Sexual compatibility made easy

Finding a partner as a fungus with 28,000 different sexes

Reproductive sex in most organisms requires compatibility. In humans, sexual compatibility is an entire field in itself populated by sex therapists, behavioral psychologists, and neuroscientists. But barring the complexity of human social behavior and returning to general biology, the biological concept of sexual compatibility is fundamentally a question of genetics: if two individuals have sex, will their genomes recombine with each other in a way that produces viable offspring?

In many species, including most animals and plants, reproduction requires compatibility of gametes, such as eggs and sperm. Typically, differences in gamete production among sexes are accompanied by physiological differences related to the creation or delivery of those gametes—we call these secondary sex characteristics.

However, in mushroom-forming fungi, very few species possess specialized sex organs or show any physical manifestations of a biological sex at all. Individuals of different sexes look, grow, and mate in the exact same way. This is because in many species of fungi, sex is not determined by physiology—it is instead determined by genes. Just one or two regions of the fungal genome are capable of specifying a fungus’s mating type by encoding systems of chemical recognition and compatibility.

Sexual compatibility systems in fungi can be bipolar or tetrapolar. Bipolar species possess one mating locus in their genome that can come in two varieties. This gives bipolar fungi two different mating types, which, because they don’t possess characters that would conform to an idea of “male” or “female”, are commonly denoted as +/- or a/α. This is roughly similar to other organisms that have an “either/or” two-sex mating system—in mating, the union of one of each mating type is required to produce offspring. It follows then, that any bipolar individual is sexually compatible with half of the population, including half of its siblings.

But the real fun begins when we talk about fungi whose mating systems are tetrapolar. Tetrapolar fungi have not one, but two separate, unlinked regions in their genome that jointly contribute to mating compatibility. These two mating loci are often referred to simply as A and B. Similar to bipolar fungi, each of these two mating loci have at least two different allelic variants, i.e. A1/A2 and B1/B2. This means that tetrapolar fungi can have at least four different sexes, depending on the combinations of mating alleles they possess (at minimum, either A1B1, A1B2, A2B1, or A2B2). Mating can only be achieved if the partners possess different allelic forms at both the A locus and the B locus. Therefore, a tetrapolar fungus will only have a one in four chance of being sexually compatible with its siblings—a sharp reduction in the potential for inbreeding when compared to organisms with two sexes!

And note above that I said tetrapolar fungi can have at least four sexes—most tetrapolar fungi actually have more than four. A lot more than four. One of the most common mushrooms in the world, Schizophyllum commune (which I’ve spotted growing year-round on trees along King’s College Circle), has over 300 known variants of the A mating locus

and over 90 variants of the B locus. When these 300 different A’s and 90 different B’s are assorted into different combinations in individuals of this species, this fungus is effectively given one of 28,000 different possible sexes! This means that when it comes time for S. commune to reproduce, it could successfully have sex with 99.98 percent of the other individuals in its species. Compare this to organisms that have a binary sexual system, where an individual’s chances of encountering a genetically compatible mate are a mere 50 percent. But it gets better: S. commune also retains the added bonus of tetrapolarity—despite being highly compatible with almost all other members of its species, it is still only compatible with a quarter of its siblings.

You may not like it, but this is what peak sexual performance looks like.

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