The two-fold cost of sex should actually be refered to as being the two-fold cost of anisogamy. This is because a hermaphrodite or dioecious population –– in which every individual produces both male and female gametes –– can have a growth rate nearly as rapid as an asexual population. Anisogamy is the asymmetry in the size of gametes that is based on that gamete's sex. For example, we are anisogamous because the human egg is much larger than a sperm cell, although the two gametes are genetically equivalent. The two-fold cost of anisogamy is brought about when the following conditions exist:
1) The growth of a sexually-reproducing population is limited by the number of females.
2) Sperm are less costly to produce than eggs.
3) Fertilization occurs in an open system, such that sperm are cast into a common mixed pool, and encounter eggs randomly.

The first condition is always true for a sexually-reproducing population in which there is a sufficient number of males to fertilize all females, and for which paternal care has a negligible effect on the survival of offspring. The second is generally true because eggs are energetically costly to produce. Energy and resources needed for the growth of the embryo must be parcelled into each egg cell, regardless of whether or not it becomes fertilized. Sperm, on the other hand, only require a store of energy for travel to the egg (if the demand exists –– the flagella of human sperm, or pollen tube growth) and a structure capable of persisting in a harsh environment.

The final condition is required because individuals that cheat can obtain an evolutionary advantage. Suppose that the resources required to produce one egg can instead be converted into ten sperm. A population of hermaphrodite individuals might initially tend to produce 9 eggs and 10 sperm; it is a fair system, because there is a balanced ratio of gametes to ensure fertilization, and everyone gains an equal number of fertilizations. If a mutation arises that causes an individual to produce 8 eggs and 20 sperm, however, they obtain a disproportionately greater number of fertilizations by saturating the pool of male gametes. This sort of mutation would may be met in some species, such as in echinoderms that release sperm into the sea water, or angiosperms that release wind-borne pollen. It is circumvented in others, that have evolved a closed system of mating. For example, although hermaphrodite earthworms fertilize externally, some undergo a lengthly courtship ritual before allowing the mutual exchange of a single sperm.

Otherwise, cheaters succeed until the number of female gametes produced is halved. Thus, the hermaphrodite population incurrs a two-fold cost of anisogamy. It is important to note that although sexual reproduction is a necessary condition for this scenario, it is anisogamy that actually causes this cost.