Evolution of recombination due to random drift

In finite populations subject to selection, genetic drift generates negative linkage disequilibrium, on average, even if selection acts independently (i.e. multiplicatively) upon all loci. Negative disequilibrium reduces the variance in fitness and hence, by FISHER's Fundamental Theorem (1930), slows the rate of increase in mean fitness. Modifiers that increase recombination eliminate the negative disequilibria that impede selection and consequently increase in frequency by 'hitch-hiking'. In addition, recombinant progeny are more fit on average than non-recombinant progeny when there is negative linkage disequilibrium and loci interact multiplicatively. For both these reasons, stochastic fluctuations in linkage disequilibrium in finite populations favor the evolution of increased rates of recombination, even in the absence of epistatic interactions among loci and even when disequilibrium is initially absent. The method developed within this paper quantifies the strength of selection on a modifier allele that increases recombination due to stochastically generated linkage disequilibria. The analysis indicates that, in a population subject to multiplicative selection, genetic associations generated by drift do select for increased recombination, a result that is confirmed by Monte Carlo simulations. Selection for a modifier that increases recombination is highest when linkage among all loci is tight, when beneficial alleles rise from low to high frequency, and when the population size is small.