From a human perspective, sexes seem a relatively simple thing to get one's head around—there are females, and there are males. But our perspective seems biased and narrow when applied to life as a whole, says evolutionary biologist Laurence Hurst of the University of Bath, United Kingdom.“If you were a single-celled alga sitting in a pond, you wouldn't see the world as splitting into males and females.”
In fact, different species have evolved a bewildering number of ways to mix and match the attributes of sexes. Some do not have males and females, but have adaptations that mean each individual performs a specific role during sex. There are other species of which every member is sexually equivalent, but individuals nevertheless divide into groups for the purposes of mating. And in some species, individuals make both eggs and sperm (Box 1). This biological diversity has produced a semantic muddle among biologists—everyone who thinks about the evolution of sexes seems to have a slightly different take on what a sex is. “The literature is highly confusing—we need to clarify our terminology,” comments Rolf Hoekstra, a geneticist at the University of Waageningen in the Netherlands.
Box 1. The Best of Both Worlds? One option for dividing up the sexes is “both”—hermaphroditism. This might seem like an ideal solution—everyone becomes a potential partner, and everyone can bear offspring. In practice, however, hermaphroditism is uncommon among multicellular animals. The reasons are similar to those explaining why evolution favors unequal-sized gametes—once sexes have evolved, it's better to commit all one's resources to one role or the other, rather than try and be a jack-of-all-trades. After all, there are many good uses for mating resources other than simply producing eggs or sperm. An animal could defend a territory or provide parental care, for example. Hermaphroditism, however, is useful if one's sexual options are severely limited. In particular, it can be favored when encounters with potential mates are extremely rare. It makes no sense for an animal to invest heavily in the biological equipment of maleness, say, if it will have almost no opportunities to use it: better to hedge your bets. Animals with low or unpredictable population densities and those that are immobile, have poor senses, or lack long-distance signalling are often hermaphroditic. These include sponges, worms—whether flat, nematode, or annelid—and many molluscs (and, of course, plants, the majority of which are hermaphroditic). Most hermaphrodites still need to find at least one mate in their lifetimes: the cost of inbreeding prevents self fertilization from becoming common. Hermaphroditic animals have some weird sexual adaptations. Helix aspersa snails shoot calcareous love darts into one another. And when the marine flatworm Pseudobiceros bedfordi mates, each worm has two penises, which they fence with in a battle to smear one another with sperm without being fertilized themselves in the process (Figures 1 and 2). Such oddities result when the mating opportunities of a hermaphroditic species increase, and specialization starts to become more favorable, says evolutionary biologist Nico Michiels, of the University of Muenster in Germany. In a species with two separate sexes, males and females often have different ideas about whether a mating is a good idea—males tend to be keener, females tend to be choosier. The result can be an evolutionary arms race, with each sex evolving adaptations that help them get their way. By exercising mate choice, each sex has some influence on the types of adaptations that evolve—anything too outlandish is unlikely to be favored. This counterbalance is not present in hermaphrodites, however. Rather than having one half of a species resist a particular mating strategy, the whole species is just as likely to adopt it. “Hermaphrodites run into awkward and bizarre mating conflicts,” says Michiels. Michiels believes that hermaphroditism was the ancestral state for animals, and thinks that we might be able to find the relics of this past in contemporary species with separate sexes. To test these ideas, he is searching for groups containing closely related hermaphroditic and bisexual species. Such taxa are very rare, however. |
As things stand, there are three main aspects to the definition of a sex: who you are, who you can mate with, and who your parents are. The third part of this trinity—parental number—shows the least variation in nature. No known organism needs more than one mother and one father. But even this assumption is now starting to break down at the level of biological systems. In a recently discovered hybrid system within the harvester ant genus Pogonomyrmex, queens must mate with two types of males to produce both reproductive individuals and workers (Figure 3). These ants are the first species known which truly has more than two sexes—with colonies effectively having three parents— argues Joel Parker of the University of Lausanne, Switzerland.
Parker's ideas might reactivate evolutionary biologists' interest in sexes, which has lain somewhat dormant since the 1990s. It could also provide a new route to experiments— something often lacking in the field. Not everyone agrees that it makes sense to define the ants' genetic quirks as new sexes. Each ant is still only a mix the genes from no more than two parents, after all. But Parker believes that our current ideas about mating systems may not be adequate to describe the ingenuity of evolution. “Until you see a three-sex system, you don't know what it'll look like,” he says.