The Rewiring of Who Mates with Whom: Evolutionary Transitions of Mating Systems, Mating Classes and Their Genetic Architecture

Sexual reproduction in eukaryotes typically involves the merging of gametes, cells, or nuclei belonging to different mating classes, such as small and large gametes, mating types, or sexes. In this review, we combine theoretical results, recent genomic data, and documented changes in mating systems among ciliate, fungal, plant, algal, and animal lineages to identify general patterns in the evolution of mating classes and their underlying genetic architectures. We emphasize how interactions among distinct coexisting "layers" of mating classes within a species (e.g., anisogamy plus self-incompatibility systems) have shaped their evolution. We raise key unresolved questions, including why no species appears to maintain more than three coexisting layers of mating classes.