Multidimensional epistasis and the disadvantage of sex

Sex is thought to facilitate accumulation of initially rare beneficial muta tions by allowing simultaneous allele replacements at many loci. However, t his advantage of sex depends on a restrictive assumption that the fitness o f a genotype is determined by fitness potential, a single intermediate vari able to which all loci contribute additively, so that new alleles can accum ulate in any order. Individual-based simulations of sexual and asexual popu lations reveal that under generic selection, sex often retards adaptive evo lution. When new alleles are beneficial only if they accumulate in a prescr ibed order, a sexual population may evolve two or more times slower than an asexual population because only asexual reproduction allows some overlap o f successive allele replacements. Many other fitness surfaces lead to an ev en greater disadvantage of sex. Thus, either sex exists in spite of its imp act on the rate of adaptive allele replacements, or natural fitness surface s have rather specific properties, at least at the scale of intrapopulation genetic variability.