Behavioral Ecology Vol. 13 No. 3: 359-365
© 2002 International Society for Behavioral Ecology
The costs of avoiding matings 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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Mating is generally assumed to carry costs, particularly for females, which have to be traded off against each other and against the fitness benefits of mating. To understand any particular mating system and the evolution of sexual conflict, these costs have to be evaluated. Female dung flies, Sepsis cynipsea (Diptera: Sepsidae), typically attempt to dislodge mounted males by vigorous shaking. Such female reluctance to mate can only evolve if the cost of avoiding matings does not exceed the cost of copulation. We investigated female precopulatory costs of assessing and rejecting males in terms of increased predation, wing injuries, and (indirectly) energetics, all ultimately affecting mortality, and compared them to the costs of copulation assessed in this and a companion study. Females housed with a male had lower survivorship than females housed with another female. This was largely due to the costs of copulation rather than presumed energetic costs of avoiding males, which were minor. Male harassment augmented female wing injuries, which accumulate with age in the field and laboratory, but in laboratory experiments using one common predator, wing injuries did not increase the susceptibility of S. cynipsea to predation, nor did their mating behavior per se. Instead, predation was highest and survivorship lowest in all-male groups, probably because males are more active in search of females and harass each other. Overall, the precopulatory costs of mate assessment and rejection were low relative to the costs of copulating, explaining female reluctance behavior in this and possibly other species.
Key words: female choice, female reluctance, mating behavior, mating costs, predation, sexual conflict, wing injury.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Mating is generally assumed to be costly, both for males (e.g., Clutton-Brock and Langley, 1997
; Kotiaho et al.,
1998) and particularly for females
(Andersson, 1994;
Johnstone and Keller, 2000).
These mating costs have to be traded off against the fitness benefits of
mating such as increased fecundity, fertility, longevity, or better quality
offspring (Arnqvist and Nilsson,
2000). Typical examples of mating costs include increased
predation due to reduced mobility or greater visibility
(Gwynne, 1989;
Magnhagen, 1991;
Rowe, 1994), disease
transmission (Daly, 1978;
Kaltz and Schmid, 1995), or
loss of energy or foraging time
(Clutton-Brock and Langley,
1997; Watson et al.,
1998; Wilcox,
1984). Furthermore, deleterious effects of toxic accessory gland
products (Chapman et al.,
1998), internal (i.e., genital:
Blanckenhorn et al., 2002;
Crudgington and Siva-Jothy,
2000; Merritt,
1989), or external injuries (e.g., wing:
Leong et al., 1993; body:
Michiels and Newman, 1998;
LeBoeuf and Mesnick, 1991)
have been reported, which may increase mortality.
The nature of these mating costs varies considerably with the mating
system. All females face potential costs of copulating with a male. In mating
systems dominated by male—male competition and which are often
characterized by male-biased sexual size dimorphism
(Andersson, 1994; e.g.,
Parker and Simmons, 1994),
females may have few if any behavioral means to choose or reject a male
(however cryptic [i.e., post-copulatory] choice may occur;
Ward, 2000). In this situation
the cost of mating for the female is essentially the cost of a (forced)
copulation. In the perfect female choice situation (such as a lek; e.g.,
Höglund and Alatalo,
1995), females face a further basic cost of finding and assessing
a male. In mating systems characterized by male scramble competition, where
males willing to mate typically harass females
(Andersson, 1994; e.g.,
Crean and Gilburn, 1998;
Rowe et al., 1994), females
additionally face a cost of rejecting unsuitable mates. The latter two are the
costs females pay for being choosy. To fully understand the mating system of
any particular species and the evolution of sexual cooperation and conflict in
general, the costs and benefits of mating need to be evaluated as
comprehensively as possible (Andersson,
1994; Arnqvist and Nilsson,
2000; Eberhard,
1996; Holland and Rice,
1998; Johnstone and Keller,
2000).
In principle, the precopulatory costs of finding, assessing, and rejecting
males can be separated from the costs of copulating, as they incur before
copulation. But separating precopulatory costs from each other can be
difficult when males scramble for access to females. This is, for example, the
case in the dung fly Sepsis cynipsea (Diptera: Sepsidae), where
females shake vigorously in attempts to dislodge males trying to copulate with
them (Parker,
1972a,b;
Ward, 1983,
Ward et al., 1992).
Blanckenhorn et al. (2000)
found that shaking duration in this species reflects both direct and indirect
female choice (i.e., assessment as well as rejection of males). The latter is
an expression of a female's general reluctance to mate with any, as opposed to
a nonpreferred, male due to presumed costs of mating (the female reluctance
hypothesis: Parker, 1979;
Thornhill and Alcock, 1983),
which is also common in other species
(Arnqvist, 1989;
Rowe et al., 1994), including
the related Sciomyzoid flies (e.g., Crean
and Gilburn; 1998; Weall and
Gilburn, 2001). It seems clear 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.
Blanckenhorn et al. (2002)
evaluated the costs and benefits of copulation, and Blanckenhorn et al.
(1998,
1999,
2000) assessed the mechanisms
and benefits of female choice for large male size in S. cynipsea. In
a series of laboratory experiments, we investigated costs for the female of
assessing and/or rejecting males and related them to the costs of copulating.
We considered costs in terms of increased predation risk, wing injuries
inflicted by spines on the male's forelegs
(Blanckenhorn et al., 1998;
Hennig, 1949;
Pont, 1979), and (indirectly)
energy expenditure, all of which should ultimately affect mortality. To assess
the importance of wing injuries in nature, we supplemented these experiments
with data on the extent of wing injuries of males and females in the
field.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study animal
On hot summer days, large numbers of S. cynipsea males wait on and around fresh cow pats for females coming to lay eggs (Parker, 1972a
). Operational
sex ratios are typically highly male biased
(Blanckenhorn et al., 1999;
Parker,
1972a,b).
Males scramble to secure an arriving female by clasping her wing base with
their armored forelegs (see Blanckenhorn et
al., 1998: Figure
1), and harassment is common. Females respond with characteristic
shaking behavior to dislocate a male, indicating reluctance to mate and some
sort of male assessment (Blanckenhorn et
al., 2000). Once a female stops shaking, males guard her during
oviposition and subsequently attempt to copulate with her away from the dung
(precopulatory guarding: Parker,
1972a,b;
Ward, 1983). Only about 40% of
the pairs formed in the field eventually copulate
(Parker, 1972b;
Ward, 1983;
Ward et al., 1992), as females
(even virgins) are very reluctant to mate (Blanckenhorn et al.,
2000,
2002). Males are smaller than
females and thus cannot force copulation, and large males enjoy a mating
advantage mediated by direct and indirect female choice (Blanckenhorn et al.,
1998,
1999,
2000;
Ward, 1983). Direct aggressive
or territorial interactions among males are rare
(Blanckenhorn et al., 2000;
Ward et al., 1992). It is not
known when and where females copulate the first time
(Eberhard, 2000) or where
females spend the rest of their time in the field. From laboratory rearing we
know that adults acquire the protein needed for the production of eggs and
sperm by feeding on dung, and that individuals require sugar, which they
acquire in the field by foraging on nectar
(Warncke et al., 1993).
Sepsis cynipsea overwinter as adults
(Blanckenhorn, 1998).
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General laboratory rearing and holding conditions
On 16 August 1996 we caught about 70-80 pairs on a cow pasture in Bulle,
Canton Fribourg (46°37' N, 7°04' E), Switzerland, at an
elevation of 770 m. Experimental subjects were their
F2-F4 offspring. In the laboratory flies were kept, both
as larvae and adults, in a climate chamber at 60% relative humidity, 14 hr
light period, and 22°C. We reared the test animals in a large quantity of
dung (
1.5 g per 10 larvae) to minimize larval competition and to assure
large adult size (for details, see
Blanckenhorn et al., 1998).
Adults emerged after 10-11 days. Within 24 hr after emergence, the flies were
separated to prevent brother—sister matings and subsequently kept
individually until tested in 100-ml glass bottles with ad libitum amounts of
sugar, pollen, and fresh dung.
Experiment 1: effects of mating behavior on wing injuries and
longevity
This experiment assessed the extent to which mating behavior produces wing
injuries and affects female longevity. One- to two-week-old flies were
randomly allocated to four treatments: (1) mixed-sex pairs held together
permanently for their whole lifetime; (2) mixed-sex pairs held together for 2
days (48 h) and singly thereafter; (3) single-sex pairs held together for
their whole lifetime to control for possible density effects; and (4) virgin
males and females held alone for their whole life-time. Pairs and singles were
kept until their deaths in separate 100-ml bottles in a climate chamber, under
the conditions given above.
To relate wing injuries and longevity to male and female mating behavior,
the mixed-sex pairs in the permanent treatment were observed for 90 min after
initially placing them together in the bottle with a smear of fresh dung, but
not thereafter. (The number of replicates in this treatment was therefore much
higher; see Results.) Three to five pairs were observed continuously and
simultaneously, and each pair's behavior was checked every 5-10 s (temporal
point sampling). We thus obtained an estimate of the cumulative (i.e., total)
duration of female shaking by adding all bouts during which shaking occurred
and multiplying this number by the average bout length of 7.5. s, as well as
the total number of male mating attempts performed, during the 90-min
observation period (see Blanckenhorn et
al., 2000). If copulation occurred (which lasts about 20 min), the
observation period was terminated thereafter. Thus, behavioral data were only
gathered before copulation, and the observation period was necessarily shorter
when copulation occurred. We thus obtained some information on initial mating
behavior, but we do not know whether and how often copulation and mating
behavior occurred over the individuals' lifetime.
To compare longevity between the treatments, we checked for mortality at
least every other day. We also counted the number of eggs of each female's
first clutch, as well as the number of clutches laid over her lifetime, as an
estimate of her reproductive effort. After death we measured left wing length
of all individuals as described by Blanckenhorn et al.
(1998), using a binocular
microscope at 40x magnification. We also assessed the presence or
absence of wing injuries, which typically occur on the wing's posterior end,
and estimated the magnitude of the wing area damaged for both wings (ranging
from 0 to 100%).
We assessed the cost of mating behavior in terms of longevity, independent
of that of copulation, with a supplementary experiment taken from Blanckenhorn
et al. (2002). The longevity of
single females that were confronted with three to six males once or twice in
their lifetime (for at most 3 h), but which had rejected all these males by
shaking (i.e., did not copulate), was compared to that of (virgin) females
that were never confronted with a male. The virgins were the zero-copulation
females used in Blanckenhorn et al.
(2002); the former females were
not used in the Blanckenhorn et al.
(2002) study.
Female shaking duration and the number of male mating attempts were
log10 (x + 1) transformed for analysis. The proportion,
p, of the wing area damaged was logit-transformed,
log10[p/(1 — p)], and no damage was set
(arbitrarily) to p =.0001 so that this ratio could be computed.
Binary data (wings injured or not) were analyzed using logistic regression.
For analysis of continuous data we used ANCOVAs with treatment and sex as main
factors and, where indicated in the Results, body size, fecundity, and/or life
span as covariates (wing injuries accumulate with age;
Hayes and Wall, 1999).
Survivorship was analyzed using Cox regression. For all analyses we used the
SPSS statistical package.
Experiment 2: effects of wing injuries on predation risk
In this predation experiment we tested for an effect of wing injuries on
the predation risk of males and females. We used yellow dung fly females
(Scathophaga stercoraria) originating from a laboratory stock as
predators. Yellow dung flies require prey to reproduce
(Foster, 1967; Gibbons, 1980b)
and are the most common predators of S. cynipsea on cow pastures
(Gibbons,
1980a,1980a,b).
To ensure that the predators were hungry, they were initially kept with water,
sugar and Drosophila spp. as prey until they laid eggs, and
thereafter starved on a water/sugar diet for at least 2 days. The predation
experiment took place in a climate chamber at 20°C, 50% relative humidity,
and 14-hr light period, using virgin S. cynipsea individuals about 1
week after their emergence.
We held groups of 24 S. cynipsea in 3-1 plastic containers
featuring some structure approximating natural situations. In each container
there were eight flies bearing experimentally induced wing injuries of three
different magnitudes. One-third of the flies did not have their wings
manipulated (but the flies were handled and anesthetized), one-third lost
about 10% of their wings (cut through the apical wing spot;
Blanckenhorn et al., 1998:
Figure 1), and the remaining
flies lost about 50% of their wings (cut through the posterior cross vein). We
cut their wings under CO2 anesthesia. The sexes were tested
separately. The flies were of various sizes, but this did not influence the
results, and the data are not presented.
The flies in each container were provided with sugar, some pollen grains,
and water ad libitum. After they had become familiar with their new
surroundings (about 5 h), we added one predator. After 48 hr in the climate
chamber we separated predator and prey and counted the flies killed. Under a
binocular microscope the killed flies are easy to differentiate from those
that died otherwise, as yellow dung flies bite holes of about 0.5 mm diam in
their prey's chitinous exoskeleton
(Sasaki, 1984).
For analysis, we carried out a repeated-measures ANOVA with the percentage of flies killed per initial number for each wing injury class as the dependent variable (arcsine square-root transformed to equalize variances as recommended for proportions), the within-container factor wing injury (repeated because flies were held in the same container), and sex as the between-container factor.
Experiment 3: effects of mating on predation risk
In this experiment we tested for an effect of mating activity on predation
risk by comparing predation on males and females when kept in single-sex or
mixed-sex groups. We expected that female shaking to remove a mounted male
attracts predators and, because pairs cannot fly away, predation on pairs
would therefore be more frequent (e.g.,
Rowe, 1994). As in experiment
2, we grouped 24 flies (with intact wings) in each container. There were
containers with males only, females only, and mixed-sex containers. It was not
necessary to anesthetize the flies to determine their sex. As in experiment 2,
we again added one hungry S. stercoraria female and after 48 hr
separated and counted killed and surviving flies.
For analysis, we computed the percentage of all flies of one sex killed per number of initial flies of that sex (again arcsine square-root transformed). Two comparisons were performed: the between-container comparison of the single-sex and mixed-sex treatments using one-way factorial ANOVA, and the within-container comparison of predation of the two sexes using repeated-measures ANOVA.
Field assessment of wing injuries
To demonstrate that wing injury is not a laboratory artifact and to assess
the extent of wing injuries in the field, we collected at least 30 pairs plus
30 unpaired males from fresh dung pats at our field site in Fehraltorf near
Zürich (47°23' N, 8°45' E) over the whole season in
1998 (late April to early September). Pairs were either copulating or the male
was guarding the female before copulation
(Parker, 1972b). The flies
were collected in small glass tubes using an aspirator and immediately
transported to the laboratory, where they were killed by freezing and later
stored in alcohol. We determined individual body size (head width) and
estimated occurrence and magnitude of wing injuries as described above. Using
logistic regression, we tested for variation in the occurrence of wing
injuries over the season, between the sexes and among males of different
pairing status (single, guarding, and copulating).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Experiment 1: effects of mating behavior on wing injuries and longevity
There were 173 pairs in the permanent mixed-sex treatment, 35 in the temporary mixed-sex treatment, 36 pairs in the female and 55 in the male single-sex treatments, and 32 single females and males. For the single-sex pairs we computed mean values for longevity and wing injuries to avoid pseudo-replication and obtain a precise estimate: If the mean occurrence of wing injury was 0.5, the values were randomly assigned to 0 (= no) or 1 (= yes) in an alternating fashion.
Using Cox regression, we first compared survivorship of the three
treatments with pairs of flies (Figure
1), separately for the sexes. Although our focus here were female
costs of mating, we also present the data for males for comparison. Compared
to females housed in single-sex pairs, the survivorship of females permanently
housed with males was reduced by 21.2% (odds ratio = 0.79), and the
survivorship of females housed with males for 2 days was reduced by 10.5%
(odds ratio = 0.89; treatment effect: 
2 = 14.6, p
<.001; effect of body size: 2 = 0.4, p =.528;
total n = 244; Figure
1). The survivorship of females housed permanently with males was
not lower than that of females housed with males for 2 days (planned contrast:
2 = 2.1, p =.149; odds ratio = 0.83; total n
= 208). In contrast, compared to males housed in single-sex pairs, the
survivorship of males permanently housed with females was greater by 43.1%
(odds ratio = 1.43), and that of males housed together with females for 2 days
was greater by 9% (odds ratio = 1.09; treatment effect: 2 =
29.0, p <.001; positive effect of body size: 2 =
3.7, p =.054; total n = 263;
Figure 1). (When doing the
analogous comparisons among treatments using the flies held singly instead of
in single-sex pairs, the treatment effect on female survivorship disappeared
(2 = 2.7, p =.260; total n = 241), whereas
for males the effect remained (2 = 14.7, p <.001;
total n = 241; Figure
1). When comparing the sexes using only the single-sex treatments
(both pairs and singles), females lived longer than males on average (odds
ratio = 1.25; effect of sex: 2 = 7.0, p =.008; effect
of treatment: 2 = 0.5, p =.473; interaction:
2 = 2.1, p =.152; total n = 155). However,
this occurred because males in pairs died sooner than females in pairs, as
there was no sex difference in survivorship when males and females were held
singly (Figure 1;
2 = 0.6, p =.597; total n = 64). For
clarity, Figure 1 shows average
longevities instead of overlaid survivorship curves.
We next analyzed the permanent mixed-sex treatment, for which behavioral
data were gathered. Only 42 of the 173 virgin females copulated when the males
were first introduced (24.3%). The survivorship of the females that copulated
was reduced by 22.1% (odds ratio = 0.78; mean ± SE longevity: 37.1
± 1.7 days) compared to those that did not (2 = 3.9,
p =.048; mean ± SE longevity: 41.8 ± 0.9 days; total
n = 173), replicating the result obtained by Blanckenhorn et al.
(2002). The same analysis
showed no effects of female fecundity (first clutch size: = 0.1, p
=.792, odds ratio = 1.00), the number of male mating attempts
(log-transformed: 2 = 0.1, p =.814, odds ratio =
1.02), or total female shaking duration (log-transformed: 2 =
0.5, p =.488, odds ratio = 0.98) on survivorship, indicating that
mortality costs of reproduction (clutch size) and mating behavior (shaking)
are minor compared to the costs of copulation. This could be verified by the
supplementary experiment (see Methods, experiment 1) using data from
Blanckenhorn et al. (2002). The
survivorship of females that spent up to 3 h rejecting several males but ended
up not copulating was not reduced (odds ratio = 1.01; mean ± SE
residual longevity: 28.9 ± 3.9 days, n = 17) relative to that
of females which were never confronted with a male (mean ± SE residual
longevity: 27.1 ± 2.4 days, n = 28; 2 = 0.1,
p =.968; no effect of body size, but lower survivorship with
increasing fecundity: 2 = 3.8, p =.050).
We next present the logistic analyses of the occurrence (i.e.,
presence/absence) of wing injuries as a function of treatment. Results for the
magnitude of wing injuries are qualitatively similar and thus not presented.
When comparing all four treatments, females had more wing injuries than males
(effect of sex: 2 = 5.6, p =.018; total n =
571), wing injuries varied among treatments (2 = 16.9,
p <.001) differently in males and females (sex-by-treatment
interaction: 2 = 14.5, p =.002), and longer-lived
individuals had more injuries (effect of longevity: 2 = 6.3,
p =.011; effect of wing length: 2 = 0.9, p
=.323; Figure 2). However, the
difference between the sexes was entirely mediated by females having more wing
injuries in the mixed-sex treatments
(Figure 2): When considering
only the single-sex treatments (both pairs and singles), occurrence of wing
injuries did not differ between the sexes (2 = 1.4, p
=.230; total n = 155). Females had most wing injuries when housed
with a male permanently; female wing injuries were also relatively common when
they were housed in single-sex pairs and least common when housed singly
(Figure 2). Males had most wing
injuries when housed in single-sex pairs and least injuries when housed singly
(Figure 2).
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Experiment 2: effects of wing injuries on predation risk
Containers with fewer than two flies killed were excluded from this
analysis because the predator did not eat and the results are thus
uninformative. We obtained 23 replicates (i.e., containers), 11 for females
and 12 for males. Predation rates on males and females were not different
(repeated-measures ANOVA: F1,21 = 0.78, p =.388),
but varied among the treatments (F2,42 = 4.23, p
=.021) differently in males and females (sex-by-treatment interaction:
F2,42 = 4.35, p =.019). Contrary to expectation,
severely injured females were killed much less frequently than flies of the
other classes (Figure 3).
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Experiment 3: effects of mating on predation risk
We had 30 replicates: 7 containers with only females, 9 with only males,
and 14 with flies of both sexes. Contrary to prediction, predation rates were
higher in single-sex groups (composite mean ± SE = 33.0 ± 4.6%,
n = 16) than in mixed-sex groups (20.4 ± 2.8%, n =
14; F1,28 = 5.24, p =.030). This is entirely due
to higher predation on males than females
(Figure 4; planned comparison:
t15 = 3.16, p =.008). However, we did not find a
sex difference in predation within the mixed-sex containers (paired
t13 = 0.18, p =.861;
Figure 4).
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Field assessment of wing injuries
Logistic regression showed no difference between the sexes in the
occurrence of wing injuries over the season (2 = 2.3,
p =.128; total n = 1310), a quadratic seasonal pattern with
lowest occurrence of wing injuries at the beginning and the end of the season
(linear term: 2 = 5.0, p =.025; quadratic term:
2 = 5.2, p =.027;
Figure 5) and more wing
injuries of larger flies (2 = 13.4, p < 0.001).
Considering only males, we found that the occurrence of wing injuries was
greater in guarding males (49.2%, n = 312) than in single (39.4%,
n = 341) or copulating (35.6%, n = 183) males (effect of
pairing status: 2 = 10.2, p =.006; positive effect of
male size: 2 = 9.7, p =.002). At the same time,
copulating males were larger (mean head width ± SD: 0.87 ± 0.05
mm) than guarding (0.85 ± 0.06 mm) and single males (0.84 ± 0.05
mm; effect of pairing status: F2,682 = 10.1, p
<.001, effect of sampling week: F11,682 = 8.2,
p <.001; interaction: F22,682 = 2.1,
p =.006; cf. Blanckenhorn et al.,
1999). In contrast, copulating (0.91 ± 0.07 mm) and guarded
(0.91 ± 0.06 mm) females were similar in size (single females are rare
at the dung pile).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Finding, assessing, rejecting, and copulating with a male is assumed to carry various fitness costs for a female, which have to be traded off against each other and the fitness benefits of mating. In this study of the dung fly S. cynipsea, we investigated the ultimate effects on mortality (the common currency) of some of these costs as mediated by increased predation, wing injuries, and (indirectly) energetics. Overall, we found that the precopulatory costs of mate assessment and rejection are low relative to the costs of copulating assessed here and by Blanckenhorn et al. (2002
), which explains the
presence of prominent shaking behavior by females to repel males in this and
perhaps other species.
The life span in the laboratory of females housed together with males was
reduced up to 21.2% compared to females housed in single-sex pairs. At the
same time, we note that the survivorship of females held singly was lower than
that of females held in pairs, and not different from that of females held
with males, a result which we cannot easily explain. However, we consider the
single-sex pairs the more natural and appropriate (as they control for
density) reference comparison in experiment 1 (see
Figure 1). This survivorship
decrement subsumes the copulatory and precopulatory costs of mating, as we did
not observe the flies continuously and therefore do not know whether and how
often copulation and mating behavior took place. Nevertheless, we have several
lines of evidence indicating that the precopulatory costs of mating in terms
of mortality (i.e., here, the costs of repelling and/or assessing a male by
shaking) are minor compared to the costs of copulation (see
Blanckenhorn et al., 2002).
First, we observed the permanent mixed-sex pairs for the first 90 min after
they were put together. Of those, 42 females (24.3%) copulated during that
time, and we found that their survivorship was reduced by 22.1% relative to
that of the other females that did not copulate or did so later (females
copulate rarely and reluctantly;
Blanckenhorn et al., 2000).
This replicates and strengthens our findings reported in Blanckenhorn et al.
(2002). In the same analysis,
the frequency of male attacks and the total amount of female shaking explained
at most a nonsignificant 2% of the decrease in survivorship of these females.
That is, the mortality costs of the presumably energetically costly mate
rejection and assessment behavior of females (e.g.,
Watson et al., 1998), as
performed over their whole lifetime (see below), are much smaller than those
of copulating.
Second, our supplementary data set from Blanckenhorn et al.'s
(2002) study yielded no
difference in the survivorship of females that spent up to 3 h rejecting
several males but ended up not copulating and those females that never
encountered a male. This again indicates that rejection behavior, this time
merely over the short term, is not very costly in terms of mortality. Third,
the fact that the mean longevity of females confronted with a male for only 2
days was not significantly different from that of the females confronted with
a male permanently (Figure 1)
suggests that substantial costs of mating can be incurred in a relatively
short time (i.e., presumably by copulation as opposed to precopulatory mating
interactions). We have some unpublished evidence that S. cynipsea
females behave similarly when confronted with the same or different males
repeatedly over time
(Mühlhäuser, 1998).
So even though the observation time of 90 min and the contact with a male for
at most 3 h were short relative to a female's lifetime of about 40 days, we
can assume the observed behavior to be representative of the individuals'
behavior over their lifetime. Clearly, energetic costs of mating behavior must
be present even in insects (e.g.,
Clutton-Brock and Langley,
1997; Cordts and Partridge,
1996; Watson et al.,
1998), and we plan to assess these costs in future studies of
S. cynipsea. We argue that these energetic costs are apparently not
simply cumulative and thus may not translate to substantial decrements in
survivorship, the ultimate component of individual fitness used here as the
common currency (see Alatalo et al.,
1998; Kotiaho et al.,
1998).
Females housed permanently with a male showed a higher incidence of injured
wings, presumably due to male harassment. On the other hand, activity per se
also produces wing injuries. The extent of wing injuries of both sexes was
greater when held in single-sex pairs, and more social interactions were
possible than when held singly (Figure
2). The males also harass each other. It is also well known that
wing injuries in insects accumulate with age by mechanical wear and tear, to
the extent that they may be used to age individuals
(Hayes and Wall, 1999). We
also found this in our field study, where wing injuries increased in the
overwintered generation at the beginning of the season until they reached an
asymptote at the point when subsequent (and overlapping) generations of flies
emerged (Figure 5). Overall,
our field and laboratory studies show that wing injuries accumulate with age
and are equally common in males and females.
Even though small wing injuries are ubiquitous in insects
(Hayes and Wall, 1999), it is
reasonable to hypothesize that they augment the energetic costs of flight,
impair the flying ability to some extent, and thus ultimately lead to higher
predation and mortality (e.g., Cartar,
1992). These costs are likely to apply in the field, but they are
probably unimportant in our small holding bottles used in the first
experiment. We also assessed predation rates in larger containers wherein
flies could roam freely. However, experimentally induced wing injuries did not
increase predation rates. On the contrary, predation on S. cynipsea
females missing about 50% of their wings was lowest, perhaps because they were
less active than flies with more intact wings. In our second predation
experiment we also found no evidence for our hypothesis that female shaking
attracts predators and, because pairs cannot fly away, increases predation
risk (e.g., Fairbairn, 1993;
Rowe, 1994). Instead we found
predation in all-male containers to be highest, perhaps because males are more
actively searching for females. In some species mating has even been shown to
reduce the risk of predation on males
(McCauley and Lawson, 1986)
and females (Jivoff, 1997). So
even though we have some evidence that wing injuries of females are caused by
male harassment, we have no evidence that these wing injuries lead to higher
predation or decreased survivorship in the laboratory. Of course, we only
tested one of many predators present in nature, albeit the most common
sit-and-wait predator on cow pastures in Central Europe (the yellow dung fly
Scathophaga stercoraria). However, we must continue to assume that
wing injuries to some extent impede the movements of females and males between
oviposition sites, foraging sites, and areas of shelter, and thus ultimately
affect their fitness in the field. Field investigations of the energetic and
mortality costs of wing injuries clearly would be informative, but
unfortunately these are unfeasible in this small species.
Although not specifically addressed here, our study yielded some
indications that mating behavior may be costly for males as well. Male
survivorship was lowest, and wing injuries were highest, when a male was held
with another male. Furthermore, predation was highest in all-male groups. This
could be because males are more active, probably in search of females, and
because they frequently harass each other as well. When held with females, in
contrast, male survivorship was higher and they had fewer wing injuries. This
suggests that female shaking is not very energetically costly for the male and
does not externally harm him. Furthermore, males with injured wings may be
less successful in achieving copulations. Copulating males were largest (see
Blanckenhorn et al., 1999;
Ward, 1983) and had the lowest
occurrence of wing damage. However, less wing damage may merely indicate that
they are younger, and the effect of wing damage on male mating behavior and
success remains to be experimentally addressed.
Why are S. cynipsea females so reluctant to mate? This and our
companion study (Blanckenhorn et al.,
2002) suggest that repelling males does not appear to have serious
consequences for female fitness, whereas copulating with a male does. Females
avoid superfluous copulations to prevent mortality due to internal injuries
presumably inflicted by the male
(Blanckenhorn et al., 2002;
Crudgington and Siva-Jothy,
2000; Johnstone and Keller,
2000) and/or to avoid possibly toxic physiological substances
transferred during copulation (Chapman et
al., 1998). The fitness costs of avoiding matings in terms of
increased predation, energetics, or wing injuries are minor in comparison. Our
findings are relevant to other species with similar mating systems such as
waterstriders or seaweed flies (e.g.,
Crean and Gilburn, 1998;
Rowe, 1994;
Watson et al., 1998).
|
ACKNOWLEDGEMENTS |
|---|
Thanks to T. Bakker, A. Bourke, P. Ward, D. Hosken, and two anonymous referees for comments and advice, A. Sauter and S. Zehnder for conducting part of the field study, and the Swiss National Fund for financial support.
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