occurring on those days may represent male guarding of fertile females (Birkhead and Møller, 1992
) or defense against IBP
(Fenske and Burley, 1995).
The rationale for dividing parental expenditure (PE) into active versus
passive categories is that the active behaviors, though typically of shorter
duration, are expected to have higher costs (e.g., metabolic costs; risks of
injury or death), and thus greater impact on fitness. Such costs, though
measurable in principle, were not measured here. (Thus we refer to PE rather
than PI.) Finally, the impact on fitness of some passive activities that birds
engaged in commonly might be trivial. Birds resting in a nest cup, for
example, scored here as incubating, may be expending no more energy than birds
would necessarily spend perching somewhere else in the aviary (see also
Burley, 1988).
Analyses
Nonparametric (Kruskal-Wallis, Mann-Whitney and Spearman rank correlation)
tests were used to compare treatments for a number of phenotypic,
reproductive, and behavioral attributes. Forward stepwise regression
(p to enter and p to remove set at 0.15) was used to
evaluate contributions of phenotypic and behavioral attributes to the
reproductive rates of males and females in both treatments. Behavioral data
(percent male share of four components of parental care) were arcsine
transformed before inclusion in regression analyses. These tests were
performed using Systat 7.0 routines
(Wilkinson, 1996). Fisher's
Exact test (Zar, 1984) was
performed by consulting tables in Finney et al.
(1963). The binomial exact
test (Zar, 1984) was
hand-calculated to measure the probability that a suite of results occurred by
chance.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Brood characteristics and per-brood PE of focal nests
Because parents might allocate PE based on brood characteristics (e.g., Gowaty and Droge, 1991
;
Patterson et al., 1980;
Yasukawa et al., 1990), we
examined brood characteristics of focal nests from the two treatments. No
differences were found for the following traits (except where otherwise noted,
sample sizes were 11 and 12 unique pairs for the FBT and MBT treatments,
respectively, and values for each pair were averaged over all clutch
attempts): laid clutch size (p =.25), number of hatchlings
(p =.92), number of offspring surviving to independence (p
=.85), and brood sex ratio (males/total progeny surviving to sexing age of
about 45 days: FBT, n = 10; MBT, n = 10; p =.59).
There were also no population differences in these traits for all pairs in the
experiment, with the exception of mean number of hatchlings per brood, which
was lower in the FBT (see below). We also explored whether the total (male and female) average daily PE per nest differed between treatments. We found no significant differences between the FBT and the MBT for any of the four major categories of PE (Table 2). Within "active care," the average time spent in nest inspection was marginally greater for FBT nests. Of all parental behaviors sampled, nest inspection makes the smallest contribution to the parental time budget. None of the other behaviors partitioned within major categories displayed a significant difference (Table 2).
Within-treatment correlation analyses were performed to determine whether relative participation across categories of PE was independent. One of 12 correlation analyses was significant. Specifically, in the FBT, there was a significantly positive correlation between participation in active and passive defense (0.74; p <.02). In the reciprocal population, however, this correlation was negative (-0.33; p >.20). Overall, the direction of (nonsignificant) correlation was concordant across treatments for two of six comparisons. These results indicate that relative participation in the four categories of parental activities is not inherently linked; participation in active care, for example, does not consistently predict participation in any other category of behavior. Therefore, the four categories must be treated as independent components of PE.
Differential allocation
To explore whether the percentage of PE engaged in by the sexes varied as
predicted by the differential allocation hypothesis, we compared the average
percent male contribution (male PE/total PE) for the 5-week sample of each
focal nest between treatments. Percent male contribution was significantly
higher in the MBT for three of four categories of PE: active care, passive
defense, and active defense (Figure
1). No difference was found in relative male contribution to
passive care (incubation). The binomial probability of three or more of four
comparisons being significant by chance is.0005
(Table 3); the probability that
three or more of four comparisons, all with results in the same predicted
direction, occurred by chance is.00006
(Table 3).
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In sum, results strongly support the differential allocation hypothesis: males made a greater contribution to active care and both categories of nest defense in the population (MBT) in which male access to social mates was restricted by sex ratio considerations. There were no overall differences in total PE to broods in the two treatments, however, suggesting that both sexes display similar tactical capacities to vary PE.
To explore the hypothesis that females extract greater male PI by early onset of incubation, we ran correlation analyses between the four major PE categories (Table 2) and the hatching asynchrony of focal clutches for each treatment. Six of eight correlations were negative (males at nests with greater asynchrony had lower PE), but none was significant (Table 4). (The probability of six or more of eight correlations being negative by chance is.14.) Thus, hatching asynchrony does not appear to be a mechanism by which females increase male PI (see also below).
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Reproductive success and number of mates
Reproductive rate was measured as the number of social offspring surviving
to independence divided by the duration (in days) of the treatment. For
females, reproductive rate was higher in the MBT (median: FBT, 0.006,
n = 35; MBT, 0.025, n = 20; U = 490.5, p
=.013). Females in the MBT also tended to have greater numbers of social mates
per treatment interval (FBT, 0.006; MBT, 0.004; U = 248, p
=.055).
For males, reproductive rate also varied between treatments. Males in the FBT had higher social parentage (0.031, n = 20) than those in the MBT (0.017, n = 35; U = 217.5, p =.020). Males also obtained more social mates per unit time in the FBT (FBT, 0.006; MBT, 0.004; U = 73, p <.0001).
We also examined the impact of the actual number of social mates (as opposed to their daily rate) on reproductive rate within experiments. In both treatments, the number of social mates influenced reproductive success of the overrepresented sex (Figure 2). This trend is attributable to the failure of individuals lacking social mates to reproduce successfully. For individuals of the underrepresented sex, however, having more than one social mate did not increase social parentage.
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In sum, both sexes reproduced at a higher rate when they were the underrepresented sex. This trend was caused largely by the opportunity of all individuals of the underrepresented sex to obtain social mates. Neither sex benefited from having multiple social mates.
Defenses against kleptogamy
We expected that caregivers in the two treatments would experience
different challenges to their genetic parentage. Intraspecific brood
parasitism (IBP) was expected to be higher in the FBT as a result of attempted
reproduction by females lacking social mates. Extrapair fertilization (EPF)
was expected to be higher in the MBT as the result of attempted reproduction
by males lacking social mates.
Relative incidence of IBP was measured as the fraction of parasitic eggs in
the nests of each female. As expected, IBP egg rate was much higher in the FBT
(median: FBT, 0.095, n = 28; MBT, 0.000, n = 20; U
= 126.5, p <.0001). We compared the relative number of females in
the two experiments whose nests contained IBP eggs and fledglings. At both
stages, a significantly greater percentage of nests was parasitized in the FBT
(Table 5). Data for hatchlings
are not presented here because of the ambiguity caused by eggs that disappear
at hatching time: it is not clear the extent to which such disappearances
resulted from egg burial (especially of late-to-hatch eggs) or from brood
reduction by hatchling eviction (e.g.,
Burley, 1986a).
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One defense against IBP eggs laid early in a clutch sequence is rapid
renesting (Fenske and Burley,
1995). The rate of rapid renesting is the fraction of all nesting
attempts of a female that were abandoned and replaced before the abandoned
attempt could have hatched. Rapid renesting also occurs in response to EPF
(Burley et al., 1996). The
rate of rapid renesting did not differ significantly between treatments (FBT,
0.000, n = 23; MBT, 0.167, n = 20; U = 268,
p =.34).
Rapid renesting is seldom practiced in response to IBP that occurs at the
end of the laying sequence (Fenske and
Burley, 1995). We hypothesized that caregivers in the FBT, which
were at risk for IBP, might commence incubation early to physically prevent
parasitic egg laying. By this reasoning, greater hatching asynchrony of broods
might be expected in the FBT. On the other hand, if nest attendance by fertile
females in the MBT resulted in egg warming (see Methods), comparable levels of
hatching asynchrony might be expected in the two experiments.
Differences in hatching asynchrony between clutches containing IBP eggs and those without IBP eggs could occur simply because of greater laying asynchrony of clutches containing IBP eggs. To determine if birds at risk of IBP used tactics to limit its occurrence, we compared the hatching asynchrony scores for clutches not containing IBP eggs. Hatching asynchrony of such clutches was significantly higher in the FBT (0.905, n = 10) than in the MBT (0.167, n = 19; U = 44, p =.019). Hatching asynchrony was negatively correlated with female reproductive rate in the FBT (r = -.598, n = 10; p <.05); these variables were not significantly correlated in the MBT (r =.122, n = 19; p >.50).
Finally, we explored the possible source of the different trends in the effects of hatching asynchrony on female reproductive success in the two treatments. Egg rate (number of native eggs laid divided by treatment interval) did not vary between females in the two treatments (FBT, 0.068, n = 35; MBT, 0.094, n = 20; U = 437, p =.13). Percent hatching sucess, however, was much higher for females in the MBT (0.65, n = 20) than in the FBT (0.23, n = 28; U = 456.5, p <.0001). As noted earlier (see Methods), "hatching success" actually reflects losses at both the egg stage (especially through burial) and the hatchling stage (through eviction of hatchlings from the nest). In the FBT, mean hatching asynchrony was negatively correlated with mean hatching success (r = -.730, n = 10, p =.017), whereas these variables were not correlated for females in the MBT (r =.191, n = 19, p =.43). As a result, mean number of hatchlings per clutch differed between treatments (FBT, 1.00, n = 28; MBT, 2.33, n = 20; U = 428, p <.002).
Females in the FBT compensated for low hatchling number by enhanced survival of nestlings. "Nestling success rate" (number of nestlings surviving to independence/number of hatchlings) was higher for females in the FBT (0.74, n = 22) than in the MBT (0.50, n = 19; U = 106, p =.007).
Phenotype and social parentage
Based on previous results (Burley and
Coopersmith, 1987, in
press; Price and Burley,
1994), we expected FBT females with less red beaks and MBT males
with redder beaks to have greater mate-getting ability and thus higher
reproductive success than their same-sex competitors. Results of a prior
breeding experiment (Price and Burley,
1994) indicated that red beak color in males was a sexually
selected trait unrelated to male viability, but that female beak color
reflected viability as well as male mate preference. Thus, we expected results
for females to be more likely to show an effect of beak color on reproduction
regardless of whether they were the overrepresented sex; we expected an effect
of beak color on reproduction for males only when they were overrepresented.
When males were underrepresented, all males could obtain good mates, such that
red-beaked males would lose their sexually selected advantage. We also
explored the relationship between tail stripe score and reproductive rate.
Beak color and tail stripe score were not correlated for either sex in either
treatment (all p >.5).
In the FBT, for females, the best regression model (adjusted r2 =.183, n = 36, p =.035) included beak score (r = -.002, p =.042) and tail score (r = -.015, p =.113). For males, no significant model was generated, but the best model (adjusted r2 =.066, p =.144) included tail score (r = -.049). Thus, female beak score varied as predicted, and male reproductive success was independent of beak score. For both sexes, the relationship between reproductive success and tail score was negative.
In the MBT, for females, the best regression model (adjusted r2 =.381, n = 20, p =.017) included beak score (r = -.003, p =.066) and tail score (r =.019, p =.019). For males, the best regression model (adjusted r2 =.232, n = 35, p =.006) included beak score (r =.002, p =.010) and tail score (r =.012, p =.025). Thus, for both sexes, beak scores varied in the direction predicted (females with less red beaks and males with redder beaks having higher reproductive success). Moreover, for both sexes, birds with greater numbers of tail stripes accrued higher reproductive success.
In sum, female beak score was inversely proportional to reproductive rate in both experiments. Male beak score affected male reproductive rate only when males were overrepresented. Tail stripes positively predicted reproductive rate of both sexes in the MBT, but negatively predicted female reproduction in the FBT.
Impact of male contribution on female fitness
One additional stepwise regression analysis was performed for females of
each population. In this model we added as independent variables the percent
male contributions made for each category (passive and active care, passive
and active defense) as well as major variables previously identified as
affecting female reproductive success (beak score, tail score, hatching
asynchrony). Reproductive rate remained the dependent variable.
For females in the FBT, the best model generated by this approach (adjusted r2 =.807, n = 10, p =.004) included percent male active defense (r =.001, p =.004), hatching asynchrony (r = -.045, p =.008), and female tail score (r = -.027, p =.029). For females in the MBT, the best resulting model (adjusted r2 =.889, n = 11, p =.001) included two of the four paternal contribution rates (active care: r =.001, p =.026; passive care: r =.001, p =.043), as well as two variables found to be significant previously, hatching asynchrony (r =.066, p =.001) and tail score (r =.034, p =.000).
In sum, in both treatments male PE contributed to female reproductive success. Tail scores and hatching asynchrony continued to show opposite effects on female reproductive rate in the two experiments.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Differential allocation
Results of this experiment are consistent the main prediction of the differential allocation hypothesis. In breeding populations with adult sex-ratio biases, individuals of the overrepresented sex facultatively increased relative PE to obtain and/or retain cooperative breeding partners. Significant differences in the predicted direction between treatments were found for three of four PE categories, including both categories (active care, active defense) in which PE is most likely to represent PI. Results of regression models indicate that female fitness (as measured by relative reproductive rate) in both populations improved as a result of greater male contribution of active care and/or defense. The FBT showed somewhat weaker trends than the MBT. We believe that this result occurred in part because of the shorter duration of the experiment.
Differential allocation also occurred in a previous series of experiments
in which mating attractiveness of both sexes was varied by non-neutral
band-color manipulations, but in which population sex ratios were established
and maintained at close to 50% male
(Burley, 1988). The previous
experiments were substantially longer (one ran for almost 2 years), and
observed discrepancies in relative male contribution increased over the
duration of the experiments, suggesting that mated individuals continually
assess their ability to obtain/retain mates and adjust their PE. The fact that
similar trends were observed in the current, shorter experiment indicates that
birds have some ability to make appropriate assessments and adjustments of PE
relatively early in their reproductive lives. Precisely how birds determine a
potential mate's willingness to invest and use this as a criterion of mate
choice (Trivers, 1972) has yet
to be investigated. Research on this question would require a detailed
analysis of consortship patterns during and after pair formation.
These results also indicate that an individual of either sex may practice
differential allocation in response to a variety of opportunities and
constraints that he or she may encounter. Thus, individuals of both sexes
attempt to manipulate each other's relative contribution of PI. This
perspective is in contrast to the view, reflected in the hypotheses of
Weatherhead and Robertson
(1979) and Gowaty
(1996), that individual males
are selected to be tactically manipulative of female PI and that, while
females may be selected to resist manipulation, they lack ability to extract
PI from males. Specifically, Weatherhead and Robertson predicted tactical male
manipulation, but not female resistance: in their view, females will opt to
pair with more attractive males for the genetic benefits accruing (the
"sexy son" hypothesis), even though such males tactically reduce
PI. Gowaty's (1996)
"constrained female" hypothesis also predicts male manipulation
through tactical responses after assessment of female reproductive capacity.
Thus, for example, a male may decline to provide PI if he assesses that his
mate can reproduce successfully alone. Both of these hypotheses assume that
females choose mates for heritable traits that affect offspring viability
and/or offspring mating attractiveness, not on the basis of expected male
parental care. Thus, male caregiving is determined by male assessment of its
contribution to his fitness, not in response to female manipulation.
The view that only males can tactically manipulate PI may be applicable to
some cases in which female-only care produces offspring of quantity and
quality close to that resulting from biparental care (e.g.,
Gowaty, 1996;
Ketterson and Nolan, 1994).
Even in such cases, however, females may be selected to influence male PI
patterns if there is some fitness cost to females of assuming all parental
care duties. A tactic possibly available to females of many species is the
"rewarding" of parental males by conferring them relatively high
paternity of subsequent broods
(Freeman-Gallant, 1998).
Population sex-ratio effects may also be significant here: where sex ratios
are typically female biased, females should have less influence on male
caregiving patterns; where sex ratios are even or male biased, male caregiving
performance may influence a female's tendency to attempt more than one clutch
with a given male (Johnson and Burley,
1997). In gregarious species, females might even evaluate the
tendency of neighboring males to contribute PI and use this information in
subsequent mating decisions. Thus, female manipulation of male PI may take
relatively subtle forms.
In theory, incurring high PI should reduce residual reproductive value,
most likely through decreased survivorship
(Trivers, 1972). Differential
allocation could lead to increased mortality of the overrepresented sex in
natural populations, thereby generating a frequency-dependent process that
would tend to equilibrate population sex ratios. In nature, however, other
processes may cause tertiary sex ratios to deviate significantly from 50%
male. In many birds, for example, mortality of females during natal dispersal
is thought to generate male-biased tertiary sex ratios
(Breitwisch, 1989). Thus, if
female-biased dispersal evolved early in avian lineages, differential
allocation might have contributed to the evolution of substantial male care in
birds (Burley N and Johnson K, manuscript in preparation).
To the best of our knowledge, this is the only experimental study to
investigate differential allocation in response to adult sex ratio in birds.
When Keenlyside (1983)
modestly varied the population sex ratio of captive cichlid fish, he found
that males abandoned clutches and re-paired when faced with a surplus of
females, whereas females did not abandon in a male-biased environment. His
explanation for this sex difference was that the male intermating interval was
inherently lower by virtue of the lower cost of male gamete production, thus
suggesting that the OSR differs from the population sex ratio in this species
(see Introduction). We did not find a tendency toward abandonment in zebra
finches, which produce altricial young that require biparental care. Clearly,
members of different taxa will experience different opportunities and
constraints that shape reproductive tactics
(Burley and Parker, 1997).
Sexual selection and social monogamy
Our ability to interpret results in light of sexual selection theory is
constrained by the fact that we were unable to assign genetic parentage of
offspring in these experiments. Several trends are nevertheless noteworthy.
First, individuals of the underrepresented sex in both experiments were unable
to capitalize on their scarcity by gaining an additional social mate
(Figure 1). Had the experiments
continued for a longer period of time, an increase in the occurrence of social
bigamy might have been observed (see above and
Burley, 1988). The failure of
birds to benefit from bigamy in an environment of virtually unlimited
resources clearly suggests that this species is not preadapted to evolve
"frank polygamy" (Johnson and
Burley, 1997), even under the most permissive conditions.
Variation in adult population sex ratio, then, in this species (and perhaps in
estrildine finches generally) does not appear to be a viable route to major
mating system evolution (as suggested by
Murray, 1984;
Breitwisch, 1989).
Second, results reinforce earlier conclusions regarding the significance of
beak color variation in zebra finches
(Price and Burley, 1994): (1)
male beak color is a sexually selected trait and (2) female beak color is
under both sexual and natural selection. In the MBT, where opportunities for
female mate choice were great, male beak color affected male reproductive
success. In the FBT, however, where opportunities for female mate choice were
limited, beak color did not affect male reproductive success. Female beak
color influenced female reproductive success both when males had considerable
opportunity for choice (FBT) and when male mate choice was minimal (MBT).
Tail stripes are a sexually dimorphic trait in zebra finches (males have longer striped coverts with higher contrast; Burley N, unpublished data), whose possible social function has largely been unstudied. The stripes are often a target of intraspecific aggression, and loss of stripes is typically associated with high population densities. The rapid regrowth of tail stripes by FBT males in the interval between the initiation of the MBT and the FBT experiments probably resulted from the much reduced density in unisexual cages following removal of the MBT males from those cages. The MBT results, in which presence of tail stripes contributed to high reproductive success of both sexes, suggest that number of tail stripes might be used in mate choice and/or is an accurate indicator of competitive ability. The FBT results, by contrast, do not show this pattern. Instead, they suggest that presence of tail stripes is associated with low reproductive success. Further work is needed to explore the possible significance of these conflicting results.
IBP and hatching asynchrony
IBP rate was higher in the FBT, and in that treatment it was negatively
associated with reproductive rate. Costs associated with IBP include direct
(through acquisition of PI by IBP young) and indirect costs. Asynchrony
patterns reflect a possible indirect cost. We hypothesize that increased
asynchrony in the FBT was the result of onset of incubation shortly after egg
laying began. This behavior reduced IBP but resulted in reduced brood size at
hatching. Although in some species, asynchrony may reduce parental fitness by
increasing the relative competitive advantage of older hatchlings
(Clark and Wilson, 1981), this
pattern was not observed here. Rather, brood size was reduced at such an early
stage that older siblings were unlikely to have directly caused it. It may
have been the case, however, that such a competitive advantage would have
developed within a week or so, making it unprofitable for parents to care for
late-hatched young. Thus, it is likely that parents buried slow-to-hatch eggs
or evicted late-hatched young. A similar reduction in brood sizes of
parasitized zebra finches was reported in a previous experimental
investigation of IBP (Fenske and Burley,
1995).
Future directions
With the advent of modern molecular techniques, the study of animal mating
systems is enjoying a much-needed renaissance, as the relationships between
genetic and social components of mating systems become open to investigation
(Parker and Burley, 1997). In
turn, the importance of investigating sex ratio effects will increase because
population sex ratios may have substantial effects on variation in the number
of genetic mates that individuals of each sex obtain
(Arnold and Duvall, 1994) and
consequent mating tactics displayed in populations
(Johnson and Burley, 1997).
The research reported here indicates that sex ratio influences multiple
reproductive tactics. Further work should include investigation of effects on
genetic parentage and mating success and the relationship between EPF rate and
male PI under varying population sex ratios.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank Tracey Kast, Marc Sine, and Marya Sosulski for assistance with the experiment, and Anders Brodin, Patty Gowaty, Kristine Johnson, Richard Symanski, and an anonymous reviewer for comments on earlier drafts of the manuscript. This research was supported by National Science Foundation grants BSR 8817977 and IBN 9507514 to N.T.B.
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