A theoretical test of the DNA repair hypothesis for the maintenance of sex in eukaryotes.

The DNA repair hypothesis for the maintenance of sex states that recombination is necessary for the repair of double-strand DNA damage. In a closed (mitotic) genetic system crossing-over generates homozygosity. This reduces fitness if deleterious recessive alleles become expressed. Thus, outcrossing is required to restore heterozygosity destroyed by recombination. The repair hypothesis is tested by comparing outcrossing sexuality with a hypothetical parthenogenic strategy (the Prudent Reparator) which destroys as little heterozygosity during repair as possible. In the Prudent Reparator, repair of double-strand DNA damage results in a small amount of homozygosity due to gene conversion only, since this process does not render outside markers homozygous. Diploidy, deleterious recessives, multiplicative fitness and linkage equilibrium in mutation-selection balance are assumed. The average fitness of this population increases, and complementation (i.e. masking of recessives in heterozygous form) decreases with the rate of damage per locus. The equilibrium fitness of the Prudent Reparator can be well above that of the sexual population. A lower complementation ability of parthenogens may not be an impenetrable barrier to their successful establishment if the invader's genome is relatively uncontaminated by mutant alleles: there are always such genotypes in the sexual population. Thus, the Prudent Reparator could solve the problem of repairing damage as well as that of invading an existing outcrossing population. As we do not see this strategy widely adopted instead of sexuality, the repair hypothesis is likely to miss some essential feature of the evolution of sex.