Maximum-likelihood estimation of rates of recombination within mating-type regions

Features common to many mating-type regions include recombination suppression over large genomic tracts and cosegregation of genes of various functions, not necessarily related to reproduction. Model systems for homomorphic self-incompatibility (SI) in flowering plants share these characteristics. We introduce a method for the exact computation of the joint probability of numbers of neutral mutations segregating at the determinant of mating type and at a linked marker locus. The underlying Markov model incorporates strong balancing selection into a two-locus coalescent. We apply the method to obtain a maximum-likelihood estimate of the rate of recombination between a marker locus, 48A, and S-RNase, the determinant of SI specificity in pistils of Nicotiana alata. Even though the sampled haplotypes show complete allelic linkage disequilibrium and recombinants have never been detected, a highly significant deficiency of synonymous substitutions at 48A compared to S-RNase suggests a history of recombination. Our maximum-likelihood estimate indicates a rate of recombination of perhaps 3 orders of magnitude greater than the rate of synonymous mutation. This approach may facilitate the construction of genetic maps of regions tightly linked to targets of strong balancing selection.