Behavioral Ecology Vol. 13 No. 2: 254-259
© 2002 International Society for Behavioral Ecology
Size-dependent discrimination of mating partners in the simultaneous hermaphroditic cestode Schistocephalus solidus
a Abteilung Verhaltensökologie, Zoologisches Institut, Universität Bern, 3032 Hinterkappelen, Switzerland b Abteilung Evolutionsökologie, Max-Planck-Institut für Limnologie, 24306 Plön, Germany c Institute of Animal, Cell and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, Scotland, UK
Address correspondence to A. Lüscher at Abteilung Evolutionsökologie, Max-Planck-Institut für Limnologie, 24306 Plön, Germany. E-mail: luescher{at}mpil-ploen.mpg.de .
Received 9 January 2001; revised 14 May 2001; accepted 30 May 2001.
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ABSTRACT |
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The cestode Schistocephalus solidus is a simultaneous hermaphrodite that reproduces in the gut of birds, or for this study in an in vitro system that simulates the gut of the bird. Like many other helminth parasites, S. solidus can reproduce by self- and cross-fertilization. Hermaphrodites are expected to mate not primarily to get their own eggs fertilized, but rather to get the opportunity to fertilize a partner's eggs. Because S. solidus has a size-dependent sex allocation (i.e., larger worms are more biased toward female allocation and produce more egg mass), we expect larger individuals to be attractive mating partners for smaller ones. However, this may be a one-directional preference, as smaller individuals may not be attractive to larger ones. We tested this experimentally by studying the reaction of focal worms of different sizes to a compartment containing a potential mating partner that was either smaller or larger than the focal worm. The focal worms were, on average, closer to the compartment containing the stimulus than to an empty control compartment. Moreover, they indeed showed a preference for larger stimulus worms than for smaller ones. They even tended to avoid being close to stimulus worms of very small size compared to themselves. This may reveal a general preference for cross-fertilization over selfing, but it also indicates that all the genetic benefits from outcrossing do not necessarily outweigh the costs of mating with a relatively small individual and that the worms may take this into account in their reproductive decisions.
Key words: cross-fertilization, hermaphrodite's dilemma, inbreeding avoidance, Schistocephalus solidus, self-fertilization, simultaneous hermaphroditism, size-dependent preference, two-player games.
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INTRODUCTION |
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In hermaphrodites as well as in species with separate sexes, the fecundity of the female function is normally limited by the amount of energy available for egg production, and the fecundity of the male function is normally limited by the number of eggs available (Bateman, 1948
; Charnov,
1979). Therefore, simultaneous hermaphrodites are expected to mate
not primarily to get their own eggs fertilized, but rather to get the
opportunity to fertilize a partner's eggs. If two hermaphrodites meet for
reproduction, they are normally expected to be in a conflict over who is
allowed to give how much sperm (e.g.,
Dugatkin and Reeve, 1998;
Fischer, 1980;
Leonard, 1990;
Michiels, 1998). Because of
this kind of social dilemma, simultaneous hermaphrodites are expected to be
choosy about who they mate with (Michiels,
1998), especially when individuals vary in quality (e.g.,
fecundity), copulations are costly, and mate choice is possible due to high
density (Ridley, 1983).
For a number of cestode species, multiple infection in the final host
results in multiple mating between the individual parasites
(Nollen, 1983). Moreover, many
parasite helminths are not completely outbreeding when given the opportunity.
Often, some of the sperm they collect in their receptaculum seminis are their
own, indicating some selfing even in the presence of a potential mate (Nollen,
1983,
1997;
Trouvé et al., 1996).
Apart from this, however, not much is known about the potential of cestodes
for mate-choice decisions. This is surprising because hermaphroditic cestodes
may face social dilemma situations
(Leonard, 1990) that are
probably easier to specify than in other systems
(Dugatkin and Reeve, 1998).
Their mate-choice decisions and any phenotypic plasticity in egg production
may reveal evolved solutions to two-player or multiplayer nonzero-sum games
(Colman, 1995;
Leonard, 1990). Moreover, the
techniques to study cestodes in in vitro systems that replace their
final hosts are often well developed and tested.
The tapeworm Schistocephalus solidus is a simultaneous
hermaphrodite that is able to reproduce by selfing and cross-fertilization
(Clarke, 1954). Its entire
reproduction (i.e., sperm and egg production, mating, and egg release) lasts
only few days and takes place in the gut of birds shortly after infection
(Clarke, 1954;
Schärer and Wedekind,
1999). Birds get infected by eating infected sticklebacks
(Gasterosteus aculeatus), which get the parasite by eating infected
copepods (a three-host cycle that includes two intermediate hosts). Reported
percentages of infected sticklebacks are often high, sometimes up to 100%
(Abildgaard, 1790;
Dick, 1816;
Hickey and Harris, 1948;
Hopkins and Smyth, 1951;
Jääskeläinen,
1921; Pallas,
1761; Smyth, 1947;
Vik, 1954). Infected
stickle-backs often contain more than one plerocercoid (cestode larvae), and
the total parasite weight can even exceed the fish net weight
(Smyth, 1994;
Vik, 1954; Wedekind,
unpublished data). Worm growth is positively correlated with fish size at
infection (Schärer et al.,
2001); in other words, worm size is largely conditionally
determined. Adult worm weight ranges from around 50 mg
(Tierney and Crompton, 1992)
up to at least 1029 mg (Wedekind, personal observation). In birds, up to 300
adult worms per individual host have been observed
(Nybelin, 1919;
Pallas, 1761;
Vik, 1954).
The in vitro technique that replaces the final host has been
established by Smyth (1954)
and was modified by Wedekind
(1997) and Schärer and
Wedekind (1999). S.
solidus is therefore a potential model for the study of evolved solutions
to social dilemmas that can be experimentally specified
(Wedekind et al., 1998).
Female fecundity of S. solidus is positively correlated with body
size (Schärer and Wedekind,
1999; Wedekind et al.,
1998), as it is in many invertebrates
(Coadwell and Ward, 1982;
Greenspan, 1980). Moreover,
sex allocation in S. solidus is size dependent: larger worms are more
biased toward female allocation
(Schärer et al., 2001).
Therefore, larger worms are expected to be very attractive mating partners to
smaller ones (i.e., sperm donors are expected to prefer matings with high
fecundity sperm acceptors).
In mate choice experiments, two stimulus animals who differ in a trait the experimenter is interested in are normally offered to a focal animal who is then allowed to choose. This method has a general problem that is often neglected: it cannot distinguish between a potential attraction of the focal animal toward one stimulus individual and a potential avoidance of the other one. To disentangle attraction and avoidance, we presented only one stimulus animal to each focal individual. This allowed us to test (1) whether S. solidus is able to locate and actively move toward a potential mating partner, and (2) the prediction that, given the choice between no partner and a potential mating partner, relatively larger stimulus worms are more attractive than smaller ones.
There are a number of potential benefits for outbreeding as compared to
selfing in S. solidus. Selfing is an extreme form of inbreeding that
normally causes a fitness reduction through inbreeding depression and a
general reduction of heterozygosity and of genetic diversity in the offspring
(Charlesworth and Charlesworth,
1987). Genetic diversity among the offspring can be very
advantageous in parasite—host interactions
(Baer and Schmid Hempel, 1999).
Wedekind and Rüetschi
(2000) have used S.
solidus and its first intermediate host as a model to experimentally test
the effect of genetic diversity among the parasites in a multiple exposure.
They found that copepods are more susceptible to infection when exposed to a
genetically more heterogeneous set of parasites than to a more homogeneous set
(i.e., increased genetic diversity among the offspring offers an advantage
against the defense of the first intermediate host). We therefore expect
cross-fertilization to be generally preferred over self-fertilization in
S. solidus. However, when the potential mating partner is smaller
than the focal worm, the focal worm is expected to weigh the benefits of
outcrossing with the disadvantage of mating with a smaller mate. We studied
the reaction of focal worms of different sizes to a compartment containing a
potential mating partner that is either smaller or larger than the focal
worm.
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METHODS |
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The plerocercoids came from sticklebacks that had been infected naturally, but under controlled conditions (methods described in Wedekind and Milinski, 1996
),
and had been kept in the laboratory for about 8-12 months. To obtain the
worms, the fish were killed by a cerebrospinal cut and the plerocercoids were
removed aseptically from the stickleback. Each fish contained one to four
plerocercoids. The worms were weighed on a balance to the nearest milligram
and kept in cell culture medium at room temperature for a maximum of 4 h. This
culture medium consisted of sterilized minimum essential medium with Earle's
salts, L-glutamine, 25 mM HEPES buffer (Sigma) and additives (per liter of
medium: 1 ml penicillin/streptomycin, 6.5 g D-glucose), and had been titrated
with NaOH to a pH of 7.5. We used fork-shaped, nylon mesh bags (200 µm mesh size) that consisted of three compartments for the preference tests. The three compartments were separated by seams and were folded in a way that allowed the focal worm in the middle compartment to position itself right above the stimulus worm, without the two worms touching each other (Figure 1). The mesh bags had been watered for at least 4 days before sterilization and use.
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Pairs of focal and stimulus worms came from different donor fish. Moreover, because we had been keeping different family lines of S. solidus over several generations in the laboratory, the pairs of focal and stimulus worms were chosen from different family lines [i.e., they belonged to the same original population (a pond near Bochum, Germany) but had different parents and different grandparents].
In 7 of the 45 original experimental pairs, the pH dropped below the tolerance level (as indicated by the color of the pH indicator), and the worms died before the end of the experiment. In two other cases, the focal worm entangled itself in the seam of the nylon net and was therefore not able to change position from this moment on. Neither the mean weight nor the weight ratio of these nine pairs were significantly different from the remaining sample (weight: t = -0.41, p =.69; weight ratio: t = -1.17, p = 0.25). These nine pairs were excluded from all further analyses.
In 20 of the 36 experimental pairs, we chose a focal worm that was heavier than the stimulus worm. In the remaining pairs the focal worms was lighter. We randomly assigned the worms to these two experimental groups. The average weight and the average weight difference among the two groups was similar (focus worm heavier than stimulus worm: mean weight ± SE = 411.40 ± 27.5 mg, mean weight difference = 123.10 ± 17.66 mg; focus worm lighter than stimulus: mean weight = 448.60 ± 37.42 mg, mean weight difference = 132.25 ± 19.35 mg; t tests: t < 0.82, p >.4). Overall, focal worm weights (µ = 432.75 ± 23.77 mg) did not differ significantly from stimulus worm weights (µ = 423.14 ± 27.52 mg; t = 0.264, p =.79).
We placed the focal worm in the middle prong of the nylon mesh bag, and the stimulus worm was placed at random in one of the two side prongs. All three openings of the bag were then closed by melting the ends of the nylon layers with a lighter.
One bag with a stimulus and a focal worm each was placed in a translucent
glass container, which was then filled with 400 ml culture medium. After
covering the containers with a lid, they were placed into a water bath at
40°C. We then continuously recorded the focal worm's behavior with a video
camera for 5 days. Previous studies have shown that within 5 days of
incubation at 40°C, worms have produced 95% of their total egg mass
(Schärer and Wedekind,
1999).
The culture medium in the glass containers was exchanged every 2 days. This was done with prewarmed medium without taking the containers out of the water (i.e., the worms remained in a constant temperature environment during the whole experiment).
For data analysis, five sections in the fork-shaped nylon bag were defined a priori and arbitrary scores were given (Figure 1). We determined the position of the head of the focal worm after every 1-h sequence of film. From these scores, the mean position and a measure of daily activity could be determined. We defined daily activity as total number of changes of sections within the 24 observations per day. The weight ratio of each worm pair was computed as focal worm weight divided by stimulus worm weight. This weight ratio ranged from 0.52 to 2.08.
The data were analyzed with the JMP IN 3.2.1. statistics package
(Sall and Lehman, 1996). We
used parametric statistics after data plots indicated that the assumptions of
such statistics were not violated. Directed statistics
(Rice and Gaines, 1994) were
performed when clear a priori predictions about the direction of the effects
existed.
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RESULTS |
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Overall, the focal worms showed on average a preference for the side that contained the stimulus worm (t = 2.16, n = 36, p =.02, directed, Figure 2a). Focal worms that were smaller than the stimulus worm showed a stronger preference for the side of the stimulus worm than relatively larger focal worms (one-way ANOVA with repeated measurement, using Huynh-Feldt correction: effect of treatment group: F = 3.45, df = 1, p <.05, directed). The mean positions did not differ significantly between the days of observation (effect of day: F = 1.31, df = 4, p =.19), nor was the interaction between treatment group and day significant (F = 1.16, df = 4, p =.33; Figure 2a).
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The weight of the focal worms did not significantly influence their behavior in the test apparatus (Figure 3a,c). However, the effect of our experimental treatment was confirmed by the finding that the actual weight ratio (focal worm weight divided by stimulus worm weight) influenced the preference of the focal worms in the experimental setup (Figure 3b). This effect could not be explained by mere differences in the absolute weight of pairs (partial correlation coefficient, controlling for absolute weight of pairs, rxy.z =.347, p =.03, directed).
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To test whether the threshold for focal worms to either approach or withdraw from a stimulus worm is different from equal-weight level, the origin in Figure 3b was set to the mean position 0 and the weight ratio 1. The intercept of the regression line was then positive (0.357) and significantly different from this new origin (t = 2.821, p =.008). This suggests that the focal worms have a preference for outcrossing even if the offered mating partner was a bit smaller than the focal worm itself. The regression line drops below the mean position of 0 at a weight ratio of about 1.5.
Focal worms that were smaller than their respective stimulus worm were less active in the experimental setup (repeated-measures ANOVA using Huynh-Feldt correction; effect of treatment group: F = 8.70, df = 1, p =.006, two-tailed; Figure 2b). Again, the more detailed analysis using the actual weight ratios confirmed this result (Figure 3d). The absolute weight of worm pairs would not explain this result (partial correlation coefficient, controlling for weight of pairs, rxy.z =.334, p =.05, two-tailed). The mean number of section changes of the two groups of focal worms was significantly different between days (repeated-measures ANOVA; effect of day: F = 9.03, df = 4, p < 0.0001, two-tailed; Figure 2b). The focal worms appeared to be increasing their activity from day 1 to day 2 and decreasing it thereafter. However, there did not seem to be a final resting point during the 5 days of observation. The two experimental groups did not differ significantly with respect to time (interaction treatment group x day: F = 0.99, df = 4, p =.42, two-tailed).
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DISCUSSION |
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Darwin (1871
) assumed that
intersexual selection would not occur in hermaphroditic species because the
two sexes are combined in one individual. This assumption has been disproved
by Bateman (1948), Charnov
(1979), Morgan
(1994), and Michiels
(1998). Sexual selection can
be present in hermaphrodites, although it is generally agreed to be weaker
than in species with separate sexes
(Greeff and Michiels, 1999a).
There may be several reasons for this. The most important one is that if two
sexes are combined in one individual, selection on one sex function cannot be
independent of the other one (Charnov,
1979; Greeff and Michiels,
1999a; Morgan,
1994). Another reason is the often limited access to mating
partners in hermaphrodites due to sessile life forms or low population
densities (Charnov, 1979;
Morgan, 1994), or severe sperm
competition and sperm digestion (Greeff
and Michiels, 1999b). These confounding effects could be the
reason that several empirical studies in the past have failed to detect mate
choice in simultaneous hermaphrodite species
(Baur et al., 1998;
Peters and Michiels, 1996;
Trouvé and Coustau,
1999). One exception was the study by Vreys and Michiels
(1997), which demonstrated
mate choice in the hermaphroditic flatworm Dugesia gonocephala. This
flatworm cannot reproduce by selfing, in contrast to S. solidus.
Greeff and Michiels (1999a)
have shown that sexual selection is expected to be even weaker in
hermaphrodites that do not necessarily need a partner to reproduce.
Nevertheless, we found that S. solidus responds differently to
potential mating partners and that this response depends on the size
differences between the two worms.
A sexual conflict arises when the interests of the mating partners do not
coincide. Hermaphroditic individuals are normally assumed to have a preferred
sexual role. Therefore, the mating of two hermaphrodites can often be seen as
a conflict that may lead to a dilemma situation. Leonard
(1990) called it "the
hermaphrodite's dilemma," which summarizes several nonzero-sum games
that are each defined by the payoff matrices of the two actors. The
evolutionarily stable strategy to such games may sometimes be a mating system
based on reciprocity with occasional attempts of cheating in the preferred
role (Axelrod and Hamilton,
1981; Leonard,
1990,
1999). Reciprocity can be
achieved through either egg or sperm trading depending on the preferred sexual
role and has been found for several taxa (egg trading:
Fischer, 1984;
Petersen, 1995;
Sella et al., 1997;
Sella and Lorenzi, 2000; sperm
trading: Leonard and Lukowiak,
1984; Michiels and Bakovski,
2000; Vreys and Michiels,
1998). S. solidus does not have any structures for sperm
digestion. The female reproductive success is, in contrast to the male
function in this species, constrained by size
(Schärer et al., 2001;
Schärer and Wedekind,
1999; Wedekind et al.,
1998), and the reproductive output of the male function seems
restricted only by the number of available eggs (Schärer and Wedekind,
unpublished results). This suggests that the male role is, in general, the
preferred sexual role in S. solidus. Mate avoidance is therefore
likely to be explained by a strategic decision related to the female
function.
A large worm has much egg mass to offer but will get only little in return
if it mates with a small worm. There are good reasons that S. solidus
is expected to weigh outbreeding against the number of offspring and the
degree of relationship to these offspring. On one hand, Wedekind et al.
(1998) observed a better
hatching rate in eggs of paired worms than in selfed eggs, and Wedekind and
Rüetschi (2000) found
that genetical heterogeneous progeny (that would result from outcrossing) can
infect a broader range of hosts and have, overall, higher fitness. On the
other hand, selfing reduces the costs of mating
(Schärer and Wedekind,
1999) and increases the degree of relatedness between parent and
offspring. Moreover, inbreeding depression is expected to be less severe in
species with frequent selfing than in obligate outbreeders (due to purging;
see Charlesworth and Charlesworth,
1987).
We found evidence for the kind of one-directional preference that could be predicted from an asymmetry of payoffs: Focal worms preferred to be near large stimulus worms rather than small ones. Furthermore, worms that were offered a relatively small stimulus worm spent more time moving around than those that were offered a large worm.
Our findings also demonstrate that communication takes place between
individual S. solidus and that it is based on tactile and/or chemical
cues. Pheromonal mate attraction has been suggested for other helminth
parasites (e.g., Fried et al.
1980; Imperia et al.,
1980; Miller and Dunagan,
1985). This leads to an alternative potential explanation of our
results that needs to be considered. Greeff and Michiels
(1999a) showed that
hermaphrodites should not invest too much in mate finding, but rather exploit
mate finding of other conspecifics, thus saving their own resources. In our
study species, large individuals probably produce more metabolic signals than
small ones, and therefore large worms could play a sit-and-wait-to-be-found
strategy. However, Greeff and Michiels' model is based on substantial costs of
mate finding. Mate finding is probably not very costly in S. solidus
because adults of this parasite must constantly counteract the movement of the
gut, as this species has no adhesive structure (hocks or suckers) to attach to
the gut tissue. Moreover, S. solidus has been found in high numbers
compacted in the lower intestine of bird hosts
(Vik, 1954). Moreover, Greeff
and Michiels' (1999a) model
predicts that worms that produce more pheromones play a more passive role in
mate finding than others. We cannot find any evidence for this prediction in
our study species, as the number of section changes of focal worms did not
correlate with the worms' weight.
The worms who seemed to avoid a potential mate either waited for a better
opportunity or started to reproduce by selfing. Schärer and Wedekind
(1999) tested whether S.
solidus waits for a partner if isolated. They found no difference in the
start of egg release between paired and isolated worms. After the start of egg
release, isolated worms shed eggs at an even faster rate than paired worms
(Schärer and Wedekind,
1999). For S. solidus, waiting in the final host is
assumed to be costly because constantly counteracting the movements of the gut
is probably quite energetically demanding. Therefore, while waiting,
individuals probably use energy they could otherwise allocate to reproduction.
This may be the main reason that waiting does not seem to be an option that
adult S. solidus play. The behavior we observed in the present study
indicates that S. solidus even prefers selfing over
cross-fertilization if their potential mating partner is much smaller than
they are.
There are at least two approaches that can be used to investigate the
advantages of outbreeding. First, one can measure the fitness of different
types of progeny, as done by Wedekind and Rüetschi
(2000) for the present system.
Second, one can measure the advantages of outbreeding by studying the
decisions that parents make about their reproduction, assuming that these
decisions are evolved under natural selection. The size-related behavior of
focal worms, as we observed it here, indicates that outbreeding is not always
the preferred way of reproduction. It could reflect the intention of S.
solidus to outcross depending on how much the enclosed partner can offer
in terms of egg mass, with the preference to outcross becoming stronger the
more foreign eggs could potentially be fertilized relative to own egg mass. We
observed a kind of switching point (i.e., a switch from a general tendency of
preferring to be near the stimulus worm toward a general tendency of avoiding
the stimulus worm) when the focal worm was about 1.5 times heavier than the
stimulus worm. However, this first quantitative result has to be interpreted
with care because it is possible that our experimental setup and the in
vitro system may not adequately reflect the natural situation in all
respects (e.g., movement, volume, and composition of the medium). The in
vitro system may yield different values for an optimal
inbreeding/outbreeding ratio (i.e., for a cutpoint where selfing wins over
outcrossing) than an in vivo system. Moreover, mean positions of
focal worms are only a first approximation of mate preferences.
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ACKNOWLEDGEMENTS |
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We thank Nathalie Treichel, Julian Rauch, and Rolf Eggler for technical assistance, A. Bourke and two anonymous reviewers for helpful comments on the manuscript, and the Swiss National Science Foundation for support. C.W. is supported by an IHP fellowship of the Swiss National Science Foundation.
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