The Wilder Side of Sex
by John Tidwell

So there you are, gazing proudly at all those cute, colorful reef fish in your saltwater aquarium, serene in the knowledge that you know precisely which fish is what, right down to the species’ names and the individuals’ genders. But wait—weren't there supposed to be two red female stoplight parrotfish? How the heck did a green male get in there?

Better get used to it—he used to be a she. In the wild, gender ambiguity is natural and practically anything goes, as long as it works. For the past couple billion years, plant and animal species have tried all sorts of ways to solve the problem of how to survive and make as many babies as possible. In that time, they evolved a mind-reeling array of solutions.

From protozoa to pill bugs to porgies, changing from one sex to another is not just biological ingenuity, it’s a way of life. It’s also shocking proof that gender is a much more versatile, flexible tool in Mother Nature’s kit than anyone had previously realized—and is kinkier than you ever imagined. Your very green, very male stoplight parrotfish eyes you knowingly through the glass, as if to say “You ain’t seen nothin’ yet!” What in the name of Charles Darwin is going on here?

The Spice of Life
Consider the humble two-banded anemonefish (Amphiprion bicinctus) nestled like a sultan upon a bed of pink-tipped sea anemone tentacles. Here in the shallows of the Red Sea, this small, orange-and-white fish lives in cozy symbiosis with its flower-like protector, rarely ever venturing farther than a tentacle’s reach from home. When our male anemonefish chances upon another male of the species, what happens? Does he puff himself up, large and frightening, challenging the interloper to a battle royale? Not at all. Mr. Amphiprion starts to transform into a Ms. and invites the other fish to mate. Nobody gets hurt and in time both get to loft their genes into the next generation. Perched upon their anemone, the two will live in prim monogamy until death do them part. At which time, the survivor may once again shift gender to secure a mate.

Consider the lilies-of-the-valley (Convallaria majalis) in a glade as they nod their tiny white flowers in the afternoon sun. Look a little more closely, and you might notice that those pristine flowers have male and female sex organs simultaneously. These lilies, like a wide variety of flowering plants, are hermaphrodites: They have sex with, and fertilize, themselves.

Beneath the lilies lies a rotting log, home to a tiny organism that isn’t a plant or an animal or a fungus. It looks like a blob of scrambled eggs, but in fact it’s a slime mold (genus Physarum), an otherworldly creature with 29 variants of sex-controlling genes, dispersed among eight different types of sex cells. To ensure genetic diversity, each slime mold sex cell can only fuse with a sex cell that has completely different variants of genes than its own. If you calculate all the possible combinations of genes and sex cells, you will find that Physarum have more than 500 different sexes. Reproduction for slime molds may be complicated, but it’s never boring.

Weird sex is all around us, in the earth beneath our feet, the air above our heads, and the sea from which we all evolved. In fact, sex itself remains an unanswered biological enigma that has confounded scientists for decades. Since the 1960s, when traditional models of sex were scrapped (due to lack of evidence), evolutionary biologists have spawned great schools of competing theories to explain why sex exists at all. But in this Darwinian scramble, one theory—The Red Queen—has emerged in recent years to dominate them all.

The Red Queen
This poetic model, plucked from the pages of Lewis Carroll’s Through the Looking-Glass, envisions a frenetic world where the notion “every gene for itself” reigns supreme. Just like Alice and the Red Queen, who find themselves running to stand still, evolution is a treadmill where all creatures must run like mad just to stay in the same evolutionary spot.

In his 1993 book The Red Queen, science writer Matt Ridley explains that in this theory, baby-making is more business than pleasure. “Sex is not about reproduction,” he writes. “Gender is not about males and females, courtship is not about persuasion, fashion is not about beauty and love is not about affection.” It is about getting your genes into the next generation, and trumping the Terrible Three: predators, parasites, and the neighbors. Of that trio, parasites rank as the greatest foe. According to Ridley, parasites have been more deadly to our species (for example) than all the lions, wars, and accidents that have ever killed anyone. World War I killed 25 million people in four years, he writes, while the 1918 flu that followed killed 25 million people in four months.

Sexual reproduction helps individuals get ahead in this great struggle, allowing creatures to mix their genes and produce hybrid offspring that might have better resistance to parasites. Asexual creatures, which are nearly always female, can make more babies than their sexual neighbors, but they are all clones—nearly exact copies of their mothers.

If an asexual mother were vulnerable to say, pneumonia, so would all her daughters be, and an entire generation could be wiped out by a sneeze. Many evolutionary biologists surmise that the reason males exist at all, and therefore sex exists, is to provide an extra genetic edge, even though it means that only half of a population can actually give birth.

But just because some creature wriggling in the muck billions of years ago invented boys and girls doesn’t mean parasites are beaten. The credo of the Red Queen is that for every action there is a reaction: Each time you mount a defense, the bugs will come up with a way around it. Even sex itself isn’t the only way to stay healthy and cover the Earth with progeny. For lots of creatures sexual reproduction is a choice, one wrench in their biological toolbox.


Boys Will Be Girls and Girls Will Be Boys
Water fleas (genus Daphnia) are freshwater crustaceans that look like tiny translucent Pokemons, hopping through the water on fan-like fins that never seem to tire. When tasty algae are plentiful and there’s lots of elbow room, everyone is female and asexual. But if the living gets too easy, and the pond becomes overcrowded with Daphnia, suddenly males are hatched. They mate with females, which produce eggs that hatch when the pond gets flooded again with rain. For these water fleas, sex can be turned on or off as needed. Daphnia aren’t the only ones to do this either: Your lovely green lawn remains asexual until you forget to mow it. Then sexual flower heads emerge and send pollen and seeds off on the wind. Kinky? Perhaps, but it also indicates that the world around us plays as powerful a role as DNA in determining how organisms reproduce.

There are more ways for gender to be decided than the genetic X meets Y that mammals and birds seem to prefer. Other beasties depend on cues from their surroundings. Some reptiles, such as alligators (genus Alligator) and painted turtles (genus Chrysemys), let the sand their eggs are buried in make the choice: Hot sand makes males, and cooler sand makes females. Some microscopic parasites have also been found to commandeer the sex lives of arthropods (insects, crustaceans, and spidery types), and determine not only the gender of their hosts’ offspring, but also the very direction of their evolution (see sidebar).

“These days you can’t even talk about genes being separate from the environment, the lines are so blurred,” explains Marlene Zuk, an evolutionary biologist from the University of California, Riverside. “Whether it’s reproduction or even gender determination, you start realizing that you can’t separate out the purely genetic because how the genes are manifested depends on environmental forces.”

That’s Environment with a big E, which means not only the Terrible Three, but also weather, geography, the local social group, and other organisms’ genes that are busy attacking your own (which is what happens when you get sick). What does all this have to do with sex change? Everything. For now, let’s stick with animals. Any critter that bends its own gender is, by definition, a hermaphrodite, with sex cells or organs of both male and female. Hermaphrodites come in two basic flavors: Those that permanently function as both genders are known as simultaneous hermaphrodites, while those that shift back and forth are called sequential hermaphrodites. One of the best places to find either of these varieties, should you be inclined, is beneath the ocean waves.

Here at the local reef, having the ability to fertilize yourself is great if you’re immobile, like barnacles or coral polyps: You don’t need to depend on whatever mate happens to slither by. For spineless creatures on the go, being double-sexed often leads to orgies. Sea hares (Aplysia dactylomela) are snails without shells that are male in front and female behind, leading them to form erotic daisy chains that can involve a dozen or more animals at once. Slipper limpets (aptly named Crepidula fornicata) are male while free-swimming and female when they settle down on a rock. When a male swims by a female slipper limpet, he flops onto her to mate. If another male lands on top of him, the lower male turns female, and they clasp. And so on, and so on. Scientists have recorded up to 14 limpets at a time pancaked into towers of lust. Invertebrates take the prize for most sexes, genders, sex organs, and acrobatic means of coitus, but when it comes to vertebrate hermaphrodites, something is definitely fishy.

Hamlets (genus Hypoplectrus) are small tropical fish that sometimes are blue, but are certainly not melancholy. Like most reef fish they are hermaphrodites, but of the simultaneous persuasion. When two hamlets meet they don’t soliloquize, they pair and have a lovely time assuming one sex role and then the other. And pair they do. Hamlets hold the sex-shifting record, switching from one set of gonads to the other and back in 30 seconds or less, with an average of 14 spawns in one day. An amphibious Caribbean killifish called Rivulus marmoratus takes this even further: It doesn’t even look for a mate, but fertilizes itself. Rivulus is the only vertebrate known to science that can do this. But such creatures are an anomaly, a rare few species that are acrobatic and have the energy, will, and ability to haul around two separate reproductive tracts (not an easy proposition, evolutionarily speaking). Wouldn’t it be easier to start as one gender, and then carry the other in your wallet, just in case? Welcome to the world of the sequential hermaphrodites.


Why Can’t A Woman Be More Like A Man?
Pity the poor female cleaner wrasse (Labroides dimidiatus) who has lived happily in a harem with her sisters, protected and serviced by a virile, iridescent male. One day, tragedy strikes and Mr. Wrasse vanishes. Maybe he was eaten, or scooped up for somebody’s aquarium. Who knows—he’s gone. What’s a girl to do? Be the man, of course.

Ross Robertson of the Smithsonian Tropical Research Institute in Panama has been studying sex-changing reef fish for decades. In his research on polygamous wrasses, Robertson has seen it all happen again and again: As soon as the male is gone, the largest female in the harem begins to behave like a male: chasing the girls, swaggering around, and being macho. Inside her ovary, often within 24 hours, says Robertson, the female’s immune system is reabsorbing her eggs and turning on the testosterone. Within a week she (or rather he) will be producing viable, healthy sperm.

But how’s it done? The trick, says Robertson, is that these fish may be born female, but in a tiny pocket in their ovaries are hidden little stashes of undeveloped sperm cells, waiting for their moment to shine. When the social environment demands it, girls become boys. And that’s the key—sex shifting only occurs where it’s needed for survival. You don’t see sex change in open-water fish that school and breed in large shoals. With clouds of sperm and eggs swirling around in the crowd, who cares what gender you are? But when fish are living in a very specific place, like a sea anemone or a particular head of coral, in a very socially stratified community, being able to swing both ways sexually means you will always get a date (and your eggs fertilized).

And what of our sweet young anemonefish with the hunky boyfriend and a gaggle of babies? How does such a thing happen to a guy? Actually in much the same way, says Robertson. Among these AC/DC hermaphrodites, females that turn into males are called protogynous, while boys that become girls are protandrous. Since the default sex for most vertebrates is female, more creatures tend to be protogynous. But what gender you are (at that particular moment) is of less importance among the sex-changing set than how big you are. “In protogynous fish it pays to be female when you’re small and male when you’re large,” says Robertson. “If you can’t set up your territory when you’re small because you’ll get the hell kicked out of you by a bigger male, then you’re better off being female. Once you get to a certain size, and you have the capacity to hold territory and get a harem, then you’re better served being male.”

The flipside for protandrous fish is that it’s easy for your body to make sperm when you are small, because sperm takes less energy and resources than eggs. But when you get big and beefy, you have more stuff to make large, nutritious eggs, and then it’s better (reproductively) to be a girl.

Then there are some species that put sex shifting into overdrive. The small-eyed goby (Gobiodon micropus) is a protogynous fish that is ready to dance to any tune. Put her with a larger female, and she becomes male. Plop down a bigger, meaner male, and this goby turns back into a female. And contrariwise.

Protandry and protogyny are not just for fish either. You can find them among the bees of the air and the sawgrass of the fields. Where you don’t find hermaphrodites of any stripe is in mammals and birds. How come? Why aren’t we all sex-changing hermaphrodites? Ross Robertson has a convincing answer: “In fish, all you’re doing is changing the contents of a bag—that’s all a testes or an ovary is in a fish. Whereas in mammals, you have an enormous number of differences between the sexes, probably controlled by a whole host of genes. I mean, replumbing the entire animal, redoing the whole skeleton, changing its brain and everything else, would be very difficult and extremely costly for the animal.”

Alas, the truth is no one really knows for sure. Asking evolutionary biologists such questions is like asking a group of Englishmen the best way to make tea: You get a deluge of conflicting and adamant opinions. These scientists do agree that in nature, gender is not something fixed and immutable, but a survival strategy. Some use genes, some use temperature, others use the social club, and some (probably most) use all of the above. The only rule is “survive and reproduce.” If you can manage that and it feels good, do it! “And that,” says the Red Queen with a smile, “Is what it’s all about.”

—John Tidwell is a freelance journalist living in Silver Spring. He has written numerous articles on conservation for ZooGoer, as well as articles on history for American Heritage and American Legacy magazines.

ZooGoer 33(2) 2004. Copyright 2004 Friends of the National Zoo.
All rights reserved.