Abstract

Sex chromosomes can display successive steps of recombination suppression known as “evolutionary strata”, which are thought to result from the successive linkage of sexually antagonistic genes to sex-determining genes. However, there is little evidence to support this explanation. We show that evolutionary strata have evolved repeatedly without sexual antagonism in fungi : we found in anther-smut fungi suppressed recombination extending beyond loci determining mating compatibility despite lack of male/female roles associated with their mating types. By comparing full-length chromosome assemblies from anther-smut fungi with or without recombination suppression in their mating-type chromosomes, we inferred the ancestral gene order and derived chromosomal arrangements in this group. This approach shed light on the chromosomal fusion underlying the linkage of mating-type loci in fungi and multiple independent cases of chromosomal rearrangements leading to regions of suppressed recombination linking these mating-type loci in closely related species. Such convergent transitions in genomic architecture of mating-type determination indicate strong selection favoring linkage of mating-type loci into cosegregating supergenes. We also found multiple independent evolutionary strata (stepwise recombination suppression) in several species over a range of ages in mating-type chromosomes. Several evolutionary strata did not include genes involved in mating-type determination. The existence of strata devoid of mating-type genes were found in several other fungi and even around other types of supergenes, despite the lack of sexual antagonism, calls for a unified theory of sex-related chromosome evolution. We therefore developed a theoretical model to test alternative hypotheses and showed that recombination suppression can be selected for sheltering deleterious alleles segregating in genomes near a permanently heterozygous allele.