Dr. Tatiana's Sex Advice to All Creation

by Olivia Judson

  Our friend Bateman has a lot to answer for. “Sperm are cheap” was one of his notions. But it’s the biggest myth in town. And although I’m sorry you’ve been misled, I can’t help feeling a certain smug satisfaction that Drosophila melanogaster, Bateman’s model organism, should turn out to have problems of this kind.

  To recap: Bateman argued that because one sperm is cheaper to make than one egg, the factors limiting reproduction in males and females are different. Females, he said, are limited by eggs produced, males by mates seduced. According to this view, sperm are—to all intents and purposes—unlimited, and every single egg stands a good chance of being fertilized.

  All too often this is not so. In the sea, animals from sponges to sea urchins do not rendezvous with their partners but release sperm into the water. Some species release eggs into the water, too. This means that sperm can have a tough time meeting up with eggs. In many such species, a high proportion of an individual’s eggs may go unfertilized. Small wonder that some sponges spew sperm as if they were finalists in a Vesuvius look-alike contest, sending up large thick clouds of the stuff for anywhere from ten minutes to half an hour at a time.

  On land, plants can have a similarly rough time. Pollinators—animal go-betweens, like bees—can be unreliable, preferring to eat pollen instead of delivering it to female flowers, so plants are often limited by the amount of pollen they receive. The cheeky forest flower jack-in-the-pulpit produces ten times more seeds if it is pollinated by a scientist rather than by a fly. Nor are such difficulties restricted to organisms who have to gamble on ocean currents or the wind or who are dependent on the vagaries of messengers. The lemon tetra, a small fish that lives in the Amazon, cannot fertilize all the eggs one female produces on a given day. His success at fertilizing falls the more he spawns, and he quickly gets to a point where his energy is better spent making more sperm than seducing more mates. No surprise, then, that female lemon tetras seem to prefer males they have not seen spawning with anyone else. In the bluehead wrasse, an Atlantic coral-reef fish, the biggest males husband their sperm, handing it out stingily—and often at levels below those best for females.

  The trouble is, of course, most males are not producing just one sperm for each egg. They are producing hundreds, thousands, or millions of sperm per egg. That gets expensive. Male garter snakes have to rest for twenty-four hours after sex (which, to be fair, has usually been rather vigorous). A male zebra finch, a small bird with black and white stripes, who copulates three times in three hours, will run out of sperm—and it will take him five days to refill. Male blue crabs must wait fifteen days to replenish supplies. Even rams, who supposedly hold sperm reserves for ninety-five ejaculations (a typical man holds enough for one and a half) soon find their sperm counts going into freefall. After six days of sex, the sperm in a ram’s ejaculate can fall from more than ten billion to less than fifty million—a threshold below which he’ll have a hard time impregnating anybody. And some snakes positively fade away. The adder, a poisonous European species, loses a lot of weight at the start of the breeding season even though he’s doing nothing but lying in the sun making sperm. That’s one way to burn calories.

  But the clinching proof that sperm are often limiting comes from hermaphrodites—organisms such as garden slugs and snails that are both male and female at the same time. Under the sperm-unlimited theory, hermaphrodites should run out of eggs before they run out of sperm and, given a choice, should prefer the male role over the female one. But in many species, this is not what happens.

  Consider Caenorhabditis elegans, a tiny transparent roundworm beloved of geneticists. C. elegans is different from most hermaphrodites because it comes in two sexes: hermaphrodites and males. Among conventional hermaphrodites, there are two ways to have sex. Copulation can either be bilateral—both partners inseminate each other at the same time. Or it can be unilateral—in any given bout of sex, one partner plays the male role and the other partner plays the female. In C. elegans, however, the hermaphrodites cannot mate with each other, but they do make both eggs and sperm and can fertilize themselves. (Males, obviously, make only sperm.) A hermaphroditic C. elegans who never encounters a male will run out of sperm after laying about three hundred eggs. We know that the sperm are finished up first because for a while afterward the animal carries on laying unfertilized eggs—sometimes as many as a hundred.

  But perhaps C. elegans is a special case. The hermaphrodite form does not make eggs and sperm at the same time; rather, it does sperm first. Therefore, the more sperm it makes, the longer it must wait before making eggs and the older it is when it starts reproducing. Too much delay is bad: among these worms, you’re likely to have more offspring if you get off to an early start.

  C. elegans and its relations are not, however, the only hermaphrodites that run out of sperm. Sperm limitation has also been found among sea slugs, sea hares, freshwater snails, and freshwater flatworms. (Although these organisms appear similar, they are only distantly related. Their looks and lifestyles have been arrived at independently.) In the freshwater flatworm Dugesia gonocephala (a bilateral copulator), sperm packets take two days to prepare, so individuals are thrifty with sperm and don’t give away more than they receive: they stop giving sperm when their partner does. In the sea slug Navanax inermis (a unilateral copulator), individuals appear to prefer the female role over that of the male—the opposite of what you’d expect if sperm were unlimited.

  And lest anyone still doubt that the male role can be expensive, look at banana slugs—enormous yellow slugs of the Pacific Northwest. In these hermaphrodites copulation is unilateral—and in several banana slug species, individuals may get only one shot at being male, whatever their sperm count. Banana slug penises are gigantic and complex. During sex, the penis often gets stuck. At the end of sex, therefore, the slug or its partner gnaws off the offending phallus. It never grows back: from that point on, the slug plays only the female role.

  That said, let’s take a closer look at your situation. Drosophila melanogaster males apparently suffer from two types of matinginduced sterility. The first is temporary: after mating once, a male ought to rest for a day before mating again in order to replenish supplies. The second type appears to be permanent. Unfortunately, because of the design of the experiments done so far, we don’t know how quickly permanent sterility arises. All we know is that males presented with two females every two days are completely and irreversibly sterile by day 34—just under halfway through their adult lives. Perhaps in the wild, male flies never mate often enough—or live long enough—for this to be a problem. Perhaps. But then again, perhaps not. It is surely no accident that in your species, as in many others, females prefer to mate with fresh-faced virgins.

  Dear Dr. Tatiana,

  My lioness is a nymphomaniac. Every time she comes into heat, she wants to make love at least once every half an hour for four or five days and nights. I’m worn out—but I don’t want her to know. You couldn’t suggest any performance-enhancing drugs, could you?

  Sex Machines Aren’t Us in the Serengeti

  There is a drug, but it hasn’t been approved for lions yet, I’m afraid. And anyway, you should be ashamed of yourself. A great big lion like you should be able to keep it up without fussing. I’ve heard of lions copulating 157 times in fifty-five hours with two different females. Honestly.

  But let’s look at the reason for your lady friend’s prodigious lust. The problem is, she’s got a genuine, clinical sex mania. Such manias are of two main types. In type I, the female needs lots of stimulation to get pregnant. In type II, a male copulates like mad not to stimulate the female but to ensure all the offspring in a brood are his own. Your lover is a classic type I. The affliction is not limited to lions: female rats, golden hamsters, and cactus mice, for example, all require vigorous stimulation before they can conceive. But lionesses are especially demanding: by some estimates, less than 1 percent of all copulations produce lion cubs. No wonder lions spend so much time snoozing.
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br />   What does all the stimulation do? Some species—such as rabbits, ferrets, and domestic cats—do not release eggs without proper stimulation. Others—rats, for instance—release eggs spontaneously, but a female that hasn’t been stimulated enough won’t stay pregnant even if her eggs have been fertilized. And lions? The usual assumption is that lions are like domestic cats and won’t ovulate without stimulation. But getting such information from dangerous wild animals is, well, dangerous, so we don’t know for sure.

  Whatever the mechanism, though, the underlying puzzle is the same. Massive stimulation is wildly extravagant. In nature, wild extravagance quickly vanishes if it is not beneficial. If some lionesses needed less stimulation to become pregnant—and there were no disadvantage to having less—the levels would fall. But they haven’t. So the question stands: Why do lionesses need so much encouragement to become pregnant?

  Possibly it has something to do with the structure of lion society. Lionesses live together in family groups, known as prides. A band of males lives with a pride, fighting off challenges from other bands of males. If the resident band is defeated, new males take over and kill any cubs they can find—the loss of cubs stops the females from producing milk and brings them back into heat. Frequent changes of males are therefore bad from the females’ point of view. So perhaps the extraordinary virility demanded of lions is a test in which the females make sure their lions are strong and will be able to defend the pride for at least a couple of years. In keeping with this idea, there is some evidence that lionesses have lower fertility at the start of a band’s tenure, as if they are testing the new men out. However, this is at best a partial explanation for the extravagance. Even when lionesses know their lions, they still copulate several hundred times whenever they come into heat.

  Could female promiscuity be the reason for such extravagance? This can account for type I sex mania in some species. Among golden hamsters, for example, the more energetically a female is stimulated by one partner, the less likely she is to respond to another. Among rats, vigorous stimulation will not necessarily put a female off other partners—but if her first lover is sufficiently stimulating, he is more likely to be the father of her children. And among crested tits—small songbirds—females constantly beg for sex. A male who can’t keep up with his partner’s appetites will find himself cuckolded. For lions, though, the picture is ambiguous. Lions are harder to observe than hamsters or rats or crested tits, so information on lioness promiscuity is anecdotal. By some accounts, a lioness in heat will go off alone with her partner for a few days; according to others, lionesses change mates once a day. True, genetic analysis shows that it’s rare for cubs in a litter not to have the same father, but that may not tell us much. If lionesses are like rats (excuse the comparison), the cubs’ paternity may not reflect the mother’s virtue so much as the outstanding performance of one or another of her mates.

  How to resolve the matter? Since an experiment is obviously out of the question, we could compare lions with other cat species: because all cats are related, similar behaviors may have similar underlying causes. Unfortunately, the comparison deepens the mystery: although some species of cat copulate as much as lions do, they have no other obvious traits in common. For example, sex mania cannot be explained by the fact that lions live in groups. Solitary cats such as leopards and tigers also copulate like lunatics while the female is in heat. Nor is it a Big Cat Thing. Although large cats like pumas, leopards, tigers, and jaguars copulate like lions, cheetahs and snow leopards do not. Moreover, the tiny sand cat—a little-known species that preys on rodents in the deserts of the Middle East and Central Asia—copulates wildly. Other small cats, such as the bobcat and the tree ocelot, do not. And frustratingly little is known about the tendency of females in these various species to be promiscuous. For now, I’d say that female promiscuity is the best hypothesis to explain lioness behavior, but an honest jury would have to say the case is simply not proven.

  I’d like to leave you with one final thought. Giant water bugs are type II sex maniacs, the male hogging the female to make sure no other man gets his hook in. The reason is that giant water bugs are devoted dads, carrying eggs about on their backs and then helping the young water bugs to hatch. Female giant water bugs don’t like to mate with males already encumbered with a brood, so most males only get a chance to mate with one female at a time. They make the most of it. One male I heard of insisted on copulating more than a hundred times in thirty-six hours—or almost once per egg. Surely you’re not going to be outdone by a water bug?

  Dear Dr. Tatiana,

  I think I must be deformed. I’m a long-tailed dance fly and I go to all the right parties, but night after night I’m spurned. The guys won’t come near me, let alone try to seduce me with a fancy dinner. I’ve noticed that all the other girls look like flying saucers, but I look like a regular fly. Is there anything I can do?

  Quasimoda in Delaware

  Your case is curious. In long-tailed dance-fly culture, it’s traditional to mix food and sex. An hour before sunset, the male captures a suitable insect—a juicy mayfly, perhaps—and then goes to find a female, taking his quarry with him so she can eat it while they make love. Females congregate and wait for males to arrive. Unlike many insects, however, long-tailed dance flies don’t rendezvous at hills or tree stumps. They meet at clearings in the forest, where the females’ bodies show up in silhouette against the sky.

  Male long-tailed dance flies are fussy and prefer to give the insect they’ve caught to the largest females. We don’t know precisely why. In a cousin of yours, males desire large females because they are closer to laying eggs, which means there is less risk that the female will mate with someone else in the interim. In your case, though, size does not indicate that egg laying is imminent. Still, in species from insects to fish, larger females are more fecund, so your size may indicate how many eggs you are capable of making. Be that as it may, female long-tailed dance flies have evolved an unorthodox way of displaying how big they are. They have two inflatable sacs, one on each side of the abdomen. Before a female joins the party, she sits on a bush, gulping air, blowing herself up to three or four times her normal width. Try it. I think you’ll find it’ll give you the flying-saucer look.

  In many species, females will only mate with males bearing gifts. Males who can’t produce the goods are rejected. Males bearing small gifts are often punished by not being allowed to copulate for long. This might explain why the hunting spider Pisaura mirabilis, the only spider known to give presents, takes the trouble to wrap them in silk. The more silk, the more time the female takes to feed, even when the meal itself is paltry. Perhaps the fancy gift wrapping persuades the female to overlook the meagerness of the offering.

  Presents take many forms, depending on the species of the giver. Often, presents are edible secretions that include proteins and other nutrients. Look at the tropical cockroach Xestoblatta hamata. After sex, females feast on anal secretions produced by their mates, eating right off the plate, so to speak. In many species, the secretions are not taken orally but are delivered in the same package as the sperm. During copulation in the moth Utetheisa ornatrix, the male passes the female a chemical that protects her from spiders. The spiders find her so disgusting that they actually free her from their webs as soon as she gets stuck, cutting away the threads that have ensnared her. In a bizarre variant, during copulation the beautiful and aptly named scarlet-bodied wasp moth covers his mate with a veil of filaments impregnated with spider repellent. Not all presents are so practical, however. Among balloon flies—which are related to dance flies—males make the female a large white silk balloon to play with while they make love.

  As the gifts get more expensive, males get more careful about who receives their largesse. After all, you wouldn’t take just anyone to the Ritz. Among Mormon crickets—flightless cousins of crickets and katydids—a male finds himself in severely reduced circumstances after just one mating. He secretes his gift—and loses a quarter
of his mass in doing so. You can bet that these fellows are choosy and reject all but the largest mates. Many butterflies suffer a similar loss; once a male has mated, he will be unable to produce a large present quickly. Again, male butterflies are notoriously finicky about whom they bed.

  With long-tailed dance flies, however, it is not so much the expense of the present that makes the guys so picky. Rather, they are because they can be. Female long-tailed dance flies have lost the ability to hunt and are thus completely dependent on males for food. You’d better puff yourself up to impress them.

  There’s more to being a male than dropping your trousers. Good lovemaking is physically demanding—especially in species where females take additional mates. Then, sperm is anything but cheap. Not only will you have to ejaculate huge numbers of sperm, you may find yourself able to ejaculate only infrequently. This is bad news. If a female finds you inadequate, she won’t wait around. She’ll replace you. So before leaping into bed with the first dewy young miss who happens along, remember how Lord Chesterfield, an eighteenth-century Englishman, is said to have described sex to his son: “The pleasure is momentary, the position ridiculous, and the expense damnable.”

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  FRUITS OF KNOWLEDGE

  Why do females sleep around? Because, as a rule, loose females have more and healthier children. The reasons for this vary enormously, however, from species to species.

  Dear Dr. Tatiana,

  My name’s Vikram and I’m a bronze-winged jacana. I’m a member of a harem and I’ve built a nest and everything, but my female won’t pay attention to me and won’t give me any eggs to incubate. What am I doing wrong?