Behavioral Ecology Vol. 10 No. 6: 626–635
Sex ratios and sexual selection in socially
monogamous zebra finches
Nancy Tyler Burley and Jennifer Devlin Calkins
Department of Ecology and Evolutionar y Biology, University of California, Ir vine,
CA 92697-2525, USA
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
1 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. [Behav Ecol 10:626–635 (1999)]
R
esearchers 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 reAddress correspondence to N. Burley. E-mail: [email protected].
Received 2 October 1998; accepted 30 March 1999.
q 1999 International Society for Behavioral Ecology
sulting 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 pre-
Burley and Calkins • Sex ratio and sexual selection
ferred 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.
METHODS
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
627
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 incur
parental 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 6 SE: FBT, 0.91 6 .04;
MBT, 0.55 6 .08; t 5 23.27, 53 df, p 5 .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 (6 SE) of male founders at the start
of the MBT was 145 6 6.4 days; that of females was 151 6 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 6 5.1 days, and
that of female founders was 133 6 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 ad
libitum. 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.
Behavioral Ecology Vol. 10 No. 6
628
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 6 SE of sample number per pair: FBT, 62.2 6 1.7; MBT, 57.8 6 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.
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 27
to day 21), 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 214 to day 28) 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 (Wilkin-
Burley and Calkins • Sex ratio and sexual selection
629
Table 1
Components of parental expenditure
Table 1
Continued
Category/
behavior
Category/
behavior
Description (D)/
Amplification (A)
Look out
D: A stationary nest attendant sits high in the nest,
looking out.
A: This posture is typically inconsistent with
incubation. If a bird stretches its neck far enough,
it is sometimes possible to incubate(I) and look out
(LO) at the same time. When behaviors were scored
as I/LO, half the accumulated time was assigned to
passive defense and the other half to passive care.
Description (D)/
Amplification (A)
Active caregiving
Nest building
D: A bird transports nesting material to the nest;
adds new material to the nest; and/or ‘‘arranges’’
material already present in the nest.
A: Nest material consists of straw/grass and cotton
batting. Males are much more likely to transport
and add grass; both sexes commonly transport and
add cotton, arrange nest material. This behavior
occurs during all 5 weeks of the sampling interval,
albeit at varying frequencies.
Nest inspect
D: A bird perches just outside the nest entrance with
upright posture and beak pointing toward entrance.
(Also called ‘‘look in’’; Burley 1988.)
A: Can occur throughout development, but
common in the posthatch period. Often precedes
feeding of young.
Feed
D: A bird in the nest regurgitates to nestlings.
A: Occurs only posthatching; values reported in
Table 2, however, are averaged over all samples to
preserve additivity of behaviors in this category.
Feeding of very young hatchlings is difficult to
detect and so is underrepresented in this sample.
Time spent foraging for food to feed nestlings is also
not included.
Passive caregiving
D: A stationary bird sits low in its nest in a position
consistent with incubation/brooding.
A: Actual incubation (egg warming) was not
established, and nest attendance may serve multiple
functions (see text). Data are included here for
weeks 2 and 3 only to minimize impact of other
possible functions.
Active defense
D: A nest attendant behaves aggressively toward
(an)other bird(s) in the immediate vicinity of the
nest. Behaviors scored included chase (Ch), to
pursue an interloper briefly by hopping after the
bird until it leaves the nest area; displace (Dis), to
approach an interloper very closely, causing it to
leave (but no pursuit); peck (P), to deliver a mild
peck to the body of an interloper; threaten(Th), any
of several postures (Goodwin, 1982) which indicate
imminent aggression if an interloper fails to depart;
flychase (FCh), to pursue an interloper across the
aviary in flight; and beakfence (BF), to repeatedly
(and reciprocally) peck the beak of a ‘‘combatant.’’
A: Prior to analyses, data for all days on which the
female nest attendant laid eggs were excluded. All
data for aggression toward juveniles were excluded.
(Parents are often aggressive to their own young in
the fledging phase.) For each sample, each nest
attendant was given a weighted aggression score in
which each instance of Ch, Dis, P, and Th was given
one point; each occurrence of FCh and BF was
assigned 3 points if it was scored by the observer as
intense or as lasting 50 s or longer (FCh only);
otherwise an occurrence of FCh or BF received two
points. An individual’s aggression score was the sum
of the points it was assigned as the result of
aggressive acts it initiated during a sample.
Passive defense
Survey
D: A nest attendant perches in a relaxed posture in
the immediate vicinity of the nest entrance (typically
5–20 cm).
son, 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.
RESULTS
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 5 .25),
number of hatchlings (p 5 .92), number of offspring surviving to independence (p 5 .85), and brood sex ratio (males/
total progeny surviving to sexing age of about 45 days: FBT,
n 5 10; MBT, n 5 10; p 5 .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 behavTable 2
Per-sample parental expenditure (PE) (median) of caregiving and
defensive parental behaviors
Behavior
FBT
MBT
U
p
Active care
Feed
Nest build
Nest inspect
Passive care
Active defense
Passive defense
Survey
Look out
94.00
24.86
59.56
13.88
767.00
0.64
139.23
76.71
22.83
91.36
20.06
62.30
7.35
698.00
0.39
133.79
95.39
26.94
58
54
62
34
70
51
75
75
69
.622
.460
.806
.049
.806
.356
.580
.058
.854
FBT, female-biased treatment (n 5 11); MBT, male-biased treatment
(n 5 12). See Table 1 for descriptions of behaviors included in
each category.
Behavioral Ecology Vol. 10 No. 6
630
Figure 1
Percent male contribution
(median) to caregiving and
nest defense in the female-biased (FBT; n 5 11) and malebiased (MBT; n 5 12) treatments. Active care: U 5 106, p
5 .014; passive care: U 5 44.5,
p 5 .185; active defense: U 5
110, p 5 .007; passive defense:
U 5 101, p 5 .031.
iors 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 (20.33; 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).
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).
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 5 35; MBT, 0.025,
Table 3
Binomial expansion (p1q)4 for significance of differential allocation results
Term
A
B
Interpretation
p 4q 0
4p 3q 1
6p 2q 2
4p 1q 3
p 0q 4
.00000625
.00047500
.01353750
.17147500
.81450625
.00000039
.00006094
.00356484
.09268594
.90368789
Probability
Probability
Probability
Probability
Probability
that
that
that
that
that
all 4 tests would be significant by chance.
3 of 4 tests would be significant by chance.
2 of 4 tests would be significant by chance.
1 of 4 tests would be significant by chance.
0 of 4 tests would be significant by chance.
A: Probability of obtaining statistically significant results for 0–4 tests of the hypothesis (p 5 .05; q 5
.95). B: Probability of obtaining statistically significant results, all in the expected direction, for 0–4
tests of the hypothesis (p 5 .025; q 5 .975). Observed results fall into the first to terms; text reports
cumulative probabilities of observed results.
Burley and Calkins • Sex ratio and sexual selection
Table 4
Hatching asynchrony and male parental expenditure at focal nests
r
PE category
FBT (n 5 10)
MBT (n 5 11)
Active care
Passive care
Active defense
Passive defense
2.146
.134
2.091
2.165
2.309
.200
2.269
2.245
Spearman’s test, all p . .20. FBT, female-biased treatment; MBT,
male-biased treatment.
n 5 20; U 5 490.5, p 5 .013). Females in the MBT also tended
to have greater numbers of social mates per treatment interval
(FBT, 0.006; MBT, 0.004; U 5 248, p 5 .055).
For males, reproductive rate also varied between treatments. Males in the FBT had higher social parentage (0.031,
n 5 20) than those in the MBT (0.017, n 5 35; U 5 217.5, p
5 .020). Males also obtained more social mates per unit time
in the FBT (FBT, 0.006; MBT, 0.004; U 5 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.
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
631
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
5 28; MBT, 0.000, n 5 20; U 5 126.5, 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).
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 5 23; MBT, 0.167, n 5 20; U 5 268, p 5 .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 asyn-
Figure 2
Reproductive rate (median) as
a function of number of social
mates in the female-biased
(FBT) and male-biased (MBT)
treatments. A: Kruskal-Wallis H
5 19.813, 2 df, p , .0001; B:
H 5 3.003, 2 df, p 5 .219; C:
H 5 1.013, 3 df, p 5 .798; D:
H 5 17.658, 2 df, p 5 .0001.
Behavioral Ecology Vol. 10 No. 6
632
Table 5
Relative incidence of intraspecific-brood parasitism (IBP) in the female-biased treatment (FBT) and
the male-biased treatment (MBT)
Egg stagea
FBT
MBT
a
b
Fledgling stageb
Parasitized
Not parasitized
Parasitized
Not parasitized
16
2
10
20
6
0
16
21
Fisher’s Exact two-tailed p , .002.
Fisher’s Exact two-tailed p 5 .024
chrony of such clutches was significantly higher in the FBT
(0.905, n 5 10) than in the MBT (0.167, n 5 19; U 5 44, p
5 .019). Hatching asynchrony was negatively correlated with
female reproductive rate in the FBT (r 5 2.598, n 5 10; p ,
.05); these variables were not significantly correlated in the
MBT (r 5 .122, n 5 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 5 35;
MBT, 0.094, n 5 20; U 5 437, p 5 .13). Percent hatching
sucess, however, was much higher for females in the MBT
(0.65, n 5 20) than in the FBT (0.23, n 5 28; U 5 456.5, 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 5 2.730, n 5 10, p 5 .017), whereas these variables were
not correlated for females in the MBT (r 5 .191, n 5 19, p
5 .43). As a result, mean number of hatchlings per clutch
differed between treatments (FBT, 1.00, n 5 28; MBT, 2.33,
n 5 20; U 5 428, 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 5 22)
than in the MBT (0.50, n 5 19; U 5 106, p 5 .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
r 2 5 .183, n 5 36, p 5 .035) included beak score (r 5 2.002,
p 5 .042) and tail score (r 5 2.015, p 5 .113). For males, no
significant model was generated, but the best model (adjusted
r 2 5 .066, p 5 .144) included tail score (r 5 2.049). 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 r 2 5 .381, n 5 20, p 5 .017) included beak score (r 5
2.003, p 5 .066) and tail score (r 5 .019, p 5 .019). For males,
the best regression model (adjusted r 2 5 .232, n 5 35, p 5
.006) included beak score (r 5 .002, p 5 .010) and tail score
(r 5 .012, p 5 .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 5 .807, n 5 10, p 5 .004) included
percent male active defense (r 5 .001, p 5 .004), hatching
asynchrony (r 5 2.045, p 5 .008), and female tail score (r 5
2.027, p 5 .029). For females in the MBT, the best resulting
model (adjusted r2 5 .889, n 5 11, p 5 .001) included two of
the four paternal contribution rates (active care: r 5 .001, p
5 .026; passive care: r 5 .001, p 5 .043), as well as two variables found to be significant previously, hatching asynchrony
(r 5 .066, p 5 .001) and tail score (r 5 .034, p 5 .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.
DISCUSSION
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 overrepre-
Burley and Calkins • Sex ratio and sexual selection
sented 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
633
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 malebiased tertiary sex ratios (Breitwisch, 1989). Thus, if femalebiased 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).
Behavioral Ecology Vol. 10 No. 6
634
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.
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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