Behavioral Ecology
doi:10.1093/beheco/arn100
Advance Access publication 8 August 2008
Female preferences for long tails constrained by
species recognition in short-tailed red bishops
Sarah R. Pryke and Staffan Andersson
Department of Zoology, Göteborg University, Medicinaregatan 18, 413 90 Göteborg, Sweden
Sexual selection and species recognition both play important roles in mate choice. Typically, females use the relative expression
of male sexual traits to select high-quality or attractive mates (sexual selection) of the same species (species recognition).
However, when the variation in male trait expression of both conspecifics and heterospecifics overlaps, females potentially face
a conflict between sexual selection and mate recognition. Among the highly polygynous and closely related African Euplectes
species (widowbirds and bishops), females show a general and open-ended mate preference for extreme male tail length (even in
relatively short-tailed species). To evaluate the relative strength and interaction of directional versus stabilizing selection pressures on tail length, we experimentally examined female mating preferences in the red bishop (Euplectes orix), a short-tailed
(4 cm) species sympatric with longer tailed widowbirds (tails 7–50 cm). In standardized mate-choice experiments, females
preferred naturally long-tailed males (5 cm), were indifferent to controls (4 cm), but discriminated against short-tailed
(3 cm) and supernormal-tailed (8 cm) males. Although the naturally small variation in tail length (5%) is unlikely to function
as a primary mate-choice cue, these results suggest a generalized female bias for longer tails (within the natural range). However,
directional preferences for longer tails may be constrained by selection pressures to avoid heterospecific mating with the closely
related and sympatric longer tailed widowbirds. Key words: Euplectes, receiver bias, sexual selection, species recognition, tail
length. [Behav Ecol 19:1116–1121 (2008)]
INTRODUCTION
he origin and evolution of female preferences for exaggerated signals has received much attention in studies of sexual communication (reviewed in Endler and Basolo 1998;
Rowe and Skelhorn 2004; Enquist and Ghirlanda 2005; ten
Cate and Rowe 2007). During the evolution of sexual signals
and female preferences for such signals, there are several,
nonmutually exclusive processes of evolutionary change.
Changes in signals and receivers can be genetically correlated
(e.g., runaway and certain ‘‘good genes’’ models), such that an
evolutionary change in the trait results in an evolutionary
adjustment of the preference (Andersson 1994a). Alternatively, preexisting preferences or cognitive biases (Ghirlanda
and Enquist 2003) may phylogenetically predate and drive,
but not coevolve with, the appearance and subsequent elaboration of signals (Endler and Basolo 1998; ten Cate and Rowe
2007). Although receiver biases are theoretically capable of
promoting the evolution and maintenance of costly ornamentation (Arak and Enquist 1995; Enquist and Arak 1998), it is
likely that the 2 processes complement rather than exclude
each other. Nevertheless, receiver biases provide an explanation for why most or all females in a population respond
similarly to a novel male trait and why novel or ‘‘supernormal’’
stimuli often elicit stronger responses than the natural range
of stimuli to which the receiver is genetically or phenotypically
adapted (Tinbergen 1948; Enquist and Arak 1998; Pryke and
Andersson 2002).
Another important, but rarely investigated, selection pressure on ornamental traits originates from the potential
trade-off between sexual selection and species recognition.
T
Address correspondence to S.R. Pryke, who is now at the Centre for
the Integrative Study of Animal Behaviour, Macquarie University,
Sydney, New South Wales 2109, Australia. E-mail: sarah.pryke@mq.
edu.au.
Received 2 May 2008; revised 22 June 2008; accepted 3 July
2008.
The Author 2008. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
In addition to directional biases or mate preferences (adaptive
or not) for signal elaboration, females are also under strong
selection to avoid heterospecific mating. Consequently, if a sexually selected trait is also a cue for species recognition, and if
extreme or supernormal signal expression overlaps with that of
a closely related and sympatric species (with which hybridization is likely), selection is expected to reduce female preferences for exaggerated male traits (Pfennig 2000). In other words,
instead of females having an ‘‘open-ended’’ preference, females would be expected to prefer males with traits closer
to the conspecific (rather than heterospecific) average. The
relative extent and variation in the expression of the trait will
be determined by the balance between the costs (and probability) of heterospecific mating and the benefits from conspecific mate choice. Understanding the role of these interactions
between species recognition and sexual selection may clarify
the targets and strengths of mate preferences in cases where
they are not predicted by either process alone. This should be
particularly likely when conspecific preference functions overlap with or approach trait variation in closely related heterospecifics (Pfennig 1998, 2000; Ryan and Rand 1993).
One group of closely related and commonly sympatric species, with similar but differentially exaggerated sexual ornaments, is the highly polygynous and ecologically similar
African bishop and widowbirds in the genus Euplectes. Females and nonbreeding males are streaky brown or buff
(sparrow-like), whereas breeding males molt into a black body
plumage with bright-colored patches of saturated yellow or
red carotenoid pigmentation. The male bishops have the
most extensive carotenoid displays and retain the short tails
from their nonbreeding plumage, whereas male widowbirds
have smaller color patches (typically on the wings) and also
replace their tail feathers during the prenuptial molt, displaying graduated tails of various lengths (65 mm–0.5 m). A
strong intraspecific trade-off between these 2 costly ornaments (color expression and tail length) in the red-collared
widowbird (Euplectes ardens) may also explain the apparent
interspecific negative relationship between these traits in the
genus as a whole (Andersson et al. 2002).
Pryke and Andersson • Preferences constrained by mate recognition
1117
A phylogeny of the Euplectes indicates that short tails are the
ancestral condition and that tail elongation (i.e., widowbirds)
has evolved independently twice in this clade (Prager et al.
2008). Among the widowbirds, long graduated tails are preferred by females in 3 of the longest tailed species (Andersson
1982, 1991; Pryke and Andersson 2005; Pryke et al. 2001) and
appear to function in male competition in a medium-tailed
widowbird (Savalli 1994). Although the associated aerodynamic
and energetic costs of extreme tail elongation likely enforce
honest displays (Andersson 1994b; Pryke and Andersson
2005), the female preference for supernormally long tails in
the relatively short-tailed (7 cm) red-shouldered widowbird
(Euplectes axillaris) suggests that preexisting female biases
may be responsible for the initial elaboration of tail length
(Pryke and Andersson 2002). This is further supported by the
independent gain of an elongated tail (22 cm) in the redcollared widowbird (E. ardens), which is strongly phylogenetically nested within the subclade of short-tailed bishops (Prager
et al. 2008).
If a phylogenetically ancestral female preference (or receiver
bias) has promoted the appearance and elongation of long
tails in this group, then a preference for longer tails is also
expected in the short-tailed bishop species, although they lack
both elongation and sexual dimorphism in tail length. Because
bishops are commonly sympatric with longer tailed widowbirds
(e.g., the widely distributed E. ardens), this further provides an
opportunity to test whether female preferences may be constrained through species-specific cues (i.e., short tails) to
avoid the risk of heterospecific mating (with longer tailed
heterospecific males). In this study, we experimentally manipulated the short tails of male red bishops (Euplectes orix), both
within the natural range (short, average, and long) and beyond (supernormal), and tested female mate preferences relative to tail length. In nonbreeding plumage, red bishops are
sexually monochromatic with short brown tails. For breeding,
however, males molt into a striking body plumage: glossy black
belly and face (front of crown and cheek) and a bright red
breast, rump, and head (back of crown). Similar to other
Euplectes species, the red plumage is highly variable in color
(reflectance-based hue, coefficient of variation [CV] ¼ 11.7%;
n ¼ 37; Pryke SR, unpublished data) and seems to function
primarily in settling male contest competition over territories
and food (Lawes et al. 2002). In contrast to the widowbirds,
the tail feathers of bishops are not replaced in the prenuptial
molt and instead are retained from their nonbreeding plumage
(i.e., short). Tail length is thus relatively invariable (CV ¼ 5.4%;
n ¼ 178; Pryke SR, unpublished data), typical of avian morphological intrapopulation variation (e.g., Alatalo et al. 1988;
Evans and Barnard 1995).
Using red bishops from populations that are sympatric with
long-tailed red-collared widowbirds, we tested the relative selection pressures on male tail length by experimentally examining female responses to both natural and supernormal tail
manipulations. If tail length is subject to generalized and directional sexual selection, males displaying long and supernormal
tails should attract more females. In contrast, if tail length is
under stabilizing selection, females should avoid or at least
be indifferent to supernormal tail lengths compared with tails
within the natural range.
breeding and begin to molt into their brown eclipse plumage
and can be accurately aged as adult breeding males. To ensure
that males and females had no previous experience of each
other, test females were captured from a different population
(Cedara; over 50 km from the nearest male population) in
September 2000, 3 weeks prior to the experiment. In addition,
test birds were housed separately in unisexual flocks in large
outdoor aviaries (1.5 m wide 3 2.7 m long 3 2.2 m high)
and were in visual isolation throughout the study. Both male
and female red bishops originated from populations that were
sympatric with red-collared widowbirds, and male tail length
did not differ between the populations that males (3.9 6
0.18 cm; n ¼ 136) and females (3.8 6 0.21 cm; n ¼ 42) were
taken from (t ¼ 0.87, P ¼ 0.29).
Before the experiments began, we recorded standard morphometrics of wing chord length (to the nearest 0.5 mm);
beak, tarsus, and natural tail length (to the nearest 0.1 mm);
and body mass (to the nearest 0.5 g). From the 3 body size
measures (wing, culmen, and tarsus), we used a principal component (PC) analysis to calculate an index of body size for the
captive males. The first PC1 accounted for 73.5% of the variation in body size measurements, and PC1 was used as a body
size index.
Male red bishops vary continuously in their body plumage
coloration from yellow–orange to bright red. The stimulus
birds used in this experiment were also involved in a diet experiment, such that at the time of this experiment, 3 aviaries
housed recently molted males displaying different colors
(yellow, orange, and bright red). Because of the large variation
in color among (but not within) diet treatments (Isaksson C,
Pryke SR, Andersson S, unpublished data), the males used in
each mate-choice trial were all taken from 1 of the 3 diet treatments (i.e., each trial consisted of 4 males of similar coloration). To further control for, and determine the influence
of plumage color on mate choice, objective color measurements (reflectance) of the red crown and rump were taken
using an S2000 diode-array spectrometer (Ocean Optics,
Dunedin, FL) with illumination from an HL2000 halogen
light source. Using the C-spec software (Ancal, Las Vegas,
NV), we took 3–5 consecutive scans (removing the probe between each) from the center of each patch, and in relation
to a WS-2 white standard scanned prior to scanning each individual. The 3 main perceptual dimensions of color signals
(brightness, hue, and chroma) were computed from the raw
spectral reflectance data and then averaged for each individual.
Brightness (overall intensity; R350–700) was calculated as the reflectance over the 350–700 nm range. Hue (spectral position or
‘‘redness’’; kR50) was computed as the wavelength halfway between that of the minimum and the maximum reflectance.
Using kR50 as the individual segment divider, we calculated
chroma (spectral purity; CR50) as Rmax 2 Rmin/Raverage (further
details of the color measurements and analyses are provided
in Andersson and Prager [2006]; Pryke et al. [2001]).
For the tail manipulations, we selected 12 captive males,
4 from each of the 3 color treatment aviaries that had completed nuptial molt. Male tail lengths were altered by cutting
all 12 rectrices through the shaft with a scalpel 2 centimeters
from the base of the tail. Each apical piece was then replaced
with an appropriate feather length, by inserting minutien pins
(FST, Vancouver, Canada) into the shaft of the 2 feather sections
and gluing them in place with Superglue (Yanlan Products,
Fuzhou, China). Replacement feather tips were cut from rectrices and remiges of deceased (and preserved) red bishops
(4–5 years old). Each treatment was randomly assigned to 1
of the 4 males in each color group to produce short-, long-,
supernormal-, and control-tailed males. Short-tailed males
had their tails shortened to the lower limits of the natural population (3.1 cm, n ¼ 128; before treatment 4.1 6 0.13; after
METHODS
Mate-choice experiments were performed during October to
November 2000 at the University of KwaZulu-Natal (Pietermaritzburg), South Africa. Males were captured about 6 months
prior to these experiments (March to April 2000) at 3 discrete
locations in KwaZulu-Natal (Balgowan, Beacon Vlei, and Lions
River). At this time of the year, individuals have completed
Behavioral Ecology
1118
3.0 6 0.07 cm). Long-tailed males had their tails lengthened
to the upper range of the population (4.9 cm, n ¼ 128; before
4.0 6 0.21; after 5.0 6 0.06 cm). Supernormal-tailed males
had their tails lengthened to more than double the mean tail
length (before 3.9 6 0.27 cm; after 8.3 6 0.03 cm). To control for the effects of both tail manipulation and adding
another bird’s tail feathers, the control males were manipulated as above to a length equal to that of the population
mean (3.9 cm, n ¼ 178; before 3.8 6 0.19; after 3.9 6 0.08).
Feather repairs were performed as needed throughout the
course of the trials (a total of 5 repairs were made between
different trials: 3 to supernormal tails, 1 to a long tail, and 1 to
a control tail).
Mate-choice trials were conducted in large outdoor aviaries
(identical in size to the housing cages) during the first few
hours of daylight (typically 05h30min–09h30min). The stimulus males were held in 4 parallel aviaries with a wire mesh roof
and front, but otherwise surrounded by solid partitions, visually isolating the stimulus males from each other. Each cage
contained 2 perches in both the feeding area (back of the
cage) and display area (front). The test female was placed
in the main U-shaped adjoining cage that ran perpendicular
along the length of the 4 test aviaries but also included 2 isolated areas on either side of the male aviaries, from which the
female could access food and water but not view the males.
From the main area, the female was able to individually view
stimulus males from perches placed outside each cage. The
mesh wire allowed visual and vocal contact throughout the
trials but precluded physical contact.
The experiment consisted of 48 mate-choice trials, each with
a new female as the respondent. Due to a limited number of
fully molted males available within each diet treatment group,
we were unable to manipulate a new set of males for each trial.
Instead, to minimize individual effects influencing mate
choice, tail manipulations were removed (by dissolving the
glue using acetone and removing the pin) and rotated so that
each of the 4 males (per diet group) received each of the 4 tail
treatments for an equal number of trials (i.e., each male participated in 4 different trials, but in each he received a different
tail manipulation). Furthermore, to reduce the potential confounding effect of cage position, we also rotated tail-treated
males such that each male (with a different tail treatment)
was placed in a different test aviary for each of the 4 trials. Once
a trial ended, birds were returned to their housing aviaries to
maintain a standardized housing setting for all males.
At the beginning of a trial, males were placed in their experimental cages and allowed 15 min to acclimatize before the
trial began. Trials lasted 1 h during which we recorded female
behavior. Trials were considered successful only if the female
visited all males during the first 15 min of the trial. As a measure
of mate choice, we extracted data on the total time individual
females spent in association with a male (on a perch facing
a male or moving back and forward along the perch, usually
with the male leading or following at close range), the number
of solicitations (typical passerine quivering of wings and tails),
and the solicitation rate (number of solicitations when associated to a particular male). These measures of female mate
preferences were consistent: females spent more time in association with males that they solicited to (93% of experiments;
r38 ¼ 0.92, P , 0.001).
These trials focused on determining female responses to
male tail length. Nevertheless, males given different tail treatments may adjust their behavior accordingly (Barnard 1990),
which could influence female decisions. Although we were
unable to monitor female and male behavior simultaneously,
in a further additional trial for each rotation of tail treatments
(4 treatments per male) we monitored only male behavior.
In other words, in a further 16 trials in which each male
randomly displayed a different tail treatment, we investigated
only the male’s response. The females used for this experiment had already been tested in the mate-choice trials
(described above), but a different stimulus female was used
in each of these 16 trials. For analyses, we used the 1) time
spent in courtship flight displays (characteristic ‘‘bumblebee’’
flight with the long red rump feathers erected in a large
‘‘puff’’ as they drone slowly on rapidly and noisily vibrating
wings); 2) time spent in perched courtship display (stiff,
sometimes vibrating, upright posturing, with a swaying or swiveling motion); and 3) sexual courtship behavior (closely
approach female while pumping the body up and down).
Statistical analyses
Outcomes from all experiments were analyzed with generalized linear models (GLM), using a logarithmic link function
and Poisson distribution (GenStat 7.1; VSN, Hemel Hempstead, UK). For these analyses, we initially modeled all possible
combinations and interactions of the measured variables
including: body size (PC1), body mass, colorimetrics (hue,
chroma, and brightness), natural tail length, color/diet group,
male identity, tail treatment, capture and housing locality, trial
number, time and date, and position in experimental cage.
The significance of the predictor variables was tested by the
change in deviance of the different models using a chi-square
approximation. Second-order Akaike’s information criterion
(AICC) weights were calculated for each model. AICC (used
for smaller sample sizes) balances the fit of the model against
the number of parameters used in the model and was used to
effectively compare different models; only final models are
presented (all final AICC models 88% weight compared
with other potential models).
RESULTS
Female mate choice
Females actively visited all the stimulus males within the first
15 min of a trial, except for 5 females (10.4%), which were removed from subsequent analyses. During the remaining 43 trials, females solicited to a single male in 33 (76.7%) of the trials,
2 different males in 6 (14.0%), and no male in 4 (9.3%) trials.
Overall, females spent an average of 35.4 6 10.2 min of the
trials in front of males, and only one female spent more time
feeding than with the average stimulus male. Females appeared to preferentially associate (.90% of their time) with
a particular male; females associated with a single male in
83.2% of the trials, 2 different males in 16.3%, and 3 males
in 0.5%.
Using a GLM with female solicitation rate as the response
variable, the best-fitting model (AICC ¼ 192.1, v238 ¼ 10:63,
P , 0.01) identified tail treatment (F ¼ 9.97, P , 0.01) as
the sole predictor of mate choice (Figure 1). Long tails had
the strongest positive effect on mate choice (t ¼ 4.11,
P , 0.01), whereas females discriminated against short-tailed
(t ¼ 22.01, P ¼ 0.04) and supernormal-tailed males (t ¼ 22.76,
P ¼ 0.006) but showed no preference for control males (t ¼
1.44, P ¼ 0.15). Replacing solicitation rate with the number
of solicitations as the response variable produced a similar
model (AICC ¼ 203.6, v238 ¼ 8:92, P , 0.01). The effect of tail
treatment also remained when the time spent with males was
substituted as the response variable (AICC ¼ 209.1, v242 ¼ 5:97,
P , 0.01); however, in this model, only the treatment of long
tails was significant (t ¼ 3.18, P , 0.01).
In all models, none of the other potential variables (see
Methods for list) had any effect on mate preferences. In particular, there were no color-related differences in female
Pryke and Andersson • Preferences constrained by mate recognition
Frequency
Probability of female soliciting (%)
100
75
50
25
0
1
2
3
4
Short Control
5
Long
6
7
8
Supernormal
Tail length (cm)
Figure 1
The probability (%) of females soliciting to the short- (3 cm),
control- (4 cm), long- (5 cm), and supernormal-tailed males (8 cm).
Probabilities are calculated from the coefficients of the best-fit GLM
(probability ¼ e(coeff)/1 1 [e(coeff)]), and error bars represent the
95% confidence levels of the coefficients. The dashed line (50%)
indicates where females show no preference; values above the line
indicate a positive female preference, whereas values below the line
indicate female discrimination. The inner histogram shows the
natural variation of breeding male tail length in the population
(n ¼ 178), corresponding to the x axis of experimental tail length.
responsiveness: there were no significant differences in female
association time or the number of solicitations between trials
with males of the 3 different plumage color (diet) classes
(yellow, orange, and red: F , 0.15, P . 0.86) or based on
male plumage colorimetrics (brightness, hue, and chroma:
F , 0.23, P . 0.74).
Male behavior
Males responded to stimulus females by vigorously performing
their characteristic flight displays (bumblebee). When a female
approached, males would typically initiate perch displays
(upright posture while swaying or swiveling; 96% of observed
female approaches; n ¼ 219). If the female remained in association (n ¼ 91) or initiated solicitation behaviors (n ¼ 45),
males would respond accordingly (by moving their body up
and down; 97%).
Display behaviors were similar between treatments as the
4 different tail treatments (short, control, long, and supernormal) did not affect male display behaviors to females (flight:
F1,15 ¼ 0.62, P ¼ 0.65; perch: F1,15 ¼ 0.05, P ¼ 0.98; courtship: F1,15 ¼ 0.43, P ¼ 0.72). Therefore, in line with previous
studies demonstrating that male mating success is unrelated
to the variation in their elaborate courtship behaviors (Lawes
et al. 2002), it seems unlikely that differences in male activities
and display behaviors in this study (among tail treatments)
influenced female choice.
DISCUSSION
In widowbirds, females show both a strong natural (Andersson
1991; Pryke et al. 2001) and open-ended preference (Andersson
1982; Pryke and Andersson 2002) for tail elongation. However,
this study of the closely related and sympatric red bishop
demonstrated a natural but not directional female preference
for tail length. In particular, females preferred longer tailed
males (within the natural range) but were adverse to shortand supernormal-tailed males.
1119
The observed female preference for long tails in a species
without the exaggerated tail ornamentation of its close relatives (i.e., neither prenuptially molted nor sexually dimorphic)
may have arisen via 2, not mutually exclusive, selection processes. First, because it was not examined in previous field studies of red bishop mating success (Friedl and Klump 1999,
2000; Lawes et al. 2002), it may be that females in wild populations are choosing males on the basis of tail length. However, given the lack of sexual dimorphism in tail length,
especially compared with the extreme expressions of other
male plumage and behavioral displays, female choice seems
unlikely to be a strong selection pressure. Furthermore, it is
questionable whether females could detect sufficient variation
in tail length in natural populations because of the low phenotypic variability (CV ¼ 5.4%) compared with that of other
longer tailed widowbirds (CV ¼ 6–17%; Andersson 1982,
1993; Savalli 1994; Pryke et al. 2001). Instead, unless tail
length is discretely manipulated (as in this study), female
mate choice may direct attention away from the normally
small variation in tail length, and instead target other traits,
such as male territories containing more male-built nests
(Friedl and Klump 1999; Lawes et al. 2002), similar to other
shorter tailed widowbirds (Euplectes macrourus: Savalli 1994;
E. axillaris: Pryke and Andersson 2003).
Second, female preferences for long tails in a short-tailed
species may indicate a general female (receiver) bias for longer
tails. Preferences for heterospecific traits have been documented in a number of taxa (fish: Basolo 1990a, 1995; frogs:
Ryan and Rand 1990, 1993; and arthropods: Proctor 1992;
McClintock and Uetz 1996), suggesting some type of female
sensory or cognitive bias (Endler and Basolo 1998). Demonstrating a receiver bias requires that the absence of the signal
trait is the ancestral state, that the preference phylogenetically
predates the evolution of the trait, and that both the preference and the trait are usually present in subsequently derived
species (Basolo 1990b; Endler and Basolo 1998; but see Wong
and Rosenthal 2006). Among the Euplectes, a molecular phylogeny (Prager et al. 2008) suggests that the tail ornament is
a derived trait having evolved twice from a short-tailed ancestor and been retained in all subsequent taxa (i.e., in the widowbirds, of which the red-collared widowbird proved to be
a long-tailed bishop). In addition, females in the 3 longest
tailed widowbird species prefer males with longer tails (Pryke
et al. 2001; Pryke and Andersson 2005), and the strong female
preference for long (and supernormal) tails in the shorttailed red-shouldered widowbirds supports a generalized receiver bias promoting the evolution of long tails in this group
(Pryke and Andersson 2002).
The present study, however, failed to demonstrate an openended or generalized female bias for long tails in red bishops.
Nevertheless, these results do not completely exclude the role
of receiver biases in the evolution of tail length. First, one possibility is that the female preference for long tails arose along
with the divergence of widowbirds from the short-tailed
bishops. However, this seems unlikely considering the close
phylogenetic distance between short-tailed red bishops and
long-tailed red-collared widowbirds (long-tailed bishops), as
well as the female red bishops’ preference for naturally long
tails. A second possibility is that females avoid supernormaltailed males simply because of the unfamiliarity or novelty
of red bishop males displaying super-long tails. Alternatively
or in addition to this, female preferences for long tails may
be constrained by effective species or mate recognition. In particular, red bishops are closely related to the sympatric longtailed red-collared widowbirds, as judged from a molecular
phylogeny (Prager et al. 2008), hybridization in captivity
(Colahan and Craig 1981), and the strong similarities in their
behavior. Compared with other widowbirds, territorial, and
Behavioral Ecology
1120
threat behaviors displayed by these 2 species are particularly
similar (e.g., body and head feathers ruffled). Furthermore,
while red bishop territories are often contained within other
widowbird territories without any apparent conflict (Skead
1965), male red bishops and red-collared widowbirds aggressively defend contiguous but mutually exclusive territories in
sympatry (Emlen 1957; Pryke SR, personal observations).
From their territories, male Euplectes commonly display to all
eclipse plumaged birds, irrespective of species (Craig 1980;
Pryke SR, personal observations), and male red bishops will
vigorously court red-collared widowbird females in both field
and captive conditions. If tail length plays a role in maintaining the reproductive barrier between these 2 species, in this
experiment using red bishops from populations that are sympatric with the closely related and long-tailed red-collared
widowbirds, red bishop females (who appear to be solely
responsible for mate recognition) should therefore prefer
males with longer, but not supernormal, tails. At this stage,
it is unknown whether red bishop females from allopatric
populations also discriminate against supernormal tails, but
because divergent mate preferences are expected to be stronger in sympatric populations (Pfennig 2000), we would expect
females from these sympatric populations to exhibit stronger
mate discrimination against heterospecific traits.
In mate recognition, individuals are expected to utilize
species-specific characters that are particularly diagnostic.
Although tail length differs between bishop and widowbirds,
the bright red plumage displays of male red bishops are also
particularly conspicuous and diagnostic (at least to the human
observer) and would perhaps be a more reliable speciesspecific cue. For example, no species display the extent (e.g.,
all widowbirds), intensity (e.g., Euplectes afer), or pattern (e.g.,
Euplectes hordeaceus) of red plumage, yet other species grow tails
of similar lengths (e.g., E. afer, E. hordeaceus). Therefore, it
seems likely that the color and extent of plumage should also
be used in mate recognition. However, the large variation in
male coloration displayed by the males in this study (light
yellow to bright red) did not affect mate choice. Although all
males within a trial displayed the same coloration (from the
same diet treatment), if color is an important species-specific
cue, females would be expected to reduce their relative
response (i.e., not associate or solicit) in trials where males
displayed supernormal coloration. For example, females would
be expected to discriminate against males with light yellow
plumage, which perhaps more closely resembled the sympatric
golden bishops (E. afer) than the average orange–red plumage
displayed by red bishops. However, because females were
unable to simultaneously assess the relative extent of male
coloration (normal and supernormal) within each trial, they
may have instead focused primarily on the prominent (and
discrete) variation in tail length. Until further experiments
are undertaken, the relative importance of male plumage
traits (carotenoid based vs. tail length) in species recognition
cannot be evaluated. Perhaps, however, similar to sexually
selected signals where females benefit by assessing multiple
ornaments (Johnstone 1995; Pryke et al. 2001; Candolin
2003), evaluating multiple traits may also be beneficial in
species recognition (Hankison and Morris 2003).
The female preference for long tails in this short-tailed red
bishop suggests that female choice is a general selective force
behind the evolution of tail ornaments in this genus. Given
that the short tails (no elongation) of red bishops are an ancestral state (Prager et al. 2008), the experimentally revealed
preference for long tails (within the natural range) may
represent a preset receiver bias that has subsequently been
reinforced in the longer tailed widowbirds. However, in this
species, the evolution of tail length appears to be constrained
by species recognition.
FUNDING
The Swedish Foundation for International Cooperation in
Research and Higher Education (to S.P. and S.A.) and Swedish
Science Council (to S.A.).
We thank the owners and managers of Balgowan, Beacon Vlei, Cedara,
and Lions River for allowing us to work on their land and Mike Lawes
for logistical help. Permission to collect, house (permit no. 28562/
2001), and work with red bishops (permit no. 28561/2001) was granted
by the KwaZulu-Natal Wildlife Services, and all experimental work was
approved by the University of Natal’s Animal Ethics Committee
(AE/01/10).
REFERENCES
Alatalo RV, Höglund J, Lundberg A. 1988. Patterns of variation in tail
ornament size in birds. Biol J Linn Soc. 34:363–374.
Andersson M. 1982. Female choice selects for extreme tail length in
a widowbird. Nature. 299:818–820.
Andersson M. 1994a. Sexual selection. Princeton: Princeton University Press.
Andersson S. 1991. Bowers on the savanna: display courts and mate
choice in a lekking widowbird. Behav Ecol. 2:210–218.
Andersson S. 1993. Sexual dimorphism and modes of sexual selection
in lekking Jackson’s widowbirds Euplectes jacksoni (Ploceinae). Biol J
Linn Soc. 49:1–17.
Andersson S. 1994b. Costs of sexual advertising in the lekking Jackson’s widowbird. Condor. 96:1–10.
Andersson S, Prager M. 2006. Quantification of coloration. In: Hill
GE, McGraw KJ, editors. Bird coloration. Vol. 1. Mechanisms and
measurements. Cambridge: Harvard University Press. p. 40–89.
Andersson S, Pryke SR, Ornborg J, Lawes MJ, Andersson M. 2002.
Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird. Am Nat. 160:683–691.
Arak A, Enquist M. 1995. Conflict, receiver bias and the evolution of
signal form. Philos Trans R Soc Lond B Biol Sci. 29:337–344.
Barnard P. 1990. Male tail length, sexual display intensity and female
sexual response in a parasitic African finch. Anim Behav. 39:652–656.
Basolo AL. 1990a. Female preference for male sword length in the
green swordtail, Xiphophorus helleri (Pisces, Poecilidae). Anim Behav.
40:332–338.
Basolo AL. 1990b. Female preference predates the evolution of the
sword in swordtail fish. Science. 250:808–810.
Basolo AL. 1995. A further examination of a pre-existing bias favouring a sword in the genus Xiphophorus. Anim Behav. 50:365–375.
Candolin U. 2003. The use of multiple cues in mate choice. Biol Rev.
78:575–595.
Colahan BD, Craig AJFK. 1981. Euplectes hybrids. Ostrich. 52:58–59.
Craig AJFK. 1980. Behavior and evolution in the Genus Euplectes. J
Ornithol. 121:144–161.
Emlen JTJ. 1957. Display and mate selection in the whydahs and
bishop birds. Ostrich. 28:202–213.
Endler JA, Basolo AL. 1998. Sensory ecology, receiver biases and sexual selection. Trends Ecol Evol. 13:415–420.
Enquist M, Arak A. 1998. Neural representation and the evolution of
signal form. In: Dukas R, editor. Cognitive ecology: The evolutionary ecology of information processing and decision making.
Chicago: University of Chicago Press. p. 21–87.
Enquist M, Ghirlanda S. 2005. Neural networks and animal behavior.
Princeton: Princeton University Press.
Evans MR, Barnard P. 1995. Variable sexual ornaments in scarlettufted malachite sunbirds (Nectarinia johnstoni) on Mount Kenya.
Biol J Linn Soc. 54:371–381.
Friedl TWP, Klump GM. 1999. Determinants of male mating success in the red bishop (Euplectes orix). Behav Ecol Sociobiol. 46:
387–399.
Friedl TWP, Klump GM. 2000. Nest and mate choice in the red bishop
(Euplectes orix): female settlement rules. Behav Ecol. 11:378–386.
Ghirlanda S, Enquist M. 2003. A century of generalization. Anim
Behav. 66:16–36.
Hankison SJ, Morris MR. 2003. Avoiding a compromise between sexual selection and species recognition: female swordtail fish assess
multiple species-specific cues. Behav Ecol. 14:282–287.
Pryke and Andersson • Preferences constrained by mate recognition
1121
Johnstone RA. 1995. Honest advertisement of multiple qualities using
multiple signals. J Theor Biol. 177:87–94.
Lawes MJ, Slotow R, Andersson S. 2002. Male nest building but not
display behaviour directly influences mating success in the polygynous Red Bishop, Euplectes orix. Ostrich. 73:87–91.
McClintock WJ, Uetz GW. 1996. Female choice and pre-existing bias:
visual cues during courtship in two Schizocosa wolf spiders (Aranea:
Lycosidae). Anim Behav. 52:167–181.
Pfennig DW. 2000. Female spadefoot toads compromise on mate quality to ensure conspecific matings. Behav Ecol. 11:220–227.
Pfennig KS. 1998. The evolution of mate choice and the potential for
conflict between species and mate-quality recognition. Proc R Soc
Lond B Biol Sci. 265:1743–1748.
Prager M, Johansson EIA, Andersson S. 2008. A molecular phylogeny
of the African widowbirds and bishops, Euplectes spp. (Aves:
Passeridae: Ploceinae). Mol Phylogenet Evol. 46:290–302.
Proctor HC. 1992. Sensort exploitation and the evolution of male
mating behaviour: a cladistic test using water mites (Acari: Parasitengona). Anim Behav. 44:745–752.
Pryke SR, Andersson S. 2002. A generalized female bias for long tails in
a short-tailed widowbird. Proc R Soc Lond B Biol Sci. 269:2141–2146.
Pryke SR, Andersson S. 2003. Carotenoid-based status signalling in redshouldered widowbirds (Euplectes axillaris): epaulet size and redness
affect captive and territorial competition. Behav Ecol Sociobiol.
53:393–401.
Pryke SR, Andersson S. 2005. Experimental evidence for female
choice and energetic costs of male tail elongation in red-collared
widowbirds. Biol J Linn Soc. 86:35–43.
Pryke SR, Andersson S, Lawes MJ. 2001. Sexual selection of multiple
handicaps in the red-collared widowbird: female choice of tail
length but not carotenoid display. Evolution. 55:1452–1463.
Rowe C, Skelhorn J. 2004. Avian psychology and communication. Proc
R Soc Lond B Biol Sci. 271:1435–1442.
Ryan MJ, Rand AS. 1990. The sensory bias of sexual selection for
complex calls in the Tungara frog, Physalaemus pustulosus. Evolution.
44:305–314.
Ryan MJ, Rand AS. 1993. Species recognition and sexual selection as
a unitary problem in animal communication. Evolution. 42:647–657.
Savalli UM. 1994. Tail length affects territory ownership in the yellowshouldered widowbird. Anim Behav. 48:105–111.
Skead CJ. 1965. The ecology of the ploceid weavers, widows and
bishop-birds in the south-eastern Cape Province, South Africa. In:
Davis DHS, editor. Ecological studies in southern Africa. The Hague
(the Netherlands): W.H. Junk. p. 219–232.
ten Cate C, Rowe C. 2007. Biases in signal evolution: learning makes
a difference. Trends Ecol Evol. 22:380–387.
Tinbergen N. 1948. Social releasers and the experimental; method
required for their study. Wilson Bull. 60:6–51.
Wong BBM, Rosenthal GG. 2006. Female disdain for swords in a swordtail fish. Am Nat. 167:136–140.