Four steps to two sexes.

Four steps through which parasitic intracellular symbionts could bring about the evolution of two sexes are considered. In the first step, a primitive host population has biparental cytoplasmic inheritance and lacks gametic differentiation: parasitic cytoplasmic elements readily invade and spread by vertical transmission through such host populations, even if they have major deleterious effects on their hosts. The second step leads to the establishment of a nuclear mutant in the host (locus A) that prevents inheritance of the cytoplasm in gametes in which it occurs. This mutant comes to equilibrium at an intermediate frequency, because a double dose of symbionts is more deleterious than a single dose, and zygotes lacking cytoplasm from both gametes are inviable. The third step involves the spread of a mutant at another nuclear locus (B), causing self-incompatibility of gametes in which it occurs. If this is closely linked to locus A, the mutant may become established by preventing the deleterious gamete unions. The mutant at locus B must, however, start both with an appreciable frequency and be in gametic disequilibrium with locus A. In the fourth step a second mutation causing self-incompatibility occurs at locus B. This allele spreads by becoming associated with the other allele at locus A, eventually leaving the population with two gamete types, or sexes, one predominantly transmitting the cytoplasm, and the other eliminating it. It is argued that this is a feasible mechanism for the origin of two sexes.