Coalescence and Linkage Disequilibrium in Facultatively Sexual Diploids

Abstract

Abstract Under neutrality, linkage disequilibrium results from physically linked sites having nonindependent coalescent histories. In obligately sexual organisms, meiotic recombination is the dominant force separating linked variants from one another, and thus in determining the decay of linkage disequilibrium with physical distance. In facultatively sexual diploid organisms that principally reproduce clonally, mechanisms of mitotic exchange are expected to become relatively more important in shaping linkage disequilibrium. Here we outline mathematical and computational models of a facultative-sex coalescent process that includes meiotic and mitotic recombination, via both crossovers and gene conversion, to determine how linkage disequilibrium is affected with facultative sex. We demonstrate that the degree to which linkage disequilibrium is broken down by meiotic recombination simply scales with the probability of sex if it is sufficiently high (much greater than 1/N for population size N). However, with very rare sex (occurring with frequency on the order of 1/N), mitotic gene conversion plays a particularly important and complicated role because it both breaks down associations between sites and removes within-individual diversity. Strong population structure under rare sex leads to lower average linkage disequilibrium values than in panmictic populations, due to the influence of low-frequency polymorphisms created by allelic sequence divergence acting in individual subpopulations. These analyses provide information on how to interpret observed linkage disequilibrium patterns in facultative sexuals and to determine what genomic forces are likely to shape them.