Dr. Tatiana's Sex Advice to All Creation

by Olivia Judson

  But you can console yourself a little. When the harlequin beetle carrying your girlfriend arrives at a new log, she and the other females will disembark. Your girlfriend will give birth to her family there in the decaying wood. Because she has the ability to store sperm, some of her children will probably be yours. So as you sit on your island, think about all the baby pseudoscorpions bearing your likeness.

  As to finding a female harlequin-beetle-riding pseudoscorpion who will be true—well, you might as well try to catch a falling star. These females like to gallivant: they regularly spurn the attentions of previous lovers, preferring to make fresh conquests. Why? It’s simple. Females who mate with two different males are more likely to have children than females who mate with the same male twice. This is not because lots of males are sterile. Rather, females who mate with only one male are more likely to abort their broods. Apparently genes from the father and genes from the mother are sometimes incompatible and cannot act in concert to produce children. By mating with several different males, females avoid this problem.

  My hunch is that avoiding genetic incompatibilities will turn out to be the reason that females of many species are promiscuous. This is still a new idea and has been tested only in obvious candidates such as the honeybee. Incompatibilities between male and female genes, however, are probably common. In the beetle Callosobruchus maculatus, for example, whether or not a male is successful in sperm competition depends in part on the genes of his mate. And certainly, genetic incompatibility is an important cause of infertility in a number of species.

  In humans, for example, perhaps 10 percent of couples are infertile. Of those, between 10 and 20 percent of cases are apparently due not to either partner’s being sterile but to a genetic incompatibility. Furthermore, some women are prone to the spontaneous abortion of healthy fetuses. Again, the problem often lies with interactions between the partners’ genes. Does this cause women to be unfaithful? I can only wonder.

  Still, there is tantalizing tentative evidence that people might have inbuilt mechanisms to avoid such problems in the first place. Consider this. The genes typically implicated in spontaneous abortions are part of a vast gene complex known as the major histocompatibility complex, or MHC. These genes are important in the immune system. They help determine resistance to infectious diseases and, in humans, cause the rejection of transplanted organs. There may be as many as a thousand different genes in the complex—and some of them come in as many as a thousand different forms, so they are exceptionally variable. Indeed, the MHC seems to give each individual a unique odor. For example, people and mice can both smell the difference between mice that are genetically identical except at the MHC. And in a number of “smelly T-shirt” experiments—experiments in which humans sniff T-shirts that have been worn for a couple of days by members of the opposite sex—people consistently prefer the smells of those whose genes at this complex are different from their own. Yes, you guessed it. Spontaneous abortions are more likely when couples match at particular MHC genes.

  Of course, a woman can’t love on smell alone, and so when you look at who actually pairs up with whom, you don’t find a consistent pattern. But it is intriguing that in the smelly T-shirt experiments, the only women who liked the smells of men who matched them at the MHC happened to be those taking the oral contraceptive pill. We don’t know why. But I’m sure you’ll agree that if this result turns out to be generally true, the implications would be most disturbing.

  Dear Dr. Tatiana,

  I’d prefer to keep my identity secret, since I am writing to you not about me or my species but about my noisy neighbors—a group of chimpanzees. When those girls come into heat, it’s enough to make a harlot blush. Yesterday I saw a girl screw eight different fellows in fifteen minutes. Another time I saw one swing between seven fellows, going at it eighty-four times in eight days. Why are they such sluts?

  Mind Boggling and Eyes Popping in the Ivory Coast

  You raise an excellent question. The extraordinary promiscuity of female chimpanzees has intrigued many a scientist, and to be frank, we don’t know why they are so incredibly wild. However, two theories are regularly bandied about.

  The first is that female chimpanzees mate promiscuously to create competition between sperm from different males. In other words, sperm competition is not merely the consequence of females mating with more than one male, but the cause. I know this sounds outlandish. But it gets wheeled out to excuse the licentious behavior of females in many species, so it’s an idea worth scrutinizing. Here’s how it’s supposed to work.

  The starting assumption is that some males are much better at fertilizing eggs than others. The reason they are better doesn’t matter much—what matters is that the ability is heritable. That is, excellence at fertilizing eggs must have a genetic basis and those genes must be handed on from father to son. Then females who sleep around—and thereby encourage sperm competition—will have sons who are better at fertilizing eggs than females who mate once.

  The evidence, however, is circumstantial at best. I don’t deny that it’s possible, but I have yet to see a rigorous demonstration that setting up a sperm race is the main reason that females of any species sleep around. Although biologists have arranged endless contests to find out who wins when sperm are in competition, a huge number of variables affect the outcome; there is no general rule. Sometimes it’s a question of who’s on first, sometimes it’s a matter of timing, sometimes it depends on the number of males competing—and so on. Certainly, many of the variables are not under genetic control. In the rat, for example, the female’s reproductive tract is bifurcated—and the outcome of sperm competition often differs between the left and right halves.

  But suppose you succeed in showing that one guy always beats everyone else. That does not mean his superiority is passed to his sons. At least one crucial ingredient for successful sperm cannot be passed from father to son, namely, the engines that sperm need in order to move. These engines are known as mitochondria. They are tiny organs that generate energy for cells. In most animals, mitochondria are inherited only from the mother. Can engine trouble ruin a guy’s chances at fertilizing eggs? You bet. Faulty mitochondria cause infertility in men, rams, and roosters, for example. Conversely, some guys with otherwise unremarkable sperm may find theirs move as if turbocharged, as if someone put rocket engines on a wheelbarrow. So you see the difficulty. Just demonstrating that one guy’s sperm is consistently more competitive is not enough. You have to show that this is due to a characteristic that can be inherited. I’d even guess that unreliable engines could explain why sperm tend to be larger, more numerous, and more complicated in species where there is sperm competition. All those other traits are heritable and may partially compensate for unreliable engines.

  The second theory that aims to explain why female chimpanzees are so promiscuous is the obfuscation theory. The idea here is that by mating with every guy in sight females can create confusion over the paternity of their child. And clearly, if a girl’s enjoyed the gang bangs you’ve described, even she won’t know who’s the dad. Why would this be an advantage? Well, perhaps if a male thinks a child may be his, he will refrain from killing it. Infanticide is a risk, after all: male chimpanzees do sometimes murder infants. But whether they are more likely to murder the children of females they haven’t copulated with is, for now, a mystery.

  As for you, if your biology allows for it, might I suggest a move to a nicer neighborhood?

  Dear Dr. Tatiana,

  I’m a yellow dung fly, and I’ve heard rumors that in my species sperm are actually chosen by the egg. Is this true, and if so, what can I do to make my sperm more attractive?

  The Dandy on the Cowpat

  That’s a tricky one. The question of whether eggs—or females—actively select one sperm over another is contentious. To be sure, females can reject sperm from particular males. Consider the Caribbean reef squid. Males place packets of sperm anywhere on the female’s head or tentacles. The
female either moves the sperm packet to her sperm storage organ, the seminal receptacle, or she picks it off and throws it away. Then there’s the farmyard chicken. Females who copulate with a male low in the pecking order are likely to eject his sperm as he dismounts. But whether females store sperm from several males and then choose the winning sperm or whether each egg actively prefers particular sperm, that’s another matter altogether. I know of only one case where something like this does seem to be going on.

  Have you ever met a comb jelly, or ctenophore? No? There are about a hundred known species, although given their penchant for life in the vasty deep, many more probably await discovery. To the untutored eye, comb jellies resemble jellyfish—the typical member of each group is translucent, lives in open water, and can give a nasty sting. The similarity, however, is superficial. For one thing, comb jellies have firmer bodies. But the chief distinction is the eponymous “comb”—eight ridges of cilia that run down the sides of each comb jelly and that wave in unison to propel the animal languidly along. Beroë ovata, one of the biggest species of comb jelly, is shaped like a bell. For whom does it toll? Ask not. If you’re another comb jelly, I’m afraid it tolls for thee: Beroë is a voracious predator, swimming along mouth first to engulf comb jellies of other species. (If a Beroë’s not hungry, it zips its mouth shut to cut down on drag.) But to get to the point, Beroë has some singular reproductive habits.

  Like most other comb jellies, Beroë ovata is a hermaphrodite and sends both eggs and sperm out into the sea. Self-fertilization is rare: sperm released by the same comb jelly that released the egg are not usually allowed through the egg’s outer covering. Nothing odd so far. The going only gets peculiar after the egg has been fertilized. As long as just one sperm enters the egg, the baby comb jelly will begin its development as you’d expect. But if several sperm enter the egg, things become interesting.

  If several sperm penetrate a human egg, it won’t develop. But for many animals—sharks, for example—polyspermy is not a terminal condition but the norm. In our friend Beroë, it seems to provide an arena for the ultimate in mate choice. The nucleus of the egg moves around and “visits” each of the sperm nuclei in turn, before eventually “deciding” which one to fuse with. The process can take hours—and the egg nucleus won’t necessarily fuse with the last sperm it inspected but will sometimes turn around and go back to one that took its fancy earlier on. How does it decide? This system has been studied so little that it is hard even to speculate.

  Of course, it’s possible that, unbeknownst to us, similar shenanigans go on in other species. Finding out will be difficult, however. You see, Beroë eggs are fertilized outside the body and are easy to look at under a microscope. In species with internal fertilization—such as those that copulate—it’s hard to get a microscope to the scene of the action. That means we can only draw inferences about sperm selection. Just because one male succeeds in fertilizing more of a female’s eggs than another doesn’t mean the sperm have been expressly chosen. The successful sperm may be more competitive or more compatible. Or the effect may be due to chance. In the mallard, for example, females who have been artificially inseminated with a mixture of sperm from several males tend to use the sperm of one male for a given clutch. Which male is the lucky one changes each time, however, even though the female receives the same mixture of sperm—suggesting that the effect is due to sperm clumping rather than to an active preference for the sperm of one male in particular.

  As for yellow dung flies, claims have been made that the female’s decision to use one male’s sperm rather than another’s depends on whether she lays her eggs on a cowpat in the shade or one in the sun. It is a fascinating idea but extraordinary claims require extraordinary evidence, which we do not currently have. In any event, if I were you I’d concentrate on eliminating the option of your mate’s choosing sperm. If a male yellow dung fly copulates for long enough, he can displace the sperm of previous males (to achieve this effect, small males have to copulate for longer than big males, because small males transfer sperm more slowly). Having replaced the sperm of your predecessors with your own, you should then guard the female until she has laid her eggs. That way, you won’t have to worry: your sperm will be the only ones available. Go for it!

  So you see, there are lots of reasons females might play the field, although we don’t necessarily know the reasons in any given instance. Just in case you meet a girl on the prowl and you want to understand her motives, here’s a checklist of possibilities:

  She has run out of sperm

  Her other lovers were sterile

  Her other lovers had lousy genes

  Her other lovers had incompatible genes

  Her other lovers were ugly

  She wants diversity in her children

  She wants you for your food

  She wants help raising her kids

  She wants to enter your sperm in a competition

  She wants to give herself or her eggs a selection of sperm to choose from

  She wants to confuse everyone about who’s the father

  You’ll notice that one obvious possibility is missing from the list—namely, that females sleep around for pleasure. The omission is deliberate: we know next to nothing about the evolution of sexual pleasure. I’d bet, though, that sexual pleasure is most likely to evolve when females have a lot to gain from promiscuous behavior.

  Folks, it’s time to bury forever the notion that female promiscuity is an unfortunate accident—a “malfunction,” the result of coercion, or simply a last resort to get a pesky guy to go away (known as “convenience polyandry,” this notion presumes that a male will stop harassing a female once he’s had his way with her). Which is not to say that females are never coerced or harassed into having sex. Or that sleeping around is always good. In the wasp Macrocentrus ancylivorus, for example, a female who mates too often gets clogged up with sperm and can’t fertilize her eggs. But like it or not, in countless species—from grasshoppers to fruit flies, pseudoscorpions to spiders, red-winged blackbirds to prairie dogs—it is not simply that females mate with lots of males. It’s that doing so is good for them: promiscuous females have more and healthier children. Natural selection, it seems, often smiles on strumpets. Sorry, boys.

  4

  SWORDS OR PISTOLS

  The art of dueling is knowing when to fight, when to flee—and when to play dirty.

  Dear Dr. Tatiana,

  I’m a fig wasps, and I’m in a panic. All the males I know are psychos. Instead of wooing us girls, they bite each other in half. What can I do to stop them?

  Give Peace a Chance in Ribeirão Prêto

  You can’t do anything, I’m afraid. Your society is one of the most violent on earth. For every crop of figs from your fig tree, millions of young male wasps have died in combat. That’s why they all have huge heads, gigantic scything mandibles, and heavily armored shoulders. And that’s why they all seem deranged: in your species, it’s kill or be killed. Still, you shouldn’t fret. Once he’s vanquished his rivals, the winner will mate with you. Why has such brutality evolved? The answer lies in your unusual lifestyle.

  Throughout the sun-drenched tropics, monkeys, birds, rodents, and bats feast on the fruits of the fig tree. The trees are one of nature’s successes: ancient, and abundant, they come in hundreds of different species of every shape and size. Some, such as the banyan tree, spread sideways, dropping thick roots from their branches. Others are tiny shrubs. Still others are parasites that eventually strangle their host plants. But whatever their way of life, fig trees have one feature in common. All of them depend on tiny wasps to pollinate them. Without the wasps, they cannot reproduce. On the Hawaiian island of Kauai, for example, fig trees were introduced without wasps and thus have not been able to multiply.

  Although each species of fig has its own private species of wasp, the different systems work in much the same way. The cycle begins when a female arrives at a fig flower, an enclosed urn with several hundred tiny flowers i
nside. This whole structure will later develop into a fruit. The arriving wasp struggles into the urn, often losing her wings and antennae in the process, and pollinates individual florets within. Depending on the species of wasp, she may pollinate by accident, brushing against the florets as she moves around inside the fig; or she may deliberately smear pollen on the appropriate organs of chosen flowers. After this, she lays her eggs, placing each into an ovary of a floret. Then she dies.

  Her children awaken to find themselves inside fig seeds—so they are minute. Each seed is only one or two millimeters long. The young wasps eat their way out—levying a pollination tax on the fig of one seed per pollinator. This may not sound like much, but it adds up. Some trees lose more than half their seeds to the tax collector. Males emerge first and help the females out of their seeds. They mate at once, then the males gallantly chew an exit out of the fruit so that the females can escape. Since the males have no wings, they die in the fig they were born in. The females, meanwhile, having collected pollen, fly off to find a new fig to struggle into—and so on. (Does this mean that humans eat dead wasps every time they eat a fig? Yes and no. Not all cultivated fig varieties require wasps to make fruit. However, some do—and then, yes, eating figs means eating dead wasps. But it’s no big deal. As I said, the wasps are tiny. And they’re not poisonous. On the contrary, they provide a little extra protein.)