Dr. Tatiana's Sex Advice to All Creation

by Olivia Judson

  Group Sexists in Santa Catalina

  Orgies beneath the waves! I can just see it: a cozy, copulating chain of beautiful creatures that resemble snails who’ve lost their shells and are hiding the fact with delicate colored folds of membrane. You sea hares are obviously so intent on your orgies that you’re ignorant of the ways of other hermaphrodites. Not all hermaphrodites have orgies—they get up to all kinds of other hanky-panky instead. Let me give you a sampler.

  Exhibit A: the black hamlet fish, a small carnivorous fish that lives in the tropics. An hour or two before sunset, any fish in a sensual mood will cruise the edge of a reef and find a mate. The couple will then take turns playing the male or the female, swapping roles after each bout of spawning.

  Exhibit B: Diplozoon gracile, a parasitic fluke that lives on the gills of fish. Mating pairs turn into a fluke version of Siamese twins: they actually fuse together permanently, their genitalia in contact in perpetuity. I hope they never take a dislike to each other.

  Exhibit C: the European giant garden slug, Limax maximus. To prepare for a tryst, two slugs sit together on a tree branch and secrete mucus for about an hour—pretty kinky. Then they wrap their bodies together and dive headfirst off the tree. Instead of plunging to the ground below, they hang in the air, suspended on a mucus rope. As they dangle upside down, they unfurl their pale, ribbonlike penises from the sides of their heads. The penises also dangle (about three centimeters below the loving couple), entwined, their tips pressed together to exchange sperm. Neither partner actually penetrates the other—and the session lasts for hours. In Limax redii, a close cousin, which likewise has its penis on its head and conducts sex upside down in midair, the penises dangle a full eighty-five centimeters, the length of three champagne bottles end to end. Talk about a head rush.

  Nonetheless, you ask an intriguing question: why aren’t we all hermaphrodites? Or, to put it another way, when is it better to be a hermaphrodite than to be a girl or a boy? The answer has nothing to do with orgies, I’m afraid.

  In the most general terms, hermaphrodites are predicted to evolve whenever the payoff—measured in nature’s usual currency, children—is greater for hermaphrodites than for individuals of only one sex. And when is this the case? Well, hermaphrodites may have an advantage if individuals live at low density, a situation that can make it difficult to find a mate. A hermaphrodite might be able to self-fertilize, and even if it can’t (or doesn’t want to), it will in principle be able to mate with everyone it meets. Alternatively, hermaphrodites may be better off when the extra trouble of being both sexes is negligible. Plants pollinated by bees or other creatures have to make beautiful, showy flowers whichever sex they are—so they incur little additional cost if they are both. Indeed, if pollinators are primarily attracted by pollen, then flowers that are exclusively female—and thus produce no pollen—may have no visitors. In contrast, plants pollinated by wind are limited not by how many pollinators they attract but by how much pollen they spread about or how much fruit they produce. In this case, then, individuals may do better if they specialize, making either pollen or fruit.

  How closely does the theory match the data? Well, flowering plants pollinated by wind do tend to be one sex or the other whereas those pollinated by animals do tend to be both. Beyond that observation, however, picking out trends is extremely difficult. Hermaphrodites are even more diverse than their sexual practices. They are found among most major groups of animals, from flatworms to fish, and among many groups hermaphroditism is the norm. In some groups, however, hermaphrodites are rare or absent. Of all the thousands and thousands of insect species, there are just one or two known hermaphrodites, for example. And among mammals, birds, reptiles, and amphibians, hermaphrodites are unheard of. More perplexing still, when you look at the distribution of hermaphroditic animals, there are no clear ecological associations (such as low density) that reliably occur with the trait. Among fish, for example, most species have males and females. Nonetheless, where hermaphroditism has evolved, it has done so in species that live in wildly different environments. You may recall our friend Rivulus marmoratus, who makes its home in mangrove swamps. Then there’s the aforementioned black hamlet fish, along with its relations, all tropical reef fish. And then there are the deep-sea hermaphrodites. In contrast, all comb jellies are hermaphrodites—except for a few species that live in the deepest seas. Or worse, compare bivalves—animals that have hinged shells, such as clams and mussels—with barnacles. Among bivalves, parasitic species tend to be hermaphrodites, while respectable free-living types tend to be one sex or the other. Among barnacles, however, it’s the reverse: free-living species are typically hermaphrodites, parasites have separate sexes. What’s going on?

  There are three reasons the picture is so confused. First, evolving from separate sexes to hermaphroditism—or vice versa—may not be easy. This is not something we know much about. But certainly to evolve from being one sex to being a hermaphrodite, an organism has to evolve a second functioning reproductive tract. Achieving this may be tricky, requiring several unlikely genetic events. Making such a transition is surely easier in some groups than in others. And even if the transition is genetically easy, other considerations may stand in the way. For example, hermaphrodites may have behaviors that stop separate sexes from catching on. In hermaphrodite societies—such as that of the black hamlet fish—where mating is based on the reciprocal trading of eggs or sperm, an individual who is only one sex may be discriminated against as a partner because he or she cannot play the game.

  The second reason for so confusing a picture is that such a variety of circumstances favors hermaphrodites: there’s no trademark hermaphrodite lifestyle. Finally, just where you might expect the emergence of hermaphrodites—as in low density—other, equally successful solutions may emerge. For example, being a hermaphrodite might not be the only way to find a mate when mates are few and far between. Instead, all candidates could assemble at a fixed time and place. The extraordinary mass spawnings of many marine animals, where millions mysteriously know to convene in the lagoon when the July moon is full (or whatever the signal happens to be), might be an instance of this. And I’d guess the dearth of hermaphroditic insects is due to the evolution of equally fruitful alternatives.

  I’d like to leave you with this last thought. Not all species have either males and females or hermaphrodites. Some have hermaphrodites and males. Some have hermaphrodites and females. And a few daring sorts—such as the Mexican bat-pollinated cactus Pachycereus pringlei—have some of everybody. Now that gives a tingle to “ménage à trois.”

  Dear Dr. Tatiana,

  There’s been a frightful accident. I was happily sitting in my usual spot at the bottom of the sea when I felt an itch on my nose. Being a green spoon worm, I don’t have arms and I couldn’t scratch. So I sniffed. And I inhaled my husband. I’ve tried sneezing, but he hasn’t reappeared. Is there anything I can do to get him back?

  Too Much Heavy Breathing near Malta

  There, there, it’s no use crying over snuffled husbands. He wanted to be snuffled, and he’s not coming back. By now he’ll have assumed his position in your androecium—literally, “small man room”—a special chamber in your reproductive tract where he can sit and fertilize passing eggs. How does he fit? The little chap is 200,000 times smaller than you: it’s as if a human male were no bigger than the eraser on the end of a pencil. You could keep a score of husbands without trouble.

  But you mustn’t disdain your diminutive lover. It’s only by chance that you escaped his fate. You see, when a green spoon worm larva first hatches, it has no sex. Instead, its sex is determined by the events of its first days. If, during this time, the larva encounters a female, it becomes male. If, after about three weeks, it hasn’t met a female, it settles into a comfortable crevice and becomes female itself.

  This probably sounds amazing—and in many ways it is. However, before talking about the strangeness of your sex life in more detail, I’d like to draw your
attention to a phenomenon that’s even more peculiar. You’ll probably agree that “male” or “female” is one of the most basic attributes an organism can have: after all, males and females reliably occur in millions of species. So you might imagine that the way a creature becomes male or female varies little from one species to the next—and that your situation is unique. You’d be wrong on both counts. Surprisingly, an organism’s sex is determined in ways that vary enormously. And you green spoon worms aren’t the only ones whose sex is determined by social milieu.

  Broadly speaking, sex is determined either by genetic or by environmental factors; within these two categories, however, there are all sorts of possible variations, many of which have evolved over and over again. For example, one of the most common ways sex is decided is by special chromosomes. Among mammals, males have an X and a Y chromosome, females have two X chromosomes. For birds, the situation is reversed. Males have two Z chromosomes, females have one Z and one W Fruit flies have XY males; butterflies have ZW females. Lizards swing both ways: some species have ZW females, others have XY males. It’s crazy. And that’s just chromosomes. I haven’t even mentioned all the critters where the males hatch from unfertilized eggs—a system thought to have evolved at least seventeen times—let alone species where sex is determined through horribly complicated interactions of many different genes.

  What about environmental factors? For many reptiles, what matters is the temperature at which their eggs are incubated. Thus, in alligators (and in still more lizards), you get girls when eggs are buried in cool sand and boys when the sand is warm; for many turtles, it’s the other way around. Snapping turtles and crocodiles are even wackier: eggs buried either in mounds of cool sand (around 20°C or 68°F) or hot sand (40°C or 104°F) hatch out girls, eggs buried in warm sand hatch out boys. More curious still, in Stictococcus sjoestedti, a tropical insect that sucks the sap of cocoa trees, eggs infected with a particular symbiotic fungus become females, uninfected eggs become males. And then, there are those like you whose sex is determined by social circumstance.

  For many individuals, this involves changing sex. In one species of Capitella, a worm partial to sewer sludge, males turn into hermaphrodites if they fail to encounter a female within a certain time. In the slipper limpet Crepidula fornicata (a notorious pest of oyster beds), everyone starts his career as a male. A fellow who finds himself alone, however, quickly turns into a female and starts attracting mates. Other slipper limpets pile on, gradually forming a louche limpet stack. In slipper limpet sex, it’s males on top: although small, they have splendidly long penises so they can fornicate with the female at the bottom. But as the stack continues to grow, the guys who were once at the top of the heap find themselves in the middle and change sex, resorbing their penises in the process, to become female. More exotic: the marine worm Ophryotrocha puerilis. If two females find themselves together, the smaller one changes into a male. But because females grow at a slower pace than males, the male will soon become the larger member of the pair. At this point—shazam!—both individuals change sex. Such reversals happen repeatedly. In the end, though, pairs that have been together for a long time end up by both turning into hermaphrodites. An enviable life.

  As a general rule, flexible gender is expected to evolve whenever an individual’s reproductive success as a male, female, or hermaphrodite differs greatly according to circumstances. Social milieu may not be the sole influence at work—if, for example, males can’t reproduce successfully unless they are big, it could be advantageous to start life as a female and become male only on achieving a good size. The ability to choose your sex is particularly handy, however, when being one sex leads to a riskier life than being the other.

  Which brings me back to you. A female green spoon worm takes a greater gamble in life than a male does. She needs two years to mature, during which she may be eaten by a bat ray, and on reaching adulthood she may never find a mate. So it makes sense for a larva who meets a female to become male: not only is he guaranteed a mate, but he can start reproducing as soon as he’s installed himself. What is it about you that makes a larva want to be a man? Well, your lovely bulbous body—but particularly your long, twitchy proboscis—secretes a substance known as bonellin, after your formal name, Bonellia viridis. A whiff of bonellin makes any larva stand up and fly right.

  But what you’re really dying to know, I suspect, is why your lovers are so minute: what strange circumstances prompt natural selection to reduce a man to a testicle? Two factors are thought to be conspiring here. The first is if females are sedentary, the second if they are sparsely sprinkled across the landscape. Then a male’s biggest challenge is finding a mate. The smaller he is, the faster he can mature (he doesn’t have to waste time growing) and the sooner he can start looking.

  This size business is not just a quirk of green spoon worms: lilliputian lovers appear in widely separate groups. Take anglerfish, monsters that live in the coldest, deepest seas. The females don’t swim much but float in the darkness, ready to ambush their prey. Like wreckers of old, these formidable girls have special dangles and lanterns to lure the curious to their doom. Victims are swallowed whole, engulfed by toothy mouths and grossly distendable stomachs. Like your hubby, male anglerfish are minute. But these guys win the all-species Cyrano de Bergerac Award for the largest nose in proportion to body size. Presumably, the males follow their noses to find females in the vasty deep. When they meet one, they bite into her leathery black underbelly and fuse with her body, becoming a permanent appendage, little more than a pair of gonads. Still, it seems to me, their fate isn’t quite as ignominious as a life sentence in your small man room.

  Dear Dr. Tatiana,

  I’m a spotted hyena, a girl. The only trouble is, I’ve got a large phallus. I can’t help feeling that this is unladylike. What’s wrong with me? Can anything be done?

  Don’t Wanna Be Butch in Botswana

  No one expects hyenas to be ladylike. Least of all the biggest and baddest of them all—the spotted hyena. The brown hyena and the striped hyena squabble with vultures over a rotting carcass, and both sometimes eat fruit. The aardwolf, a dainty black and white hyena, eats harvester termites, lapping up more than 200,000 a night with its sticky tongue. But the spotted hyena is a fearsome predator. A single hyena can run down and kill an adult male wildebeest, an animal more than three times its weight. And despite their respective reputations, lions scavenge from hyena kills more often than the other way around. At least, they do if they get there in time. A spotted hyena can devour a Thomson’s gazelle fawn (2.5 kilos or 5.5 pounds) in under two minutes. Twenty-one hyenas can dispose of a yearling wildebeest (100 kilos or 220 pounds) in thirteen minutes, and there won’t be much trace of him left. Having massive jaws, hyenas can pulverize bones, even rhinoceros bones, and not just to get to the marrow: unlike other carnivores, hyenas can digest bones. That’s why hyena scats are white—they’re mostly bone powder. All the same, the first hyena on a kill will begin by taking delicacies such as the victim’s testicles or udders, or a fetus if there is one.

  So you see, yours is no tea-drinking, cake-eating, genteel society; ladies would be distinctly out of place. And not just with respect to table manners. Spotted hyenas typically live in big groups, each presided over by a dominant female. But while they sometimes hunt in packs (especially when hunting zebra), cooperation on anything else is rare. Instead, it’s a mad scramble. That’s one reason hyenas eat so fast—they gobble as much as they can before anyone else arrives. The only moderating influence is the social hierarchy, aggressively enforced, where the dominant female and her cubs take precedence over everybody—and all other females take precedence over all other males. Unlike the other hyena species, where males and females are roughly the same size, but like many birds of prey, female spotted hyenas are bigger and heavier than males. But a phallus? At least no one can accuse you of penis envy.

  On the outside, male and female genitalia look so similar that for many years the spotted h
yena was thought to be a hermaphrodite. In females, however, what looks like a phallus is actually a grossly enlarged clitoris, fully capable of erection. The lips of the vagina have fused shut and form a pseudo-scrotum. Urination, copulation, and birth must, therefore, be done through the clitoris.

  How? Well, if you really want to know … At puberty, the mouth of the clitoris becomes elastic, able to open to about two centimeters (one inch) in diameter. To allow copulation, the female retracts the clitoris, folding it up like a concertina, thus creating an orifice and allowing the male to slide in. It’s the birth of a spotted hyena, however, that is particularly bizarre. For starters, the birth canal is a funny shape. Instead of being a straight passage as in most mammals, it features a sharp bend. Worse, at sixty centimeters (twenty-three inches), it’s twice as long as in other mammals of a similar size. The umbilical cord, however, is short—only eighteen centimeters (seven inches) long. Once the placenta detaches, the young hyena will asphyxiate if it is not born promptly. But a baby hyena’s head is too big to pass through the clitoris. So when a mother gives birth for the first time, the clitoris tears to let the cub out. This is not just agonizing. It is often lethal. Scientists estimate that more than 10 percent of females die the first time they give birth, and more than half of firstborn cubs are stillborn. (Paradoxically, since the clitoris never recovers from this trauma, subsequent births don’t put the mother’s life at risk.)