The evolution of sex reconsidered: Resource limits offset the twofold cost of males

Abstract In anisogamy (sexual reproduction by egg and sperm), the population growth rate is half that of thelytoky (all-female parthenogenesis) because half of the offspring are males, which do not lay eggs¹,². The present dominance of anisogamy in multicellular organisms despite this “twofold cost of male production” is the greatest enigma in evolutionary biology³⁻⁸. Various proposed benefits (e.g., Red Queen) of sex are insufficient to compete with thelytoky, which increases 2¹⁰ = 1024-fold in 10 generations over anisogamy. Why is anisogamy protected from thelytoky invasion? However, the 1024-fold increase requires the 1024-fold resources and resources are finite in the real world. Here, using a very simple mathematical model and simulations, we show that the twofold cost disappears under resource limitations. Thelytoky can exhibit a twofold increase only at low densities with abundant resources, but anisogamy can coexist with thelytoky because competitive exclusion does not occur in such an unsaturated population. Once the population reaches the carrying capacity, thelytoky and anisogamy have the same realized fitness. If males offer slight advantages (e.g., lower resource requirements or greater resource competitiveness than thelytokous females), anisogamy has greater fitness than thelytoky and will displace thelytoky. Therefore, twofold benefits to compensate for the twofold cost are unnecessary.