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Bateman's Principle and Simultaneous Hermaphrodites: A Paradox1

Abstract 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.