Behavioral Ecology Vol. 10 No. 3: 227-233
© 1999 International Society for Behavioral Ecology
Female remating propensity contingent on sexual cannibalism in sagebrush crickets, Cyphoderris strepitans: a mechanism of cryptic female choice
Behavior, Ecology, Evolution and Systematics Section, Department of Biological Sciences, Illinois State University, Normal, IL 61790-4120 USA
Address correspondence to J.C. Johnson, who is now at the Center for Ecology, Evolution and Behavior, T.H. Morgan School of Biological Sciences, University of Kentucky, Lexington, KY 40506-0225, USA.
Received 2 April 1998; revised 24 July 1998; accepted 8 August 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Male sagebrush crickets (Cyphoderris strepitans) permit females to engage in an unusual form of sexual cannibalism during copulation: females feed on males' fleshy hind wings and ingest hemolymph oozing from the wounds they inflict. These wounds are not fatal, and normally only a portion of the hind wings are eaten at any one mating, so that mated males are not precluded from mating again. As a result, nonvirgin males have fewer material resources to offer females than do virgin males, such that females should be selected to preferentially mate with high-investment virgin males. We tested the hypothesis that female mating preferences favor males capable of supplying females with the highest material investment. Our results indicate that both female diet and opportunities for sexual cannibalism influence female mating behavior. Females maintained on a low-nutrient diet mounted males significantly sooner than females maintained on a high-nutrient diet, indicating that a female's overall nutrient intake may determine her propensity to mate. In addition, females were significantly more reluctant to mount and mate with males whose hind wings had been surgically removed and thus were incapable of providing females with a wing meal. Finally, females initially mated to dewinged males remated with winged males significantly sooner than females allowed to feed freely during their initial mating, resulting in cryptic female choice of investing males.
Key words: courtship feeding, cryptic female choice, Cyphoderris strepitans, sagebrush crickets, sexual cannibalism, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Cryptic female choice refers to mechanisms of mate choice that operate after copulation has begun but before fertilization occurs (Eberhard, 1996
;
Thornhill, 1983). Female
control over the reproductive process and the resultant potential for
postcopulatory forms of female choice to affect sexual selection are currently
receiving widespread attention (Eberhard,
1996, 1997;
Eberhard and Cordero, 1995).
Insect mating systems that involve male-donated courtship food gifts provide
ideal systems for the study of cryptic female choice because they offer an
obvious target for such preferences. In sagebrush crickets, Cyphoderris
strepitans, males permit females to engage in an unusual form of sexual
cannibalism during copulation: females feed on males' fleshy hind wings and
ingest hemolymph oozing from the wounds they inflict
(Dodson et al., 1983). These
wounds are not fatal, and normally only a portion of the hind wings are eaten
at any one mating, so that mated males are not precluded from mating again.
However, nonvirgin males have fewer material resources to offer than virgin
males, such that females should be selected to mate preferentially with virgin
males (Dodson et al., 1983;
Thornhill and Alcock,
1983).
Previous studies have shown that virgin males do secure significantly more
matings than nonvirgin males, based on their relative abundance in the
population (Morris et al.,
1989; Snedden,
1996). Although this effect has been shown to be partly a result
of the decreased calling activity of recently mated males
(Sakaluk and Snedden, 1990;
Sakaluk et al., 1987), the
degree to which female choice contributes to this virginmale mating advantage
remains uncertain. Studies to date suggest that females do not differentiate
among virgin and nonvirgin males based on qualitative differences in males'
songs (Sakaluk and Ivy, unpublished data;
Snedden and Greenfield, 1995),
nor do they appear to discriminate in terms of their willingness to mount and
complete copulations with nonvirgin males
(Snedden and Sakaluk, 1992).
However, Eggert and Sakaluk
(1994) showed that virgin
males whose hind wings had been surgically removed were less likely to
complete matings than males with intact wings, even though males of both
treatments did not differ in the time taken to elicit female mountings. They
concluded that wing feeding keeps females preoccupied during the time needed
by males to transfer the spermatophore. However, the degree to which this
result can be extended to nonvirgin mating success in the field remains
uncertain because typically nonvirgin males retain at least some wing material
with which to provision other mates (Dodson
et al., 1983; Eggert and
Sakaluk, 1994; Morris et al.,
1989).
The lack of evidence showing any discrimination against nonvirgins calls
into question the prevalence and efficacy of precopulatory female choice in
this mating system. Benefits of outright mate rejection would appear to be low
given that the duration of mating is short relative to the time required by
females to localize calling males
(Snedden, 1995) and that
females can usually derive a meal, albeit reduced, from most nonvirgin males.
For these reasons, one might expect females to adopt a strategy of
material-benefit polyandry (Thornhill and
Alcock, 1983), accepting matings and wing-feeding without regard
to a male's mating status. However, if the nutrition derived through courtship
feeding is important to female reproduction, nonvirgin males could still be
subject to cryptic mate choice exerted after copulation has occurred. Females
may accept matings with nonvirgin males, but if the resources derived through
wing feeding on these males are insufficient to satisfy females' nutritional
requirements, they may remate sooner than they otherwise would after matings
with virgin males. Such postcopulatory behavior, in conjunction with the
last-male sperm precedence that is common in insect mating systems
characterized by high male material investment
(Gwynne, 1984), would result
in higher reproductive success of those males offering the greatest
nutritional rewards. Although a female's choice under these circumstances
might best be viewed as an incidental consequence of adopting a strategy of
exchanging matings for food, this does not preclude the possibility that
females secure indirect genetic benefits as well, particularly if a male's
investment at mating is an honest indicator of his viability
(Thornhill and Alcock,
1983).
The objective of this study was to test the hypothesis that postcopulatory female mating preferences favor males capable of supplying females with the highest material investment. Specifically, we predicted that females paired with dewinged males, and thus experimentally prevented from wing feeding during their initial matings, would remate sooner than females allowed to feed freely in their initial mating. In addition, we predicted that if nutrient intake influences female mating decisions, then females maintained on a low-nutrient diet should have a higher propensity to mate than females maintained on a high-nutrient diet.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Overview and natural history
C. strepitans is one of only five extant species belonging to an obscure orthopteran family, the Haglidae, and occurs exclusively in mountainous areas of the western United States, where it is often found in high-altitude sagebrush meadows (Morris and Gwynne, 1978
). Adults become sexually active in late spring,
shortly after the snow melts, and remain active for the next 4-6 weeks. The
acoustic signals produced by males function to attract females
(Snedden and Irazuzta, 1994)
and are the principal means of pair formation
(Sakaluk et al., 1995b;
Snedden and Sakaluk, 1992).
Copulation is initiated when a receptive female climbs onto the dorsum of a
male, immediately after which the female chews on the male's fleshy hind wings
that the male exposes by raising his forewings. Successful mating requires the
transfer of a spermatophore, the bulk of which remains outside the female's
body after mating. Females may prevent mating by dismounting the male before
spermatophore transfer has occurred, but they are hindered from doing so by
the gin trap, an abdominal clasping device used by the male
(Sakaluk et al., 1995a).
Completed matings, however, are terminated by the male, who pulls away from
the female as soon as spermatophore transfer has been accomplished
(Dodson et al., 1983).
Approximately 3 h after mating, on average, females begin feeding on the
spermatophore, which they eventually consume (Sakaluk and Snedden, unpublished
data).
Study site and collection procedures
The study was conducted at the University of Wyoming-National Park Service
Research Center, the site of previous studies
(Eggert and Sakaluk, 1994;
Sakaluk et al., 1995b;
Snedden and Sakaluk, 1992).
Male and female crickets were collected early in the breeding season
(May-June) from several populations within Grand Teton National Park and
transported to the field station. All males used in the study were virgins, as
evidenced by the presence of intact hind wings; females were of unknown mating
status. Crickets were maintained according to standard procedures
(Eggert and Sakaluk, 1994;
Snedden and Sakaluk,
1992).
Matings were staged in specially constructed, Plexiglas viewing chambers divided into two equal compartments (10x6.8x4.4 cm). Each compartment was equipped with a small stick placed diagonally across the chamber to provide males with a calling perch. Experimental pairs were established early in the evening when the crickets become sexually active, and their mating behavior was directly observed over the next 8 h under red light. Throughout the observations we used a 5-min sampling protocol to determine the number of 5-min intervals in which a male called. No food or water was provided during mating trials. Upon completion of the experiment, crickets were returned to the population from which they were collected. Two different experiments were conducted over consecutive field seasons.
1996: diet and female mating behavior
The objective of this experiment was to examine the effect of dietary
regime and wing feeding on female mating and remating propensity. We
established two dietary regimes, one in which females were maintained solely
on lettuce (low-nutrient diet), and another in which females were maintained
on apple and bee pollen supplied ad libitum (high-nutrient diet). Feeding
regimens were initiated the morning after females were collected. Females were
held on their respective dietary regimes for a minimum of 48 h before being
used in a mating trial and thereafter until they completed the study. Females
from each of the dietary regimes were first paired either with virgin males
whose hind wings had been left intact or with virgin males whose hind wings
had been surgically removed, thereby precluding wing feeding. The hind wings
of dewinged males were removed 24 h before the beginning of mating trials to
permit their full recovery from the procedure (see
Eggert and Sakaluk, 1994;
Sakaluk et al., 1995a,
b).
Females were randomly assigned to one of four experimental treatments for
their initial matings (sample sizes in parentheses): (1) females held on the
low-nutrient diet and paired with a winged, virgin male (n = 12); (2)
females held on the high-nutrient diet and paired with a winged, virgin male
(n = 14); (3) females held on the low-nutrient diet and paired with a
dewinged, virgin male (n = 11); (4) females held on the high-nutrient
diet and paired with a dewinged, virgin male (n = 6). We recorded the
time at which females first mounted males and the time at which spermatophore
transfer (i.e., mating) occurred relative to the beginning of the trial.
Females that did not mate within the 8-h observation period were paired with a
different male the next night and each subsequent night until mating occurred;
in calculating the time to mating, we included only those hours during which
females were paired with males. Whenever a female mated, another replicate
within the treatment was established; this resulted in unequal sample sizes
across treatments, but there was no significant difference in the date on
which pairs across treatments were established (
2 = 3.78,
p =.28), thereby ameliorating any seasonal effects should such
exist.
After females of the four different treatments had completed their initial matings, they were given an opportunity to remate with an unmanipulated (winged) virgin male on each subsequent night until remating occurred or the season ended. Rematings were staged under identical conditions as the initial matings (see above). Thus, the intervals between initial spermatophore transfer and time to mounting and time to mating with the replacement male were used as measures of each female's propensity to remate.
1997: wing feeding and postcopulatory female choice
Results from 1996 allowed us to assess the influence of diet on female
mating propensity, but a paucity of initial matings of females paired with
dewinged males (see below) precluded any assessment of postcopulatory mating
preferences. Accordingly, our focus in 1997 was on sexual cannibalism and its
influence on female remating behavior, with all females maintained on the same
diet of natural vegetation (fresh sagebrush clippings). Upon their capture,
females were assigned to either of two experimental treatments: (1) females
allowed to wing feed on their initial mate (n = 13) or (2) females
prevented from wing feeding on their initial mate (n = 15). Males
paired with females of treatment 2 had their hind wings surgically removed 24
h before the mating trial. Mating trials were staged as in the previous field
season. As before, we used the time from trial initiation to mounting and
mating as measures of female willingness to mate.
One hour after initial copulations had been completed, mated males were replaced with unmanipulated virgin males, and females of both treatments were given the opportunity to remate with a winged male. The intercopulatory interval was used to assess female remating propensity across treatments.
Statistical analyses
We conducted analyses using procedures of SAS for personal computers
(SAS Institute, 1988).
Student's t tests were used to evaluate any potential effect of wing
removal on male calling ability. All of our measures of the latency to mount
and mate were non-normally distributed. Therefore, comparisons between
treatments of the time to mounting and time to remounting were made on
log-transformed data using log-transformed ANOVA and t tests.
In contrast to data on female mounting latency, comparisons of time to
mating and remating were performed using the nonparametric testing procedures
of failure-time analysis (Fox,
1993b; Kalbfleisch and
Prentice, 1980). Failure-time analysis accommodates censored data,
observations in which an event such as mating may not have occurred by the end
of the study, as was the case here. Omission of such data, as is frequently
done in behavioral studies, may lead to a serious bias in comparisons across
treatments (Fox, 1993b). For
the 1996 two-way design, we performed four planned contrasts across treatments
within (1) dietary regime and (2) wing treatment when the initial analysis
indicated significant differences existed across groups; in these comparisons,
the appropriate Bonferroni-adjusted significance level was employed.
In principle, we also could have employed failure-time analysis in the analysis of mounting data, but we did not do so because all females in both years mounted males at least once, even if all of them did not successfully complete a mating. When there are two main effects, as in the case of the 1996 experiment, a two-way ANOVA is preferable because, unlike failure-time analysis, it allows the interaction between the two main effects to be assessed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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1996: diet and female mating behavior
We compared the calling activity of winged and dewinged males, restricting our analysis to each male's first mating trial to ensure statistical independence of observations. Dewinged males (n = 27) called on average in 62% of the 5-min sampling intervals monitored over the 8-h observation period, whereas winged males (n = 84) called in 63% of the intervals; this difference is not statistically significant (t = 0.24, p =.81). For males successful at mating, there were no differences in the time spent calling by winged males (n = 40, 57% of intervals) and de-winged males (n = 8, 50% of intervals; t = 0.65, p =.52).
Table 1 summarizes female mounting, mating, remounting, and remating data across diet regimes and wing treatments for the 1996 experiment. For initial pairings, a log-transformed, two-way ANOVA [reported as back-transformed least square means (hours) ± SE] revealed that diet had a significant influence on a female's latency to mount, with low-diet females mounting males sooner than high-diet females (3.80 ± 1.29 and 8.70 ± 1.35 h, respectively; F = 4.51, p =.04). The effect of wing condition on latency to mounting was not statistically significant (F = 3.00, p =.09). There was no interaction between diet and wing condition on the latency to mounting (F = 0.08, p =.77).
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For initial pairings, failure-time analysis revealed significant
differences across treatments in the time taken by females to mate
(Figure 1; 2 =
10.26, p =.02). There was no significant effect of diet on the time
to first mating (p >.05). The wing condition of males had a
significant effect on the time at which females first mated, with females
paired with dewinged males taking much longer to mate than those paired with
winged males. However, this difference was significant only for low-diet
females (2 - 6.98, p =.01; high-diet females:
2 = 2.00, p =.16).
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Too few of the females paired with dewinged males completed their initial
matings, precluding any assessment of the effect of wing condition on a
female's propensity to remate (see instead results for 1997). There were,
however, a sufficient number of initial matings by females paired with winged
males to assess the effect of diet on remounting and remating propensity. In
pairwise comparisons of females allowed to wing feed on their initial mate,
there was no effect of diet regime on the time taken by females to mount the
replacement male (t = 0.58, p =.56) or the time taken by
females to remate (2 = 0.004, p =.95).
1997: wing feeding and postcopulatory female choice
There was no difference in the proportion of time spent calling across wing
treatments (winged males: n = 29, 60% of intervals; dewinged males:
n = 33, 59% of intervals; t = 0.06, p =.95). Among
males successful at acquiring matings, calling proportions were also similar
across wing treatments (winged males: n = 9, 64% of intervals;
dewinged males: n = 12, 68% of intervals; t = 0.27,
p =.79).
Table 2 summarizes female
mounting, mating, remounting, and remating data for the 1997 experiment.
Female latency to mount (log-transformed) was significantly greater for
females paired with dewinged males than for those paired with winged males
(t = 2.09, p =.05). In addition, failure-time analysis
showed that females took significantly longer to mate with dewinged males than
they did with winged males (Figure
2; 2 = 15.83, p =.0001). Females
initially mated to a dewinged male remounted replacement males significantly
sooner than females allowed to feed on their initial mate (t = 2.81,
p =.01). Failure-time analysis showed an equally strong effect of
wing feeding on the latency to remating. Females prevented from wing feeding
on their initial mate took one-third of the time to remate compared to females
who were allowed to feed on their initial mate
(Figure 3; 2 =
13.00, p =.0003).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Our results suggest that opportunities for sexual cannibalism, as well as female nutrient load, influence precopulatory mechanisms of mate choice through both female mounting and mating propensity. In addition, our results provide evidence of cryptic mate choice employed after mating, manifest in a female remating propensity that is contingent on a male's ability to provide wing material. Differential male mating success across treatments cannot be attributed to a lowered calling ability resulting from the surgical removal of a male's hind wings because in both years of the study dewinged males called at rates equivalent to winged males (see also Eggert and Sakaluk, 1994
).
Given that stridulation is perhaps the most energy-consuming activity in which
a male can engage (Hoback and Wagner,
1997; Lee and Loher,
1993; Prestwich and Walker,
1981), this observation suggests that dewinged males were not
appreciably weakened by their operations.
Precopulatory mate choice
Our manipulation of female diet in 1996 revealed that low-diet females
mount their mates more readily than high-diet females. Similarly, when paired
with a winged male, low-diet females took only about one-third as long to
mate, on average, as did high-diet females. A similar effect of heightened
female mating propensity under conditions of food stress has been documented
in a variety of gift-giving insects (Brown,
1997; Fox, 1993a;
Gwynne, 1990;
Markow and Ankney, 1984;
Simmons and Gwynne, 1991;
Steele, 1986). These findings
are consistent with the hypothesis that polyandry in gift-giving species
functions, at least in part, in the acquisition of material benefits from
males (Thornhill and Alcock,
1983).
In the 1997 experiment, females mounted winged males significantly sooner
than they mounted males whose hind wings had been removed. This result is in
direct contrast to a previous study showing no difference in the time at which
winged and dewinged males were first mounted
(Eggert and Sakaluk, 1994).
The only obvious difference in the two studies is in the diet on which
experimental females were maintained; in the 1997 experiment, all females were
maintained on a natural diet of moistened sagebrush clippings, whereas in
Eggert and Sakaluk's (1994)
study, females were fed on pieces of apple and carrot. Any mounting preference
for winged males would require a discriminatory mechanism that operates prior
to mounting and before the onset of female wing feeding. Perhaps the most
efficient mechanism for discrimination at this level would be acoustic
differentiation of certain aspects of males' calls. Morris et al.
(1989) suggested that the loss
of hind-wing material lying beneath the sound-producing tegmina might alter
male calling parameters. The ability to acoustically discriminate between
virgin males and non-virgins at long distances would carry obvious selective
advantages for females by eliminating situations in which females expend
energy locating a male incapable of providing a large wing meal
(Boggs, 1990) and/or by
minimizing predation risks associated with phonotaxis
(Sakaluk, 1990;
Sakaluk and Belwood, 1984).
Indeed, acoustic analyses of digitized calls of virgin, non-virgin, and
experimentally de-winged males indicate possible differences in the amplitude,
and perhaps, spectral components of the signals
(Snedden and Greenfield, 1995;
Ritchie MG, personal communication). A more recent study has shown, however,
that the asymmetrical removal of one hind wing does not influence female
willingness to mount males in the laboratory or reduce male mating success in
the field (Sakaluk and Ivy, unpublished data), results that are inconsistent
with an acoustically mediated mounting preference.
Other proximate mechanisms that potentially could mediate female mounting preferences include visual and/or tactile detection of the presence/absence of wing material before mounting. One possibility is that the creamy white color of the hind wings against a dark background could serve as a close-range visual cue alerting females to wing-feeding opportunities. Alternatively, there may be occasions in which the females do not mount the male, but get sufficiently close to palpate the dorsum of the male with their mouthparts. In support of this possibility, females occasionally were observed hanging upside down from the calling perch above a calling male in an apparent attempt to wing feed without mounting the male.
In the 1997 experiment, and within the low-diet treatments in the 1996
experiment, we found a statistically significant female mating preference for
winged males. In both cases females were markedly more reluctant to complete
matings with dewinged males, waiting on average 50 h longer to mate than
females allowed to wing feed. These findings support previous studies showing
that wing-feeding females are much more likely to allow spermatophore transfer
than females prevented from wing feeding
(Eggert and Sakaluk, 1994;
Sakaluk et al., 1995b).
Postcopulatory mate choice
Due to small sample sizes in 1996, we were able to compare the effect of
diet regime on female remating propensity only for females initially mated to
males with intact hind wings. Following such matings in which wing feeding was
permitted, low-diet females did not remount or remate significantly sooner
than their high-diet counterparts. Thus, while female mating propensity
appears to be accelerated by a lack of adequate nutrition, the refractory
period following an initial mating involving wing feeding is not affected by
diet regime. This raises the possibility that consumption of the food gift in
the initial mating may weaken the effect of previous food stress, rendering
females from both diet regimes equally ready to remate. Similarly, Simmons and
Gwynne (1991) showed that
nutrient stress in a zaprochiline katydid shortens female refractory periods
only when females are restricted from feeding on their initial male's food
gift, a gelatinous spermatophylax.
Previous studies of C. strepitans have focussed on factors that favor male success in obtaining matings. Unique to the present study is the finding that female refractory periods vary as a function of the ability of the initial male to provide wing material. Our data indicate that 9 of 12 females restricted from wing feeding on their initial mate remated within the same night, with the remaining 3 females remating within the first hour of the following night's mating trial. In contrast, only 3 of 13 wing-fed females remated within the same night, and the remaining 10 females typically waited 3 nights before remating. While little is known of female oviposition patterns in this species, this differential in remating propensity should almost certainly influence male fertilization success given any degree of last-male sperm precedence.
The existence of cryptic female choice via remating propensity in sagebrush
crickets adds to a growing number of studies that implicate sexual conflict
over female remating intervals as a potential source of sexual selection. When
food gifts are given at mating, females often remate more quickly following
matings with low-investment males (Boggs,
1981; Kosal and
Niedzlek-Feaver, 1997;
Oberhauser, 1992;
Savalli and Fox, 1998;
Simmons and Gwynne, 1991;
Thornhill, 1976,
1983). The results of our
study closely parallel those of Thornhill's
(1983) pioneering work on
cryptic female choice in gift-giving scorpionflies, Harpobittacus
nigriceps. In the mating systems of both species, female postcopulatory
mating preferences impose strong selection on males to maximize their
nutritional contributions. Additionally, females of both species exhibit
precopulatory mating biases against low-investment males, suggesting that
female choice may routinely be a complex of discrimination at multiple
levels.
Much of what has been interpreted as cryptic female choice could
alternatively be viewed as a form of male manipulation. For example, if
chemical substances contained in male hemolymph function to diminish female
sexual receptivity, then the inability of dewinged males to transfer such
substances might explain the heightened mating propensity of females mated to
these males. However, even if it could be shown that substances contained in
the male's hemolymph induce a refractory period in females, their existence
per se would not be sufficient evidence of male manipulation because
"manipulation" implies that females are forced to behave in a way
that is contrary to their own reproductive interests. Although males clearly
benefit from a reduction in the sexual receptivity of their mates, females
might also benefit from the refractory period that follows copulations with
males offering substantial food rewards. Having met their immediate
nutritional needs and secured sufficient sperm to fertilize their eggs,
females' interests might best be served by focussing their efforts on
oviposition and foregoing the attendant risks of seeking out additional mates
(Csada and Neudorf, 1995;
Hedrick and Dill, 1993;
Sakaluk and Belwood, 1984).
Hence, it might be advantageous for females to respond to any hormonal cues
present in male hemolymph, in which case these substances might more properly
be regarded as chemical signals rather than as a form of male
manipulation.
Future studies should focus on assessing the degree to which female mating
biases serve female interests and the degree to which these biases are the
product of male manipulation. A complete understanding of mating system
dynamics requires that they be viewed as the net result of an ongoing sexual
arms race (Parker, 1979;
Alexander et al., 1997). Just
as male-male competition occurs at multiple levels before and after mating,
precopulatory and postcopulatory mechanisms of female choice offer females an
array of potential counter-adaptations to maintain control over the
reproductive process.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank Pamela Brady, Matthew Deitch, Anne-Katrin Eggert, Madeline Ostrander, Marion Sakaluk, and Jennifer Schaus for field and laboratory assistance and Steven Juliano, Charles Thompson, and two anonymous reviewers for constructive comments on the manuscript. Members of the Behavior, Ecology, Evolution and Systematics Section at Illinois State University provided valuable input on the design of the project. This study was supported by grants from the National Science Foundation (IBN-9601042 and REU supplemental award), University of Wyoming-National Park Service Research Center, and Illinois State University to S.K.S. and by a grant from the Phi Sigma Biological Honors Society (Beta Lambda Chapter) and an Omar Rilette travel award to J.C.J.
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