Evolution of the Two Sexes under Internal Fertilization and Alternative Evolutionary Pathways

Transition from isogamy to anisogamy, hence males and females, leads to sexual selection, sexual conflict, sexual dimorphism, and sex roles. Gamete dynamics theory links biophysics of gamete limitation, gamete competition, and resource requirements for zygote survival and assumes broadcast spawning. It makes testable predictions, but most comparative tests use volvocine algae, which feature internal fertilization. We broaden this theory by comparing broadcast-spawning predictions with two plausible internal-fertilization scenarios: gamete casting/brooding (one mating type retains gametes internally, the other broadcasts them) and packet casting/brooding (one type retains gametes internally, the other broadcasts packets containing gametes, which are released for fertilization). Models show that predictions are remarkably robust to these radical changes, yielding (1) isogamy under low gamete limitation, low gamete competition, and similar required resources for gametes and zygotes, (2) anisogamy when gamete competition and/or limitation are higher and when zygotes require more resources than gametes, as is likely as multicellularity develops, (3) a positive correlation between multicellular complexity and anisogamy ratio, and (4) under gamete competition, only brooders becoming female. Thus, gamete dynamics theory represents a potent rationale for isogamy/anisogamy and makes similar testable predictions for broadcast spawners and internal fertilizers, regardless of whether anisogamy or internal fertilization evolved first.