The genetic architecture of the load linked to dominant and recessive self-incompatibility alleles in Arabidopsis halleri and A. lyrata

Abstract

The long-term balancing selection acting on mating-types or sex determining genes is expected to lead to the accumulation of deleterious mutations in the tightly linked chromosomal segments that are locally “sheltered” from purifying selection. However, the factors determining the extent of this accumulation are poorly understood. Here, we take advantage of the large number of alleles at the sporophytic self-incompatibility system of the Brassicaceae along a complex dominance hierarchy to evaluate how the pace at which linked deleterious mutations accumulate varies with the intensity of balancing selection. We first experimentally measured the phenotypic manifestation of the linked load at three different levels of the dominance hierarchy. We then sequenced and phased polymorphisms in the chromosomal regions linked to 126 distinct copies of S -alleles in two populations of Arabidopsis halleri and three populations of A. lyrata . We find that linkage to the S -locus locally distorts phylogenies over about 10-30kb along the chromosome. The more intense balancing selection on dominant S -alleles results in greater fixation of deleterious mutations, while recessive S -alleles accumulate more linked deleterious mutations that are segregating. Hence, the structure rather than the overall magnitude of the linked genetic load differs between dominant and recessive S -alleles. Our results have consequences for the long-term evolution of new S -alleles, the evolution of dominance modifiers between them, and raise the question of why the non-recombining regions of some sex and mating type chromosomes expand over evolutionary times while others, such as that the S -locus of the Brassicaceae, remain restricted to small chromosomal regions.