Sex Without Sexes: Can the Cost of Finding a Mate Explain Diversity in Fungal Mating Systems?

Abstract

Synopsis Eukaryotes have evolved myriad ways of uniting gametes during sexual reproduction. A repeated pattern is the convergent evolution of a mating system with the fusion of larger gametes with smaller gametes (anisogamy) from that of fusion between morphologically identical gametes (isogamy). In anisogamous species, sexes are defined as individuals that produce only one gamete type. Although sexes abound throughout Eukarya, in fungi there are no biological sexes, because even in anisogamous species, individuals are hermaphroditic and produce both gamete types. For this reason, the term mating types is preferred over sexes, and, thus defined, only individuals of differing mating types can mate (homoallelic incompatibility). In anisogamous fungal species, there is scant evidence that there are more than two mating types, and this may be linked to genetic constraints, such as the use of mating types to determine the inheritance of cytoplasmic genomes. However, the mushroom fungi (Agaricomycetes) stand out as having both large numbers of mating types within a species, which will allow nearly all individuals to be compatible with each other, and reciprocal exchange of nuclei during mating, which will avoid cytoplasmic mixing and cyto-nuclear conflicts. Although the limitation of mating types to two in most fungi is consistent with the cyto-nuclear conflicts model, there are many facets of the Agaricomycete life cycle that also suggest they will demand a high outbreeding efficiency. Specifically, they are mostly obligately sexual and outcrossing, inhabit complex competitive niches, and display broadcast spore dispersal. Subsequently, the Agaricomycete individual pays a high cost to being choosy when encountering a mate. Here, I discuss the costs of mate finding and choice and demonstrate how most fungi have multiple ways of reducing these costs, which can explain why mating types are mostly limited to two per species. Nevertheless, it is perplexing that fungi have not evolved multiple mating types on more occasions nor evolved sexes. The few exceptions to these rules suggest that it is dictated by both molecular and evolutionary constraints.