Theoretical population genetics of mating-type linked haplo-lethal alleles

The anther-smut fungus Ustilago violacea normally produces haploid sporidia of two mating types, and conjugation between them is thought to be a prerequisite for infection of the host plant Silene alba. However, some natural populations contain high frequencies of individuals with mating-type bias, from which sporidia of only one mating type, usually A1, can be isolated. Such populations show no reduction in fungal transmission rate. The bias is most readily interpreted as caused by the presence of deleterious recessive alleles, "haplo-lethals," that are linked to mating type. Haplo-lethals may persist in a heterozygous state if, during teliospore germination, there is premature conjugation among the immediate products of meiosis, i.e., intratetrad selfing, whereby the free-living haploid stage is bypassed We develop a theoretical model that shows how such alleles may spread if they provide a compensatory advantage in the diploid or dikaryotic phase, for example, through increased disease transmission. There is a limited range of conditions under which such haplo-lethal alleles may be maintained in a stable polymorphism, but if intratetrad selfing is high and/or they have substantial advantage in the dikaryotic phase, haplo-lethal alleles linked to mating type can spread to fixation. The occurrence of populations with a high degree of mating-type bias is therefore readily explained. Haplo-lethal alleles unlinked to mating type are much less likely to spread. In U violacea, mating type shows first-division segregation; under such situations, haplo-lethal alleles may also readily spread if they are linked to another centromere.