The disruptive selection theory of the evolution of anisogamy posits that the evolution of a larger body or greater organismal complexity selects for a larger zygote, which in turn selects for larger gametes. This may provide the opportunity for one mating type to produce more numerous, small gametes, forcing the other mating type to produce fewer, large gametes. Predictions common to this and related theories have been partially upheld. Here, a prediction specific to the disruptive selection theory is derived from a previously published game-theoretic model that represents the most complete description of the theory. The prediction, that the ratio of macrogamete to microgamete size should be above three for anisogamous species, is supported for the volvocine algae. A fully population genetic implementation of the model, involving mutation, genetic drift and selection, is used to verify the game-theoretic approach, and accurately simulates the evolution of gamete sizes in anisogamous species. This model was extended to include a locus for gamete motility, and shows that oogamy should evolve whenever there is costly motility. The classic two-fold cost of sex may be derived from the fitness functions of these models, showing that this cost is ultimately due to genetic conflict.