Abstract The evolution of gametic sex (meiosis and fertilization) and subsequent transition from isogamy (fusion between two equal-sized gametes) to anisogamy (dimorphism into eggs and sperm, namely, females and males) is one of the largest enigmas of evolutionary biology. Meiosis entails genome-dilution cost and anisogamy entails male-production cost. Despite much progress has been made for the maintenance mechanisms of sex, its origination events under such “twofold cost of sex” are still unsolved. Here, we posit two hypothetical scenarios as follows: the “Seesaw Effect” hypothesizes that automictic selfing between isogametes effectively purged deleterious mutations from an organism’s lineage and simultaneously fixed the sex-controlling allele and all other loci (no genome-dilution cost raised). The high relatedness among homoeologous cell colonies led to multicellularization. The “inflated isogamy” hypothesizes that multicellularity increased the reproductive investment of both mates, resulting in excessively large isogametes. This redundancy induced cheating of one sex (evolving to male) to reduce gamete size. However, the other sex (evolving to female) allowed this cheat because her cost did not change. Therefore, anisogamy originated as a kind of commensalism but turned into beneficial for females because it solved the gamete limitation problem inherent to isogamy. Thus, smooth transition to anisogamy had been attained.

Search, encounter rates, and the evolution of anisogamy. We describe analytical and numerical models to study gamete encounters in two and three dimensions between differently sized gametes without assuming pre-existing mating types. Our results indicate that an isogamous population can be successfully invaded by a gametangium if it produces gametes of a different size. The existence of a low adaptive peak for isogamy and a much higher adaptive peak for anisogamy suggests that stochastic forces may be initially important in driving isogamy through the fitness saddle to anisogamy. Published in Proceedings of the National Academy of Sciences of the United States of America (1984)

In Stylorhynchus the difference between the conjugating gametes is not quite so pronounced (fig. 13), the male elements being of about the same bulk as the females, but pyriform instead of round, and possessing a distinct flagellum; a most interesting point about this parasite is that certain highly motile and spermatozoon-like male gametes are formed (fig. 13), which are, however, quite sterile and have acquired a subsidiary function. In other cases, again, the two kinds of element exhibit either very slight differences (Monocystis) or none (Urospora, Gonospora), in size and appearance, the chief distinction being in the nuclei, those of the male elements being smaller and chromatically denser than those of the females. Lastly, in Lankesteria, Gregarina, Clepsydrina, Diplocystis and Diplodina complete isogamy is found, there being no apparent difference whatever between the conjugating elements. Nevertheless, these forms are also to be regarded as instances of binary sexuality and not merely of exogamy; for it is practically certain that this condition of isogamy is derived from one of typical anisogamy, through a stage such as is seen in Gonospora, &c.