Evolution of a bipolar sexual compatibility system in <i>Marasmius</i>

Sexual compatibility in the Basidiomycota is governed by genetic identity at one or two loci, resulting in compatibility systems called bipolar and tetrapolar. The loci are known as <i>HD</i> and <i>P/R</i>, encoding homeodomain transcription factors and pheromone precursors and receptors, respectively. Bipolarity is known to evolve either by linkage of the two loci or by loss of mating-type determination of either the <i>HD</i> or the <i>P/R</i> locus. The ancestor to basidiomycete fungi is thought to have been tetrapolar, and many transitions to bipolarity have been described in different lineages. In the diverse genus <i>Marasmius</i> (Agaricales), both compatibility systems are found, and the system has been shown to follow the infrageneric sections of the genus, suggesting a single origin of bipolarity. Here, we tested this hypothesis using a comprehensive phylogenetic framework and investigated the mode by which bipolarity has evolved in this group. We utilized available genomic data and marker sequences to investigate evolution of sexual compatibility in <i>Marasmius</i> and allied genera. By generating a concatenated multilocus phylogeny, we found support for a single transition to known bipolarity within <i>Marasmius</i>. Furthermore, utilizing genomic data of the bipolar species <i>Marasmius oreades</i>, we found that the <i>HD</i> and <i>P/R</i> loci likely have remained unlinked through this transition. By comparing nucleotide diversity at the <i>HD</i> and <i>P/R</i> loci in <i>Ma. oreades</i>, we show that the <i>HD</i> locus has retained high diversity, and thus likely the function of determining sexual identity, as similarly in other bipolar mushroom-forming fungi. Finally, we describe the genomic architecture of the <i>MAT</i> loci of species of both sexual compatibility systems in Marasmiaceae and related families.