Behavioral Ecology Vol. 13 No. 3: 353-358
© 2002 International Society for Behavioral Ecology
The costs of copulating in the dung fly Sepsis cynipsea
Zoologisches Museum, Universität Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
Address correspondence to W.U. Blanckenhorn. E-mail: wolfman{at}zoolmus.unizh.ch .
Received 23 February 2001; revised 16 July 2001; accepted 30 July 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Finding, assessing, rejecting, and copulating with a mate is assumed to carry fitness costs, particularly for females, that have to be traded off against fitness benefits of mating such as increased fecundity, fertility, longevity, or better quality offspring. Female dung flies, Sepsis cynipsea (Diptera: Sepsidae), typically attempt to dislodge mounted males harassing them by vigorous shaking. Shaking duration has been shown to reflect both direct and indirect female choice in this species. The latter is an expression of the females' general reluctance to mate due to presumed costs of mating. We investigated the costs of copulation in the laboratory. Females were randomly assigned to one of three treatment groups and allowed to copulate either not at all, once, or twice. The males' armored genitalia injured females internally during copula. Injuries were visible as sclerotized scars in the female ovipositor, and their occurrence increased with mating frequency. Presumably due to these injuries, mated females showed higher mortality. This effect was statistically independent from additional costs of reproduction related to oviposition, as copulation also increased lifetime egg production and tended to augment oviposition rate (eggs per day), while fertility (proportion of offspring emerged) was unaffected. We thus found high mortality costs of copulating, indicating substantial sexual conflict, which helps explain female reluctance to mate in this species.
Key words: female reluctance, genitalia, internal injuries, mating behavior, mating costs, sexual conflict, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Mating is a costly activity. Over the past decades, a slow paradigm shift has occurred from regarding mating as a process of mutual benefit to one loaded with conflict (Arnqvist, 1989
; Eberhard,
1996; Gowaty and Buschhaus,
1998; Holland and Rice,
1998; Parker,
1979; Partridge and Hurst,
1998; Rice, 1996;
Rowe et al., 1994;
Thornhill and Alcock, 1983).
It is now accepted that finding, assessing, rejecting, and copulating with a
mate can carry fitness costs, particularly for females, which have to be
traded off against fitness benefits of mating such as increased fecundity,
fertility, longevity, or better quality offspring
(Andersson, 1994;
Arnqvist and Nilsson, 2000;
Chapman et al., 1998;
Johnstone and Keller, 2000).
Mating costs include increased predation due to reduced mobility or greater
visibility (Arnqvist, 1989;
Fairbairn, 1993;
Gwynne, 1989;
Hosken et al., 1994;
Magnhagen, 1991;
Moore, 1987;
Rowe, 1994;
Ward, 1986), disease
transmission (Daly, 1978;
Kaltz and Schmid, 1995), or
loss of energy or foraging time (Bailey et
al., 1993; Clutton-Brock and
Langley, 1997; Cordts and
Partridge, 1996; Watson et
al., 1998; Wilcox,
1984). Furthermore, deleterious effects of toxic accessory gland
products (Chapman et al.,
1995,
1998;
Chen, 1984), internal (i.e.,
genital: Crudgington and Siva-Jothy,
2000; Kummer,
1960; Merritt,
1989; von Helversen and von
Helversen, 1991), or external injuries (e.g., wing:
Cartar, 1992; body:
LeBoeuf and Mesnick, 1991;
Leong et al., 1993;
Michiels and Newman, 1998)
have been reported, all of which may increase mortality. The costs and
benefits of mating need to be evaluated as comprehensively as possible to
fully understand the mating system of any particular species and the evolution
of sexual conflict (Arnqvist and Nilsson,
2000; Eberhard,
1996; Johnstone and Keller,
2000; Parker,
1979). Recent evidence suggests the intriguing possibility that
males actively harm females (Crudgington
and Siva-Jothy, 2000;
Johnstone and Keller 2000;
Michiels and Newman, 1998),
using armored genitalia to increase their reproductive success (which have
been known for quite some time; Eberhard,
1985).
In many species, (presumed) mating costs can result in obvious female
reluctance to mate (Crudgington and
Siva-Jothy, 2000; Godin and
Briggs, 1996; Rowe et al.,
1994; Thornhill and Alcock,
1983). This is the case in the dung fly Sepsis cynipsea
(Diptera: Sepsidae), in which females shake vigorously, attempting to dislodge
males trying to copulate with them
(Blanckenhorn et al., 2000;
Parker,
1972a,b;
Ward, 1983,
Ward et al., 1992). Ward et
al. (1992) suggested that
females may minimize their copulation frequency to reduce the risk of internal
injury by the male's armored genitalia
(Figure 1a) because internal
injuries may cause mortality or decrease fecundity. These are the costs of
copulating. Female rejection behavior also may carry costs in terms of
increased predation risk, energy expenditure, or wing injuries inflicted by
spines on the male's forelegs (Blanckenhorn
et al., 1998; Hennig,
1949; Mühlhäuser and
Blanckenhorn, 2002; Pont,
1979). These are the costs of assessing and/or rejecting a mate
before copulation, which likely vary in space and time. The mating system of
S. cynipsea thus suggests substantial sexual conflict
(Gowaty and Buschhaus, 1998;
Holland and Rice, 1998;
Partridge and Hurst, 1998;
Rowe et al., 1994). It seems
obvious that female reluctance to mate can only evolve if the cost of avoiding
matings does not exceed the cost of copulation; otherwise females would try to
offset one cost with another (Blanckenhorn
et al., 2000). Therefore, both types of cost need to be evaluated
in the same currency (Rowe,
1994; Watson et al.,
1998).
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In this study we experimentally assessed the costs and the benefits of
copulating in S. cynipsea. We compared the mortality, fecundity, and
fertility of females mated zero, one, and two times in the laboratory. We also
screened females specifically for genital injuries in an attempt to link the
expected reproductive costs of copulation to these injuries. The costs of
avoiding and/or assessing mates were also investigated and are presented in a
companion paper (Mühlhäuser and
Blanckenhorn, 2002).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We performed two laboratory experiments, one to assess female internal injuries and another to assess the reproductive consequences of copulation frequency. The two experiments were performed separately because from preliminary work we knew that dead individuals disintegrate quickly (within 24 h) so that internal injuries are no longer possible to score reliably. We therefore deemed it necessary to experimentally assess these injuries in a standardized manner (i.e., after a predetermined time and not at the end of a female's life).
Female internal injuries as a function of copulation frequency
Females emerging over a period of 3 days from S. cynipsea
laboratory stocks originating from our field site in Fehraltorf, near
Zürich, Switzerland, were isolated within 24 h of emergence. They were
randomly assigned to one of three treatment groups and allowed to copulate
either not at all, once, or twice. As even virgins do not mate readily
(Blanckenhorn et al., 2000),
individual females aged 5-10 days were placed with three to six randomly
chosen males from the same population (to increase the likelihood of mating)
in a 50-ml glass vial containing one large grain of sugar and a miniature dish
(ca. 5 g) of recently defrosted cow dung, their oviposition medium. As soon as
copulation was initiated, all other males were removed, and after copulation
ended (which lasts about 20 min), the females were kept singly in their vial
until they were frozen for later analysis of internal injuries. When no
copulation occurred within 90 min, the same females underwent the same
procedure once again 2-3 days later. A random subset of the females that
copulated once were then subjected to the same procedure 3-5 days later so
they could copulate a second time. Females were thus in contact with males for
at most two times 90 min, during which they were under constant observation.
Females were frozen for later analysis 4-9 days after their last (i.e., first
or second) copulation. Virgins of the zero-copulation treatment were never
confronted with males and frozen 7-20 days after the first copulation of the
females in the other treatments to keep life span approximately equal across
all treatment groups. We deemed 4-7 days necessary and sufficient for female
internal injuries to heal and develop scars at the climate conditions given
below so they could later be scored (see
Crudgington and Siva-Jothy,
2000). Females that died within 4 days after copulation were
discarded because they could not be reliably scored (see above), as were
females preassigned to the copulation treatments that did not copulate at all
during two trials (see
Mühlhäuser and Blanckenhorn,
2002).
To assess internal injuries, each female was placed on a slide, in a drop of Ringer solution, under a stereo microscope. The protruding end of the ovipositor was grasped with fine tweezers and the whole reproductive tract pulled out. Using a microscope, the ovipositor was then examined for scars. All females were scored blindly (i.e., without knowledge of their copulation frequency) by the same person. We analyzed differences in the extent of internal scars (presence or absence) among the three treatment groups using stepwise (backward elimination) logistic regression with treatment as a fixed factor and female age at freezing as a covariate.
Female reproductive success as a function of copulation
frequency
For this separate experiment, three treatment groups (zero, one, and two
copulations) were generated as for the internal injury experiment. Again, care
was taken to randomize age and size among treatments (see Results). After
their last copulation, females were kept singly in their vials until their
death, in a climate chamber at 25°C, 50% relative humidity, and 14-h light
period. Females of the zero-copulation treatment were held likewise. They had
access to ad libitum sugar and a miniature dish of defrosted cow dung
twice a week for food, moisture, and oviposition. For each female, we scored
her day of death, the total number of eggs laid over her life-time (and per
week), and her fertility as the percentage of offspring emerged per week from
her eggs, at the environmental conditions given above.
For analysis, we subdivided the reproductive data for all females of all treatment groups into two time periods, the period before the date of the second copulation of the females in the two-copulation treatment group (henceforth the date of second copulation), and the period thereafter. Only the latter period was analyzed in most cases. This was done to control for systematic age differences among the treatment groups, as effects of copulation(s) on reproductive performance necessarily appear later in the females that copulated more often. All females that died before the date of second copulation were discarded, except that their mortality (dead or alive) was related to whether they had copulated once or not, using logistic regression. Females that survived this date were also discarded if they never laid any eggs (n = 14 females, 13%), as they were apparently unable to reproduce due to unknown causes and thus were uninformative with regard to the study questions.
Individual fecundity was expressed both as total eggs laid before/after the date of second copulation and eggs laid per day (i.e., mean oviposition rate: total eggs laid divided by days of life before/after the date of second copulation). Both these estimates of fecundity after the date of second copulation were compared among the three treatment groups using one-way factorial ANOVA (copulation treatment) with days of life before and after the date of second copulation, body size (head width), and fecundity before the date of second copulation as covariates. We did this to control for differences among the females in emergence date and life span, as well as to control for potential costs of reproduction relating to the period before the date of second copulation. In addition, we analyzed lifetime fecundity with total life span and head width as covariates (combining the estimates before and after the date of second copulation).
Fertility, a log[p/ (1 — p)]-transformed proportion p, was expected to decline with age due to sperm depletion or aging and was calculated per week and compared only for the females which copulated once and twice (as fertility of the virgins was necessarily zero). Fertility was regressed on week with copulation treatment as a factor and days of life before and after the date of second copulation, body size (head width), and fecundity before and after the date of second copulation as covariates. As there is no repeated-measures regression, this analysis was additionally performed using the mean fertility per week of all females of a copulation treatment, without covariates, to avoid pseudoreplication. To assess the immediate effect of the second copulation on fertility, we additionally compared only the fertility during the 7 days immediately before and after the date of second copulation, using repeated-measures ANOVA with treatment as the between-subject and week as the repeated factor, and the same covariates as above. Only females that laid eggs during both weeks were included in this analysis.
We analyzed survivorship after the date of second copulation using Cox regression (the appropriate analysis for survivorship curves) with treatment as a fixed discrete factor, and days of life before the date of second copulation, body size (head width), and fecundity as covariates. The latter tests for mortality costs of reproduction and was expressed either as mean oviposition rate or total number of eggs laid during the entire lifetime (thus combining the estimates before and after the date of second copulation). In all analyses, total eggs laid, oviposition rate, and days of life were square-root transformed to equalize variances.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Female internal injuries as a function of copulation frequency
We detected scars in the female ovipositor (Figure 1b), the occurrence of which increased with copulation frequency (Figure 2; logistic regression:
2 = 8.77, p =.012, n = 131; the effect of
age at freezing was eliminated from the final model). Only 1 of 28 virgins had
a scar (for unknown reasons), whereas 6 (of 61) females of the one-copulation
and 12 (of 42) of the two-copulation had a scar. This sample includes 37
females in the one-copulation treatment that refused a second copulation
(i.e., were not preassigned). However, the result was qualitatively the same
when only analyzing those females originally preassigned to the one copulation
treatment (2 = 6.45, p =.039, n = 94).
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Female reproductive success as a function of copulation
frequency
Copulation had an obvious and drastic immediate effect on female mortality.
Of the original 43 females preassigned to the zero-copulation treatment and
the 125 females preassigned to both copulation treatments, respectively, 8
(18.6%) and 51 (40.8%) died before the date of second copulation. Females that
copulated had a 67% greater probability of dying within a week after
copulation (logistic regression: 2 = 5.00, p =.025,
odds ratio = 1.67; positive effect of female age: 2 = 4.42,
p =.036, odds ratio = 1.09, n = 168). For the remaining
females that survived this date and laid eggs, Cox regression indicates a
further effect of copulation on survivorship after the date of second
copulation (2 = 15.67, p =.004, n = 91;
Figure 3,
Table 1): relative to virgins,
females that copulated once had a 21% (odds ratio = 1.21) and those that
copulated twice a 88% greater mortality rate (odds ratio = 1.88). (Note that
this analysis does not include the many females that copulated once and died
before the date of second copulation.) The same analysis showed (expected)
elevated mortality rates when females were older at the date of second
copulation (2 = 8.78, p =.003, odds ratio = 1.62) and
when they had higher lifetime fecundity (2 = 21.48, p
<.001, odds ratio = 1.15), but there were no effects of body size
(2 = 0.32, p =.572, odds ratio = 0.98). (Using mean
oviposition rate yielded not quite as strong, but qualitatively similar,
results, except that the effect of fecundity was no longer significant.)
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Oviposition rate (eggs per day) after the date of second copulation did not decrease with copulation frequency; if anything, oviposition rate showed a tendency to increase (F2,83 = 2.44; p =.093; Table 1). Virgins also laid eggs, though at a reduced rate (planned contrasts; zero vs. one and two copulations: t83 = 4.25, p <.001; one vs. two copulations: t83 = 1.44, p =.154; Table 1). The same analysis showed an expected positive correlation between fecundity before and after the date of second copulation (partial r =.28, p =.005), and a negative effect of age at the date of second copulation on oviposition rate (partial r = -.20, p =.030; all other covariates p >.2). Total eggs laid after the date of second copulation (i.e., residual lifetime reproductive success) increased with copulation treatment (F2,83 = 4.41; p =.015; effect of eggs laid before the date of second copulation: partial r =.22, p =.004; effect of days of life after the date of second copulation: partial r =.70, p <.001; effect of days of life before the date of second copulation: partial r = -.13, p =.066; effect of head width: partial r =.17, p =.091; Table 1). Analogous analysis of the lifetime number of eggs laid, with life span and head width as covariates, yielded qualitatively similar results: egg output increased with copulation treatment (F2,85 = 12.82; p <.001), correlated strongly with life span (partial r =.46, p <.001), and also correlated with head width (partial r =.28, p =.012). The mean ± SE lifetime egg output of all females that laid eggs, including those that died before the date of second copulation, as a function of copulation treatment was 103.84 ± 14.11 (n = 29) for the zero-copulation, 153.40 ± 18.51 (n = 49) for the one-copulation, and 151.68 ± 19.53 (n = 30) for the two-copulation treatment (F2,104 = 3.34; p =.039). This estimate includes the probability of dying after the first copulation, by randomly allocating those females that died after the first copulation to the one or two copulation treatments in proportion to the treatment frequency.
We expected a second copulation to enhance fertility, counteracting sperm
depletion (Arnqvist and Nilsson,
2000). This should have resulted in a steeper decline in fertility
with time in the one- compared to the two-copulation treatment (i.e., an
interaction of treatment with week in our multiple regression). Fertility
obviously declined with time (age) due to sperm depletion (raw data:
F1,238 = 138.56; mean data: F1,12 =
158.3; both p <.001), but there was no interaction of treatment
and time (raw data: F1,238 = 0.18; p =.670; mean
data: F1,12 = 0.95; p =.350;
Figure 4). However, there was
an effect of copulation (raw data: F1,238 = 8.28;
p =.004; mean data: F1,12 = 6.24; p
=.028), as females that copulated twice were more fertile to begin with,
perhaps by chance (Figure 4).
Comparing only the weeks immediately before and after the date of second
copulation showed no effects of copulation on fertility whatsoever (effect of
treatment: F1,42 = 2.52; p =.122; effect of time:
F1,42 = 1.93; p =.172; interaction:
F1,42 = 0.30; p =.589; all covariates p
>.2; Table 1).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Our study revealed drastic costs of mating in S. cynipsea, both in terms of increased mortality immediately after the first copulation and decreased survivorship given a second copulation. These may relate partly to standard costs of reproduction, as we also found increases in fecundity with copulation frequency. Physiological substances transferred by the male during copulation that stimulate oviposition (and sometimes also increase mortality) may be responsible (e.g., Drosophila spp.: Baumann, 1974
; Chapman et al.,
1995,
1998;
Chen, 1984). However, there
was an additional, statistically independent effect of copulation on
mortality, which we believe is linked to the male's armored genitalia injuring
the females. The sclerotized scars in the female ovipositor
(Figure 1b) appear to have been
caused by the spines of the male's copulating organ, the aedeagus
(Figure 1a). Of course, this
connection can only be inferred by correlation, as done here and in a recent
study by Crudgington and Siva-Jothy
(2000). Alternatively,
mortality could be a side effect of male substances that reduce female
receptivity (Chapman et al.,
1995,
1998), but such substances
remain to be identified in this species. These mortality costs of copulating
are sufficient to explain the strong female reluctance to mate in S.
cynipsea (Blanckenhorn et al.,
2000; Ward et al.,
1992).
We do not know the precise function of the male's armored genitalia. They
may function to remove sperm from previous males (e.g., damselfly:
Waage, 1979) or to inject
accessory gland material (e.g., sheep blowfly:
Merritt, 1989), but to date we
have no evidence for either phenomenon in S. cynipsea. A possible
general function of thorns and spines is to lock the male's genitals within
the female tract, making it difficult, if not impossible, for her to eject him
(Eberhard, 1985). Sepsis
cynipsea males have to twist about 180° to disengage from copula
(Parker, 1972a). In our
laboratory cultures, we have repeatedly (but rarely) observed dead males
permanently attached to the female's abdomen. This suggests copulation is also
costly for males, but additionally that females are unable to disengage from
copula without the male's assistance. Sepsis cynipsea is thus another
case of a growing number of species showing obvious sexual conflict in genital
morphology, reproductive physiology, or mating behavior
(Chapman et al., 1998;
Gowaty and Buschhaus, 1998;
Holland and Rice, 1998;
Partridge and Hurst, 1998;
Rowe et al., 1994).
How can a male gain from actively harming his mate? Three related arguments
have been put forward (Crudgington and
Siva-Jothy, 2000; Johnstone
and Keller, 2000). By making mating costly and females reluctant
to mate again, successful males (1) indirectly reduce the risk of sperm
competition and thus increase their relative share of paternity, and (2) may
indirectly force females to augment oviposition rates because of the imminent
threat of her death soon after copulation (provided, of course, the female
survives copulation; Polak and Starmer,
1998). (3) Males may also stimulate female ovipoistion and reduce
their recipitivity directly using physiological accessory gland stimulants
(Chapman et al., 1998; see
below). In the first two cases, the male's strategy of producing possibly
lethal injuries is the necessary selection pressure to modify female behavior;
in the third case female mortality may just be a side effect. Johnstone and
Keller (2000) have recently
shown theoretically that such spiteful male behavior can evolve if males
inflict strongly accelerating costs on females that remate. This might be the
case here (see Figure 2), but
S. cynipsea females typically copulate too rarely to test this idea
quantitatively. Nevertheless, females can apparently avoid internal injuries
during copulation, as a majority of them did not show any. Also, the wounds
inflicted can effectively heal, although healing will likely carry a cost.
Aside from these very general counteradaptations, S. cynipsea females
at this point may be able to do little more than shake off males to avoid
superfluous matings (Blanckenhorn et al.,
2000; Parker,
1972a,b;
Ward et al., 1992), but by
doing so they incur other potential costs
(Mühlhäuser and Blanckenhorn,
2002).
Although our study demonstrated costs of mating in terms of survivorship,
there were no such costs in terms of fecundity or fertility. For example,
genital injuries may cause oviposition problems and thus reduce fecundity. On
the other hand, mating multiply in many species confers benefits in terms of
increased fecundity or fertility (Arnqvist
and Nilsson, 2000). This may be simply because more sperm allows
fertilization of more eggs, but also because male accessory substances may
increase female oviposition rate (e.g., Chapman et al.,
1995,
1998). Whether male accessory
substances are transferred during copula and effective in S. cynipsea
remains to be demonstrated. Our study revealed increased fecundity with
copulation frequency, but no benefits in terms of fertility. As mentioned
above, females might increase their reproductive effort because of the
elevated mortality risk after copulation, an effect demonstrated in another
fly (Polak and Starmer,
1998).
Because mating confers both costs and benefits, an optimal copulation
frequency likely exists for a given species or individual
(Arnqvist and Nilsson, 2000),
but this will most certainly be different for males and females
(Andersson, 1994;
Bateman, 1948; Darwin, 1871),
generating the mating conflict apparent in this and many other species.
Whereas males are generally expected to maximize their number of matings
(Andersson, 1994;
Bateman, 1948), females need at
least one copulation, but perhaps few more. Predicting the optimal copulation
frequency for females involves assessing and trading off the costs and
benefits of copulating (Arnqvist and
Nilsson, 2000). Here we found a decrease in survivorship after the
date of second copulation but at the same time an increase in oviposition
rate, resulting in overall increased lifetime fecundity
(Table 1). However, when
accounting for the large increase in the probability of female death after the
first copulation, the latter was entirely caused by the reduced fecundity of
virgins. (We were surprised to find virgins reproducing at all; apparently
they cannot detect their virginity, halt egg production, or resorb
unfertilized eggs.) Calculating trade-offs is further complicated because the
costs of rejecting and assessing a mate also have to be included
(Blanckenhorn et al., 2000;
Mühlhäuser and Blanckenhorn,
2002), and all these costs and benefits are difficult to estimate
in the same fitness currency (such as the probability of death or lifetime
reproductive success). Qualitatively at least, the costs of copulating
documented in this study are more obvious than the costs of mating (i.e.,
shaking) behavior (see
Mühlhäuser and Blanckenhorn,
2002) and help explain female reluctance to mate in S.
cynipsea and perhaps many other species
(Blanckenhorn et al., 2000;
Crudgington and Siva-Jothy,
2000; Rowe et al.,
1994; Ward et al.,
1992).
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ACKNOWLEDGEMENTS |
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We thank the Swiss National Science Foundation for funding and A. Bourke, L. Rowe, and an anonymous referee for comments.
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