Cooperation promotes the evolution of separate sexes from hermaphrodites with unitary growth

Most animals have specialized into separate sexes but most plants remain hermaphroditic. The underlining cause for this is still unclear. Here we address this question by evolutionary stable strategy analysis and exact calculation of frequency-dependent selection and genetic drift in geographically structured populations. Reproductive investments of hermaphrodites are divided into male and female functions, and each sex requires linear investments that increase linearly with successful gamete number and reusable investments (RIs) that increase less than linearly. Individuals specializing into one sex require RIs of only this sex and thus can produce more gametes. However, these gametes suffer strong kin competition as they are of the same sex and gamete number of the other sex decreases. The success of individuals specializing into one sex requires individuals specializing into the other sex to cooperate with them, providing them with more opposite-sex gametes and relaxing them of the same-sex competition. The evolution of this cooperation does not require two rare mutations to happen simultaneously at the same place, because single-sex mutants can sparsely spread in a hermaphroditic population with RIs despite genetic drift and wait for mutants of the other sex to arise. RI resembles fixed cost in previous theories. However, previous theories considered all costs except for costs for gametes as fixed costs and this does not capture an important plant–animal difference; modular growth of sexual organs in most plants and some animals promotes reproductive investments to increase linearly with offspring number, so their investments in sexual organs are linear investments rather than fixed costs. This study shows the evolution of separate sexes from hermaphrodites as an example of the evolution of cooperation and mutualism as in harmony games, and highlights modular growth as an important factor that prevents most plants and some animals from evolving into separate sexes.