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The Society for Integrative and Comparative Biology
Bateman's Principle and Simultaneous Hermaphrodites: A Paradox1
1 Joseph M. Long Marine Laboratory, University of California, 100 Shaffer Road, Santa Cruz, California 95060
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Bateman's principle states that reproductive success is limited a) in females by the resources available for egg production; and b) in males, only by access to females and/or eggs. The principle has been used to generate predictions for two aspects of hermaphroditism; a) the advantage of hermaphroditism and b) sexual conflict. Comparing these predictions to the empirical data offers tests of Bateman's principle. Charnov's prediction that hermaphroditism would occur under circumstances where Bateman's principle does not apply is found to be largely correct. However, the prediction as to the association of hermaphroditism and low fixed costs is inconsistent with the data. Alternative explanations that predict that hermaphroditism is a strategy for reducing variance in reproductive success may better explain the data. Probability theory demonstrates that where two strategies have equal mean fitness, which must be the case for male and female function, the strategy with the lower variance in reproductive success must have higher fitness (Gillespie's principle). Bateman's principle predicts that this will be the female role in hermaphrodites. However, Charnov, assuming Bateman's principle, predicted that sexual conflict stemming from a preference for the male role would be important in hermaphrodite mating systems, creating a paradox. Many hermaphrodite mating systems are based on conditional reciprocity with a preferred sexual role indicating sexual conflict. The data demonstrate that the preferred role varies among taxa, contrary to the predictions of Bateman's principle. It has been suggested that Bateman's principle can explain cases in which the female role is preferred (sperm-trading) as involving energy rather than gamete trading. However, energetic considerations suggest that energy trading would only be adaptive if Bateman's principle does not apply, paradoxically. The gamete trading model, based on the prediction that the role that offers control of fertilization will be preferred, is more consistent with the data. Application of Bateman's principle to hermaphrodites leads to contradictory predictions and does not offer the basis for a coherent theory of sexual selection, as Bateman proposed.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONBATEMAN'S PRINCIPLE AND...SEXUAL CONFLICT AND THE...BATEMAN'S PRINCIPLE AND...References |
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Although the sexual behavior and reproductive biology of hermaphroditic organisms have been of interest for as long as biology can be traced, interest in sexual selection and such allied topics as mating systems, mate choice and sexual conflict, in hermaphrodites, is relatively recent. In "The Descent of Man, and Selection in Relation to Sex" Darwin (1871)
explicitly excluded such hermaphrodites as snails and earthworms from the influence of sexual selection, arguing that their intellectual powers were insufficiently developed to allow for mate choice. A. J. Bateman laid the foundation for a more modern understanding of sexual selection in a seminal paper based on experiments on reproductive success in Drosophila melanogaster using genetic markers to estimate paternity (Bateman, 1948). Bateman started with the generally accepted assumptions that "intra-sexual selection almost invariably involves competition between males, the females exercising choice, and not the reverse" (Bateman, 1948, p. 350), and that "a sex difference in variance of fertility is therefore a measure of the sex difference in intensity of selection"(ibid, p. 353). His stated goal was to "search for a fundamental cause of intra-masculine selection ...this same cause should show us why it is a general law that the male is eager for any female, without any discrimination whereas the female chooses the male." The results of his experiments demonstrated that variance in both offspring number and mate number were higher in males than in females (but see Sutherland, 1987 and Fig. 1A) and the correlation between number of mates and number of offspring was stronger in males than in females (Fig. 1). Bateman proposed that the fundamental cause of sexual selection is that, because "...the fertility of the female is limited by egg production ...(ibid, p. 364)," female reproductive success is, in general, restricted by the availability of energy to produce eggs, whereas male reproductive success is usually limited only by access to mates, or their eggs. This statement is what is referred to as Bateman's principle by Charnov (1979) and in the current review (see Table 1). (The definition of Bateman's principle has varied among authors [see other papers in this volume]. For example, Arnold [1994] identified three Bateman's principles: 1) "males show greater variance in number of offspring than do females" (ibid, p. S126); 2) males have higher variance in number of mates than do females; and 3) there is a direct correlation between number of mates and fecundity in males, but in females fecundity increases little after the first mating [for tests of Arnold's version of Bateman's principles see Jones, 2005; Jones et al., 2000, 2002]. Here Arnold's three Bateman's principles are considered assumptions contributing to Bateman's principle.) Bateman concluded that, "The primary cause of intra-masculine selection would thus seem to be that females produce much fewer gametes than males. Consequently there is competition between male gametes for the fertilization of the female gametes" (ibid, p. 365). Bateman (1948) explicitly predicted that, if true, this principle would extend to all anisogamous organisms, including plants and hermaphrodites, saying, "If ...differentiation into ...gametes is the basis ...there should be signs of this selection in plants .... Since plants are usually hermaphroditic ...such selection would only be expected to show in the pollen, (ibid, p. 367)."
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Although the range of phenomena associated with hermaphroditism came under consideration by biologists focusing on selection acting on selfish individuals very early on (Ghiselin, 1969
, 1974; Williams, 1975), the first author to follow up on Bateman's prediction explicitly was Eric Charnov. In a seminal paper, Charnov (1979) began to explore the predictions that Bateman's principle makes for hermaphrodites, saying "I propose here that ‘Bateman's principle’ is also valid for these organisms [simultaneous hermaphrodites]— that fertilized egg production by an individual is limited not by the ability to get sperm, but by resources allocated to eggs. This is a strong assumption .... If it is approximately true, then the theory ... has several important implications for reproductive biology" (ibid, p. 2480). Charnov then went on to explore the implications of Bateman's principle for two major aspects of hermaphroditism; a) the circumstances under which there is an advantage to hermaphroditism over dioecy; and b) the potential for male-female conflict in mating hermaphrodites. A comparison of Charnov's predictions with the data that have accumulated from simultaneous hermaphrodites over the last 25 years offers an opportunity to test Bateman's principle. In the process of testing these predictions, it is useful to compare the performance of Bateman's principle with that of alternative explanations.
Bateman's principle, Gillespie's principle and a paradox
Bateman's principle (Table 1) is a hypothesis founded on data from D. melanogaster. It assumes that males are eager and females "choosy" or "coy" and predicts that reproductive success is limited a) in females by the resources available for egg production; and b) in males, only by access to females and/or eggs. Therefore, variance in reproductive success should be higher in males than in females and the eagerness of males in mating encounters can be explained by the greater "upside potential" (to use a term from economics) available to males. For simultaneous hermaphrodites, Bateman's principle also predicts that the male role will be preferred (Charnov, 1979). However, this creates a clear paradox. It is an axiom of probability and gambling theory that where two games or investments have equal mean return, the game or investment with the lower variance will be a better investment, if capital and/or the length of the game are finite (Epstein, 1977). This is true because choice of the high variance investment will be more likely to lead to bankruptcy (or extinction, in biological terms). Applied to biology this axiom is termed Gillespie's principle (Table 1), which states that where two strategies (or alleles, etc.) have equal mean reproductive success, which must be the case for male and female function across a finite population, the strategy with the lower variance in reproductive success will have higher fitness (Gillespie, 1974, 1977; Leonard, 1999). The sexual role with greater variance will in general have greater "upside potential" (has the greatest potential success) but, also greater "downside potential" (has the greatest potential for failure): the higher the variance, the greater the probability of zero success, and therefore, the higher the probability of zero fitness. Bateman's principle predicts that, all else being equal, that will be the male role. This would not be a problem in an infinite, panmictic population but there is no such thing as an infinite population and the larger a population is, the less likely it is to be panmictic. Application of Gillespie's principle predicts then that a hermaphrodite, faced with two strategies with equal mean success should behave prudently and try to avoid the role with the greater "downside potential" (see Leonard, 1999 for discussion) due to the higher probability of reproductive failure. Therefore, from a mathematical point of view, Charnov's prediction from Bateman's principle is paradoxical in that it predicts that hermaphrodites should prefer the sexual strategy that has greater "upside potential" although, it will yield lower fitness for most individuals due to the greater variance. Application of Gillespie's principle to mating hermaphrodites predicts that hermaphrodites will prefer the role with lower variance in reproductive success (Leonard and Lukowiak, 1991; Leonard, 1999), contrary to the expectation from Bateman's principle. Both Bateman's principle and Gillespie's principle predict that mating hermaphrodites will have a consistently preferred sexual role, creating sexual conflict (see below). Moreover, the two principles suggest alternative explanations of the advantages of hermaphroditism relative to dieocy.
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BATEMAN'S PRINCIPLE AND HERMAPHRODITISM VS. DIOECY |
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The adaptive significance of the ecological and taxonomic distribution of separate sexes (here, dioecy) relative to hermaphroditism has been a recurrent question in evolutionary biology (Table 2; Muller, 1932
; Altenburg, 1934; Ghiselin, 1969, 1974; Williams, 1975; Maynard Smith, 1978; Charnov, 1982 ; Leonard, 1990, 1999; Crowley et al., 1998; Wilson and Harder, 2003; etc.). As H. J. Muller (1932) phrased it "the existence of the two sexes in separate individuals, is of advantage in the same way as any other division of labor.... But in cases where conditions are such that these functions in the same individual would not greatly interfere with one another ... the efficiency may not be increased ... enough to compensate for ... halving the number of individuals giving each type of gamete and in reducing the proportion of contacts which would be of service in fertilization, and so these organisms may have retained or developed hermaphroditism" (ibid, p. 124) (but see Crowley et al., 1998). The problem was formulated graphically by Charnov, et al. (1976; see also Charnov, 1979; Maynard Smith, 1978). These authors pointed out that where fitness through each sexual role increases proportionately to investment in that sexual role, a "concave" fitness curve in Figure 2, separate sexes will be favored, whereas hermaphrodites will have higher fitness when investment in one sexual role does not interfere with fitness in the other sexual role, a ‘convex’ fitness curve (Fig. 2). The question, then, becomes one of determining which factors will produce a convex vs. a concave fitness curve.
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It had long been known that low mobility and low population density would provide an advantage to hermaphroditism (e.g., Muller, 1932
; Tomlinson, 1966; Ghiselin, 1969; see Table 2). Leonard (1999) suggested, based on the Modern Portfolio Theory from economics (first applied to biology by Real, 1980), that by partitioning reproduction between eggs and sperm a hermaphrodite might reduce the covariance in fitness among offspring, thus producing a convex fitness set and increased fitness over either pure males or pure females. In a similar vein Wilson and Harder (2003) developed a formal mathematical model that shows that dioecy produces greater variance in reproductive success for both males and females and thereby reduces mean recruitment, giving an advantage to hermaphroditism. Both of these studies are consistent with Gillespie's principle. In a different vein, Crowley et. al. (1998) found, in a modeling study, that the evolution of simultaneously hermaphroditic strategies was favored by high costs of serial egg production.
Charnov (1979, 1982) explicitly considered the implications of Bateman's principle for the advantage to hermaphroditism (Table 2). He pointed out that where there is a linear relationship between investment and number of offspring produced, separate sexes will be favored, whereas if the fitness curve saturates for both sexes, that is both sexes reach a plateau where increased investment does not increase fitness, then hermaphroditism will be favored. Bateman's principle assumes a linear relationship between investment and fitness for males but a saturating fitness curve for females (Tables 1, 2; Fig. 2B). According to Charnov (1979; Table 2), where Bateman's principle holds, hermaphroditism could invade a population with separate sexes if something were to act to lower the plateau of the female fitness curve such that female fitness was no longer limited by the energy available to produce eggs but by a second factor, such as the space available for brooding offspring, or by sibling competition created by a lack of dispersal of offspring. This would create a reserve of resources so that individuals could increase their fitness by becoming hermaphrodites and investing the resources not needed to produce eggs in male function. Another situation that would favor the evolution of hermaphroditism according to this model, would be a saturation of the male fitness curve, inconsistent with Bateman's principle. Such a flattening of the male gain curve could arise if males have access to only a very limited number of females (and their eggs), due to low mobility, small population size, or lack of pollinators, etc. A convex fitness curve could also be produced if male and female function drew on separate pools of resources (Charnov et al., 1976; Maynard Smith, 1978; Charnov, 1979, 1982) and there is some evidence, from attempts to measure sex allocation, that the resources important for male vs. female reproductive success do differ (see review in Klinkhamer and de Jong, 2002).
The unique insight of Charnov's (1979) analysis was to identify sexual conflict as a factor that could limit male reproductive success in such a way as to make hermaphrodites violate Bateman's principle. That is, if the recipient of sperm does not use all of the sperm to fertilize eggs, perhaps digesting the sperm, male fitness will not be proportional to investment, and hermaphroditism would be adaptive because individuals can increase fitness by reallocating resources from sperm to eggs. Bateman's principle predicts, therefore, that simultaneous hermaphroditism will, in general, occur in regions of fitness space where Bateman's principle does not apply either because female reproductive success is limited by factors other than energy available for egg production or because male reproductive success reaches a plateau due to lack of access to mates or their eggs. If reproduction in each sexual role requires "fixed costs" in the form of the development and maintenance of structures dedicated to each sexual role (Heath, 1977; Charnov, 1979) then even more stringent conditions must apply in order to give hermaphroditism an advantage over dioecy. Charnov summarized the results of the analysis by saying, "Under Bateman's principle, SH {simultaneous hermaphroditism} will be favored by a combination of low fixed costs and limited opportunities for an individual to reproduce through male function" (1979, p. 2481). However, many hermaphroditic taxa, such as stylommatophoran gastropods and turbellarians are characterized by very elaborate reproductive anatomy and the ability of the recipient to digest sperm and/or mobility and population densities similar to those of related dioecious taxa (see Leonard, 1990 for discussion).
Comparison of these predictions to the distribution of hermaphroditism among metazoans (Leonard, 1990) suggests that while the formal mathematical analysis provided by Charnov and colleagues (Charnov et al., 1976; Charnov, 1979, 1982) has contributed to a much deeper understanding of the relative fitness advantages of hermaphroditism vs. dioecy, it has not resolved "Williams's paradox," i.e., that these predictions as to the conditions that favor hermaphroditism do not explain the taxonomic or ecological distribution of hermaphroditism today (Williams, 1975; Leonard, 1990, 1999). For example, while gastropods are slow-moving in general, opisthobranchs and pulmonates are simultaneously hermaphroditic whereas the other gastropod subclasses, the so-called, "prosobranchs" are predominantly dieocious. Moreover, the opisthobranchs and pulmonates are characterized by rather elaborate reproductive tracts that should represent high "fixed costs" whereas dioecious prosobranchs show a range from taxa with internal fertilization and elaborate internal genitalia in both sexes, to simple broadcast spawners with low fixed costs, contrary to Charnov's prediction (see Williams, 1975; Leonard, 1990). The available data suggest that both dioecy and hermaphroditism are stable under a wider range of ecological conditions than would be predicted by theory. The models based on variance in reproductive success (Table 2), do not seem to address Williams's paradox, either.
Further progress in theory will require attention to factors that may stabilize either hermaphroditism or diocey. Mate choice and/or sexual conflict may be such a factor. Eric Fischer (1980) pointed out (see also Axelrod and Hamilton, 1981; Leonard, 1990), that once hermaphroditism has evolved, conditionally reciprocal mating among hermaphrodites (as a result of sexual conflict, see below) would produce a convex fitness set by linking fitness in the male and female roles. Leonard (1990) argued that sexual conflict would act to produce conditionally reciprocal mating systems among pair mating hermaphrodites. Berglund (1991) has shown that mate choice may stabilize hermaphroditism in the polychaete Ophryotrocha puerilis puerilis, since, in this protandrous species, hermaphrodites prefer small males as mates. Although larger males are more successful in male-male competition, they are rejected by hermaphrodites with eggs to be fertilized, and therefore individuals that become hermaphrodites at a small size have higher fitness. One might expect that in dieocious species, sexual selection would act to put hermaphrodites at a disadvantage, stabilizing dioecy even when ecological conditions might otherwise favor hermaphroditism. The most important predictions of Charnov's (1979) analysis, therefore, are that a) Bateman's principle will seldom apply to hermaphrodites; b) sexual conflict in hermaphrodites will produce a flattening of the male gain curve, creating a violation of Bateman's principle; and c) sexual conflict will be important in shaping mating systems in hermaphrodites.
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SEXUAL CONFLICT AND THE SIMULTANEOUS HERMAPHRODITE |
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Including male-female (sexual) conflict as an arena of selection on reproductive parameters (Trivers, 1972
; reviews in Andersson, 1994; Eberhard, 1985, 1996; Birkhead and Møller, 1998; Simmons, 2001; Shuster and Wade, 2003; etc.) has been one of the major advances of sexual selection theory over the last few decades. Since Bateman's 1948 paper, the ultimate source of differences between the sexes in sexual behavior has come to be seen as differential variance in reproductive success. Bateman's principle assumes that the two sexes (or sexual roles) differ in variance in fitness and predicts that this difference plays a major role in shaping mating systems. That is, females are expected to have a narrow variance in reproductive success because they are limited by the energy available to produce eggs or offspring, whereas males are expected to have a high variance because their reproductive success is more open-ended due to the low cost of sperm production and they also are expected to experience high rates of reproductive failure due to failure to compete with other males or to attract females. For simultaneous hermaphrodites, the potential fitness gains from the two sexual roles may differ (Bateman, 1948; Charnov, 1979; Fischer, 1980 1987; Axelrod and Hamilton, 1981; Leonard and Lukowiak, 1984; Sella, 1985; Leonard, 1990, 1999; Arnold, 1994; Morgan, 1994, Michiels, 1998; Baur, 1998, etc.). Both the mean and the total fitness through male function across the population must be exactly equal to the mean and total fitness through female function. However, if the variance in fitness for the two sexual roles differs, the potential, or the probable, pay-off to an individual may be greater through mating in one sexual role than in the other (Bateman, 1948; Charnov, 1979; Leonard, 1990, 1999). An individual that specializes in the more profitable sexual role, should have greater likelihood of positive fitness than an individual that does not. Therefore, it ought to be the case that there will be a preferred sexual role in a simultaneously hermaphroditic species that is the same for all individuals in a species, all else being equal.
Charnov (1979) predicted that sexual conflict would be important in pair-mating simultaneous hermaphrodites, saying, "Bateman's principle suggests that individuals copulate not so much to gain sperm to fertilize eggs as to give sperm away (to gain access to another's eggs). ...There must often be a conflict of interest between mating partners—as a recipient each should be inclined to accept sperm (not necessarily for fertilization of its own eggs) in order to give sperm away" (1979, p. 2482). The predictions from Bateman's principle (Table 2) are therefore that a) sexual conflict will be important in pair-mating hermaphrodites; b) the male role should be preferred; c) the variance in fitness through male function should be greater than that through female function; and d) female reproductive success should be limited by the energy available to produce eggs rather than sperm availability.
The identification of sexual conflict as an important aspect of sexual selection in hermaphrodites has major implications for understanding not only hermaphrodites but sexual selection in general. The question of whether sex differences in variance in fitness play the decisive role in shaping mating systems remains an important one (see review in Shuster and Wade, 2003) and the prediction of sexual conflict in simultaneous hermaphrodites (Charnov, 1979) is an important test of sexual conflict theory (see above). It is often difficult to establish whether sexual conflict exists in species with separate sexes since, on the level of fitness in each generation, males compete with males and females with females (but see Rice, 1996 etc.; review in Simmons, 2001). In outcrossing simultaneous hermaphrodites, on the other hand, the fitness of an individual will depend on its allocation of reproductive effort between male and female function (Charnov, 1982, etc.). In simultaneous hermaphrodites, therefore, sexual conflict is expected to be direct, suggesting that such species will provide good models for testing theories based on sexual conflict (Leonard, 1990, 1999; Leonard and Lukowiak, 1991).
Evidence for sexual conflict in simultaneous hermaphrodites
The first evidence for sexual conflict in pair-mating hermaphrodites came from Eric Fischer's descriptions (Fischer, 1980, 1981) of egg-trading in the black hamlet, Hypoplectrus nigricans, a serranine fish. In H. nigricans, fertilization is external and unilateral with one individual releasing eggs and the other, sperm, while in a spawning clasp. The same two individuals will then reverse roles repeatedly in a bout of spawnings. The behavior was called "egg-trading" because the egg clutch of each individual is parceled out over the series of spawnings. In egg-trading, "individuals give up eggs to be fertilized in exchange for the opportunity to fertilize the eggs of a partner." (Fischer, 1988, p. 119). Fischer (1980) assumed, on the basis of theory (Charnov, 1979) that the male role would be preferred and concluded from his observations that the reciprocity was conditional; i.e., that individuals would abandon a partner that failed to reciprocate by offering its own eggs. Axelrod and Hamilton (1981) were the first to relate the egg-trading mating system of H. nigricans directly to sexual conflict. Similar mating systems in which a pair of hermaphrodites actively alternate sexual roles in a bout of matings (Fig. 3) have now been described for several taxa with both internal and external fertilization (e.g., opisthobranchs, Navanax inermis [Fig. 3], Leonard and Lukowiak, 1984, 1985, 1991; Bursatella, Ramos et al., 1995; two species of polychaete Ophryotrocha, Sella, 1985, 1991; Premoli and Sella, 1995; Sella et al., 1997; and other serranines, see reviews in Fischer and Petersen, 1987; Leonard, 1993). In the stylommatophoran slug Ariolimax californicus, typical mating encounters involve bouts of unilateral copulations which may involve alternation of sexual roles, although it is not clear that that is the rule (Leonard et al., 2002). As Axelrod and Hamilton (1981) pointed out, mating systems based on serial alternation of sexual roles during a bout of matings represent a potentially equitable resolution of such conflicts. These authors suggested that such mating systems represent a cooperative (Tit-for-Tat) solution to a Prisoner's Dilemma problem created by sexual conflict (see also Fischer, 1987, 1988). A more detailed analysis suggests that, while Prisoner's Dilemma is a first approximation, the situation created by a sexual role preference in mating hermaphrodites is somewhat more complex (Leonard, 1990; see also Connor, 1992; Landolfa, 2002).
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The Hermaphrodite's Dilemma
The Hermaphrodite's Dilemma model (Table 3; Fig. 4; Leonard, 1990
) describes the situation faced by a pair of hermaphrodites which both prefer the same sexual role. It is a conditional, iterated, non-zero-sum game of strategy which includes both Prisoner's Dilemma (Rapoport, 1966) and Game of Chicken (Riechert and Hammerstein, 1983) as special cases (see Table 3). Game theorists have long recognized that Prisoner's Dilemma and Game of Chicken shared a motivational structure (Rapoport and Dale, 1966). Both games present two selfish players with two choices; to cooperate or to defect. In each case the highest payoff is to the player that chooses to defect when the other player chooses to cooperate. For a pair of mating hermaphrodites with a preference for one sexual role (Hermaphrodite's Dilemma) the choices are to defect (insist on mating only in the preferred role) or to cooperate (offer to mate in both roles) (Leonard, 1990). The reasoning is that mating in the non-preferred role, while it may yield fitness gains, will also involve costs that decrease the player's reproductive value to a greater extent than mating in only the preferred role. The pay-off matrix that defines Hermaphrodite's Dilemma is T > R > S; R > P. The fame of Prisoner's Dilemma and Game of Chicken, stems from the fact that both have stable solutions involving cooperation between selfish players (see Table 3). A major difference between Prisoner's Dilemma and Hermaphrodite's Dilemma is that while an all-defector strategy (never reciprocate, insist on the preferred role) is an evolutionarily stable solution to Prisoner's Dilemma, a population of defectors would not mate at all and all individuals would have zero fitness in Hermaphrodite's Dilemma. The Hermaphrodite's Dilemma is more complex than either Prisoner's Dilemma or Game of Chicken because Hermaphrodite's Dilemma is a conditional game in which the pay-off matrix can change over the course of the game (see also Gardner et al., 1987; Dugatkin et al., 1992) whereas Prisoner's Dilemma and Game of Chicken are static, symmetrical games. The pay-off matrix for Hermaphrodite's Dilemma is conditional since for example, if an individual may expect many mating encounters in its lifetime, and mating in the less-preferred role decreases reproductive value to a greater extent than does mating in the preferred role an individual may find itself in a Prisoner's Dilemma situation early in its life but as the probability of future mating opportunities decreases its pay-off matrix may switch to Game of Chicken.
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In the Hermaphrodite's Dilemma model, an individual will benefit, under most circumstances, from choosing to cooperate (offer to mate in both sexual roles), but there will be circumstances under which it will pay an individual to defect (insist on mating only in the preferred role) (see Leonard, 1990
; Table 3). Like both Prisoner's Dilemma and Game of Chicken, Hermaphrodite's Dilemma has both start and end effects. On the last mating encounter, a hermaphrodite has nothing to lose from mating in both roles since its reproductive value becomes zero in any case. Therefore, for hermaphrodites meeting for the last (or only) mating encounter of their lives, there is no conflict of interests and they should mate reciprocally. If Prisoner's Dilemma conditions prevail (that is, mating encounters are sufficiently frequent that it pays to sit out an encounter rather than mate only in the non-preferred role) then an individual should defect frequently near the start of the game (early in its reproductive life) and cooperate more frequently toward the end of its life since its reproductive value is approaching zero in any case. The juvenile protandric phase found in Ophryotrocha spp. (Premoli and Sella, 1995) may represent such a start effect. Prisoner's Dilemma may in fact obtain in cases, such as H. nigricans (Fischer, 1980; Axelrod and Hamilton, 1981; but see Connor, 1992) or those in which self-fertilization is an option. Under Game of Chicken conditions however, any mating is better than no mating at all and an individual should always cooperate near the start of the game and choose to defect more frequently toward the close of the game. Similarly if Tit-for Tat is a stable solution, it will pay an individual to defect near the end of the game since opportunities for retaliation are limited. Two egg-trading hermaphroditic species of the polychaete genus Ophryotrocha may illustrate the two types of game within Hermaphrodite's Dilemma. Game of Chicken conditions may prevail for O. diadema; fertile partners are rare and defection occurs at a low frequency regardless of the partner's behavior (Sella and Lorenzi, 2000). In O. gracilis, on the other hand, a higher proportion of individuals carry eggs at any given time and pair bonds are more labile; desertion occurs at a higher rate (Sella et al., 1997), as predicted for Prisoner's Dilemma parameters under Hermaphrodite's Dilemma. Similarly, in the serranine S. psittacinus (=S. fasciatus; C. W. Petersen, personal communication) Petersen (1990) reported that the tendency for individuals to specialize in male behavior, defending harems of hermaphrodites and/or losing ovarian function to become pure males, increased with increasing population density as predicted by Hermaphrodite's Dilemma. Isolated pairs reciprocated in a monogamous relationship, suggesting that they are experiencing Game of Chicken conditions.
Sexual conflict, reciprocity and cheating: testing Hermaphrodite's Dilemma
From the assumption that sexual conflict exists, that is, that one sexual role is potentially more profitable than the other for all individuals of a species, the Hermaphrodite's Dilemma (Leonard, 1990) predicted that 1) mating systems in hermaphrodites will be based on reciprocity; and 2) cheating (defection) will exist in a consistent sexual role. A further prediction is that selection will favor mechanisms to prevent cheating and/ or retaliate against cheaters, except perhaps under Game of Chicken conditions (Table 3). The predictions made by the Hermaphrodite's Dilemma were strong predictions since at that time little was known about the mating systems of simultaneous hermaphrodites. However, it had long been known that many hermaphroditic organisms have simultaneous reciprocal intromission, such as earthworms, leeches, many land snails, many opisthobranchs, planarians (Jenkins and Brown, 1964; Michiels and Streng, 1998; reviews in Michiels and Streng, 1998; Baur, 1998; etc.). Reciprocity in mating may also involve reciprocal transfer of external spermatophores (e.g., the nudibranch, Aeolidiella, Karlsson and Haase, 2002). De facto reciprocity might be expected to occur among members of a group of sessile invertebrates or plants in a local mating group. The question then becomes whether such familiar systems involve conditional reciprocity as would be predicted if sexual conflict is important. Normal mating behavior involving a single alternation of sexual roles, inconsistent with expectations from a Prisoner's Dilemma model, has been described for the freshwater pulmonates, Lymnaea stagnalis (van Duivenboden and ter Maat, 1985), and Biomphalaria glabrata (Webster, 2002), for the opisthobranch, Chelidonura sandrana (Anthes and Michiels, 2004) and for stylommatophoran slugs of the genus Deroceras (Reise, 1996).
Is reciprocity conditional?
Pongratz and Michiels (2003) argued that the many reciprocal mating systems in hermaphrodites might not represent cooperative solutions to sexual conflict but simply be a direct consequence of Bateman's principle, saying "one would expect hermaphrodites to attempt to inseminate as many mates as possible, in accordance with Bateman's principle ...leading to ‘unconditional reciprocity" (ibid, p. 1426). These authors apparently assume that hermaphrodites will always be willing to accept sperm, but perhaps, as has been previously suggested (Charnov, 1979; Leonard and Lukowiak, 1984, 1985, 1991), not for use in fertilization. Review of the few hermaphrodite mating systems that have been examined for conditional reciprocity, suggests that it is common. Although behavioral observations suggested that the alternation of sexual roles was conditional in both H. nigricans (Fischer, 1980; see discussion in Maynard Smith, 1982) and the opisthobranch Navanax inermis (Leonard and Lukowiak, 1985, 1991), the first direct evidence for conditional reciprocity came from the polychaete, Ophryotrocha diadema.
In O. diadema, observations from laboratory culture using genetic strains that produce yellow or white eggs, show that pairs of simultaneous hermaphrodites form long-lasting associations that may persist as long as both individuals have oocytes and that members of the pair lay alternate clutches of eggs (Sella, 1985). This species shows protandry in that young individuals of 5–11 body segments produce sperm only (Sella, 1985). Gabriella Sella (1988) demonstrated that this egg-trading mating system was based on conditional reciprocity in experiments that showed that a) hermaphrodites prefer other hermaphrodites as partners and will reject young males; and b) hermaphrodites paired with young males spawn fewer eggs and at longer intervals than hermaphrodites paired with other hermaphrodites. In flatworms, conditional reciprocity has been demonstrated in the form of exchange of equal volumes of sperm during simultaneously reciprocal copulation in the planarian Dugesia gonocephala (Vreys and Michiels, 1997; Michiels, 1998). Vreys and Michiels (1997) demonstrated both size assortative mating in this species and that the volumes of sperm exchanged between mating partners were more similar than expected on the basis of autosperm stores. In Schmidtea polychroa, another flatworm with simultaneously reciprocal intromission, unilateral sperm transfer was less common than expected by chance, whereas both non-transfer and reciprocal transfer were more common than expected, suggesting that individuals were reluctant to give sperm to a partner that did not reciprocate (Michiels and Bakovski, 2000). In a very interesting case in the basommatophoran gastropod Biomphalaria glabrata, Webster et al. (2003) gave free-moving snails, which either were or were not infected with the parasite, Schistosoma mansoni, a choice between two tethered potential mates, one from a genetic strain selected for resistance to the parasite and one from a susceptible strain. The results show that reciprocation was common with both types of tethered mates when the free-moving snail was uninfected. When the free-moving snail was infected, resistant tethered snails refused to reciprocate with it. The resistant tethered snails would mate as males, but not as females, with infected free-moving individuals. Susceptible tethered individuals, on the other hand, did reciprocate with infected free-moving individuals (Webster et al., 2003). Spermatophore exchange in the stylommatophoran Arianta arbustorum has also been reported to be conditionally reciprocal (Baur et al., 1998) and in the nudibranch gastropod, Aeolidiella glauca, individuals are less likely to retain a spermatophore received from a partner if there was not reciprocal exchange of spermatophores (Karlsson and Haase, 2002). In another stylommatophoran, Reise (1996) reported that if intromission was not reciprocal the male-acting individual would chase and bite the partner (see below). In contrast, Anthes and Michiels (2004) argued, based on a lack of evidence for retaliation against vasectomized individuals, for unconditional reciprocity in the opisthobranch, Chelidonura sandrana which has a mating sytem involving a single alternation of sexual roles. This mating system, a single alternation of sexual roles, is a relatively poorly understood one from a theoretical standpoint. Under a Prisoner's Dilemma pay-off matrix (Table 3) such a mating system could not evolve since the stable solution for this game is to defect on the last turn; an unknown length of the game is a requirement for cooperative solutions to Prisoner's Dilemma (Rapoport, 1966; Rapoport and Dale, 1966). One would not expect Tit-for-Tat behavior therefore, in C. sandrana. Such single exchanges of sexual role have been observed in other hermaphrodites (see above; Leonard, 1991) and the Hermaphrodite's Dilemma model predicts that they represent responses to Game of Chicken situations, for which always reciprocate, or reciprocate most of the time with occasional defections are stable solutions (see Table 3).
The examples cited above show that most of the studies that have examined hermaphrodite mating systems, in pair-mating animals, specifically with a view to identifying conditional reciprocity, have found it. Unconditional reciprocity, which Michiels (1998) cited as a prediction of Bateman's principle, although it may occur, does not appear to be the rule. In conclusion, therefore, reciprocal mating systems appear to be common in hermaphrodites, as predicted from the Hermaphrodite's Dilemma model, and the reciprocity appears to be conditional where studied. This is strong evidence that sexual conflict is common in pair-mating hermaphrodites, as Charnov (1979) predicted from Bateman's principle. However, other models also predict sexual conflict over a preferred role in pair-mating hermaphrodites (see below). In contrast, Connor (1992) has argued that reciprocal systems such as egg-trading may evolve without an advantage to defection or punishing cheating if parceling is used as a mechanism to keep T < R. From a practical standpoint, this would suggest that parceling is in fact a mechanism to prevent or punish cheating, as Fischer (1980) predicted. While Connor's (1992) distinctions may be important from a purely game theoretical standpoint, it is unclear that they predict differences in behavior or represent mating systems without sexual conflict.
It is important to remember that, in reality, few, if any, encounters between pair-mating hermaphrodites will meet the conditions of formal game theory models. For example, a key element of Prisoner's Dilemma is the requirement that there is not interaction or communication between the participants. This is clearly violated by the hermaphrodites discussed here. It may be more appropriate in situations of broadcast spawning or pollinator-mediated fertilization. The interest in models such as Prisoner's Dilemma and Hermaphrodite's Dilemma is that they make clear, falsifiable predictions from a few basic assumptions and the general validity of the predictions offers a test of fundamental assumptions of sexual selection theory, such as sexual conflict. More recently, Landolfa (2002) has argued that egg trading in H. nigricans should be viewed as an exchange of sexual signals rather than as a game involving sexual conflict. He regards interpretation of mating systems in terms of games involving sexual conflict as peculiar to the hermaphrodite literature as opposed to the emphasis on exchange of sexual signals in the literature on dioecious species. Viewing sexual behavior in terms of games of strategy involving sexual conflict and interpreting individual behaviors as sexual signals are in no way mutually exclusive. A conflict of interests between the sexes has been seen as fundamental to understanding the evolution of mating systems in animals with separate sexes for 30 years (see above and reviews in Andersson, 1994; Gowaty, 2004). The relationship between signal evolution and conflicts of interests between sender and receiver has been discussed by Zahavi (1977, 1987; Zahavi and Zahavi, 1997). The question of how hermaphrodites should behave under conditions of continuous mutual assessment is an important one, however, and will require a new generation of models.
Another open question is to what extent the reciprocal mating behaviors that have been studied represent reciprocal fertilization. In the cases of the externally fertilizing hamlets, paternity is clearly reciprocal. Similarly in monogamous pairs of Ophyrotrocha, the members of a pair fertilize each others eggs (Sella and Lorenzi, 2000). However in the case of internally-fertilizing hermaphrodites with sperm storage, pair-mating hermaphrodites may have little certainty of paternity when transferring sperm to a partner (Charnov, 1979; Leonard and Lukowiak, 1984; reviews in Michiels, 1998; Baur, 1998). In fact, a key aspect of the gamete-trading (Table 3; below) model of mating systems is that the preferred sexual role is the one that offers greater control over the fate of gametes. Reciprocity in sexual behavior can evolve without complete reciprocity in paternity as long as hermaphrodites that reciprocate produce more offspring than hermaphrodites that do not; that is, certainty of paternity does not need to be 100% to select for reciprocity in mating behavior.
In the first study to use microsatellites to look at reciprocal paternity in pair-mating hermaphrodites, Pongratz and Michiels (2003) collected Schmidtea polychroa (planarian flatworms) from the field and held them in groups of ten individuals for four weeks. Their results show very high levels of multiple paternity with more than 80% of cocoons (3–5 eggs/cocoon) having more than two sires and more than 28% of offspring sired by unknown individuals, suggesting that sperm can be stored more than a month and that they persist in the sperm storage organ in spite of many subsequent matings by the recipient. Overall, reciprocal paternity was found in only 41/110 "registered mate combinations" and these authors estimated that at best an individual giving sperm to a mate could expect only 25% immediate paternity. The individuals used in this study were not known to be virgins so the role of the sexual history of individuals could not be assessed. It is difficult to say whether 25% represents a high or low certainty of paternity without other data for comparison. One of the assumptions made by Charnov (1979) in predicting a preference for the male role in pair-mating hermaphrodites was that there would be a strong last male advantage in paternity, which is clearly not the case in these planarians. Pongratz and Michiel's (2003) data showed a strong correlation between the number of female partners and male reproductive success as predicted by Bateman's principle but also a strong correlation between the number of male partners and female reproductive success, contrary to Bateman's principle. No correlation was found between either the number of female partners and female reproductive success or the number of male partners and male reproductive success in these planarians (Pongratz and Michiels, 2003) as might be expected if success through male and female function positively associated as required for a convex fitness curve (Fig. 2; Charnov, 1979). In this pioneering study it was not possible to relate variations in mating behavior to variations in reciprocity or to success through either sexual role.
It is clear that although sexual conflict is probably common in pair-mating hermaphrodites, the behavioral reciprocity that has been considered a resolution of this conflict (Axelrod and Hamilton, 1981; Leonard and Lukowiak, 1984; Leonard, 1990) does not necessarily lead to exactly reciprocal paternity. Moreover, there are many apparent exceptions to even behavioral reciprocity, in which internally fertilizing simultaneous hermaphrodites have been described as having unilateral copulation such as the freshwater pulmonate Physa (DeWitt, 1991, 1996; Wethington and Dillon, 1991, 1997); hypodermic insemination by multiple individuals (Rivest, 1984) or chain copulation in species such as Aplysia (Pennings, 1991; Angeloni and Bradbury, 1999; see reviews in Leonard, 1991; Michiels, 1998; Baur, 1998). These exceptions offer very interesting tests of the Hermaphrodite's Dilemma model and the role of sexual conflict in hermaphrodites.
Is there a "preferred" sexual role?
Charnov (1979) argued, on the basis of Bateman's principle, that hermaphrodites would be more eager to donate sperm than to receive it; i.e., they would prefer to mate as males (the Eager Male Model, Table 3). This formed the basis of his prediction of sexual conflict in hermaphrodites. The empirical data reviewed above demonstrates that pair-mating simultaneous hermaphrodites behave as predicted if sexual conflict were important in their mating system. The next question is whether the sexual conflict is in fact over a preferred sexual role. That is, when hermaphrodites meet to mate is there a temptation to "cheat" by mating only in the preferred role as predicted by the Hermaphrodite's Dilemma model. The best evidence for cheating on a reciprocal mating system in a preferred sexual role comes from a comparison of mating systems in the simultaneously hermaphroditic serranine fishes (review in Leonard, 1993). Comparison of the variety of mating systems in that have been described for serranines (Fischer, 1980, Fischer, 1984b; Pressley, 1981; Hastings and Petersen, 1986; Petersen and Fischer, 1986; Fischer and Petersen, 1987) suggests that the basic mating system is a form of conditional reciprocity called egg-trading (see above) and deviations from egg-trading consist of attempts by individuals to get extra spawnings in the male role. For example, in Serranus tigrinus, a monogamous serranine, the members of a pair defend a joint territory and at sunset fertilize each others' eggs. At other times both members of a pair compete with each other to mate as males with neighboring solitary individuals. Solitary individuals spawned only in the female role until they were joined by another solitary individual to form a new pair (Pressley, 1981). In S. tortugarum and S. tabacarius, pairs form for egg-trading as in H. nigricans, but in these two Serranus species, which lack the tight spawning clasp found in H. nigricans, additional individuals may be attracted to the mating pair (Fischer, 1984b; Petersen, 1990). These "streakers" attempt to dart in and probably release sperm, apparently trying to "cheat" on a reciprocal mating system by getting extra matings in the male role. Specialization in the male role is associated with social dominance in two territorial species, S. baldwini and S. psittacinus (previously S. fasciatus). These two species apparently have an androdioecious sexual system with individuals starting life as hermaphrodites and some large individuals losing ovarian tissue and becoming pure males. In both species, the common social system is for large males to defend territories which contain the home ranges of a harem of smaller simultaneous hermaphrodites (Hastings and Petersen, 1986; Petersen and Fischer, 1986). The hermaphrodites spawn eggs with the harem holder but otherwise attempt to sneak spawnings as males when the harem holder spawns with other hermaphrodites (Hastings and Petersen, 1986; Petersen and Fischer, 1986, etc.). In S. psittacinus, the social system varies with population density (Petersen, 1990). Under low density conditions, monogamous pairs of hermaphrodites may form which alternate spawns each evening as in S. tortugarum. Harem polygamy is the common pattern under moderate density conditions and under high density conditions, a complex system of harem polygamy whereby large individuals become pure males and defend harems of simultaneous hermaphrodites, some of whom may have subharems of smaller simultaneous hermaphrodites, is found. Comparison of these systems indicates that social dominance is associated with the ability to monopolize the male role in spawning and that deviations from the pair mating system occur in the form of attempts by individuals to obtain extra spawnings in the male role. There is, therefore, strong evidence from serranines for a preference for the male role as predicted by Bateman's principle (Charnov, 1979; Leonard, 1993). Other evidence for a male role preference comes from the observations that 1) O. diadema give fewer eggs to a male than to a hermaphrodite partner (see above; [Sella, 1988]), although apparently the protandrous males may be unable to fertilize a full clutch, and 2) parasite-resistant B. glabrata will mate as males regardless of the infection status of a partner but would only reciprocate with uninfected individuals (see above; Webster et al., 2003). These data would appear to be evidence against the prediction that reciprocal mating behavior may be unconditional as predicted by the Eager Male model (see Table 3; above; Connor, 1992; Pongratz and Michiels, 2003).
There is also evidence from several systems that hermaphrodites prefer to mate in the female role. In a series of experimental observations using groups of three individuals, Leonard and Lukowiak (1991) found that the opisthobranch Navanax inermis were unlikely to initiate male courtship behavior when they were already copulating as females and that they were more likely to terminate intromission as males when they got an opportunity to mate in the female role. In a later study, Michiels et al. (2003) also concluded that the evidence favors a preference for the female role in Navanax. Reise (1996) described mating behavior in stylommatophoran limacid slugs, of the genus Deroceras in which copulation is typically reciprocal, and if it is not, the slug that performed intromission will follow and bite the defector. Karlsson and Haase (2002) demonstrated in the opisthobranch Aeolidiella glauca, which transfers external spermatophores, that although 30% of spermatophores fell off before sperm had penetrated into the body of the recipient, spermatophores were more likely to remain attached if there had been a reciprocal exchange. Comparative data from a group of planarian species comes from the work of Michiels and colleagues (see above, review in Michiels, 1998; Michiels and Bakovski, 2000; Pongratz and Michiels, 2003); who have demonstrated that planarians give sperm preferentially to partners that reciprocate with sperm. These authors have concluded that, in these species, individuals donate sperm in order to obtain sperm. There is strong evidence, then, that the preferred sexual role varies among taxa. Sexual conflict in hermaphrodites may stem from a species-typical preference for either the female or the male role.
What determines the preferred role?
The empirical evidence from many species of pair-mating hermaphrodites suggests that sexual conflict over a preferred sexual role has led to the evolution of mating systems based on conditional reciprocity. There are several theories that would explain why a particular sexual role should be preferred. Bateman's principle (Table 1, above), in its simplest form, would predict that the male role should be preferred (Charnov, 1979); that hermaphrodites would be eager to mate as males because fitness in the male role would have a linear correlation with the number of mates, whereas fitness in the female role would be limited by the resources available for egg production. That is, hermaphrodites should prefer the male role because it has the greatest "upside-potential" (see discussion in [Leonard, 1999]). More sophisticated applications of Bateman's principle argue that the preferred role will be the role with the lower energy investment in matings, which may be either role, depending on circumstances (see below). In contrast, application of Gillespie's principle (Table 1, Gillespie, 1974, 1977; see above) to hermaphrodites predicts that hermaphrodites will achieve higher fitness through the sexual role with the lower variance in reproductive success, the role with the lower "downside potential" (Leonard and Lukowiak, 1991; Leonard, 1999). Where the two roles have equal mean fitness, as must be true for male and female function, the lower variance role will offer higher fitness because individuals assuming that role will be less likely to experience reproductive failure (see discussion in Leonard, 1999; Gillespie, 1974, 1977