Ó Springer-Verlag 1999
Behav Ecol Sociobiol (1999) 45: 87±93
ORIGINAL ARTICLE
George W. Uetz á Elizabeth I. Smith
Asymmetry in a visual signaling character and sexual selection
in a wolf spider
Received: 26 February 1998 / Accepted after revision: 12 September 1998
Abstract Fluctuating asymmetry (FA) can indicate
developmental instability in bilaterally symmetric organisms, and studies have shown that the degree of
asymmetry in male secondary sexual characters in¯uences female mate choice in a number of taxa. In male
Schizocosa ocreata wolf spiders, conspicuous tufts of
bristles on the forelegs are a critical component of visual
courtship signals, which appear to play a role in female
mate choice. Previous studies have shown that females
exhibit reduced receptivity to males with regenerative
asymmetry, a consequence of leg loss and regeneration
that causes males to be grossly asymmetric with respect
to this important signaling character. We provide data
on the occurrence of FA in the tufts of S. ocreata, and
examine further the in¯uence of asymmetry on female
mate choice. The distribution of tuft area asymmetry
values from a sample of ®eld-collected males was normal, with a mean value of zero, indicating true FA. For
a subset of males measured directly after ®eld collection
and prior to feeding, tuft asymmetry was signi®cantly
negatively correlated with measures of body size (body
length) and condition (abdomen volume/cephalothorax
width). Receptivity responses of females to visual signals
from live males of similar size varied with the degree of
asymmetry in male tufts. Since FA covaries with male
body size and condition, which may also in¯uence behavioral vigor, we used video image manipulation to
alter the degree of asymmetry in tufts of a courting male
while holding size and condition constant. Asymmetry
treatments represented values within the range of
natural FA variation as well as more extreme values
characteristic of regenerative asymmetry. With the
confounding e€ects of male size, condition, and behavior held constant, female spiders exhibited reduced
G.W. Uetz (&) á E.I. Smith
Department of Biological Sciences
University of Cincinnati. Cincinnati, OH 45221-0006, USA
e-mail: uetzgw@email.uc.edu
Tel.: +1-513-5569752, Fax: +1-513-5565299
receptivity responses to all experimental asymmetric
video images relative to a control video stimulus. There
were no di€erences in the frequency of female receptivity
among the various asymmetry treatments, suggesting
that discrimination against asymmetry in conspeci®c
male signal characters is not simply a rejection of extreme phenotypes. Results suggest that asymmetry in a
key male secondary character used in visual signaling,
independent of any concomitant behavioral or size factor, is an important criterion in mate choice.
Key words Fluctuating asymmetry á Sexual selection á
Female choice á Wolf spider
Introduction
Female choice based on symmetry of male characters
has been an important and controversial topic in sexual
selection research, because ¯uctuating asymmetry (FA)
in bilaterally symmetric organisms can indicate developmental instability (Ludwig 1932; Palmer and Strobeck
1986; Leary and Allendorf 1989; Mùller 1990, 1997;
Thornhill 1992; Watson and Thornhill 1994; Hill 1995;
Mùller and Swaddle 1997). Numerous studies in the ®eld
and laboratory have demonstrated that asymmetry plays
a role in female mate choice, and that asymmetry in male
characters is a good predictor of male ``quality'' and
reproductive success (Mùller 1992a,b, 1993, 1997;
Swaddle and Cuthill 1994; Swaddle 1996, but see Dufour and Weatherhead 1998a,b; Jennions 1998). This
research area remains controversial, as measurements of
FA often indicate very slight di€erences among males,
raising questions about detectability and biological relevance (Pomory 1997; Swaddle and Cuthill 1997; Gangestad and Thornhill 1998). Moreover, FA may covary
with size and behavior, confounding interpretation and
posing challenges to experimental study (Palmer 1996).
Males of the brush-legged wolf spider, Schizocosa
ocreata (Hentz), have conspicuous tufts of dark bristles
88
on the tibiae of the ®rst pair of legs, which are used in
courtship and agonistic signaling (Aspey 1976, 1977;
Stratton and Uetz 1981, 1983, 1986; Sche€er et al. 1996).
Previous studies with live males and video images have
shown that these decorations function in species recognition and female mate choice (Sche€er et al. 1996;
McClintock and Uetz 1996; Uetz et al. 1996). Male S.
ocreata exhibit two forms of asymmetry in their tufts: (a)
regenerative asymmetry (RA), i.e., gross asymmetry
arising from a missing or reduced tuft as a consequence
of prior foreleg autotomy and regeneration (Uetz et al.
1996) and (b) FA, i.e., small random deviations from
perfect left-right symmetry arising from developmental
instability (Markow 1995; Palmer 1996). Females exhibit
lower receptivity to males with RA (Uetz et al. 1996),
but female receptivity in response to FA in male
Schizocosa has not yet been examined.
Video imaging in studies of animal behavior has
shown considerable promise as an experimental tool for
controlling covariates (Clark and Uetz 1992, 1993; Evans and Marler 1992; McClintock and Uetz 1996;
Rosenthal et al. 1996; Uetz et al. 1996; Kodric-Brown
and Nicoletto 1997). While not all species respond to
video images, it is apparent that for spider species with
higher visual acuity (including the Salticidae and
Lycosidae), video stimuli are reasonable substitutes for
live animals, and allow critical experimental manipulations in studies of species recognition and mate choice
(Clark and Uetz 1991, 1992, 1993; McClintock and Uetz
1996). Because FA may covary with body size, tuft size
and/or behavioral vigor (which might also in¯uence female mate choice), in this study we use video image
manipulation and playback to test the hypothesis that
female wolf spiders recognize asymmetry and discriminate against asymmetric males.
Methods
Spiders used in behavioral studies were collected as immatures
from their deciduous forest litter habitat at the Cincinnati Nature
Center, near Milford, Clermont County, Ohio, in April and May
1995, then brought to the laboratory and reared to maturity under
controlled conditions. A second set of adult males was collected for
measurement of tuft asymmetry later in the breeding season (early
June) in 1995. Laboratory conditions included a 13:11 light:dark
cycle, temperature range of 25±27 °C, and 60±75% relative humidity. Spiders were housed individually in opaque ``deli dish''
plastic food containers (12 cm diameter, 4 cm height) with clear
lids. Spiders were fed three to ®ve newly hatched ``pinhead''
crickets (2±3 mm body length) twice a week and provided with
water ad libitum.
Measurement of asymmetry in male tufts
Adult male spiders collected from the ®eld site (n = 47) were
brought into the laboratory and maintained under conditions described previously. Males were anesthetized with CO2, and placed
under a stereomicroscope for measurement of tuft asymmetry and
other body dimensions. One of us (G.U.) measured the length and
height of each tuft three times with an ocular micrometer, calculated tuft area as their product, then used the average area for each
tuft in estimation of asymmetry (L±R). This was done to compensate for potential measurement error arising from di€erential
repeatability of measures (tibia length is highly repeatable and low
in measurement error, while tuft height varies more along the
length of the tibia and is subject to some error depending on where
it is measured).
The distribution of signed values of male tuft area asymmetry
was tested for normality about a mean of zero, as predicted for FA
(Palmer 1996). In addition to tuft area, measures of cephalothorax
width (CW), body length (BL), abdomen width (AW) and abdomen length (AL) were made for a subset of ®eld-collected males
(n = 16) prior to laboratory feeding (to control for di€erences in
body condition as a consequence of laboratory maintenance). A
commonly used body condition index was calculated for these
males as the ratio of abdomen volume to CW (see Jakob et al.
1996). Data on asymmetry in this subset of males was analyzed by
regression and correlation with the above variables (Gangestad and
Thornhill 1998).
Response of females to asymmetry of live males
We tested the hypothesis that female receptivity responses to male
visual cues vary with the degree of tuft symmetry, using live males
as stimuli. Selected male S. ocreata similar in body size (body
length 7.0±7.6 mm) were paired randomly with conspeci®c females
(n = 33 pairs) in an apparatus used in previous studies (Sche€er et
al. 1996; Uetz et al. 1996). The distribution of FA values (see
above) was used to designate categories of degrees of asymmetry
corresponding (approximately) to thirds of the range: low
(< 0.4 mm2), intermediate (0.4±0.7 mm2) or high (> 0.7 mm2) for
live males used in behavioral studies. Females were virgin individuals selected at random from the available pool, of approximately the same age (to control for di€erences in behavior on
account of reproductive state). Observations of spider behavior
were made in adjacent clear plastic boxes (7 cm wide ´ 13 cm
long ´ 7 cm high) about 5 mm apart, but on separate foam blocks
to control for vibratory communication. Male courtship behavior
was stimulated by placing a piece of paper with female silk in the
box. An opaque paper barrier between boxes was removed when
the male began courting. Trials lasted 10 min, and were videotaped
for later analysis and scored blind. Data on female receptivity were
analyzed using a log-linear contingency test of independence based
on categories of the degree of male tuft asymmetry.
Video image manipulation and playback studies
We examined further the response of females to asymmetry in male
tufts with video playback studies. We used video imaging because it
allowed manipulation of the tufts while controlling for behavior
and size di€erences among males. Some spiders with acute vision
(e.g., Salticidae, Lycosidae) respond to video images as if they are
real (i.e., when presented with televised images of prey insects,
conspeci®c and heterospeci®c spiders they behave appropriately;
Clark and Uetz, 1991, 1992, 1993; McClintock and Uetz 1996; Uetz
et al. 1996; Persons and Uetz 1997). Since the visual component of
male courtship is by itself sucient to elicit receptivity in female S.
ocreata (Sche€er et al. 1996), moving video images of male courtship behavior are a reasonable substitute for live male stimuli
(McClintock and Uetz 1996; Uetz et al. 1996). This test has the
advantage that only the asymmetry of the tufts as a visual signal is
manipulated ± all other aspects of male body size, morphology, and
behavior are identical between treatments.
A courting male S. ocreata was videotaped with standardized
background and illumination, and images from this videotape were
digitized, modi®ed, and animated as described in previous studies
(Clark and Uetz 1991, 1992, 1993; McClintock and Uetz 1996; Uetz
et al. 1996). The control video was an unmodi®ed courting S.
ocreata male with tuft size close to the population median and
fairly symmetric tufts (``low'' FA as above; L±R = 0.24). The four
experimentally modi®ed video stimuli derived from this video had
di€erent degrees of asymmetry (Fig. 1), and were created to ad-
89
behaviors indicate that it has seen the other spider; direct approach
toward the stimulus, receptive body postures and leg displays are
obvious and unequivocal responses). Female display behaviors
noted in previous studies (Montgomery 1903; Uetz and Denterlein
1979; Stratton and Uetz 1983) were used to determine potential
receptivity as in previous studies. Just prior to copulation, females
orient to males and assume a body position that allows males to
mount (slow turn, settle, tandem leg extension, or lowering the
cephalothorax while raising the abdomen). Copulation will usually
not occur unless the female indicates receptivity by displaying one
or more of these behaviors (Sche€er et al. 1996; K. Delaney and
G.W. Uetz, unpublished data).
Results
Asymmetry in male tufts
Fig. 1 Video stimuli used in this study: control control male
Schizocosa ocreata; removed one tuft was removed completely;
reduced one tuft was reduced in size by approximately 25%;
balanced both tufts were modi®ed to retain the total on-screen area
of the spider's image, i.e., one tuft was reduced by approximately
25% and the other increased by the same amount; enlarged one tuft
was increased in size by approximately 25%. The individual frames
selected for display here are from a lateral view; the courting male
on video may be viewed from various angles by the female
dress di€erent aspects of asymmetry manipulation: (1) removed:
one tuft was removed, representing the most extreme level of FA or
RA (L±R = 2.4); (2) reduced: one tuft was reduced in height such
that the overall area was decreased by 25%, representing a midpoint within the range of natural FA variation (L±R = 0.9); (3)
enlarged: one tuft was increased in size by approximately 25% to
counteract any in¯uence of reduced tuft size (L±R = 0.9), and
could also be interpreted as a male with larger, but asymmetric
tufts; (4) balanced: both tufts were modi®ed to retain the total onscreen pixel area of the spider's image ± one tuft was reduced by
approximately 25% while the other was increased by the same
amount (L±R = 1.8). While the ``removed'' and ``balanced''
treatments may represent asymmetry levels closer to extremes of
natural variation, the ``reduced'' and ``enlarged'' manipulations
were well within the range of natural variation of the trait (based
on the distribution of values presented below).
Videos were used to test the null hypothesis of independence of
female receptivity and asymmetry of the male stimulus. Videotaped
images were presented to females on a Sony Watchman liquid
crystal display (LCD) color microtelevision unit (2 inch diag.
screen) in an arena used in previous studies (McClintock and Uetz
1996; Uetz et al. 1996). Female spiders used as subjects in video
experiments were virgins selected at random from the pool of spiders collected in the ®eld (n = 143). Female spiders were used only
once [a sample of 15±20 female spiders was used for each stimulus
tested; unresponsive spiders (those not indicating any response to
the stimulus) were eliminated from the analysis]. Female S. ocreata
were presented with one of several digitized and re-animated video
stimuli from a courting male S. ocreata ± either the control (symmetric) video, or one with tufts modi®ed to be asymmetric (as
above). Trials lasted 10 min, during which female behaviors were
videotaped for later analysis. After each trial, arenas were cleaned
with an alcohol-dipped cotton swab to remove all silk and traces of
pheromones from the previous occupant.
Behavioral responses of female spiders were scored using
qualitative measures of response (presence/absence of orientation,
approach, and receptivity display behaviors). As the behavior of
these wolf spiders is highly stereotyped, responses are easily scored
(e.g., if a female swivels and orients to the male or the screen, those
The distribution of tuft area asymmetry values from a
sample of ®eld-collected males (Fig. 2) was distributed
normally (Wilk-Shapiro Rankit statistic = 0.9477,
P > 0.50) about a mean value of zero (one sample ttest, t = )1.18, P > 0.2), as predicted for ``true'' ¯uctuating asymmetry (Palmer and Strobeck 1986; Palmer
1996). As it was impossible to determine repeatability of
FA measures for these samples, we used the post hoc
method suggested by BjoÈrklund and MerilaÈ (1997),
based on coecients of variation (1.18 for the sample of
47 males above, and 0.558 for the sample of 16 males
described below). The results suggest a potential for FA
measurement error of +55% to ±27%, respectively, less
than many published values.
A subset of males was measured directly after ®eld
collection and prior to feeding, to assess body condition
under ®eld conditions during the breeding season. These
measures (untransformed) were used in correlative analyses as suggested by Gangestad and Thornhill (1998).
In ®eld-collected males, tuft asymmetry was signi®cantly
negatively correlated with both body size (BL,
r = )0.673, P < 0.05; Fig. 3a) and the ratio index of
Fig. 2 Frequency distribution of tuft area asymmetry values from
a sample of ®eld-collected male S. ocreata (n = 33)
90
Fig. 4 Receptivity of female S. ocreata to video images of
symmetric and asymmetric males (for treatments, see legend to
Fig. 1 and text)
the ``intermediate'' and ``low'' asymmetry categories
(Table 1).
Video image manipulation and playback studies
Fig. 3 Regressions of male tuft asymmetry on body size (length in
mm) (a) and condition (index of abdomen volume/cephalothorax
width) (b) from a subsample of male S. ocreata measured directly
after collection from the ®eld
body condition (abdomen volume/CW, r = )0.782,
P < 0.05; Fig. 3b).
Response of females to asymmetry of live males
Female receptivity responses to live males from three
asymmetry categories were not independent of degree of
asymmetry (log-likelihood ratio test, GWilliams correction = 10.43, P < 0.005). Females exhibited no receptivity to males in the ``high'' asymmetry category, while
approximately 60% of females were receptive to males in
Table 1 Number of female Schizocosa ocreata exhibiting receptivity to males with varied degrees of asymmetry. The categories
correspond to approximate thirds of the range of asymmetry values
in the frequency distribution in Fig. 2
Asymmetry category
Receptive
Not receptive
Lowest third (< 0.4 mm2)
Middle third (< 0.4±0.7 mm2)
Highest third (> 0.7 mm2)
7 (63.6%)
9 (60.0%)
0
4 (36.3%)
6 (40.0%)
7 (100.0%)
Female receptivity was not independent of the symmetry
of the video stimulus (log-likelihood ratio test, GWilliams
correction = 33.89, P < 0.001), and was clearly reduced
in response to all asymmetric male video stimuli compared to the symmetric male video control (Fig. 4). The
video treatments were treated above as qualitatively
di€erent categorical treatments in a contingency analysis, allowing rejecton of the null hypothesis of independence. However, while the degree of asymmetry in the
video stimuli ranges from a low of approximately 0.24
(control) to a high of approximately 2.40 (``removed''),
two treatments ± ``reduced'' and ``enlarged'' ± are
qualitatively di€erent but equal in asymmetry. An alternate analysis may therefore be appropriate, and we
have taken two additional approaches: (a) we tested
each of the asymmetry manipulations against the control
separately, and all were signi®cantly di€erent (removed:
v2 = 3.88, P < 0.01; reduced: v2 = 8.42, P < 0.05;
balanced: v2 = 4.40, P < 0.05; enlarged: v2 = 3.70,
P £ 0.05), and (b) we tested all four asymmetry treatments in a contingency test of the null hypothesis of
independence (to address the concern that previous rejection of the null hypothesis was based on females responding to extreme values); the result was not
signi®cant (GWilliams correction = 2.40, P > 0.60).
Discussion
Numerous studies have demonstrated that asymmetry of
secondary sexual characters in¯uences male mating
success in a variety of animals, including insects, ®sh,
birds, and mammals (Mùller 1990; Thornhill 1992;
91
Swaddle and Cuthill 1994; Watson and Thornhill 1994;
Mùller and Swaddle 1997; Sheridan and Pomiankowski
1997; but see Dufour and Weatherhead 1998a,b; Ligon
et al. 1998). Data presented here and elsewhere (Uetz
et al. 1996) suggest that this may be true for S. ocreata
wolf spiders as well. Earlier work has shown that female
S. ocreata discriminate against males whose foreleg tufts
are grossly asymmetric owing to limb loss and incomplete regeneration (Uetz et al. 1996). In this study, we
present evidence for FA in these decorative tufts, and
that it may in¯uence female mate choice. Female wolf
spiders exhibited reduced receptivity responses to live
males with higher asymmetry values, as well as to video
images of courting males with varying degrees of
asymmetry. While concerns over reduced response to
extreme phenotypes might well be raised here (e.g., male
wolf spiders with high asymmetry in tufts might be behaviorally impaired and exhibit less vigorous courtship,
or be perceived as heterospeci®cs), the results of the
video playback experiments suggest that the asymmetry
of the visual signal presented by the tufts, rather than
any concomitant behavioral or size factor, is the cue to
which female wolf spiders are responding.
Criticisms are often raised concerning FA and mate
choice because few studies are able to experimentally
separate the asymmetry of the male character from other
covarying qualities that might also in¯uence mate choice
(Palmer 1996). Video playback has been increasingly
used as an experimental tool in studies of animal behavior in numerous taxa, including ®sh (Rowland 1995;
Rowland et al. 1995a,b; Rosenthal et al. 1996; KodricBrown and Nicoletto 1997), birds (Evans and Marler
1992; Adret 1997), reptiles (Macedonia and Stamps
1994; Macedonia et al. 1994) and amphibians (Roster
et al. 1995). Of particular value, as demonstrated in this
case, is the ability to manipulate a single aspect of the
visual signal to test its potential importance. The
responses of female Schizocosa spiders to video stimuli
from male conspeci®cs are identical to those seen with
live males, and receptivity displays are clear indications
of a female's willingness to mate (McClintock and Uetz
1996; Uetz et al. 1996). The video studies conducted here
clearly demonstrate that with male size and behavior
held constant, female wolf spiders prefer symmetrical
over asymmetrical males.
In several recent experiments, Swaddle and Cuthill
(1994), Bennett et al. (1996) and Fiske and Amundsen
(1997) successfully altered female mate preference in
birds using manipulated asymmetry of colored leg bands
(but see Jennions 1998). Follow-up studies demonstrated
that not only mating success but also reproductive success (number of surviving o€spring) are related to experimental manipulation of symmetry in leg bands
(Swaddle 1996). Recent criticism of this approach by
Rohde et al. (1997) has centered on the use of a highly
arti®cial ornamental trait, such that ``the female's lack of
preference may potentially re¯ect no more than the nonacceptance of extremely deviant or physically defective
males'' (but see responses by Swaddle 1997; Swaddle and
Cuthill 1997). In our study, the trait in question was not
an arti®cial addition (e.g., colored leg bands), and manipulation of asymmetry in the trait was (in part) within
the range of natural variation. Even so, the absence of
receptivity must be interpreted with some caution. While
we can be certain that a female perceives the video
stimulus by the presence of orientation toward the
screen, it is possible that asymmetry in the tufts may be
perceived by the female as an extreme phenotype outside
the range of species-typical display, and lack of response
might indicate non-acceptance on that basis (Rohde et al.
1997). However, while the frequency of females responding receptively was signi®cantly reduced relative to
the control across all asymmetric stimuli, some receptivity responses were seen (14±35% of females). This
would suggest that asymmetric video stimuli are recognizable as conspeci®c males. Moreover, the absence of
statistically signi®cant di€erences between those treatments within the range of natural variation in asymmetry (``reduced'' and ``enlarged'') and the more extreme
manipulations (``balanced'' and ``removed'') argues for
discrimination against asymmetry, and not simply a lack
of species recognition or rejection of extreme phenotypes
or deviant forms.
There are several plausible explanations why female
wolf spiders should recognize and discriminate against
asymmetric males. Visual signaling with leg-waving
displays is a critical element of the signal-receiver process in S. ocreata, as their complex leaf litter habitat may
constrain female perception of male vibratory courtship
(Uetz 1990; Sche€er et al. 1996). Asymmetry in the tufts
might therefore reduce the ecacy of the male's visual
signal. Studies with neural net models suggest that sensory systems may have the innate capacity to discriminate against asymmetric signals or select for symmetry
as a by-product of mate recognition (Enquist and Arak
1994; Johnstone 1994; Enquist and Johnstone 1997).
Alternatively, asymmetry in this highly visual secondary
sexual characteristic may re¯ect some aspect of male
``quality'' and/or developmental instability, and serve as
an indicator trait for female mate choice. Data presented
here for live ®eld-collected males show that tuft asymmetry is negatively correlated with body condition, and
thus may re¯ect a male's feeding history. If asymmetry
re¯ects prior leg autotomy and regeneration owing to an
aggressive encounter, it may also serve as an indicator of
reduced ®ghting success (Uetz et al. 1996). Conversely,
asymmetry of regenerated legs may indicate developmental stability in a direct way, as those with superior
ability to regenerate autotomized limbs would be more
symmetric. If asymmetry was related to any of these
possibilities, female choice based on symmetry in
S. ocreata might enhance female ®tness indirectly by
a€ecting o€spring success, and be subject to selection as
well.
Acknowledgements This research was supported by grant IBN
9414239 from the National Science Foundation, and a supplement
from the Research Experiences for Undergraduates Program.
We thank the Cincinnati Nature Center, Milford, Ohio, for
92
allowing us to collect spiders. We gratefully acknowledge the
assistance of A. DeLay, K. Delaney, E. Hebets, M. Persons,
R. Mendoza, B. Kilinc, H. Kuyper and E. Sanborn in collecting
and maintaining spiders for this research project. We also appreciate statistical advice from R.Z. German, and comments on the
manuscript from J. Calos, J.A. Roberts, M. Orr, D. Kroeger, M.
Porter, M. Elgar, T. Amundsen and two anonymous reviewers.
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Communicated by M.A. Elgar