Behavioral Ecology
doi:10.1093/beheco/arl101
Advance Access publication 4 January 2007
Discrete genetic variation in mate choice and
a condition-dependent preference function in
the side-blotched lizard: implications for the
formation and maintenance of coadapted
gene complexes
Colin Bleaya and Barry Sinervob
School of Biological Sciences, University of Bristol, Woodland road, Bristol BS8 1UG, UK and
b
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064, USA
a
Variation in female preference functions, both genotypic and phenotypic, has been largely ignored in the literature, despite its
implications to the maintenance of genetic variation in populations and the resolution of the ‘‘Lek paradox.’’ Polymorphic
populations, such as in the side-blotched lizard, provide ideal study systems for its investigation, especially in the context of
incipient processes of sympatric speciation. Females of the side blotch lizard exist in 2 genetically distinct morphs, yellow
throated and orange throated, that experience disruptive selection for life history traits. Males express 3 throat color morphs,
blue, orange, and yellow, that exhibit alternative strategies in intrasexual competition. We experimentally tested for female
preference in triadic mate choice trials to identify the presence of discrete genetic and condition-dependent variation in female
preference function. We found that females did in fact show genetic variation in preference for males but that females also
operate a multicondition preference function dependent upon the genotype of the female and her state (number of clutches
laid). Females exhibited positive assortative mating prior to the first clutch. However, prior to later clutches, orange females
switched choice, preferring yellow males. These findings are discussed in relation to the maintenance of coadapted gene
complexes within populations and the prevention of divergent directional selection (population bifurcation) by conditiondependent variation in mate choice. Key words: coadapted gene complex, condition dependent, disruptive selection, genetic
variation, lek paradox, mate choice, polymorphism, side-blotched lizard, sympatric speciation. [Behav Ecol 18:304–310 (2007)]
pecies with genetically distinct alternative strategies are
useful model systems for investigating mechanisms for
the formation and maintenance of coadapted gene complexes
that serve as a requisite for processes of sympatric speciation
(West-Eberhard 1979; Sinervo and Svensson 2002). To date,
the majority of research on species that exhibit alternative
strategies has focused on the role of intrasexual selection
(Austad 1984; Gross 1996; Brockmann 2001), with few studies
examining the impact of intersexual selection (Fox et al. 2002;
Morris et al. 2003). Mate choice has far reaching implications
for the maintenance of genetic polymorphisms, depending
on the preference function employed by the choosing sex.
Mate choice is expected to occur where the costs of choosiness are exceeded by the benefits accrued from exhibiting
a preference. Two possible adaptive reasons exist for mate
choice: 1) indirect benefits, the result of genetic benefits to
offspring fitness. This can be further subdivided into a) the
maintenance of genetic compatibility or the reduction of recombinational load that results from sexual reproduction
(Tregenza and Wedell 2000), b) additive genetic benefits to
offspring reproductive success (the ‘‘good genes’’ hypothesis;
Williams 1966, p. 193), and c) selection for ‘‘arbitrary’’ male
display traits, a nonadaptive sensory exploitation model (Fish-
erian ‘‘runaway’’ hypothesis; Fisher 1930; Lande 1981; Kirkpatrick 1982); 2) direct benefits to the chooser, such as increased
survivorship or fecundity (Reynolds and Cote 1995; Godin and
Briggs 1996).
Address correspondence to C. Bleay. E-mail: colin.bleay@Bristol.
ac.uk.
Received 29 July 2004; revised 31 August 2006; accepted 2
November 2006.
ADDITIVE GENETIC BENEFITS TO OFFSPRING
REPRODUCTIVE SUCCESS
S
The Author 2007. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
THE MAINTENANCE OF GENETIC COMPATIBILITY
When the viability of offspring is highly dependent upon genetic compatibilities within the genotype of the individual
(Tregenza and Wedell 2000), coadapted gene complexes are
built up under the action of correlational selection (Brodie
1992; Sinervo et al. 2001; Sinervo and Svensson 2002; Sinervo
and Clobert 2003), and so recombination should not be
a strong force in determining female preference functions.
Alternatively, for unlinked traits, in linkage disequilibrium,
any covariance will decay by 50% per generation (Pomiankowski and Sheridan 1994), leading to strong selection for
assortative mating to maintain linkage disequilibrium. This
axiom is central to theories of sympatric speciation by sexual
selection (Dobzhansky 1940). Therefore, in populations that
are inherently polymorphic and experience cyclical selection,
we expect that females will exhibit positive assortative mating.
Choice would be dependent upon not only male genotype
but also on the genotype of the chooser.
If males exhibit genetic variation in alleles that contributes
to offspring survivorship or reproductive success, indirect
Bleay and Sinervo • Discrete genetic variation in mate choice
selection will favor those females that adopt a preference function to sequester ‘‘good genes.’’ Selection for purely additive
genetic fitness effects should be independent of the genetic
background of the male unless differences in male display
indicate differences in linked fitness loci (David et al. 2000).
If preferences were independent of genotype, this would result in the break down of coadapted gene complexes built up
under the action of correlational selection. Directional selection for additive fitness loci will result in those loci reaching
fixation. Direct selection would result in the loss of premating
isolation and the break down of coadapted gene complexes.
DIRECT BENEFITS TO THE CHOOSER
Theoretical (Bulmer 1989; Kirkpatrick 1996) and empirical
(Moller and Jennions 2001) evidence exists for direct selection on female preference as a stronger force than selection
for indirect benefits. Although it has been suggested that any
effect of a direct preference function acts independently of its
genetic background (Servedio 2001), it is difficult to see how
differentiation in female choice could evolve in sympatry under its control, unless an individual’s ability to absorb direct
fitness costs has a heritable component. Differences in female
‘‘quality,’’ whether genetic or phenotypic, may lead to patterns
of assortative mating, whereby selection favors females of
lower quality mating with males that have a reduced impact
on female fitness. Alternatively, condition-dependent female
choice may be a possible mechanism to maintain genetic variation within a population. Therefore, it is possible that in
polymorphic systems that experience strong indirect selection
for assortative mating, variation in female abilities to weather
direct fitness costs adds stochasticity to preference functions.
Thus, maintaining genetic variation and the production of
morph hybrid offspring.
In this study, we looked for the presence of positive assortative mating in light of the costs of recombinational load to
offspring fitness. Throat color was used as a proxy for an individual’s genotype. In addition, we examined changes in the
context of female mate choice by investigating differences in
female preference function prior to the first clutch and before
the second clutch. We predict that females may choose to
mate with males of the same morph but that changes in female condition may add some context-dependent variation in
female preference.
THE STUDY SYSTEM
Inherent in populations of side-blotched lizards (Uta stansburiana) are 3 distinct throat color polymorphisms (orange, blue,
and yellow). Throat color acts as an honest signal of relative
male quality, being genetically hard wired and not condition
dependent (Alonzo and Sinervo 2001). The most parsimonious explanation for the genetic architecture appears to be, a
3 allele, single locus model that simultaneously links male and
female strategies (Sinervo 2001). Color morphs in both males
and females are manifest as alternative reproductive strategies,
which oscillate in frequency as a function of intrasexual competition in both sexes. Males cycle in a rock–paper–scissors
game where orange usurpers invade blue mate guarders, which
are then invaded by a yellow sneaker strategy that is in turn
invaded by the blue mate guarder strategy (Sinervo and Lively
1996; Zamudio and Sinervo 2000). This male cycle is intrinsically propagated (Bleay C, Sinervo B, in preparation) and entirely frequency dependent. Females are caught in a classic r-K
game that is density dependent (Sinervo, Svensson, and
Comendant 2000). Female reproductive allocation is genetically
predetermined (Sinervo, Svensson, and Comendant 2000) in
that orange females invest in quantity (larger clutches of
305
smaller offspring) and yellow females invest in quality (smaller
clutches of larger offspring). Female fitness or the survivorship
of offspring is density dependent, where large hatchlings from
yellow females gain an advantage in periods of high density
(Sinervo, Svensson, and Comendant 2000). Conversely, orange
females produce larger clutch sizes of smaller hatchlings that
gain an advantage in periods of low density. In addition to the
tight coupling of female reproductive strategies with throat
color, an individual’s socially mediated stress response, humoral
immunocompetence, and their ability to absorb the costs of
reproduction (Svensson et al. 2001a, 2001b) are linked to female throat color. Yellow females showed an increased reduction in postlay mass as a function of clutch size compared with
orange females (Svensson et al. 2001a). This suggests genetic
differences between morphs in their ability to weather the impacts of reproductive allocation. These differences should manifest themselves in a female’s preference function, as direct
fitness costs for a female’s progeny should have varying effects
depending on the genotype of the female and the state of the
population cycle (Alonzo and Sinervo 2001).
As a result of fluctuations in selection pressure, it is believed
that a runaway process of correlational selection has resulted
in the tight coupling of phenotypic traits to specific throat
color alleles (Sinervo 2001; Sinervo et al. 2001). The action
of positive assortative mating would also serve to maintain the
linkage between what we refer to as strategic loci, which are
any loci unlinked to the main morph determining locus, that
serve to enhance the fitness of specific genotype combinations
at the morph locus (Sinervo and Clobert 2003). Therefore, we
predict that female phenotypes may exhibit variation in mate
preference and can be used as a baseline to indicate the genetic control of female preference. The female has 2 basic
mate choice strategies. The first is to maintain the integrity
of the coadapted morph complex and participate in homologous genotype matings (e.g., orange 3 orange) (Sinervo 2001).
The second is to adopt matings that enhance female lifetime
reproductive success. Therefore, females may make contextdependent mate choice decisions.
METHODS
We designed an experiment to test for asymmetric patterns
of intersexual selection in the side-blotched lizard. Genotypespecific mate preferences were easy to examine because females of the side-blotched lizard exist in 2 morphs, orange
throated and yellow throated. The presence of a single orange
allele causes the female to adopt the r-strategy type. Therefore,
genetic variation in mate preference was assigned on the basis
of differences in female morph mate preference. The role of
conditional effects was investigated by examining changes in
mate preference prior to the first clutch and the second clutch.
Females show a marked reduction in condition after the production of their first clutch of eggs (Svensson et al. 2001a).
In order to test for the presence of female mate preference,
relative choice trials were carried out in a triadic choice chamber (Figure 1). During February, prior to the onset of the
mating season, 47 female and 45 male lizards were removed
from a population at Los Banos and brought into the lab.
Females were housed in vivaria (approximately 20 l), given
food ad libitum, with both light and heat on a 12-h cycle. They
were then left for 5 days in order to acclimatize. When females
reached a period of reproductive receptivity, determined by
abdominal palpation (ovarian follicle size of 3–5 mm), they
were presented with 3 males, one from each male morph,
matched for size, in a relative preference trial. Extensive
fieldwork over the course of 14 years indicates that courting
females have an ovarian follicle size of 3–5 mm (Sinervo B,
unpublished data).
306
Behavioral Ecology
Figure 1
A diagrammatic representation of the relative choice trial
chamber with dimensions. (A)
top view and (B) side view, note
the angled glass front to avoid
reflections obscuring the camera’s view.
Each trial was videotaped, the duration of each trial being 20
min, and carried out at times when animals would be normally
active in the field (9–12, 15–18 h). Males were randomly assigned a chamber, and temperature readings were taken for
each chamber so that these effects could be removed in any
subsequent analysis, if detected. Temperature gradients of 25–
40 C (thermal preference in this population is 35 C) were
maintained in each chamber. Between each trial, the sand was
changed to remove any effect of prior occupation as a result of
pheromonal cues (Martin and Lopez 2000). Males were tethered in their respective chambers so that females had free
access to each male, yet males could not see or physically interact with each other, removing any effect of male–male competition. Females were placed at the center of the choice
chamber and given 5 min to acclimatize prior to revealing
the males with the raising of a partition situated between
the male and female areas of the choice chamber. All males
exhibited courtship behavior, including the least dominant
yellow morph males, and were not inhibited by being tethered
or by a possible effect of ambient male odor. In all, 42 (24
orange, 18 yellow) first clutch and 25 (9 orange, 16 yellow)
second clutch females were tested using 36 (9 blue, 13 orange,
14 yellow) males on the first clutch and 29 (10 blue, 10 orange,
9 yellow) on the second. Males were never presented to the
same female more than once but were used for both the first
and second clutch trials. All females used on the second trial
were used in the first mate choice trial. Videos were then analyzed using Etholog v2.2. Both male and female behaviors
were scored. Spatial associations of females with males were
calculated based on the time spent in a particular male area.
The number and incidence of female head bobs, rejection and
acceptance displays to a specific male, and ‘‘tastes’’ were also
noted. We classed ‘‘tastes’’ as where a female samples the sand
in the environment using tongue projections (Bleay C, personal observation). The number and incidence of male head
bobs toward the female was also scored so that the effects of
male activity on female preference could be examined. While
no copulation was observed, acceptance and rejection displays
can be easily identified by the body posture of females. When
push-up displays, used by Iguanid lizards in communication,
are accompanied by arching of the body and lateral flattening,
it is a sign of rejection (Martins 1993, 1994). If female head
bobs were associated with tail raising or tail movement (in the
absence of lateral compression), this was classified as an acceptance display (Sinervo B, personal communication).
RESULTS
Not all females exhibited acceptance displays (unambiguous
choice, 24 trials) so discriminant function analysis using data
from the unambiguous trials was employed to assign a choice
to all other trials (ambiguous choice, 43 trials). Using discriminant function analysis is a more rigorous approach than simply using association time per se because, unlike the majority
of studies of mate choice that use only one criterion (time),
we have used independent indicators of choice (rejection and
display) to determine the weight assigned to other behavioral
indicators of choice. In the side-blotched lizard, we are fortunate enough that there are both a conspicuous rejection and
acceptance display that are unambiguously indicative of
choice, lack of these displays did not imply no choice. Discriminant function analysis works by determining the relationship
between a dependent categorical variable and a number of
continuous independent variables. This relationship is expressed in the form of a discriminant prediction equation that
can then be used to assign individuals to a category based on
their position in independent variable space. In total, 24 trials
(13 first clutch, 11 second clutch) were unambiguous and so
used in the discriminant function analysis. Independent variables were calculated as a relative value, proportionate to the
total time of the trial or as proportionate incidence, and arcsine transformed. The time that a female spent in a particular
male chamber, the residuals of female head bobs regressed on
male head bobs and time, and the number of ‘‘tastes’’ were
used as determinants for the model. Each variable was entered
in a forward stepwise model until any subsequent contribution would be r , 0.01. Both time and residuals of female
head bobs were retained in the model with a canonical correlation of 0.73 (Wilks’ Lambda; F2,24 ¼ 8.98, P , 0.005). Two
trials were misclassified; however, these were positives that
were wrongly assigned, so any classification based on the discriminant function analysis was conservative. The forthcoming discriminant prediction equation was then used to assign
a choice to females in the ambiguous trials so that the total
sample size used in subsequent analyses was 45 females from
the first clutch and 25 females from the second clutch.
There were a number of factors that may have contributed
to observed patterns of female preference. Logistic regression
of temperature (v2 ¼ 0.218, degrees of freedom [df] ¼ 1, P .
0.05), male mass (v2 ¼ 0.46, df ¼ 1, P . 0.05), male snout vent
length (SVL) (v2 ¼ 1.79, df ¼ 1, P . 0.05), male body condition defined by the residuals of male mass on SVL (v2 ¼ 1.03,
df ¼ 1, P . 0.05), and a chi-square of male chamber position
(v2 ¼ 4.08, df ¼ 2, P . 0.05) were all found to have no
significant effect on female preference. So as to remove any
effect of pseudoreplication, both male and female IDs were
entered into subsequent models as a random effect.
Nominal logistic regression was used to look for the effect of
male phenotype and female state on the probability of acceptance by female morph. Both male morph and female state
Bleay and Sinervo • Discrete genetic variation in mate choice
307
Table 1
The effects of male phenotype and female condition on the
incidence of female preference by morph (yellow females and
orange females)
v2
df
P
Yellow females
Full model
Male phenotype
Clutch no.
Male phenotype 3 clutch no.
19.28
16.92
0.007
0.90
5
2
1
2
0.002**
0.0002***
0.933
0.637
Orange females
Full model
Male phenotype
Clutch no.
Male phenotype 3 clutch no.
14.82
0.86
0.01
8.97
5
2
1
2
0.011*
0.651
0.922
0.011*
*P ,0.05, **P ,0.005, ***P ,0.0005.
a female displays toward a particular male) toward females
than orange and blue males (F2,36 ¼ 5.075, P , 0.05). Males
that did not exhibit any head bobs during the trial were classified as null responses and removed from the analysis.
DISCUSSION
Figure 2
Incidence of female preference for male phenotypes. The solid line
shows the expected frequency assuming random probability of
preference at 0.33. (A) Yellow female preference and (B) Orange
female preference.
had a significant effect on the pattern of choice for a particular
female morph. In yellow-throated females (Figure 2A), there
was a strong, significant, preference for yellow-throated males
irrespective of female condition (Table 1). Orange females, on
the other hand, exhibited a different pattern of choice (Figure
2B). There was a significant interaction between female state
and preference for a particular male morph (Table 1). Prior to
the first clutch, orange females showed a preference for orangethroated males, but this preference shifted toward yellowthroated males prior to the second clutch. A possible explanation for the shift in orange female preference as a function of
female condition may be the reduced aggressiveness of yellow
males (Figure 3). Reproduction has a dramatic effect on female
condition; however, irrespective of the male, female sideblotched lizards exhibit genetic differences in the ability to
weather the impact of reproduction.
Yellow females lost less weight (as a proportion of their pre–
first clutch mass) as a result of laying their first clutch than did
orange females (yellow mean ¼ 0.27 6 0.03, orange mean ¼
0.34 6 0.01, t ¼ 1.69, df ¼ 65, P , 0.05).
That is to say, females may experience a direct fitness benefit
by mating with less aggressive males for their second clutch
when their body condition is greatly reduced. Yellow males did
show significantly less activity (where activity is measured as the
residuals of male head bobs from both proportionate time
a female spends with a male and the proportion of head bobs
It was evident that female side-blotched lizards exhibit morphspecific variation in their preference function. Females mated
assortatively, orange females exhibited a preference for orange males and yellow females preferred yellow males, prior
to the first clutch. Furthermore, we also found evidence of a
condition-dependent change in mate choice that was associated with the production of first and second clutches.
The difference in preference function, between female
morphs, is inferred to be genetic. Although no measure of
repeatability (Godin and Dugatkin 1995) or genetic correlations across generations (Houde 1992) were possible, given
the highly heritable nature of throat color (Sinervo and
Svensson 2002), female preference and throat color should
be genetically linked. Evidence for the genetic control of mate
preference in other species is strong (Houde 1992; Bakker
Figure 3
The difference of yellow males from both orange and blue males
activity. Where Activity is measured as the residuals of male head
bobs from both proportionate time a female spends with a male and
the proportion of head bobs a female displays toward a particular
male.
Behavioral Ecology
308
1993), with several examples of discrete variation in female
preference function (Sappington and Taylor 1990; Fox et al.
2002; Morris et al. 2003).
In systems that experience disruptive selection for fitness
traits, such as female reproductive allocation in the sideblotched lizard (Sinervo, Svensson, and Comendant 2000;
Svensson and Sinervo 2000), genetic variation is increased
(Thoday 1972; Halliburton and Gall 1981; Sappington and
Taylor 1990). Positive assortative mating, as exemplified by
female preference functions in the side-blotched lizard, would
act to reduce genetic diversity and so maintain the discrete
nature of the genetic polymorphism. Assortative mating will
reduce genetic variation in the broad sense by creating a number of discrete genetic combinations within the population.
Mate choice for assortative mating can be ascribed to indirect female fitness if offspring generated from between-morph
matings lie at the antimode of a bimodal fitness distribution
created by disruptive selection. Females may be choosing males
on the basis of good genes (Williams 1966), yet this is dependent on the phenotype, and ultimately the background genetic
architecture of the female. If females selected mates based
purely on an additive good genes model, then female preference functions would be expected to resemble those of Alonzo
and Sinervo (2001) where the optimal female preference
switches between males of different morphs based on their
relative fitness in the population, irrespective of female morph.
In our study, we also found that orange-throated females
exhibit a state-dependent switch point in their preference
function. Prior to the first clutch, orange females showed positive assortative mating, mating with orange males; however,
prior to their second clutch, orange females switched, showing a preference for yellow males. The probability of switching
mate preference was morph specific with yellow females showing no such adaptive behavior.
State-dependent variation in female choice strategies has
received little attention in the literature. Theoreticians have
understood the consequences of female state on reproductive
decision making, but little empirical evidence exists in relation to mate choice decisions.
Age or timing of breeding in relation to the duration of
the breeding season is known to alter female mate choice
decisions (Backwell and Passmore 1996; Gray 1999; Moore PJ
and Moore AJ 2001). Predictions are that females will become
less choosy as their potential for future reproductive success
diminishes (Gray 1999; Moore PJ and Moore AJ 2001), a random preference is expected. This was not found in the present
study. Previous examples of state-dependent switches in female
preference are mainly linked to changes in direct fitness costs
(Koga et al. 1998; Luttbeg et al. 2001). Changes in predation
pressure have resulted in female guppies changing their
preference from brightly colored males to duller males in
the presence of cichlid predators (Gong and Gibson 1996).
Females may exhibit differences in their abilities to weather
direct fitness costs of reproduction that could have reciprocal
effects on differences in preference function. Orange males
were found to be more active, displaying more readily to females, and are known to have higher levels of testosterone
making them more aggressive (Sinervo, Miles, et al. 2000).
Females that mate with orange males may incur a higher direct
cost to reproduction as a result of male harassment (Wilcox
1984; Rowe 1994; Muhlhauser and Blanckenhorn 2002). Classically, manifestations of variation in female choice in relation
to male harassment are a function of female size, with smaller
females unable to endure the costs of mating with larger males
(Bourne 1993). Neck-biting behavior by males is a component
of courtship and mating in the side-blotched lizard that has the
potential to result in female injuries (Hiruki et al. 1993a,
1993b; Le Galliard et al. 2005). The probability of sustaining
an injury of this type may therefore be increased with the
aggressiveness of the male in combination with the reduced
ability of the female to defend herself. In populations of the
common lizard, Le Galliard et al. (2005) found that as the
proportion of males in the population increased so did maleinflicted mating injuries along with reduced female survivorship and fecundity. Differences between females in respect to
the impact of direct fitness costs may be a function of differences in condition generated by alternative reproductive allocation strategies. In the side-blotched lizard, the different male
morphs may offer alternative fitness consequences such that
a female can ameliorate any cost by picking and choosing her
mate based on her condition.
Alternatively, it is possible that orange females switch choice
of mate based on indirect fitness benefits (Lesna and Sabelis
1999; Alonzo and Sinervo 2001; van Gossum et al. 2001). Unpublished data (Sinervo B, personal communication) on male
survivorship suggest that yellow males are recruited from the
second clutch, with few surviving from the first clutch. Only
orange and blue males from the first clutch survive into the
next breeding season. Orange females may be sequestering
yellow strategic loci for investment into males in the second
clutch. If this is true, orange females should invest disproportionately in males on the second clutch.
CONCLUSIONS
Here it is impossible to distinguish between the alternative
hypotheses for the proximate mechanisms of selection that
promote mate choice. Whether it is good genes, a Fisherian
runaway process, maintenance of genetic architecture, direct
selection, or even sensory exploitation, the same patterns of
covariance between preference trait and mate choice could be
observed. What is shown is that there exists a great deal of
variance in female choice within populations. Variation in female choice has the potential to maintain genetic variation in
populations even in the presence of divergent directional selection. A standard population-wide optimum strategy does
not exist. The optimum choice of mate is dependent upon
the context, whether it is genotypic or phenotypic, in which
a decision is made and can result in females switching preference to the extent that multiple optimal pairings within a population can exist. The number of optimum mates should
increase exponentially as a function of genotype 3 genotype 3
environmental interactions to the extent that variation in
both female mate choice and its reciprocal effects on male
display trait could never be exhausted, even in the face of
strong directional selection. Fitness traits are under continually fluctuating selective environments, with the effects of
genes being context dependent, that context being the
background genetic architecture with which it interacts, the
background gene frequencies within the population, and
environmental fluctuations in natural selection pressures.
Stochastic, frequency dependent, density dependent, and
epistatic interactions maintain genetic variation within
populations. If females differ in the fitness consequences of
sequestered ‘‘good genes,’’ this will maintain genetic variation;
as a result, epistatic interactions will be different between females causing females to select different males. The fact that
female choice can be unrepeatable may indicate a large context dependent or conditional rule in female preference functions. In systems with alternative strategies, disruptive selection
can result in concomitant selection for assortative mating; however, pleiotropic effects on condition-dependent preference
functions can act to maintain genetic variation preventing
reproductive isolation. Whether these preference functions
manifest themselves in population mating patterns depends
on the cost of choosiness (Slagsvold et al. 1988; Dawkins and
Bleay and Sinervo • Discrete genetic variation in mate choice
Guildford 1995) or the encounter rate for preferred males
(Alatalo et al. 1988; Arak 1988) and antagonistic effects of
male–male competition (Alatalo et al. 1986; Lifjeld and Slagsvold 1988) obscuring female preference.
We would like to thank Professor Alasdair Houston and Professor
Innes Cuthill for their helpful comments in the preparation of this
paper, along with numerous undergraduates who attended University
of California, Santa Cruz for their animal husbandry skills.
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