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Authors: Olivia Judson

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For your lovers, this is the way the world ends—with a bang, not a whimper. When a male honeybee reaches his climax, he
explodes, his genitals ripped from his body with a loud snap. I can see why you find it unnerving. Why does it happen? Alas, Your Majesty, your lovers explode on purpose. By leaving their genitals inside you, they block you up. In doing so, each male hopes you will not be able to mate with another. In other words, his mutilated member is intended as the honeybee version of a chastity belt.
You may think this is no way to treat a queen. But even queens are not exempt from the battle of the sexes. Indeed, I'm afraid your situation appears to exemplify the full, complex, and dynamic conflicts of interest that can arise as a consequence of female promiscuity.
To see how the conflict unfolds, let's first look at matters from the male's point of view. His plight is desperate. A young queen such as yourself spends a mere few days mating before going off to start a nest. After that, you'll never bother with sex again; you'll be too busy having your half million children. Worse, his chances of mating with you are small to start with. Honeybees have sex on the fly: you take to the skies and mate with any male who can catch you. The competition can be fierce: as many as twenty-five thousand males may assemble to contend for a single queen. But you probably won't mate more than twenty times, so most male honeybees die virgins. Any male who succeeds in catching you has nothing to lose by exploding: he'd be unlikely to mate again anyway. What's more, he may have something to gain. If, by blocking you up, he can prevent just one other male from copulating with you, he will fertilize a larger proportion of your eggs—and more of his genes will be passed to the next generation.
But the problem is, while his interests are best served if you mate only with him, you do better if you mate with several males. Indeed, a queen who mated only once could be at risk of losing
half her brood. Why? Because of the complicated way that gender is determined in honeybees.
Usually, male honeybees hatch from unfertilized eggs, females from fertilized eggs. But bees have a gene, known as the sex-determining gene, that can mess up this arrangement. If a queen mates with a male who has the same version of this gene as she does, then half her fertilized eggs will hatch out sons—and sterile sons at that. Thus, instead of producing a mixture of dutiful daughters working hard to rear their sisters and a few fertile males waiting for their once-in-a-lifetime opportunity to explode with joy, half her children would be good-for-nothing infertile males—which the dutiful daughters would eat alive. Such a reduction in the workforce increases the risk that the nest will fail. If, therefore, the queen mates with several males instead of just one, any male whose sex-determining gene matches hers will fertilize a smaller proportion of her eggs. This way, only that small proportion of her offspring will be sterile males. So the more a queen mates, the more likely she is to avert disaster.
That's not all. Males, obviously, will also gain if they can thwart previous lovers by removing the plug and mating with the female in their turn. You might imagine, then, that male honeybees would have evolved some way of removing the chastity belt. You'd be right. If you look closely, you'll see that each male honeybee sports, on the tip of his phallus, a hairy structure that can dislodge the severed genitalia of his predecessor.
This suggests the following evolutionary scenario. Once upon a time, queens mated with only one male. Then a mutant queen appeared who mated with more than one. She was more successful at reproducing than her virtuous sisters, and the gene for multiple mating spread throughout the honeybee population. Then a male appeared who, by exploding, prevented the queen
from mating again. Genes for exploding males spread throughout the population. In a counter-countermove, the queen evolved to block the male's advantage, either removing the plug herself or perhaps having it removed by the workers (this step would have happened swiftly, since any female who did not remove the plug would not have been able to lay eggs). Then males evolved their own counter-counter-countermove. And so on.
As you've probably guessed, such a situation is far from unusual. It is generally the case that whenever females mate repeatedly, males are sure to lose. Any male who can prevent a female from mating with his rivals will sire more of her children than a less controlling fellow and will thus spread more of his genes. So you shouldn't be surprised to learn that chastity belts are a popular evolutionary invention, in vogue among bats, rats, worms, snakes, spiders, butterflies, fruit flies, guinea pigs, squirrels, chimpanzees—I could go on. I must admit, however, that most of these fellows opt for the more traditional plugs, cements, and glues rather than for amputating their genitalia. In many species of rodent, for example, males have enormous glands to secrete tough, rubbery corks that they place deep in their partners' reproductive tracts as they finish copulating. The house mouse makes a plug so tough that a scalpel virtually bounces off it; once the plug has formed inside a female, attempts to remove it can tear the ligaments of her womb.
But alas, poor males. Whenever repeated mating is beneficial to the female, she will gain by resisting male efforts at control. Thus, as males evolve to control, females evolve to resist. Which is why not all chastity belts are as effective as they might be. A female fox squirrel, for example, reaches around and pulls out the plug right after sex (and sometimes then eats it—how delicious). Moreover, males will also be under pressure to evolve to remove
the plug. Again, this skill has appeared repeatedly. In the rat, the male's penis is almost prehensile: it can do some glorious gymnastic flips to dislodge plugs left by previous lovers, making like a toilet plunger and pulling them out with suction.
So you see, the battle of the sexes is fought on two fronts. Conflicts of interest between males and females mean that every new weapon or behavior evolved by one sex will favor traits in the other sex that can counter that development. At the same time, males evolve to manipulate and thwart a female's previous and subsequent lovers. If you watch through the generations, you'll witness a mighty evolutionary battle.

 

Men, you're in a cruel bind. Female promiscuity puts your genes at risk: it's no good seducing all the women in sight if none of them uses your sperm. A woman's potential for promiscuity curbs your own and exerts a powerful force on your evolution. Rather than maximizing the number of girls seduced—that is, acting like a cad—you should try to maximize the number of eggs fertilized. For some men, some of the time, this will amount to the same thing: more skirt chasing. On many occasions, though, cads who spread their bounty will have fewer offspring than more loyal fellows, and so genes for pure caddishness will decline in frequency Far better would be to attach yourself like the stick insect, explode like the honeybee, or evolve still other fates stranger than your strangest dreams.

THE EXPENSE IS DAMNABLE
I
t's not easy being a male. Especially if you have to make sperm twenty times longer than you are. Or produce billions and billions of sperm in every ejaculate. Or copulate a hundred times a day to satisfy your partner. Or perform some other feat of prodigious sexual prowess.
Dear Dr. Tatiana,
 
I'm a splendid fairy wren, and I'm concerned about my husband. He keeps going to the doctor because he's convinced his sperm count is too low and we won't be able to have children. But he ejaculates eight billion sperm at a time, so I don't see how he can have a shortage. Has he really got a problem, or is he being neurotic?
 
Bewildered Down Under
The doctor, eh? I'd say your mate is not a hypochondriac but a liar. His “appointments” are a thin disguise for philandering.
Splendid fairy wrens are notorious for their extramarital adventures. Let me give you a tip. You can tell when a fairy wren's going a-wooing: he'll be carrying a pink petal in his beak to offer to his paramour. Why pink? It looks pretty when he fans his iridescent blue cheek feathers.
But the real question is why a bird smaller than my fist should need an ejaculate containing more than eight billion sperm. In human beings, the average dollop contains only 180 million or thereabouts. Even that's odd when you think about it, though. All those sperm for one little egg. Why?
Sperm numbers are a crude index of the difficulty of reaching an egg. If you're a tree, for example, the amount of pollen you make depends in large part on how it gets delivered. Take fig trees. Some species are pollinated by virtuous wasps, wasps that actively collect and distribute pollen; these figs can afford to be frugal with the stuff. Other fig species are forced to rely on lazy wasps that just brush against the flowers; these figs are, perforce, profligates. So in species like yours or mine, where a male delivers his sperm personally, you would imagine that sperm counts would drop.
Not necessarily. In some species—of fish, for example—males and females meet up, but instead of copulating, they spawn eggs and sperm into the water. And yes, in such cases sperm do not dramatically outnumber eggs. But when you turn to birds, mammals, and other groups that copulate, the picture changes. Instead, you find that males make the most sperm in species where—drumroll, please—females are sluts.
Two factors are thought to produce massive sperm counts in species where the girls are promiscuous. The first is what biologists call “sperm competition”—that's right, sperm from different males vie with each other to fertilize eggs. If sperm competition proceeds according to a raffle—the more tickets you buy
the more likely you are to win—then the males that produce the most sperm will have the best chance of fertilizing a female's eggs. And if the number of sperm they make has a genetic basis, then over time the repeated success of males with the highest sperm counts will lead to an increase in the number of sperm each male produces. Reflecting this, males regularly exposed to sperm competition should also have larger testes—sperm factories—for their body size. Indeed, an experiment with yellow dung flies—hairy flies that mate and lay eggs on fresh cowpats—has shown that testes size can evolve in response to sperm competition in as few as ten generations.
Carrying the argument to its logical conclusion, then, males who are never at risk of sperm competition should produce only enough sperm to fertilize each egg. Unfortunately, few fellows are in this luxurious position. But males in one group are—seahorses and their close cousins, pipefish. (Pipefish look like seahorses that have been straightened and streamlined.) These males are famous for their pregnancies. Females typically deposit eggs in the male's brood pouch, and he fertilizes them there—so there's no chance of his sperm encountering those from another male. Most species of seahorse have not had their sperm counted. But one that has is the seaweed pipefish, a species common in seagrass beds around Japan—and sure enough, his sperm count is vanishingly low.
The second factor thought to produce high sperm counts is that sperm die in huge numbers on their travels through the female reproductive tract: of the millions that set out, just a few succeed in reaching their goal. Fantastically high sperm death has been remarked upon for more than three hundred years, yet there is still no good theoretical explanation for why so many sperm die in the first place.
You see, the surprising fact is that female reproductive tracts
are often hostile to sperm. No one knows why this is so. But rather than cosseting sperm and helping them on their way as you might expect, reproductive tracts are full of hazards and treachery. Sperm may be digested, ejected, or rounded up and removed. Even in species where the females store sperm for years, they only keep a few of the sperm that they get. A honeybee queen who mates with seventeen lovers, for example, will receive an average of 102 million sperm (6 million from each fellow); yet she'll keep a mere 5.3 million to fertilize her eggs. In species that don't store sperm—it's carnage.
In humans, for example, sperm start their odyssey in the acidic environment of the vagina. But acid is lethal to sperm (which is why strategically placed lemon slices make a good, if rudimentary, contraceptive), and fewer than 10 percent will continue their onward voyage. Survivors must then traverse the cervix, a barrier coated with mucus that even at the best of times permits a mere 10 percent of sperm to cross. Mucus is only one of the cervical hazards, though. At the first hint of sperm, white blood cells—the foot soldiers of the immune system—swamp both the cervix and the lining of the womb and destroy any intruders they encounter. In rabbits, within an hour of copulation an enormous army of white blood cells assembles at the cervix; in women, the army amasses within fifteen minutes of copulation, and within four hours it numbers more than one billion. By the time sperm reach the fallopian tubes—the place where any fertile eggs might be hanging about—their numbers will have dwindled from millions and millions to a few hundred. Which is why men with a sperm count of fifty million—which might seem generous—are likely to be infertile.
Measuring hostility is much harder than counting sperm, so we don't know how hostility varies among species or even among individuals of the same species. I would guess, however, that
females respond to escalating sperm numbers by increasing the hostility of their reproductive tract. This in turn would favor males who produce more sperm. In the rabbit, for example, the number of sperm arriving at any given stage of a female's genital tract depends on how many sperm started out. But what do females gain from being hostile? After all, it seems counterproductive: if they are too hostile, their eggs won't be fertilized and they'll have no children. One idea is that hostility ensures that only the most superior sperm succeed in fertilizing eggs. Another is that hostility may initially evolve as a defense against infection. This would then be met by male attempts to bypass the defenses. Indeed, the semen from humans and many other mammals contains substances known to suppress the female's immune response. To counteract male attempts at suppression, females may respond by increasing the magnitude of their immune response—setting up an escalating evolutionary cycle of response and counterresponse.
Which brings me back to why your husband needs so much sperm. In splendid-fairy-wren societies, couples live together and rear children together—but free love prevails. Splendid fairy wrens are splendidly promiscuous, and most females have at least one lover as well as a husband. As a result, sperm competition is intense. Often, none of the chicks in a nest will have been sired by the male who is rearing them. So while your husband is off philandering, perhaps you've engaged in a little mischief of your own?
Dear Dr. Tatiana,
 
I've heard it's going to take me three weeks to make just one sperm. Apparently this is because it's going to need a tail twenty
times longer than my whole body. This seems awfully unfair: I'm just a little fruit fly,
Drosophila bifurca.
Can't I get a prosthesis?
 
Waiting for Sperm in Ohio
There's no market in artificial sperm tails: you're going to have to make them yourself. You're right—it's not fair. Why should a fruit fly three millimeters long—smaller than this dash—have to make sperm that measure fifty-eight millimeters? A human is far bigger than you, but gets away with sperm one thousand times smaller. Indeed, if a man were to make a sperm on your scale, it would be as long as a blue whale. Now, that I'd like to see.
Unlike sperm number, the evolution of sperm size and shape is something we know little about. All we can say for sure is that sperm tend to be smaller and simpler in species where the eggs are fertilized outside the female's body.
Consider sperm shape first. A conventional sperm looks like a tadpole, with a big head and undulating tail. But in many species, sperm deviate from this model. A popular invention is the tandem sperm—sperm that always swim in teams of two. They've evolved in American opossums, water beetles, millipedes, firebrats, and some seafaring snails. Hooks are also fashionable. Koalas, rodents, and crickets all have hooked sperm. The protura, tiny critters related to insects, were the first to play Ultimate Frisbee: their sperm are flat discs. Crayfishes have sperm that resemble Catherine wheels. Some land snails make corkscrews. Some termites make bearded sperm—sperm with one hundred tails. Roundworms make amoeboid sperm: these don't swim, they crawl. And all this before you begin to look at spermatophores, the sperm packets that many creatures deliver. After a lengthy lovemaking session, the giant octopus, for example, hands over a
spermatophore that is a huge bomb. Over a meter (three feet) long, it contains more than ten billion sperm and explodes inside the female reproductive tract.
Since these various shapes have evolved independently in different groups, they must be repeatedly beneficial in some way. Hooks, for example, might help sperm grapple their way along the reproductive tract—but to my knowledge, this has never been demonstrated. The possible advantages of other shapes? Your guess is as good as mine. But as far as we can tell, sperm shape has nothing to do with female promiscuity.
Sperm size, however, probably does. In roundworms, big sperm are more successful at fertilizing eggs, apparently because they crawl faster than small sperm and are less likely to be pushed aside by rivals. Similarly, in the bulb mite, an agricultural pest, males who boast big sperm fertilize more eggs than males whose sperm are puny. Indeed, as a general rule, where females are promiscuous, males don't just make more sperm, they make bigger sperm. Yet both attributes can't increase indefinitely: at some point, making sperm bigger must mean producing them in smaller quantities. In most species, pressure to keep the numbers up probably precludes a substantial increase in sperm size.
In a few species, though, numbers are apparently reduced in favor of making enormous sperm. The Giant Sperm Hall of Fame contains a diverse scattering of animals. Although you,
Drosophila bifurca,
are the reigning champion, in the last hundred years the title of Most Massive Sperm has been held by featherwing beetles, back-swimming beetles, ostracods (small shrimp that look like kidney beans on legs), ticks, the Australian land snail
Hedleyella falconeri,
the painter's frog, and many other species of fruit fly. The ostracod sperm, by the way, are rumored to fight, smashing one another to smithereens—although as best as I know this has never been investigated in a laboratory.
Unfortunately, work on giant sperm hasn't advanced much beyond openmouthed gawking, so I can't say a great deal about why some animals make gargantuan gametes. But what we do know suggests that big sperm have nothing to do with big eggs, although this idea has been considered. People don't study eggs as much as they study sperm (in species where fertilization is internal, sperm are easier to observe), but other fruit flies make both bigger eggs and smaller sperm than you do. Another idea is that giant sperm are a present from the male to the female to provide nutrition for her eggs. But in many species with giant sperm, only a tiny piece is taken into the egg, so I'm not convinced by this explanation either. Could giant sperm block the female reproductive tract and therefore serve as a chastity belt? This may be true for featherwing beetles: giant sperm from one male appear to fill the female's reproductive tract, effectively stopping the addition of sperm from anyone else. But this is not the case for ostracods: the females have a bizarre system of sperm storage whereby sperm are deposited and stored in an area that has no direct opening into the chamber where eggs are made. To fertilize an egg, an ostracod sperm must actually leave the waiting room and travel outside the female's body to reach the egg chamber. And in your closest competitor,
Drosophila hydei
(sperm 23 millimeters), not only does a female mate repeatedly but the various sperm she receives will mix. As a result, if she mates with several fellows on one day, each sires an equal proportion of her brood.
Still, there must be a good reason for colossal sperm. After all, where the cost of making them has been measured, it turns out to be considerable. Whereas your distant cousin
Drosophila melanogaster
(sperm 1.91 millimeters), can begin copulating a few hours after he tumbles out of his pupa, you must wait at least seventeen days—the time it takes for you to build your enormous testes. But
things could be worse. If you stay out of trouble, you can expect to live for six months—a long time for a fruit fly—so having to wait seventeen days to lose your virginity isn't such a trial. In another of your cousins,
Drosophila pachea
(sperm 16.53 millimeters), a male spends the first half of his adult life unable to reproduce. And here's something you can feel good about: while most males need armies of millions, apparently you can thrive with a few good sperm.
BOOK: Dr. Tatiana's Sex Advice to All Creation
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