Evolution of Sexual Reproduction: a View from the Fungal Kingdom Supports an Evolutionary Epoch with Sex Before Sexes

Sexual reproduction is conserved throughout each supergroup within the eukaryotic tree of life, and therefore thought to have evolved once and to have been present in the last eukaryotic common ancestor (LECA). Given the antiquity of sex, there are features of sexual reproduction that are ancient and ancestral, and thus shared in diverse extant organisms. On the other hand, the vast evolutionary distance that separates any given extant species from the LECA necessarily implies that other features of sex will be derived. While most types of sex we are familiar with involve two opposite sexes or mating types, recent studies in the fungal kingdom have revealed novel and unusual patterns of sexual reproduction, including unisexual reproduction. In this mode of reproduction a single mating type can on its own undergo self-fertile/homothallic reproduction, either with itself or with other members of the population of the same mating type. Unisexual reproduction has arisen independently as a derived feature in several different lineages. That a myriad of different types of sex determination and sex determinants abound in animals, plants, protists, and fungi suggests that sex specification itself may not be ancestral and instead may be a derived trait. If so, then the original form of sexual reproduction may have been unisexual, onto which sexes were superimposed as a later feature. In this model, unisexual reproduction is both an ancestral and a derived trait. In this review, we consider what is new and what is old about sexual reproduction from the unique vantage point of the fungal kingdom.