Read more from Slate's Sex Issue.
Why is the mating game almost always a dance of two, whether the scene is a swank Manhattan watering hole or the shallows of an average pond? Why not three or four possibilities, or even more?
Binary mating began to evolve way back when, and over time became entrenched, especially in more complex creatures. Biologists inevitably disagree about what, exactly, constitutes a sex, and therefore how "sexes" are to be counted. (They also wonder why sexual reproduction came to exist at all.) But if the working definition focuses on the type of sex cell being produced, we can say that sperm-producers are males and egg-producers are females. And it becomes clear that no third sex cell—and so no third sex—has appeared in multicellular animals. There are oddball critters, like clam shrimp and some harvester ants, in which three- or even four-sex scenarios might be said to exist. But only if we're willing to expand (or finagle) the definition of a sex.
Why do most sexual creatures do binary mating? It's actually a counterintuitive system. Consider the plight of single-celled green algae trying to hook up in a pond. At first glance, the lack of more than one mating choice among these algae seems strange. After all, if there were 10 equally prevalent types of mates, and a cell could fuse with any type other than its own, it would have nine shots in 10 of bumping into a potential partner just floating around blindly. If there were three mating types, its chances would drop to two in three. And with only two, they fall to one in two. In other words, assuming that it takes some effort to find a mate, the two-type system is "the least efficient solution" for this population, says Laurence Hurst, an evolutionary geneticist at the University of Bath.
The best-known answer to this apparent puzzle involves the inheritance of DNA outside the nucleus of a cell. Hurst focuses on crucial cellular structures called mitochondria. Their job is to generate energy for the cell, and they contain their own DNA, separate from the nuclear genome. When two parent cells fuse, we might expect both to contribute mitochondria to the offspring. But that's typically not what happens. Because genetic mutations can make mitochondrial DNA replicate faster, at the expense of some genes that are good for the cell, normal mitochondria would be driven out if both parent cells contributed. To avoid this problem, Hurst argues, natural selection may have favored divvying up the roles, so that one mating type would usually pass on mitochondria (and other goodies) and the other usually would not. (For mathematical modeling of these ideas, click here and here.)
Hurst has some evidence for his theory, albeit indirectly. In some single-celled ciliates, mating occurs by swapping nuclei rather than by fusing. Mitochondria from both parents are unlikely to end up in the same cell, so there's less reason to expect these creatures to be restricted to two mating types. And indeed, they aren't. Here's another take on precursors to two-mating-type systems.
Once binary mating systems were in place, they probably helped set the stage for the familiar sperm-and-egg odd couple. In most animals, some individuals (males) produce lots of small, motile sperm, while others (females) invest in a smaller number of larger eggs and try to position them to get fertilized. These approaches are evolutionary winners. Mathematical models suggest that "anything in between would be at a selective disadvantage," says Brian Charlesworth of the University of Edinburgh. This may explain why no third type of sex cell has evolved in multicellular animals—and therefore, no third sex.
Still, nookie can get weird out there. Consider clam shrimp, for instance, which are crustaceans with folded carapaces and antennae that spin around like helicopter blades while the creatures swim, rather inefficiently. According to Stephen Weeks of the University of Akron, clam shrimp seem to come in three reproductive varieties: males, who carry two Z chromosomes, and two subgroups of hermaphrodites, one of which is ZW and the other WW. In other words, there are three sexual genotypes created by three possible pairings of sex chromosomes. Here's how these pairings came about. Does this count as three sexes? Weeks says he prefers to say clam shrimp have three "breeding types" to get around the question of whether the hermaphrodites (ZW and WW) should be considered distinctive sexes.
Certain harvester ants (of the genus Pogonomyrmex, if you really want to know) could also be said to have three sexes, or even four. These ants live in colonies, each of which has a queen. For the ants to be fruitful and multiply, she needs to mate with two different strains of male. She needs the sperm of one type of male to make future queens and the sperm of the other type of male to make future workers. So, the colony must include sex cells from "parents" of three different sexes, says Joel Parker, an evolutionary biologist at the University of Southampton. Two parents for each ant, three parents for each colony.
And four sexes for the population, Parker argues. That's because there are two strains of queens in this ant population, which is probably a hybrid of two different species that became genetically interdependent. If any one of these four types were to go missing, the system as a whole would collapse, Parker argues. And so, the four types necessary for systemwide survival could be considered sexes.
Clearly, clam shrimp and harvester ants are way out on a biological limb, where Middlesex meets Big Love—and where sex therapists would have a field day if only these critters could talk.