Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution

Cell type in budding yeasts is determined by the genotype at the mating-type (MAT) locus, but yeast species differ widely in their mating compatibility systems and life cycles. Among sexual yeasts, heterothallic species are those in which haploid strains fall into two distinct and stable mating types (MATa and MATα), whereas homothallic species are those that can switch mating types or that appear not to have distinct mating types [1, 2]. The evolutionary history of these mating compatibility systems is uncertain, particularly regarding the number and direction of transitions between homothallism and heterothallism, and regarding whether the process of mating-type switching had a single origin [3-5]. Here, we inferred the mating compatibility systems of 332 budding yeast species from their genome sequences. By reference to a robust phylogenomic tree [6], we detected evolutionary transitions between heterothallism and homothallism, and among different forms of homothallism. We find that mating-type switching has arisen independently at least 11 times during yeast evolution and that transitions from heterothallism to homothallism greatly outnumber transitions in the opposite direction (31 versus 3). Although the 3-locus MAT-HML-HMR mechanism of mating-type switching as seen in Saccharomyces cerevisiae had a single evolutionary origin in budding yeasts, simpler "flip/flop" mechanisms of switching evolved separately in at least 10 other groups of yeasts. These results point to the adaptive value of homothallism and mating-type switching to unicellular fungi.