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In the majority of sexual organisms, reproduction occurs almost exclusively through the combination of distinct and alternate forms, called sexes or mating types. In some fungi, there can be dozens to hundreds of alternate alleles that determine compatible mating types. Such extensive polymorphism is expected to be maintained by balancing selection, and in extreme cases may give rise to trans-specific polymorphism. Here, we analyzed sequences of two pheromone receptors in the Microbotryum fungal species complex (Basidiomycota), which has only two alternate mating types. Several lines of evidence strongly suggest that the pheromone receptors are two allelic sequences acting to determine the alternate A1 and A2 mating types required for mating in Microbotryum. Phylogenetic trees of pheromone receptors in the Microbotryum species complex indicated a trans-specific polymorphism: the Microbotryum sequences from a given mating type were all more similar to the pheromone receptors of distantly related classes of fungi than to the alternate pheromone receptor in the Microbotryum species. A phylogenetic tree built using other known pheromone receptors from basidiomycetes showed that trans-specific polymorphism is widespread. The pheromone receptor alleles from Microbotryum appeared as the oldest, being at least 370 million years old. This represents the oldest known trans-specific polymorphism known in any organism so far, which may be due to the existence of sex chromosomes, obligate sexuality, mitochondrial inheritance linked to the mating type, and a highly selfing mating system in Microbotryum.

Ancient Trans-specific Polymorphism at Pheromone Receptor Genes in Basidiomycetes