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Behavioral Ecology Vol. 13 No. 6: 791-799
© 2002 International Society for Behavioral Ecology
Sexual selection and condition dependence of courtship display in three species of horned dung beetles
Department of Zoology, University of Western Australia, Nedlands, WA-6907, Australia
Address correspondence to J.S. Kotiaho, who is now at the Department of Biological and Environmental Sciences, University of Jyväskylä, PO Box 35, FIN-40351, Jyväskylä, Finland. E-mail: jkotiaho{at}cc.jyu.fi.
Received 1 June 2001; revised 19 December 2001; accepted 18 February 2002.
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ABSTRACT |
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Sexual selection has traditionally been divided into competition over mates and mate choice. Currently, models of sexual selection predict that sexual traits are expressed in proportion to the condition of their bearer. In horned beetles, male contest competition is well established, but studies on female preferences are scarce. Here I present data on male mating success and condition dependence of courtship rate in three species of horn-dimorphic dung beetles, Onthophagus taurus, Onthophagus binodis, and Onthophagus australis. I found that in the absence of male contest competition, mating success of O. taurus and O. australis was unrelated to their horn length and body size, whereas in O. binodis horn size had a negative effect but body size had a positive effect on male mating success. Overall, in O. binodis major morph males had greater mating success than minor morph males. In all three species male mating success was affected by courtship rate, and the courtship rate was condition dependent such that when males were manipulated to be in poor condition they had lower courtship rates than males that were manipulated to be in good condition. My findings provide new insight into the mating systems of horned dung beetles and support an important assumption in indicator models of sexual selection.
Key words: condition dependence, horn dimorphism, horned dung beetles, logistic regression, mating success, Onthophagus, selection gradient, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sexual selection may be defined as fitness differences that arise from variation in traits that affect reproductive success (Andersson, 1994
;
Endler, 1986). Traditionally,
sexual selection has been divided into competition over mates and mate choice,
with males normally being the competing sex and females being the choosing sex
(Andersson, 1994;
Andersson and Iwasa, 1996;
Darwin, 1871;
Emlen and Oring, 1977).
However, these two mechanisms are closely related, and it is likely that in
most species they both contribute to evolution through sexual selection. It
has been shown that male traits that are traditionally thought to be used as
armaments in male contest competition are in fact often targets of female
choice (Berglund et al., 1996;
Tomkins and Simmons, 1998). It
may also be that male contest cmpetition facilitates female choice by making
the differences between males more pronounced, thus increasing the ease and
accuracy of female choice (Candolin,
1999a,
2000).
Currently favored sexual selection models predict that, because sexual
traits are costly, they should covary positively with condition
(Andersson, 1994;
Andersson and Iwasa, 1996;
Johnstone, 1995;
Rowe and Houle, 1996). The
prediction of condition dependence of sexual traits is particularly critical
for viability indicator or good genes models of sexual selection because
condition dependence is a prerequisite for the use of sexual traits as honest
indicators of quality (Andersson,
1986; Grafen,
1990; Kokko, 1998;
Zahavi, 1977; for reviews, see
Andersson, 1994;
Andersson and Iwasa, 1996;
Johnstone, 1995). Moreover,
condition-dependent expression of sexual traits and signals has recently
gained increasing importance in the theory of good genes sexual selection
(Andersson, 1986;
Rowe and Houle, 1996); because
it is expected that there is little genetic variance in traits that are
closely related to fitness (Charlesworth,
1987; Falconer,
1989; (Roff,
1997), it seems evident that there is little potential for female
choice to result in genetic benefits. Among the lines of Andersson
(1986), Rowe and Houle
(1996) suggested that this
"lek paradox" (Borgia,
1979; Kirkpatrick,
1982; Taylor and Williams,
1982) will be resolved if two assumptions are met: there is
genetic variance in condition itself, and traits exhibit positive condition
dependence. For this reason, condition-dependent expression of sexual traits
has an important role in the theory of sexual selection.
Empirical evidence suggesting that sexual traits and displays are expressed
in proportion to condition is accumulating (David et al.,
1998,
2000;
Emlen, 1994;
Frischknecht, 1993;
Griffith et al., 1999;
Hunt and Simmons, 1997;
Keyser and Hill, 1999;
Kotiaho, 2000;
Kotiaho et al., 2001;
Mappes et al., 1996;
Wilkinson and Taper, 1999). It
is likely that most traits show some degree of condition dependence. However,
there is some evidence that the condition-dependent expression of sexual
traits is not always so clear cut. For example, in the three-spined
sticklebacks, the red breeding coloration of the males plays an important role
in sexual selection (Candolin,
1999a,
2000) and is generally
positively condition dependent
(Frischknecht, 1993;
Milinski and Bakker, 1990).
However, experiments show that, not only males in good condition, but also
males manipulated to be in poor condition, show increased red coloration
(Candolin, 1999b).
We need more experimental studies on condition dependence to better
understand the dynamics of the expression and condition of sexual traits.
Direct manipulation of condition is important because quantifying condition
for correlational studies is an almost impossible task. This is because
condition is a somewhat abstract concept and, as yet, we do not really know
what constitutes a good empirical measure of condition
(Kotiaho, 1999). As far as
sexual selection models are concerned, the condition should be seen as an
internal state of an individual reflecting the overall pool of resources
available for allocation in different traits, and thus condition should
account for a large proportion of individual fitness
(Rowe and Houle, 1996).
My aim in this study was twofold. First, my objective was to determine if,
in the absence of male contest competition, male mating success varies with
male horn length, body size, or courtship rate in three species of horned dung
beetles: Onthophagus taurus, Onthophagus binodis, and Onthophagus
australis. I used three species in order to make more general conclusions
about the role of measured characters for male mating success in horned
beetles. Male contest competition in horned beetles has been extensively
studied, and it has been repeatedly concluded that horns function as armaments
in male-male combat (Eberhard,
1987; Emlen, 1997;
Moczek and Emlen, 2000;
Rasmussen, 1994;
Siva-Jothy, 1987). However,
studies reporting data relating to the role of these elaborate structures for
male mating success in the absence of male contest competition are scarce. My
second objective was to experimentally determine if courtship rate of males in
these three species show condition dependence. I did this by directly
manipulating male condition by altering food intake. By manipulating the food
intake, I was able to alter the pool of resources available for allocation to
different traits and thus change the condition of individuals.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study organisms
Individuals of O. australis were collected from a field population in Canberra, Australian Capital Territory, and transported to the laboratory in Perth, Western Australia, where all experiments were conducted. Individuals of O. binodis were laboratory-reared F1 offspring of females that were collected from a field population in Walpole, southwestern Western Australia. Individuals of O. taurus were field-collected adults also originating from Walpole.
O. australis and O. taurus have head horns, and O.
binodis has pronotal horns. O. taurus and O. binodis
males are dimorphic in their horn expression; "minor" males
express only rudimentary horns, whereas "major" males express
large, well-developed horns (Hunt et al.,
1999; Kotiaho and Tomkins,
2001; Simmons et al.,
1999). Dimorphism in O. australis males has not been
previously analyzed, but an analysis of individuals used in this study
revealed that O. australis males also exhibit horn dimorphism: The
relationship between natural log-transformed pronotum width and horn length
was nonlinear (t test for the second-order polynomial in quadratic
regression; t44 = -8.07, p < .001), and the
best fitting switch point occurred at a pronotum width of 5.7 mm
(R2 = .924). At this point the dimorphism was best
characterized by no change in linear slope (ß2 = 0.15 ±
0.63; t44 = 0.24, p = .812) but by a
discontinuous distribution of horn lengths (ß3 = 1.13 ±
0.21; t44 = 5.31, p < .001; for methods, see
Eberhard and Gutiérrez,
1991; Kotiaho and Tomkins,
2001). Females of these species have no horns. In all species I
used pronotum width as a size measure.
Courtship in all of the three species is similar. Males court by tapping the female's back with their head and forelegs in bouts lasting a few seconds. Courtship rate is calculated as number of such courtship bouts per unit time.
Condition dependence and mating success
Before the experiments, I measured the initial body mass (to the nearest
0.01 mg), horn length, pronotum width, and courtship rate of males. Horn
length and pronotum width were measured under binocular microscope to the
nearest 0.05 mm. Courtship rate of the males was observed in artificial dung
beetle tunnels. Tunnels were constructed from 60-mm long clear plastic vials
measuring 13 mm in width and 36 mm in depth. Vials were half-filled with
plaster of Paris to create 60-mm long, 13-mm wide, and 17-mm high dung beetle
tunnels. The plaster of Paris floors of the tunnels were smeared with dung and
dried. Before the trials the floors were moistened with water. One randomly
selected female and a male were introduced into a tunnel, and the courtship
rate of the males was observed constantly until a mating occurred or up to 30
min (O. australis) or 60 min (O. binodis and O.
taurus). The maximum observation time in O. australis was
shorter because the initial courtship rate of O. australis males was
much higher than that of O. binodis and O. taurus males (see
Table 1). Because some males
mated during the observations, the time for courtship observations varies.
Therefore, I used courtship rate per minute rather than total number of
courtship bouts in the analysis. All of the observations were conducted in
controlled temperature room in constant temperature and humidity under red
lighting.
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After initial measurements males were divided between two food ration treatments, assuring that morphological measures and initial courtship rates did not differ between the groups. After measurements beetles were housed individually in small plastic containers (7 x 7 x 5 cm) two-thirds filled with moist sand. High food ration males were provided with a constant supply of fresh cow dung, and low food ration males were provided no dung but only moist sand. After 5 (O. taurus) or 10 (O. australis and O. binodis) days on the food manipulation, I repeated the measurements and observations as described above. The duration of the feeding treatment for O. taurus was 5 days because from previous experience with this species I knew that feeding treatment of 5 days is enough to affect male condition. This information was not available for O. australis or O. binodis. Because O. australis and O. binodis are approximately twice the body mass of O. taurus, and because I wanted to be sure that the feeding treatment is effective in changing the condition of the males, I treated males of these species for 10 days.
With the data from the above courtship rate observations, I was able to analyze the effects of horn length, body size, and courtship rate on mating success of the males. In O. binodis there were few matings during the above observations (referred to as experiment 1), and thus I conducted another experiment (experiment 2) to determine the effects of courtship rate on male mating success with a set of 211 virgin labreared F1 males and females. The protocol for the experiment 2 followed that for experiment 1, with the exception that there was no feeding treatment (all males had a constant supply of fresh dung) and that horn length or pronotum width were not individually known. Only the morph (minor or major) of the male was known.
Statistical analysis
I analyzed the effect of food ration treatment on the change in courtship
rate and body mass with repeated-measures ANOVAs. The probability of mating
was tested with logistic regressions using analysis of deviance. I included in
the logistic regressions analyses only those individuals who engaged in
courtship during the trial because without courtship there is no possibility
for mating to occur. In some instances the data was natural log-transformed to
meet the parametric assumptions. If the assumptions could not be met,
nonparametric alternatives were used. The sample sizes in the tests are based
on 29 individuals of O. australis, 30 individuals of O.
binodis in the first, and 211 in the second experiment, and 80
individuals of O. taurus.
To quantify the sexual selection acting on courtship rate, horn length, and
pronotum width simultaneously, one needs to use multivariate analyses.
Multiple linear regression methods (Arnold
and Wade, 1984; Lande and
Arnold, 1983) are not suitable for dependent fitness variables
that are non-normally distributed, as in my case the mating success is 0 or 1.
For this reason, I used multivariate logistic regression analysis and then
used a transformation on the logistic regression co-efficients that is
specifically developed for such purpose
(Janzen and Stern, 1998; see
also Hardy and Field, 1998).
The resulting values can be interpreted the same way as can selection
gradients obtained from traditional regression analyses
(Arnold and Wade, 1984;
Brodie et al., 1995;
Janzen and Stern, 1998;
Lande and Arnold, 1983). To
compare results from this study with results of an earlier study on O.
taurus (Kotiaho et al.,
2001), I also calculated the selection intensity (i) and
its 95% confidence interval (CI) for courtship rate in all three species
(Arnold and Wade, 1984;
Endler, 1986).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Body mass
Overall, in all three species males lost mass (repeated-measures ANOVA; O. australis: F1,27 = 158.15, p < .001; O. binodis: F1,28 = 159.97, p < .001; O. taurus: F1,78 = 24.69, p < .001), but nevertheless there was an effect of the food treatment such that males on high food ration lost less mass than males on low food ration (repeated-measures ANOVA, interaction term; O. australis: F1,27 = 7.78, p = .010; O. binodis: F1,28 = 42.18, p < .001; O. taurus: F1,78 = 160.37, p < .001; Figure 1).
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Condition dependence of courtship rate
I analyzed the condition dependence of male courtship rate with
repeated-measures ANOVA having food ration as a factor and pronotum width as a
covariate. In all three species the three-way interaction between food ration,
pronotum width, and repeated measure was not significant (O.
australis: F1,25 = 0.26, p = .613; O.
binodis: F1,26 = 1.73, p = .200; O.
taurus: F1,76 = 0.99, p = .323) and was left
out from the final analysis. Overall, in all species males increased their
courtship rate (repeated-measures ANOVA; O. australis:
F1,27 = 26.63, p < .001; O. binodis:
F1,28 = 13.50, p = .001; O. taurus:
F1,78 = 18.62, p < .001), but males on the
high food ration increased their courtship rate more than males on low food
ration, as indicated by the significant interaction between food treatment and
the repeated measure (repeated-measures ANOVA; O. australis:
F1,27 = 5.49, p = .027; O. binodis:
F1,28 = 6.89, p = .014; O. taurus:
F1,78 = 6.15, p = .015;
Figure 2). Pronotum width had
no influence on the change in courtship rate (repeated-measures ANOVA,
interaction term; O. australis: F1,26 = 1.10,
p = .304; O. binodis: F1,27 = 0.03,
p = .861; O. taurus: F1,77 = 0.44,
p = .507). There was a positive correlation between initial courtship
rate and courtship rate after food manipulation in O. australis
(rs29 = .39, p = .035) and in O. taurus
(rs80 = .28, p = .013), but not in O.
binodis (rs30 = 0.02, p = .906). In all of the
species, neither initial courtship rates nor after manipulation were
correlated with pronotum width or horn length
(Table 1).
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Sexual selection on courtship rate, horn length, and pronotum
width
In O. australis and O. taurus, male mating success was
tested twice: first when initial courtship rate was observed and second after
the food manipulations (Tables
2 and
3). The two tests produced
similar results: In both species courtship rate was a significant determinant
of male mating success (Figure
3), but horn length and pronotum width were not important (Tables
2 and
3).
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In O. binodis the mating success of males was tested three times with two different experiments. The first experiment used the same methodology as above, and mating success was tested twice: first time when initial courtship rate was observed and second after the food manipulations. During the initial courtship-rate observations, the mean courtship rate of males was low (0.07 bouts per min), and there was only one mating. For this reason, testing for male mating success was not conducted. After food manipulation the courtship rate increased, but there were still only four matings. Nevertheless, I tested the probability of mating after food manipulation with logistic regression. The overall logistic regression model including courtship rate, horn length, and pronotum width was significant (Table 4). Courtship rate significantly improved the model in which horn length and pronotum width were in the model alone. However, when courtship rate was already in the model, both horn length and pronotum width improved the model significantly (Table 4). I analyzed the second experiment on O. binodis male mating success with a logistic regression with male morph (minor or major) as a categorical covariate and courtship rate as continuous covariate. Courtship rate had a strong positive effect on the probability of mating (Figure 3 and Table 4), but male morph also had an effect such that major males had greater probability of mating than minor males (Table 4). In those males that engaged in courtship (117 out of 211), major males had marginally higher courtship rates than minor males (independent samples t test, t63.6 = -2.06, n1 = 73, n2 = 44, p = .043).
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I calculated the selection gradients for courtship rate, horn length, and
pronotum width for each species from the second courtship observation using
the methodology of Janzen and Stern
(1998). The selection
gradients for courtship rate in all species were moderate but statistically
significant (Table 5). For horn
length and for pronotum width, the gradient was not significantly different
from zero in O. australis and O. taurus, but in O.
binodis the gradient was negative for horn length but positive for
pronotum width (Table 5). The
statistical significance of the selection gradients can be addressed using the
results from the logistic regression (Tables
2,3,4).
In Figure 3 I have depicted the
logistic regression selection surface for courtship rate. In this analysis I
used the second courtship observations for O. australis and O.
taurus, and for O. binodis I used the observations from the
second experiment. Selection differentials show directional selection for
greater courtship rate in all species, and the intensity of this selection
(standardized univariate selection differential) was moderately high and
significantly different from zero for all three species (intensity of
directional selection [i] with 95% confidence intervals and
significance test; O. australis: i = 0.976, CI =
0.265-1.688; t37 = 2.78, n1 = 29,
n2 = 10, p = .009; O. binodis:
i = 0.894, CI = 0.516-1.273; t80.3 = 4.70,
n1 = 211, n2 = 62, p <
.001; O. taurus: i = 1.191, CI = 0.499-1.883;
t22.7 = 3.57, n1 = 80,
n2 = 19, p = .002).
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), their standard errors,
significance levels, and estimated average selection gradients (ß) for
courtship rate, horn length, and body size in O. australis and O.
binodis in the first experiment, O. binodis in the second
experiment, and O. taurus
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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It has been well documented that horns in several beetle species function as armaments that are used in combats with conspecific males over access to females (Eberhard, 1979
,
1982,
1987;
Emlen, 1997;
Moczek and Emlen, 2000;
Otronen, 1988;
Palmer, 1978;
Rasmussen, 1994;
Siva-Jothy, 1987). Males often
show bimodal variation in their horn morphology
(Cook, 1987;
Emlen, 1994;
Kotiaho and Tomkins, 2001;
Simmons et al., 1999), and
this variation has been shown to be associated with various alternative
reproductive strategies: Minor males have been described to adopt sneaking
roles trying to avoid confrontations with competitively superior major males
(Emlen, 1997;
Moczek and Emlen, 2000), while
major males have been described to guard females
(Cook, 1990;
Emlen, 1997) and provide
females with paternal care (Cook,
1988; Hunt and Simmons,
1998,
2000). Generally, horn
morphologies have been examined from the male contest competition perspective,
and the few scattered studies or descriptive observations on male mating
success suggests that females do not reject courting males but engage in
mating regardless of male horn morphology
(Brown et al., 1985;
Emlen, 1997;
Moczek and Emlen, 2000). Here I presented data on mating success of three species of horned dung beetles in the absence of male contest competition. It is clear that in O. australis and in O. taurus, male horn morphology was not related to males mating success. However, in O. binodis male mating success was related to their horn morphology: major males had higher mating success than minor males. Having said this, it seems that body size is under positive sexual selection, whereas horn size is under negative sexual selection.
There are some important differences in the reproductive behavior of O.
binodis and O. taurus that may explain the above difference in
male mating success with respect to the size of the male. When O.
binodis females are paired with large males, they produce more offspring
than females paired with small males
(Cook, 1988), but in O.
taurus such a difference does not exist (Hunt and Simmons,
1998,
2000). In O.
australis these aspects have not been studied. It may be that in O.
binodis the benefit in terms of greater number of offspring from mating
with large males (Cook, 1988)
is large enough to result in evolution of female preference for larger males.
In contrast, O. taurus females do not benefit from mating with larger
males by having more offspring but rather by having larger offspring (Hunt and
Simmons, 1998,
2000;
Hunt et al., 2002). Currently
it is not entirely clear how female O. taurus might benefit from
having large offspring, although it may be that major males have higher
reproductive success than minor males: competition experiments on different
morph frequencies suggest that in most morph frequencies, major males
fertilize the majority of eggs produced (Hunt J and Simmons LW, unpublished
data). Yet, if the fitness benefit of mating with a large male is not
substantial enough in comparison to mating with a small male, female
preference for male size may not have evolved in O. taurus. The
result that there was positive selection on body size but negative selection
on horn size in O. binodis was surprising. To determine the reason
for these differential selection pressures requires further in-depth
examination.
Courtship rate consistently had a strong positive effect on male mating
success across all three species. In earlier studies with O. taurus
we found that male courtship rate is heritable
(Kotiaho et al., 2001),
suggesting that females may benefit from their preference through increased
mating success of their male offspring. However, whether increased mating
success results from female preference is not clear. There is a possibility
that the same result may be found if resisting matings is costly for females
and to reduce this cost females accept matings from persistently courting
males more easily than from males that court with low frequency. If this is
the case, then differential mating success does not necessarily result from
females seeking fitness benefits but rather from females seeking to reduce the
fitness costs. There is some evidence from O. taurus that male
harassment may be costly for the females in terms of reducing the number of
offspring produced (Hunt and Simmons,
1998; but see Hunt and
Simmons, 2000). The duration of mating in these three species is
less than 10 min, and after mating males do not immediately engage into
further courtship (Kotiaho, personal observation). How long males refrain from
harassing females with their courtship is not known. If the time spent mating
with a male is less than the time that would be spent resisting male mating,
and if there are few other costs of mating, it is likely that females will
mate with highly courting males with little resistance. To determine whether
higher mating success resulting from high courtship rates is female preference
in search for fitness benefits or female avoidance of harassment in search of
reduced costs is complicated and cannot be answered with the current data.
However, it is important to note that whatever the proximate mechanism for the
higher mating success of males with high courtship rates is, the ultimate
benefit of mating with such males remains the same. In other words, because
courtship rate is heritable (Kotiaho et
al., 2001), females preferring males of high courtship rate would
benefit from having sons with higher mating success. Similarly, females that
do not choose but simply allow high courtship males to mate with them benefit
by having sons with higher mating success.
In this study I used field-collected adult O. taurus females that
are likely to be mated, and the selection intensity for higher courtship rate
was 1.191 with a lower 95% CI of 0.499. In an earlier study with the same
methodology but using virgin females, the selection intensity for higher
courtship rates was only 0.331 with an upper 95% CI of 0.491
(Kotiaho et al., 2001). As the
95% CIs do not overlap, this difference may be considered to be statistically
significant. This difference suggests that virgin females mate with less
rigorous mating rules than already mated females do. Unfortunately, these data
are not able to discriminate between the above-mentioned two mechanisms of
differential mating success of high courtship rate males. The selection
intensity may increase because females increase their mate choice criteria
after first mating or because females do not need another mating and begin to
resist matings to reduce the possible costs of mating. However, because virgin
females also discriminate against males based on their courtship rate
(Kotiaho et al., 2001), it
seems that mate choice may be the mechanism that is at least partly driving
the observed patterns of male mating success.
A critical prediction in all currently favored sexual selection models, and
in particular in indicator or good genes models, is that, because sexual
traits are costly, they should covary positively with condition (Andersson,
1986,
1994;
Andersson and Iwasa, 1996;
Johnstone, 1995;
Rowe and Houle, 1996). Along
the lines of Andersson (1986),
Rowe and Houle (1996)
suggested that the "lek paradox"
(Borgia, 1979;
Kirkpatrick, 1982;
Kirkpatrick and Ryan, 1991;
Taylor and Williams, 1982)
will be resolved if two assumptions are met: Traits exhibit positive condition
dependence and there is genetic variance in condition itself
(Andersson, 1986;
Rowe and Houle, 1996). In this
study I found that the courtship rate of the males in all three species
responded to the manipulation of male phenotypic condition. In all species,
males that were manipulated to have abundant resources had higher courtship
rate than males manipulated to have limited resources. As resources are
generally expected to be in short supply, experimentally constraining males
from resource intake is likely to manifest a trade-off between expenditure in
the displays and expenditure in other life-history traits, something which is
impossible to unravel with correlational studies. Thus, it may be that most
behavioral sexual traits will respond to an experimental manipulation of
available resources because displays typically require some expenditure of
resources (Kotiaho, 2001).
In conclusion, in the absence of male contest competition, male mating success in three species of dung beetles was dependent on their courtship rate. In O. binodis larger males had higher mating success than smaller males, but horn length had a negative effect on male mating success. In O. taurus and in O. australis male mating success was independent of body size and horn length. In all three species manipulation of available resources had an effect on courtship rate, indicating that courtship rate is positively condition dependent.
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ACKNOWLEDGEMENTS |
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I thank John Hunt, Esa Koskela, Silja Parri, Leigh Simmons, and Joseph Tomkins for comments on the manuscript and discussions and John Hunt for discussion of his viewpoints and unpublished results. This work was funded by the Academy of Finland.
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