Sexual metazoans can be classified as hermaphroditic or dioecious. Hermaphrodism occurs in 70% of the animal phyla and about a third of all non-insect species, and has previously been regarded as derived from dioecy. We reexamine this view by considering the distribution of simultaneous hermaphrodism and dioecy across the animal phylogenetic tree. Reconstructing ancestral traits using the maximum parsimony method provides evidence that hermaphrodism is ancestral to metazoans, although secondarily derived in the speciose and well-studied taxa such as molluscs, annelids and arthropods. We also classify the fertilization behavior of each taxon as either broadcasting sperm to eggs produced by a number of individuals or localizing sperm around the eggs produced by a single individual (‘broadcast spawning’/’localized fertilization’), to find that broadcast spawning is ancestral. We hypothesize that the two trends from hermaphrodism to dioecy and from broadcast spawning to localized fertilization are coupled. Hence dioecy may be regarded as a specialization to ensure sperm delivery to the site of egg production. We build a population genetic model to formalize this idea.

Results/Conclusions

To derive conditions for the stability of hermaphrodism and dioecy, we conceptualize a trade-off between the concentration of sperm delivered by an individual and the amount of resources available for gamete production. When investment in sperm concentration is adaptive, but decreases the resources available for both sperm and egg production, evolution causes specialization into males that invest in sperm concentration and females that do not. Males then invade a hermaphroditic population to reach a polymorphism between males and hermaphrodites. Subsequent invasion by females leads to the displacement of the hermaphrodites and evolution of dioecy. We suggest that conditions of high resource availability, population density and mobility may decrease the cost of sperm concentration relative to its benefits, and hence favor the evolution of dioecy from hermaphrodism.

Previous models for the evolution of hermaphrodism and dioecy consider the effects of locating and competing for mates, opportunities and costs to selfing and trade-offs between resources available for the male and female functions in selecting for hermaphrodism or dioecy. Compared to some of these models, we provide a more mechanistic basis for selection on hermaphrodism or dioecy, and also shift attention from the number of matings to the effectiveness of each mating as a selective force. We outline tests for support of our model.