Behavioral Ecology Vol. 11 No. 3: 260-264
© 2000 International Society for Behavioral Ecology
Partner fidelity and egg reciprocation in the simultaneously hermaphroditic polychaete worm Ophryotrocha diadema
a Department of Animal and Human Biology, University of Turin, via Accademia Albertina 17, 10123 Torino, Italy b Department of Veterinary Morphophysiology, University of Turin, viale Mattioli 25, 10125 Torino, Italy
Address correspondence to G. Sella. E-mail: sella{at}dm.unito.it .
Received 21 July 1998; revised 11 June 1999; accepted 21 July 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The mating system of the simultaneously hermaphroditic polychaete worm Ophryotrocha diadema consists of a regular egg exchange between partners of a pair. Such reciprocal egg exchange has been considered a form of cooperation, where one partner cooperates by offering its eggs to be fertilized and expects to receive partner's eggs to fertilize. Frequency of cases in which hermaphrodites cheated (i.e., failed to give up eggs at their turn) and responses to cheating were estimated by analyzing the behavior of 38 triplets of ovigerous hermaphrodites over a 2-week period. The partner did not reciprocate 8% of egg layings. The cheated partner did not detect most cases of cheating (16 out of 25). Such a low frequency of cheating can explain why no retaliation mechanism evolved in this species. Sixty-eight percent of the individuals from the original pairs deserted even if their partners never cheated them; therefore, cheating cannot be considered the cause of desertion. Rather, desertion appeared to be a consequence of availability of a new partner whose oocytes were riper than those of the old partner. It occurred because the opportunity arose for an immediate reward, indicating that O. diadema egg exchange differs from that originally described in some serranid fish as egg trading. The relationship between costs of desertion and population size is discussed.
Key words: cheating, cooperation, desertion, egg reciprocation, Ophryotrocha diadema, Polychaeta, simultaneous hermaphroditism.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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It is generally assumed that there is a conflict of interests between sexual partners, as different selective pressures are associated with reproduction through eggs and reproduction through sperm, according to Bateman's (1948
) principle.
Reproductive success of females is limited by the availability of egg
production resources, while male reproductive success is determined by
availability of females.
In simultaneous hermaphrodites, both male and female roles are present in
the same individual. Therefore, if present, sexual conflict is directly
experienced by the same individual. If the male role is less costly in terms
of energy expenditure, mating time, and so on, then all the hermaphroditic
individuals of a population should prefer this role. When a pair is formed,
partners of that pair should compete for the preferred sexual role. According
to Leonard's (1990,
1991) hermaphrodite dilemma
hypothesis, the best strategy to solve this conflict should be based on
reciprocation in assuming both sexual roles during a mating encounter and a
low level of cheating in the preferred sexual role. The Leonard model suggests
that mechanisms should exist to prevent or to punish cheaters.
Some pair mating, externally fertilizing, simultaneously hermaphroditic
serranid fish (reviewed by Fischer and Petersen,
1987) have resolved the
conflict for the preferred role by evolving a very peculiar mating system
called egg trading (Fischer,
1980). A similar mating system
was also described by Sella
(1985) and Sella et al.
(1997) in the simultaneously
hermaphroditic polychaete worms Ophryotrocha diadema and O.
gracilis. Egg trading consists of reciprocal egg fertilization by regular
alternation of sexual roles within the mating pair. By means of such a
reciprocal egg exchange, each individual fertilizes as many eggs as it lays.
The egg-trading mechanism, however, severely restricts the potential
advantages of the male role: an individual cannot fertilize more cocoons than
it releases.
In this mating system reciprocity in egg exchange is not simultaneous; it
is delayed and therefore open to the risk of cheating by nonreciprocating
partners (Axelrod and Hamilton,
1981; Trivers,
1971). A nonreciprocating partner is expected to prefer the male
role because sperm are cheaper to produce than eggs, and egg laying entails
some costs (e.g., in O. diadema, histolysis and production of the
mucous cocoon). Upon receiving a clutch of eggs to fertilize, a cheater should
offer no eggs in return; in other words, it will try to play the male role
instead of the female role.
Some aspects of the mating system of O. diadema
(Premoli and Sella, 1995;
Sella, 1988) and O.
gracilis (Sella et al.,
1997) could be considered mechanisms that have evolved to reduce
vulnerability to cheating. First, at any reproductive bout, one of the
partners lays all its mature eggs. A clutch contains a few eggs and is laid
approximately 2 days after each clutch laid by the other partner
(Premoli and Sella, 1995). In
contrast to serranid fish, which parcel available eggs, in O. diadema
and O. gracilis no eggs are saved for successive matings because each
clutch contains all the ripe eggs an individual has in its coelom. This,
however, might be considered a sort of temporal parceling of ripe eggs. In
this way the cheated egg donor will detect a nonreciprocating partner and
eventually desert it to cut its losses.
Second, in isolated pairs made up of an ovigerous hermaphrodite and an
adolescent male (which cannot reciprocate egg exchange), time intervals
between successive egg spawnings by the hermaphroditic partner are
significantly longer than time intervals between successive egg spawnings of a
hermaphrodite paired with another hermaphrodite
(Sella, 1988). It has thus
been inferred, but not demonstrated, that a nonreciprocated hermaphrodite
should have the ability to lower the reproductive success of a
nonreciprocating partner.
Up to now cheating and safeguards that evolved against cheating were
studied in isolated pairs only (Sella,
1988). We do not know how these worms behave in situations in
which multiple partners are available, which leads to the possibility of
deserting a nonreciprocating partner.
The aim of this study was to analyze the reciprocal egg-exchange mechanism in triplets of worms of O. diadema to determine (1) how stable the pair bond is, (2) whether cheaters (i.e., individuals that play the male role instead of the female role) are present, and (3) how cheated individuals respond when they detect cheating. Moreover, we checked whether nonreciprocated individuals respond by deserting their partner. If this was not the case, we investigated the possible causes of desertion.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study animals
Populations of O. diadema were found among the fouling fauna of California harbors by
kesson
(1976) and D.J. Reish (personal
communication). According to Reish (personal communication), such populations
are at low density (1 animal per 300 m2 of surface of fouling
mussels). However, adults produce a network of mucous trails that can be
followed by conspecifics, and thus the spatial distribution of animals is
probably clumped. Because adults are 4-5 mm long (14-21 setigerous segments)
and live in a heterogeneous environment, their behavior cannot be studied in
natural conditions. All the O. diadema life cycle data
(kesson,
1976,
1982) and the main features of
its mating system (Premoli and Sella, 1995a; Sella,
1985,
1988, 1990,
1991) have been obtained
through laboratory observations. A brief male phase precedes the
simultaneously hermaphroditic phase, but pairs are formed preferentially
between simultaneous hermaphrodites. Courtship is on the average 4.5 h long.
By mutual rubbing during courtship display, both partners acquire information
on the degree of their egg maturation. Mating is achieved by pseudocopulation,
a process of external fertilization in which partners maintain a close
physical association before their synchronous release of gametes. Partners
regularly alternate sexual roles by reciprocally exchanging a cocoon of 20-25
eggs every 48 h on average. Immediately after mating the maternal parent
remains on the egg cocoon. Its mate stays nearby, and therefore both parents
can be easily identified. Parents alternate in egg caring, especially during
the first 3 days after egg laying, then the parental care of embryos
decreases. Cocoon walls are transparent, and egg development can be easily
followed with a stereoscopic microscope. Unfertilized eggs are generally
eaten. At the ninth day after egg laying, offspring are released from the
cocoon as small four-segment individuals, soon ready to produce their first
sperm. When worms reach a body length of 14-15 segments, they become
simultaneous hermaphrodites.
We used individuals of an O. diadema strain derived from
individuals collected by B. kesson in 1976 and
1980 in the Los Angeles and Long Beach harbors. To recognize animals, we took
advantage of a genetically determined polymorphism for a yellow or white egg
color. The yellow coloration is determined by a dominant allele that controls
the presence of lutein in egg vitellum (Y); the white egg color is
due to a recessive allele (y)
(Sella and Marzona, 1983).
Previously we ascertained that individuals homozygous for the yellow egg
allele had the same reproductive rate (i.e., number of eggs/individual/day) as
individuals homozygous for the white egg allele and as heterozygous
individuals.
Experimental design
From the offspring of 38 pairs of YY x yy and 38
pairs of yy x yy individuals, we selected 38
Yy and 38 yy individuals of the same age, body length (15
segments), and degree of egg maturation. With then we set up 38 pairs, each in
a separate 15-ml bowl, each pair consisting of a Yy and a yy
ovigerous and virgin hermaphrodite.
To synchronize pair spawning, strengthen pair bond, and avoid interference of other individuals in establishing the pair bond, each isolated pair was allowed to reciprocate egg exchange four times. This takes an average of 8 days. Then both partners were offered the option of a new partner when a third white-egg ovigerous hermaphrodite (the intruder) of the same age was added. We allowed the triplet of worms to interact for 13 days. In this time interval we could observe the stability of the pair bond. An individual was considered to be a deserter only when, after leaving its previous partner and mating with the intruder, it spawned eggs with the latter.
Yellow or white color of laid eggs allowed us to identify the female parent (which in addition could be identified because after spawning its coelom contains no more mature oocytes). Generally, paternity was assessed by closeness of the male parent to the female parent and egg cocoon. Some doubtful cases of paternity could be solved by rearing progeny to sexual maturity: if white eggs had been fertilized by a yy male, all the progeny was expected to have white eggs; if white eggs had been fertilized by a Yy male, half of the progeny was expected to mature yellow eggs.
We observed and recorded egg reciprocation of worms daily for 13 days; we also recorded body sizes by counting the number of setigerous segments (which also helped us to recognize the two individuals with the same color). Degree of oocyte maturation could be qualitatively assessed through the transparent body walls by looking at the oocyte size. When oocytes are fully mature, they mask the underlying gut.
We measured frequency of cheating of the original partners, response to this behavior, frequency of desertion and of pair fidelity, and individual reproductive success. Reproductive success was measured either as the mean number of cocoons per individual or as the total number of eggs per individual and as the total number of free living larvae per individual produced over the 13-day period. The number of cocoons per individuals is also a measure of the frequency of alternations in sexual roles.
For all statistical comparisons, sample sizes are the maximum number of cases available for a particular data analysis, so that, for example, in Table 1 reproductive success is measured in a subset of the original pairs. Test probabilities reported are two-tailed.
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RESULTS |
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Frequency of cheating
Mean time interval between egg spawnings of a pair when egg exchange was regularly reciprocated was 1.78 ± 1.12 (SD) days, and mean time interval between successive egg spawnings by the same individual was 3.66 ± 1.13 (SD) days. In the 13-day period, 23 out of the original 76 individuals (30%) that we used to form the 38 pairs cheated (i.e., did not lay eggs at their turn) at least once. Failure to supply eggs occurred in 25 out of 313 egg layings (8%).
Response to cheating
In 9 out of the 25 episodes of cheating, partners that did not receive the
expected eggs, waited on average 5 ± 1.41 days for an egg offering from
their partner (i.e., significantly longer than reciprocated individuals,
Student's t = 3.32; df = 102; p <.01), then deserted and
mated with the intruder. This behavior occurred in 9 out of 313 egg exchanges
(2.9%). In the remaining 16 episodes of cheating (performed by 14
individuals), the cheated partners re-released their eggs at a mean time
interval of 3.47 ± 1.12 days. This mean time interval is not
significantly different from the mean time interval between two successive egg
layings by the same individual (3.66 ± 1.13) when reciprocation
occurred regularly (Student's t = 0.944; df = 108; p
>.10). The 14 individuals behaved as if they had not detected defection in
egg reciprocation. Frequency of this behavior (i.e., releasing more than one
parcel without egg reciprocation by its own partner) was 16 out of 313 egg
exchanges (5%).
Frequency and causes of desertion
Among the 26 pairs that "divorced," changes of partners
occurred either once or more than once for a total of 42 times. Only after day
7 was the frequency of pairs in which one of the two partners deserted no
longer significantly different from the frequency expected under the null
hypothesis of random matings. At the end of the experiment the frequency of
divorced pairs was 26 out of 38 (Ho: random matings; G
test; G = 0.099; df = 1; p <.1). In fact, 4 pairs
divorced the day after the addition of the intruder and 12 between days 2 and
6 after the addition. Pair bonds lasted more than 6 days in the other 10 pairs
that later divorced.
In only nine of the divorced pairs had the deserting partner been cheated by its original partner. Therefore, cheating cannot be considered the principal cause of desertion. The following hypotheses to explain desertion were tested:
- Was desertion contingent upon the previous partner's behavior (i.e.,
failure of the partner to give up its eggs)? Under the null hypothesis, among
the deserted partners, individuals that had not reciprocated should be
deserted with the same frequency as those that had reciprocated. In 13 out of
36 cases desertion followed the partner's failure to give up eggs, while in
the remaining 23 cases desertion was not contingent upon failure to be
reciprocated. The hypothesis must be rejected that desertion is a retaliation
against a partner that does not give up its eggs (G test; G
= 2.78; df = 1; p >.10).
- To save energy, a deserting partner who already played the male role should
prefer to play the male role again with its new partner. Out of 28 deserting
individuals, 19 played the male role after desertion, but most of them (13 out
of 19) behaved as females before deserting. Only 6 individuals played the male
role twice. The other 9 played the female role (5 assumed the female role
twice and 4 abandoned the male role for the female role). Contrary to our
expectations, no preference for the male role resulted from our data
(G test; G = 2.62; df = 1, p >.1), but the
sample size is too small to allow us to make a reliable conclusion.
- Although all worms started the experiment with a body size of 15 segments,
growth differences during the experiment gave rise to differences of 1-3
segments in body size. Thus, we checked whether the old mate preferred its new
partner because it had a larger body size at the moment of partner desertion.
In 11 out of 23 cases the new partner had a larger body size; in the remaining
12 cases its body size was smaller than that of the deserted partner.
Therefore, data are consistent with the null hypothesis that worms mated
randomly with respect to body size (G test; G = 0.43; df =
1; p >.1).
- Was the old partner deserted because in egg exchanges before desertion it
gave its partner significantly fewer eggs than it had received? This
hypothesis can be excluded because no significant difference was found between
the mean number of eggs spawned by the deserted partner (60.78 ± 36.13)
and by the deserting partner (66.15 ± 27.49; paired t test;
t = 0.75; df = 26; p >.10).
- Was the intruder preferred by the deserting partner because its oocytes
were riper than those of the old partner? Under the null hypothesis desertion
should occur randomly with respect to egg maturation. Out of 39 intruders, 32
were preferred as mates because they had the ripest oocytes, whereas under the
null hypothesis the expected frequency is 18.5. The observed frequencies are
significantly different from those expected under the null hypothesis
(G test; G = 17.23; df = 1; p <.001).
- Did the intruder routinely check out its options, or did it simply mate
with whichever of the original pair deserted? The expected frequency under the
null hypothesis is 12.5, whereas 19 out of 25 intruders were observed mating
with the partner of the original pair which had the ripest oocytes. The
observed frequencies are significantly different from those expected under the
null hypothesis (G test; G = 6.96; df = 1; p
<.01). We can infer that the new pair was formed between the two worms that
had the ripest oocytes. However, in the first egg spawning of the new pair,
the deserting partner received no more eggs from the intruder (mean = 21.5
± 2.3) than those (mean = 22.9 ± 2.1) it received from its old
partner in its last spawning before divorce.
Twelve pairs were faithful to each other from the very beginning of the experiment to its end and spawned or fertilized their eggs on average 8.7 times. Among them, in seven cases either the intruder's oocytes were less ripe than those of either partner or resorbed; in three cases there was no difference in egg ripeness among the triplet of worms; in two cases the intruders' oocytes varied in degree of maturation during the 13-day observation period.
Reproductive success of deserting and faithful individuals
Estimations of reproductive success of deserting and faithful individuals
over the 13-day period are listed in Table
1. Differences between the three estimates of reproductive success
of individuals that changed partners and individuals that did not are not
statistically significant but would suggest a higher level of fitness in
deserting individuals.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In our laboratory population of O. diadema, approximately 30% of individuals occasionally cheat: about 8% of egg layings are not regularly reciprocated.
kesson
(1976) estimated that in the
maximum fertility phase (corresponding to the first 7 weeks), an average of 28
± 4.2 egg masses per individual are laid. Therefore, in that period,
according to our estimate of the frequency of cheating, an individual runs the
risk of being cheated only about twice. Such a frequency of being cheated does
not seem to be very relevant. In serranid fish cheating reaches a frequency of
20% (Dugatkin and Reeve, 1998),
and cheated individuals delayed the next spawning if their partners failed to
reciprocate. This behavior was considered a sort of punishment, followed by a
forgiving act (Fischer,
1988).
When cheating is present, some form of punishment is expected to evolve
(Leonard, 1990,
1991). Our results, however,
did not show this: most individuals ignored that they had been cheated and
spawned their eggs again without regard for the behavior of their partner.
Probably, because cheating is rare, no selective pressure was exerted for the
evolution of retaliatory behaviors. In O. diadema both the advantages
of cheaters and the losses by cheated individuals are sufficiently reduced by
the fact that eggs are laid frequently and in small-sized cocoons
(Premoli and Sella, 1995). We
advance the hypothesis that, by saving the energy necessary to produce a
clutch of eggs, cheaters may obtain only little gains, for example, in
lifetime expectancy. Probably other factors than punishment keep the selective
pressures for cheating low.
We cannot consider cheating to be the principal cause of desertion, which had the following timing: 42% of pairs divorced within the first week and 26% during the second week. Rather, desertion seems to be correlated with attractiveness of a new partner in terms of egg maturation. By choosing the partner who has the ripest eggs, the deserting partner probably increases its reproductive success because it obtains eggs from the new partner sooner than from the old one. This supposed reproductive advantage could not be measured for two reasons. Either individuals always chose the best between the two available partners, be it the old or the new one, or the short duration of the experiment did not allow us to highlight differences between the reproductive success of stable pairs and divorced pairs. In fish, egg trading is constrained by the necessity of laying all mature eggs within each spawning period to avoid their decay. In contrast, in O. diadema oocytes are preserved from decay because their maturation stops at the end of prophase of the first meiotic division. This frees O. diadema hermaphrodites from the constraint of performing rigorous egg trading and allows them to abandon old partners for new mate, with only minor risks compared to those incurred by egg-trading fish.
Fischer (1988) described
egg trading in serranid fish as a special case of the tit-for-tat strategy
(Axelrod and Hamilton, 1981).
In this context the tit-for-tat strategy would be providing eggs to a partner
(cooperation) unless the partner failed to provide eggs in the previous egg
exchange. In the classical tit-for-tat strategy, rewards for cooperation or
for defection are fixed, while retaliation against defection is expected and
animals should act accordingly without variation or error. However, in O.
diadema retaliation mechanisms have never evolved. According to Stephens
et al. (1995), when
reciprocation by the partner is not certain and when there is the possibility
of choosing between more than one partner, defection can be more profitable
than continuing the game or retaliating.
Cooperation in a tit-for-tat strategy requires that a player recognize its
partner among other individuals and recall the outcome of at least the last
interaction with that partner (Axelrod and
Hamilton, 1981; Dugatkin and
Wilson, 1992). One can imagine that such primitive animals lack
the ability to recognize the individual with which they had the last
interaction, but, according to Axelrod and Hamilton
(1981), partner recognition
could be obtained simply by maintaining close contact. In O. diadema,
when intruders enter the nesting sites of the old pairs, recognition (through
close contact) of the old partner would be interrupted, and individuals would
follow the rule of mating (and establishing bouts of reciprocation) with the
individual that has the ripest oocytes. Our results indicate that 68% of the
tested hermaphrodites deserted their partner due to the opportunity for an
immediate reward. They deserted independently of what their partner had done
in its previous move, contrary to what would be expected under a tit-for-tat
model.
Tit for tat is strictly a two-player game, but animals live in a
population. This means that they have the option of leaving their partners and
seeking better partners. In this case they no longer play tit for tat
(Connor, 1992). According to
the complementarity model (Crowley et al.,
1998), regular exchange of roles can evolve in hermaphrodites when
providing eggs is substantially more costly than providing sperm. Contrary to
tit for tat, the complementarity model does not exclude the possibility of
desertion.
In our experiment we tried to simulate what could happen in a high-density situation where the opportunity for deserting is maximized. An ovigerous hermaphrodite was present in a very small bowl containing a reciprocating pair and so the cost of searching for a new partner was nil. In nature, populations of O. diadema are expected to be at low density. From high-density laboratory populations we know that only about 20% of individuals chosen at random are ovigerous at any time (Sella, 1990). If in natural populations ovigerous hermaphrodites have the same frequency, costs of deserting should be different from 0 even in crowded populations. Then potential benefits of changing partners should be devaluated by the cost of deserting (searching and courtship costs, risks of predation), and benefits from protracted mutual cooperation in reciprocal egg exchange should become larger than benefits of cheating and deserting. Although our study does not give such evidence, we may advance the hypothesis that cooperation in egg-trading persists only as long as the opportunity of pairing with a more attractive partner is lacking.
The results of this study suggest that O. diadema mating system differs in some way from that of serranid fish, which persist in cooperative behavior and stable pair bonds even in high-density conditions. The effect of mating-group size on sex allocation could be analyzed in O. diadema for new insights in this kind of egg exchange.
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ACKNOWLEDGEMENTS |
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This research was supported by funds from the Italian MURST to G.S. We thank Phil Crowley, Professor Allasia, and two anonymous referees for their helpful comments on a previous version of the manuscript.
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FOOTNOTES |
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M. C. Lorenzi is now at the Department of Animal and Human Biology, University of Turin, via Accademia Albertina 17, 10123 Torino, Italy.
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