Dr. Tatiana's Sex Advice to All Creation

by Olivia Judson

  Rather than raging when they feel insecure, some females mount a charm offensive. Female starlings, for example, get all lovey-dovey and constantly beg for sex if they notice their mate courting other lasses. But whether they shower their mate with kisses or brickbats, females everywhere have the same response to girls they suspect of seducing their husbands: hostility. In the northern harrier, a bird of prey from North America, females intimidate possible rivals and attack them if they are carrying food. Female blue tits dive-bomb rivals, often knocking them out of the air. A female starling, as well as distracting her mate with canoodling, will chase a rival whenever she spots one hanging about and will sing ostentatiously to show the little tart what’s what. If she finds her mate strutting his stuff at a second good nest hole, she may resort to filling it up with straw, feathers, and other material to make it look occupied, even though she has a nest of her own. A male starling often ends up chasing his wife back to her own nest to stop her beating on potential mistresses.

  But he doesn’t have it as bad as Mr. Lamprologus ocellatus. This fish lives in Lake Tanganyika, one of the Great Lakes of tropical Africa. A male holds a territory; as for many birds, a crucial feature of his territory is the nest sites that he can offer—in this case, empty snail shells. You might not think so, but there’s fierce competition for preowned snail shells. Many creatures find them useful shelters. Hermit crabs famously depend on finding used snail shells: rather than growing shells of their own, they move from empty shell to empty shell as they get bigger. It’s not always easy to find a shell of the right size, yet many hermit crabs are finicky, preferring to squeeze into shells that are too small rather than wear a shell of the right size that has a hole in it. And just to show how central used snail shells can be to a local community, some hydroids—simple animals related to jellyfish, corals, and sea anemones—prefer to settle on shells occupied by hermit crabs. How can they tell? Hermit crabs scuttle about faster than the shell’s original owner, and baby hydroids are attracted by the motion. It’s mutually convenient. Hydroids have powerful venoms that might discourage anyone in the mood for a hermit-crab sandwich. For the same reason, some hermit crabs harvest sea anemones and stick them to their shells. In return, the hydroid (or anemone) gets scraps of food and protection from its own predators, which the crab zealously fends off.

  In Lake Tanganyika, at least fifteen species of fish want secondhand snail shells in which to lay their eggs. As males of most species cannot move the shells any distance, they have to make do with whatever they find in the vicinity. But in one species, Lamprologus callipterus, males can grow to eleven centimeters (four inches) and can easily nip shells with their mouths and carry them back to their territories. (This species may hold the record for males towering over females: females are less than half as long and fourteen times lighter. They can’t grow big because they have to fit inside the shells.) The biggest males hoard shells for females to spawn in. As usual, they have no scruples about where shells come from and often raid one another. So perhaps it’s not surprising that in the smaller Lamprologus ocellatus, where the male can only move a shell by pushing it, he buries any shells on his territory before swimming about and looking pretty as he waits for females to arrive.

  If a girl stops by and they take a shine to one another, he digs up a shell and she takes up residence until she’s ready to spawn. (If she fails to spawn within a few days, the male kicks her out—what does she think this is, a homeless shelter?) When she does spawn, she lays her eggs in the shell, gluing them to the inside; he fertilizes them, and she stays in the shell, fanning the eggs to keep them aired and clean. Once the brood hatches, she and her little ones live in the shell until the young are old enough to go out into the world.

  Female Lamprologus ocellatus hate one another. Whoever moves in first does her best to remain in solitary splendor, chasing all visiting females and otherwise terrorizing them. If a second female decides to settle in the territory anyway, she’ll have to live in a shell far from her rival’s—and even then, she’ll face constant harassment. The male ends up breaking up fights and chasing the aggressor back to her shell; since a pair of females attack each other several times an hour, the peace process takes a lot of his time. It’s vital, though. Unsupervised, the females would go on fighting until one of them moved out. So, boys, if you’re thinking of cavorting with more than one girl, remember the Chinese symbol for peace. It’s one woman under a roof.

  Females don’t have special weapons and rarely fight to the death over a man—pistols at dawn are not their style. But that shouldn’t mislead you into thinking they don’t fight over males at all. Females will fight out of:

  1. Desperation—whenever there aren’t enough males to go around. Shortages can happen for any number of reasons but are particularly likely in species where child care is time-consuming and the males do most (or all) of it.

  2. Aspiration—whenever some males are obviously superior to others, that is, when females mated to the best males have more children than those stuck with lesser fellows.

  3. Possessiveness—in species where males and females form pairs, females go to great lengths to prevent their partner from taking other lovers. To remain the one and only, females attack possible rivals—and for good measure, distract or hound the male who strays.

  So if you hear it said that there’s a grand, harmonious sisterhood, you’re probably hearing propaganda. In most species, it’s not “all for one and one for all.” It’s every girl for herself.

  9

  APHRODISIACS, LOVE POTIONS, AND OTHER RECIPES FROM CUPID’S KITCHEN

  What do homosexuality, new species, and love potions have in common? If you look closely, you may find that they are all outcomes of the battle of the sexes at its most fundamental.

  Dear Dr. Tatiana,

  I think I’ve made a dreadful mistake. I’ve just lost my virginity to a fellow who recently escaped from a local fruit fly laboratory. He’s bigger and badder than wild flies—and he says he’s put a spell on me so that I’ll never be able to have sex with anyone else. Do you think that’s possible, or is he all bluff?

  Afraid I’ve Been Bewitched in Santa Barbara

  In general, it’s a good idea for wild flies to steer clear of escapees. All manner of experiments go on behind the walls of fruit fly laboratories, and time inside can do strange things to a fly. As for laboratories breeding lovers with supernatural powers, powers that could never evolve in the wild, I fear your seducer may indeed have been telling the truth. How did he get that way? To understand, we’re going to need a more intimate look at the battle of the sexes.

  Remember: while a female may gain from mating with several males, each of her lovers will do better if she mates with no one but him. Whenever this conflict of interest occurs, it ignites an evolutionary battle that is fought on two different fronts. On the first front, each of a female’s lovers tries to thwart the lovers of her past and future while avoiding being thwarted himself. The prickly penis is one device we’ve brushed against before, and high sperm counts should sound familiar; but as always, there are other possibilities. For example, a male may use chemicals to disable his predecessor’s sperm. Or he may make his own sperm hard to remove.

  Meanwhile, the second front is male versus female: he evolves tricks to manipulate and control her, and she evolves to resist. One obvious and common ploy is for the male to try to stop the female from taking subsequent lovers: regular readers of these columns will recall chastity belts and the fanatical guarding of a female from rivals. But again, that’s only the beginning. There are many other, more exotic—and in some cases, more sinister—ways in which males of various species attempt to bend females to their will. To give just a few examples: males may attempt to increase the number of eggs a female lays right after sex. Or increase the number of their sperm that she stores. Or deliver drugs that switch off her sex drive—an invisible, chemical chastity belt. Or daub her with an “antiaphrodisiac,” a chemical that makes her st
ink, so that other males will find her repulsive. In short, the arsenal of potent weapons is enormous. With so much scope for innovation, the battle will inevitably unfold in different directions in different species—or even in different populations of the same species.

  Seminal fluid—the liquid that sperm, ahem, come in—is typically a complex brew, containing many chemicals that alter female behavior. In the Australian field cricket, for example, chemicals that accompany the sperm stimulate egg production: inject a virgin female with the right ingredient and she will start laying eggs even though she has not copulated. The seminal fluid of the housefly contains at least twelve active proteins, some of which act like a drug, binding to receptors in the female’s brain and turning her off sex. Fruit fly seminal fluid is even more complex, containing more than eighty proteins. The function of most of these is still a mystery. We do know, however, that some play a role in disabling a previous male’s sperm while others make sperm harder to remove. Yet another protein has antiaphrodisiac properties. And another, a small molecule known as sex peptide, inspires the female to lay perhaps fifty eggs and induces aggression toward males. If any male approaches within a day of her getting the molecule, the female will give him a good kicking.

  Hermaphrodites get in on the act, too. Consider Helix aspersa, the ubiquitous garden snail. Mating individuals sling arrows of outrageous fortune at each other: each has a love dart that is sharp and pointed and that, if fired, pierces the lover’s skin. As it does so, it delivers a gob of mucus. The mucus contains a substance that alters the female part of the partner’s body, widening the passage to the sperm-storage chamber and closing the entrance to the sperm-digestion chamber, thereby increasing the chance that arriving sperm will be kept for future use rather than sent to the sperm-digestion chamber and destroyed.

  The fact that males have powerful effects on females does not by itself, however, demonstrate that there’s a conflict of interest. Take red deer. During the breeding season, stags spend most of their time roaring. A stag’s roar is a long, low rumble; each roar is a single exhalation of breath. It used to be thought that roaring was simply a kind of ritual fighting, a contest to see who is stronger. But a stag with a harem roars much more than he needs to if intimidating the opposition is the only aim. He’ll typically roar at least twice a minute all day and all night—that’s nearly three thousand roars every twenty-four hours, not counting extra roaring during shows of strength. Small wonder that after a couple of weeks he’s exhausted. It’s worth it, though. For females, roars are an aphrodisiac: females exposed to vigorous roaring come into heat sooner than females who are not. But this effect is not necessarily malevolent, in his interests but not hers. Female red deer who conceive earlier in the breeding season give birth earlier the following spring and are more likely to have their calves survive. Responding to roars may help females by increasing the odds they’ll get pregnant early in the season.

  In order to demonstrate that these love philters and aphrodisiacs are nefarious, then, you need to show not only that they effect a manipulation but that the manipulation is being resisted—that the female is fighting back. One way to show this is to arrange matings between individuals from far-flung populations: if females are evolving to resist male manipulation, you’d expect them to be more resistant to their local fellows than to fellows from far away, with whom they have not been directly coevolving. Among houseflies, for example, if you capture flies from distant places—Sweden and the United States, say—and have them mate with each other, females tend to be less susceptible to the monogamy potion made by males from their hometown than they are to the potion made by the foreigners.

  A second, more powerful way to reveal the battle is to do experiments that change the underlying conflict. And I’m sure you won’t be surprised to hear that such experiments have already been carried out on fruit flies.

  In one experiment, male and female interests were forcibly aligned. How do you forcibly align their interests? Each generation, you imprison couples together for the whole of their lives, so that neither male nor female has a chance to mate with anyone else. Under such circumstances, you’d predict that males would evolve to be less manipulative of females. Correspondingly, females would have nothing to struggle against, and thus their ability to fight back should deteriorate. Sure enough, this is what happens. After eighty-four generations of enforced monogamy, male fruit flies allowed back into the meat market of the regular mating arena were much less effectual at preventing females from mating with other males. Likewise, the females had become more vulnerable to male manipulation: in comparison with flies who’d come from eighty-four generations of promiscuous mating, females accustomed to monogamy laid far more eggs for their first lover and consequently took much longer to agree to mate again.

  The forcible alignment of male and female interests occasionally occurs in nature, with couples imprisoned together forever. In some species of shrimp, for example, couples are trapped within a Venus’s flower basket, a glass sponge from the deep sea. Each sponge is shaped like a cornucopia with a lid, thanks to its elaborate—and beautiful—latticed skeleton. Shrimp arrive as babies and crawl inside; once they start to grow, they cannot get out again. Apparently, they are only ever found in pairs—I suspect they kill any latecomers. No one knows whether they’ve evolved a life of perfect sexual harmony; from the rules of war outlined above, however, that is indeed what I would predict.

  To return to the fruit flies in the trenches, though, a second experiment produced an even more compelling result. Usually, conflict is difficult to show unequivocally because males and females are evolving in lockstep. In this experiment, one of the combatants, the female, was not allowed to fight back: by dint of fancy genetic techniques, females, but not males, were prevented from evolving. This gave males a stationary target to adapt to instead of the usual moving one. In such a situation, the females can no longer hold the males in check—male evolution will no longer be constrained by the female ability to fight back—and without this opposition, males should continue to evolve in a direction beneficial to males.

  The results were clear. In less than forty generations, the males had, I’m afraid, become supermales, completely redrawing the battlefield. Females were much more likely to be seduced by these fellows, failing to reject their advances even when under the influence of a regular male’s sex peptide. At the same time, the supermales were better at inducing monogamy, and even if a girl did eventually mate with a normal fly, the supermales were less likely to have their sperm displaced. In a nastier development, some of the supermales seemed more likely to cause their mates to die, perhaps because their seminal fluid had become poisonous. So if your lover escaped from an experiment like this one, I can well believe that he breached all of your natural defenses.

  Which inspires an arresting question: if human males could evolve for forty generations while females were held still, would they become a breed of dangerous but irresistible superlovers? I wonder.

  Aloha, Dr. Tatiana,

  I’m afraid of becoming a has-been of a rock-boring sea urchin. In my species, sperm are frightful fashion victims: they constantly change their outside coats. The rumor surfing over the reef is that this is because eggs are snobs and only the trendiest sperm are allowed to penetrate them. How can I find out what this year’s fashion will be, and can I get my sperm engineered to match?

  Desperate to Be à la Mode in Hawaii

  As so often with rumors, the one you’ve heard is a garbled mix of fact and fantasy. Let me walk you through what’s really going on. You know, of course, that the first step in fertilization is for the sperm to attach to the egg. In your species—indeed, among sea urchins generally—the sperm attaches to the egg using a protein called bindin. When you hear talk of sperm changing their coats, what is actually meant is that they are changing their bindin; and it’s true that in the grand scheme of things bindin is changing rapidly. But there’s no need to get het up—rapid is relative. Your brand of
bindin will be in fashion thousands of years after your shell has smashed against the reef.

  You’re probably wondering why, if a change in bindin isn’t imminent, everyone is making a fuss about it. Well, the reason is that your brand of bindin is fundamental to your identity as a rock-boring sea urchin. I’m not exaggerating. Consider this: like rock-boring sea urchins, oblong sea urchins—your near relations—shed their eggs and sperm into the water. In principle, then, one of your sperm might encounter one of these foreign eggs. But if it does, nothing will happen: you are powerless to fertilize it. This is because your bindin is the wrong shape for attaching to an egg from an oblong sea urchin.

  So what? So a lot. Reproduction is central to the concept of a species: the working definition of a species is a group of organisms that can interbreed. Any mechanism that prevents interbreeding can thus generate new species. For example, lengthy physical separation between two groups often generates new species, as each group goes its own way. This is why islands and lakes (which are, after all, islands of water surrounded by land) tend to be rich in unusual flora and fauna.

  New species can also arise, however, through basic reproductive incompatibilities—such as egg and sperm not recognizing each other. Continuing with your case, a change to the bindin-egg interaction is enough, by itself, to generate a new species of sea urchin. To see how, suppose that the only difference between male rock-boring sea urchins is the type of bindin that they produce. To keep things simple, let’s say the bindin comes in just two types, A and B. And suppose that the only difference between female rock-boring sea urchins is the affinity of their eggs for one type of bindin or the other. If the affinity is so strong that some eggs can be fertilized only by sperm carrying type A bindin, whereas the rest of the eggs can be fertilized only by sperm carrying type B, then rock-boring sea urchins would be two species, not one—even though individuals are identical in all other respects.