Behavioral Ecology Vol. 13 No. 1: 83-86
© 2002 International Society for Behavioral Ecology
Mate sampling and the sexual conflict over mating in seaweed flies
a Institute of Genetics, University of Nottingham, Nottingham, UK b School of Biology, University of Leeds, Leeds, UK
Address correspondence to D.M. Shuker, who is now at ICAPB, University of Edinburgh, Ashworth Laboratories, Kings Buildings, Edinburgh EH9 3JI, UK. E-mail: david.shuker{at}ed.ac.uk .
Received 25 October 2000; revised 22 March 2001; accepted 22 March 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The order in which females encounter, or sample, males in a population may have important consequences for mate choice, with the information gathered about males influencing both the preference function and degree of choosiness of females. Sexual selection may be affected as a result. Sampling of particular subsets of males may be a crucial component of individual variation in mate preferences within populations. However, the sequence in which males are sampled may also be important in species without traditional, active mate choice, such as when sexual selection involves sexual conflict over mating. This would occur if the likelihood of a female mating with a male of a certain phenotype changes as a result of previous encounters. We examined the effects of encountering males differing in body size, a sexually selected phenotype, in the seaweed fly Coelopa frigida. Sexual selection occurs in this species as a result of a sexual conflict over mating. We show that the outcome of the sexual conflict is independent of the order in which males are encountered by female seaweed flies, with the overall mating advantage to large males being unaffected. In addition, we explored female preference functions and evaluate the heterogeneity in female willingness to mate. We suggest that consideration of mate sampling theory is valuable when examining mate choice in species in which sexual selection is driven by sexual conflict.
Key words: Coelopa frigida, mate choice, mate sampling, seaweed flies, sexual conflict, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Choosing a mate involves gaining information about potential mates and then making a decision based on this information (Wittenberger, 1983
).
Information gathering involves some form of sampling, with tactics based
either on examining a sample of mates and choosing from that sample (pooled
comparisons, including "best of n") or on a specific
threshold of mate quality by which each individual is evaluated (such as
sequential search; reviewed by Reid and
Stamps, 1997; Real,
1990; Gibson and Langen,
1996; Wittenberger,
1983). Decision making involves exercising individual mate
preferences, typically with females as the choosy sex, limiting the range of
males a female mates with.
The information gathering and decision-making processes are closely
associated, together influencing observed patterns of mate choice. For
instance, there are two components to mate preferences: the preference
function (the relationship between female response and size of stimulus), and
the degree of choosiness (effort invested in mate assessment)
(Jennions and Petrie, 1997;
Widemo and Saether, 1999).
Preference functions can be expressed as fixed thresholds for particular male
traits. Alternatively, preference functions can be flexible, varying with the
males actually available within a population, and thus dependent on the
particular phenotypic distribution in the population. If the latter is the
case, the way in which females encounter, or sample, males in a population can
affect the preference function of those females. Females could adaptively
alter mate preference functions in response to their prior experience of males
of differing quality and so balance the quality and quantity of mates with
strategic mate sampling decisions (Gibson
and Langen, 1996; Jennions and
Petrie, 1997; Wagner,
1998). In addition, the amount of time and energy a female invests
in choosing mates (e.g., the time assigned to search for and assess potential
mates) can interact with the preference function and vary with the particular
males encountered. Certain males could limit further searching due to costly
behavioral interactions. Mate preferences would again differ among females in
response to the specific subset of males a female encountered. Empirical
evidence for "previous male effects" of these kinds comes from
several species, including mottled sculpins
(Downhower and Lank, 1994),
sticklebacks (Bakker and Milinski,
1991), and zebra finches
(Collins, 1995).
Phenotypic plasticity in mating preferences has obvious consequences for
the strength and direction of sexual selection within a population and may be
an important component of within- and between-population variation in
preferences (Jennions and Petrie,
1997). Crucially, these considerations apply equally to mating
systems characterized by active female mate sampling (e.g., mating systems
where females visit displaying males in turn, such as lekking species;
Höglund and
Alatalo, 1995), as well as systems in which females encounter
males serendipitously without active searching or sampling tactics. Both
situations result in mate-choice decisions being based on previously
encountered males as well as the current male. Even if females only sample
males passively, choosiness and acceptance criteria could depend on male
phenotypes encountered.
Preference functions do not necessarily depend on active mate choice
because sexual conflicts over mating can also lead to female behaviors that
bias male mating success (Clutton-Brock and
Parker, 1995; Parker,
1979,
1983). The importance of
sexual conflict over mating leading to sexual selection is now well
appreciated, particularly in insects (Rowe
et al., 1994; see also reviews in
Choe and Crespi, 1997,
especially Brown et al., 1997).
For species in which mate choice is a result of sexual conflict, we need to
know whether the order in which males of particular phenotypes are encountered
influences the outcome of the sexual conflict. Possible effects include
flexible preference functions, coupled with the costs accrued through
interactions with males (such as the buildup of costs of rejecting unsuitable
males). If females vary their willingness to mate by altering the intensity or
duration of rejection responses, then a full description of the selection
pressures on males, and the variation in preferences among females, must
include these sampling effects.
In the seaweed fly, Coelopa frigida, sexual selection on males
occurs as a result of a sexual conflict over mating
(Day and Gilburn, 1997;
Shuker and Day, 2001). The
mating system is characterized by scramble competition, with females
encountering males effectively at random within the seaweed matrix (see
Day and Gilburn, 1997). Both
sexes are highly promiscuous, and female receptivity is unaffected by
copulation (Shuker and Day,
2001). Mating interactions in seaweed flies involve males mounting
females and attempting to force copulation; females usually attempt to prevent
copulation with a suite of rejection responses
(Day et al., 1990). Larger
males are best able to force copulation, so that female rejection creates a
preference for large males (Day and
Gilburn, 1997). This preference may have evolved as a side effect
of selection on females to reduce the number of potentially costly matings
(Day and Gilburn, 1997;
Gilburn and Day, 1999;
Shuker, 1998).
Much work has been done in C. frigida describing variation in
patterns of mating in natural populations
(Crean, 1997;
Day and Gilburn, 1997;
Shuker and Day, 2001),
although the effects of encountering sequences of males on mating patterns
have yet to be examined. Here we describe the results of an experiment in
which females encountered males of three size classes, with the aim of
specifically examining the effects of sampling on the outcome of the sexual
conflict. We addressed two questions. First, is there heterogeneity in
females' willingness to mate? Previous studies have shown that females'
willingness to mate varies at the population level, with average willingness
to mate being associated with a chromosomal inversion polymorphism (the
ß inversion system; Gilburn and Day,
1994,
1999). However,
within-population variation in individual willingness to mate has yet to be
quantified. Second, do females alter their willingness to mate as they
encounter and sample males of different sizes? In other words, do interactions
with different-sized males influence subsequent female responses and thus the
outcome of the conflict over mating?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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We collected flies as larvae from South Landing, Flamborough Head, Humberside, UK, in August 1996. Adult virgin males and females were aspirated from population cages twice daily during the eclosion period and immediately sexed under CO2 anesthesia. Females were isolated from males for 2 days at 26°C, with cellulose wadding soaked in 0.5% mannitol solution as a food source. While still anesthetized, we measured each male for left wing length (the standard measure of body size for C. frigida; Butlin, 1983
), and assigned him
to one of three size classes (large, medium, or small). The classes were
constructed to maximize size differences. Individual males were kept in
isolation for 2 days at 26°C with freshly minced Fucus seaweed.
All subsequent procedures were carried out without anesthesia. After isolation, a female was presented sequentially to a male of each size class in a randomly chosen order. The mating chambers were pervaded with the odor of fresh seaweed, but flies did not have access to the weed. Mate trials were carried out at room temperature (22°-24°C). A female had access to only one male at a time. We scored the outcome of the first mount, defined as the male mounted on the female for >5 s (to exclude mount attempts when males did not fully mount) with each of the three males as either a successful female rejection (ending in the male being displaced from the female), or a copulation (genitalia engaged), termed an "acceptance." We calculated acceptance rates as the proportion of trials in which females copulated. One trial in which male rejection occurred was not included in the analysis. Copulations were allowed to proceed to completion (male genitalia fully disengaged) before the female was removed for presentation to the next male. Females could only copulate once per male, and each male was used with only one female. In total, 86 females were presented to males of all three size classes; an additional 15 females were presented to one or two of the three classes (but these trials have been excluded from analyses involving mating order).
We analyzed the effects of male size class and order of presentation by log-linear analysis, with a multinomial data distribution, using SPSS 7. Because each female was used to produce three data points, we needed to take this non-independence into account. SPSS has two options for the underlying distribution of data for a log-linear analysis. These are either a Poisson distribution or a multinomial distribution. If data cells are not fully independent, then the latter should be used. Other statistics were calculated by either SPSS 7 or Statview 5.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The mean wing lengths of males in the three size classes were very distinct (mean ± SE; large males: 5.38 ± 0.02 mm; medium males: 4.77 ± 0.02 mm; small males: 4.13 ± 0.02 mm; ANOVA: F2,279 = 840.7, p <<.001). Mean wing length of females was 4.77 ± 0.04 mm. The overall female acceptance rate was 34.6%, and female acceptance rates did not differ between the first, second, and third mounts (log-linear analysis:
22 = 1.04,
p =.59; range 30.2-36.5% acceptance). The probability of a male
mating was therefore independent of temporal order. However, females differed
in the number of copulations performed, with some females avoiding copulation
and others mating with all three males. Using the overall mean acceptance rate
as an expected willingness of females to mate, we could examine whether there
is heterogeneity between females in the number of males accepted, calculating
expected numbers of females with 0, 1, 2, or 3 copulations from a binomial
expansion (Figure 1). There was
significant heterogeneity between females (chi-square test:
22 = 7.98, p <.05), which was not
associated with female body size (ANOVA: F3,83 = 1.09,
p =.36). More females than expected did not mate, and fewer females
than expected mated only once.
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Female acceptance rates differed between the three male size classes
(log-linear analysis: 22 = 29.5, p
<<.001; Figure 2a): large
males were more often accepted than medium males, who in turn had greater
mating success than small males. Within each male size class, there were no
differences in size between successful and unsuccessful males (nested ANOVA:
F3,275 = 0.9, p =.44), probably a consequence of
the range of sizes within each category. Females who mated twice were more
likely to mate with large and medium males than with large and small or medium
and small males (G test: G2 = 43.6, p
<<.001; Figure 2b), whereas
females who mated only once were more likely to mate with larger males
(G2 = 11.3, p =.004;
Figure 2c). However, three
females mated only with a small male.
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If female behavior changes with respect to the male phenotypes previously
encountered, we expect a significant interaction between the effects of order
and male size class; however, there was no such interaction (log-linear
analysis: 42 = 5.6, p =.23). This lack of
interaction indicates that male success is unaffected by female experience and
that variation between females in the number of copulations performed is not
associated with the order in which males of differing sizes are
encountered.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The processes of information gathering and decision making are central to sexual selection by active mate choice. How information is gathered and then used in mate choice can influence the outcome of sexual selection by female choice (Seger, 1985
;
Zuk et al., 1990). In
addition, individual differences in mate sampling and mate preferences lead to
variation in the strength and direction of sexual selection
(Andersson, 1994;
Jennions and Petrie, 1997;
Widemo and Saether, 1999). We
suggest that similar considerations are needed in systems without active mate
choice, such as when choice is the result of sexual conflict over mating.
Conflict-driven sexual selection may also vary if females alter their behavior
in response to the particular males they meet.
From the results reported here, it is clear that male mating success in
seaweed flies is unaffected by the phenotypes of males previously encountered
by females and that variation in overall female willingness to mate is
similarly independent of the sequence in which males of different sizes are
encountered. The information gathered by females during previous encounters
therefore does not influence subsequent interactions. The mating system and
the sexual conflict over mating effectively create a situation analogous to
sequential search with a fixed acceptance threshold. There has been much
discussion of how to study sampling strategies empirically in species with
active mate choice (Reid and Stamps,
1997; Valone et al.,
1996; Wiegmann et al.,
1996); it is important to extend this work to species in which
there are sexual conflicts over mating.
Although we used only three size classes, we can begin to consider the
decision-making process and the shape of the female preference function in
seaweed flies. Generally, the pattern of high to low mating success across the
three size classes was consistent among females, with females who mated once
or twice generally mating with the larger two size classes. These data are
consistent with the preference function being a continuous relationship with
male size, which is perhaps what we would expect given the nature of the
sexual conflict over mating in this species. However, further work will be
necessary to fully describe individual preference functions. For instance, the
importance of certain individuals, albeit few of them, mating only with small
males needs to be considered. Such data highlight the importance of examining
preference functions at both the individual and the population level
(Arnold, 1983;
Wagner, 1998). There was also
individual heterogeneity in females' willingness to mate, with an excess of
females who did not mate at all, and fewer females than expected who mated
only once. Thus far, female receptivity in this species has only been examined
as a population phenomenon, and individual variation has not been quantified.
Our data suggest that similar experimental techniques could be used to further
examine individual female mating propensity, allowing a more informative
genetic analysis of mating behavior.
Coelopa has been well studied in terms of the variation in
strength and direction of sexual selection on male size (reviewed by
Day and Gilburn, 1997). Much
of this work was carried out using single mounts in which virgin males and
females were paired once and scored for either acceptance or female rejection
(e.g., Gilburn et al., 1992).
Variation between populations was evident, but individual variation was not
examined. Recent work has revealed that multiple interactions between pairs of
males and females yield consistent mating interactions and repeatable mount
outcomes (Shuker and Day,
2001). The results described here extend our understanding of
multiple mating interactions by showing that the nonrandom mating produced by
the sexual conflict over mating is independent of the order in which females
encounter males of differing body size.
The importance of sexual conflicts over mating as a template for sexual
selection, especially among insects, is becoming clear (e.g.,
Brown et al., 1997;
Crean and Gilburn, 1998;
Rowe et al., 1994). This is
the first time that the order in which males are encountered has been examined
in a system based on sexual conflict. It is important for such systems to be
considered in similar ways to more traditional mate-choice scenarios.
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ACKNOWLEDGEMENTS |
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We thank Caroline Crean, André Gilburn, Lisa Hodgkinson, and Ray Wilcockson for their help and assistance. Allen Moore and Richard Preziosi provided may helpful comments on the manuscript, as did Innes Cuthill and two anonymous referees. D.M.S. was supported by a University of Nottingham Studentship.
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