Son’s contribution to mother’s fitness can overcome the twofold cost of sex

Abstract Sexual reproduction requires mating partners and transmits only half of their genomes to an offspring1,2. However, because the sex-controlling allele is fixed at the origin of gametic sex, where each gamete provided half amount of necessary resource (isogamy), the genome dilution cost disappears3. In the traditional view1,2, derivative anisogamy (bipolarization into egg and sperm) must have half the population growth rate of asexual thelytoky because males laying no eggs are not included in population size1,2. The present dominance of anisogamy despite this "twofold cost of male production" is the greatest enigma in evolutionary biology1,2,4-6. Sex has various advantages6-27, but none overcome this cost22. Why can anisogamy become dominant? Here, we show that a son's mating with multiple females contributes to his mother's fitness. Although only females contribute egg resources in anisogamy, at the lineage level, males from a particular lineage parasitize the egg resources of the other lineages, and their own lineage's eggs are fertilized by sperm from the other lineages. Considering it reciprocal altruism between lineages, anisogamy can offset male-production costs by yielding more grandchildren than thelytoky. Our simulations prove that anisogamy is evolutionarily stable against isogamy and thelytoky. The significance of males, a question since Aristotle's time, is clearly answered.