DR. TATIANA'S SEX ADVICE TO ALL CREATION
LET SLIP THE WHORES OF WAR!
The battle of the sexes is no myth. Success at sexual reproduction is at the heart of the evolutionary process. But greater success for her often means less success for him. The upshot? An eternal war--and an astounding diversity of strategies.
A SKETCH OF THE BATTLEFIELD
Boys are promiscuous and girls are chaste, right? Wrong. The battle of the sexes erupts because, in most species, girls are wanton.
Dear Dr. Tatiana,
My name's Twiggy, and I'm a stick insect. It's with great embarrassment that I write to you while copulating, but my mate and I have been copulating for ten weeks already. I'm bored out of my skull, yet he shows no sign of flagging. He says it's because he's madly in love with me, but I think he's just plain mad. How can I get him to quit?
Sick of Sex in India
Who'd have thought a stick insect would be among the world's most tireless lovers? Ten weeks! I can see why you've had enough. Twiggy, your suspicions are half right. Your paramour ismad, though not with love but with jealousy. By continually copulating he can guarantee that no one else will have a chance to get near you. It's a good thing he's only half your length, so he's not too heavy to carry about.
Is your case unusual? Well, it is extreme, but by no means unique. Males in many species are fiercely possessive of their mates. Look at the Idaho ground squirrel, a rare critter that lives only in (surprise) Idaho. The male won't let his partner out of his sight and follows her everywhere. If she goes into a burrow he sits at the entrance so she can't come out--and no one else can go in. Worse, he picks fights with any other male who happens to come near. Or consider the blue milkweed beetle. After sex--which by any insect standards is brief, taking only ten minutes or so--the male insists on riding around on the female's back, not so he can whisper sweet nothings but so he can stop her from gallivanting.
To be frank, though, males have good reason to be possessive. Given half a chance, girls in most species will leap into bed with another fellow. "But wait," I hear you cry, "isn't it a general law of nature that males are promiscuous and females are chaste?" That is indeed what used to be thought. But now we know this notion is nonsense.
The man who first lent scientific respectability to this notion was named A. J. Bateman. In 1948, he published a paper in the scientific journal Heredity in which he claimed to have proved that males have evolved to make love and females to make babies. His assertions were based on experiments he had conducted with the fruit fly Drosophila melanogaster. This is one of those small flies drawn to bowls of ripening fruit or to glasses of wine, and should on no account be confused with the larger housefly, which likes feces and other muck. Drosophila boasts perhaps as many as two thousand different species, with more than four hundred inHawaii alone. Little is known about most of them. But Drosophila melanogaster is beloved of geneticists and, along with the worm, the mouse, and the human, is one of the most studied animals on earth.
After keeping equal numbers of adult male and female flies together in small bottles for three or four days, Bateman noticed that the males were keen to mate as often as possible, ardently vibrating their wings for any girl who'd pay attention. If a female was receptive, the male would press his suit, licking her genitalia before gently spreading her wings and mounting her. Most of the time, however, the males were disappointed. Bateman observed that female flies tended to reject the advances of more than one or two suitors. In accordance with this observation, he also found that while males had more children the more partners they mated with, females did not.
To explain his results, Bateman appealed to what he saw as the essential difference between the sexes--that males produce lots of tiny, cheap sperm whereas females produce a few large, expensive eggs. He also noted that the females of many species can store sperm for days, months, or in some cases years, which means that sperm from one mating can, in principle, last a lifetime. Therefore, Bateman argued, one male could easily fertilize all the eggs of many females. Accordingly, he went on, females are limited in their reproduction by how fast they can make eggs, whereas males are limited only by the number of females that they can find and seduce. So, he proclaimed with a flourish, males (including humans) are natural philanderers while females (again including humans) are naturally chaste--and in all but the most unusual circumstances should be indifferent or hostile to mating more than absolutely necessary. From this perspective, Twiggy, your mate's passion is weird and inexplicable: he should be off seducing other stick insects, not sticking stubbornly to you.
Nonetheless, this "men are cads, women are saints" hypothesis--more politely known as Bateman's principle--has been all the rage. Patriarchs have extolled it. Feminists have invoked it. Scientists have expounded it and buttressed it, adding extra reasons--the risk of venereal disease or being caught by a predator while copulating--why females would naturally want to keep sexual activity to a minimum. And certainly there are some species--such as the alfalfa leaf-cutter bee--where females mate just once. There are other species where males race from one girl to the next or are so eager they'll fornicate with anything: goldfish, for example, are occasionally drowned by amorous frogs. But as a general rule? Ha!
Bateman's principle has a fundamental flaw: it's wrong. In most species, girls are more strumpet than saint. Rather than just mating once, they'll mate with several fellows, and often with far, far more than necessary just to fertilize their eggs.
How did Bateman come to be so misguided? There are two reasons. The first is a quirk of fate. As I said, Drosophila melanogaster was--and remains--the most fashionable fruit fly to study. Females of this species really are quite restrained, preferring not to mate more than once a week or so. Other species of Drosophila would have given different results: Drosophila hydei females enjoy sex several times each morning, for example. But even in melanogaster, females are not as virtuous as Bateman thought. The trouble is--and this is the second reason he blundered--his experiments were too short. We now know that if he had continued them for one more week, he would have discovered that Drosophila melanogaster females recover their appetites--and indeed that those who mate only once have fewer children than their more lascivious sisters.
The reason it took more than thirty years for anyone to detectthe problems with Bateman's theory is partly because his logic sounded reasonable. Moreover, it seemed to be supported by observation. Thousands and thousands of hours spent watching mammals and birds going about their lives had given no suggestion that females were often unfaithful to their mates. That's not the whole story, though. Even once scientists started to notice that females in some species--especially insects--do mate with a lot of males, they didn't immediately grasp the full implications. If females mated more than expected, it was assumed they had "malfunctioned" or that males had led them astray, not that females might have something to gain.
In the 1980s, the development of more sophisticated genetic techniques meant that biologists could find out who was really having whose children. And they discovered something astonishing, something that no one had predicted. Namely that, from stick insects to chimpanzees, females are hardly ever faithful.
This discovery was swiftly followed by another that was even more surprising: in species after species, rampant promiscuity is no malfunction. Rather, females benefit from it. My files bulge with examples. To pick a few at random, female rabbits and Gunnison's prairie dogs both show higher rates of conception if they mate with several partners while they are in heat. The female sand lizard hatches out more eggs the more lovers she's had. The female slippery dick--a pale fish that lives on coral reefs--will have more of her eggs fertilized if she spawns with a gang than if she spawns with just one fellow.
These discoveries have forced a reevaluation of male and female behaviors that is still under way But one conclusion is inescapable. As we shall see, when females mate with more than one male, War capers nimbly through the boudoirs, imps of discord frolicking in his wake.
Dear Dr. Tatiana,
My boyfriend is the handsomest golden potto I ever saw. He's got beautiful golden fur on his back, creamy white fur on his belly, he smells delicious, and he has ever such dainty hands and feet. There's just one thing. Please, Dr. Tatiana, why is his penis covered with enormous spines?
Spooked in Gabon
All the better to tickle you with, my dear. At least, I'll bet that's a big part of the reason. Golden pottos are little-known relations of bushbabies--small, night-climbing primates that are distant cousins of monkeys and apes. If you look at your cousins, you'll see your beloved is not alone. Bushbabies and many other primates have monstrous penises--many of them look like medieval torture instruments. They have spikes and knobs and bristles and are often twisted into weird and sinister shapes. By comparison, the human penis is dull, notable only for its girth.
Penises are for more than just sperm delivery, you see. If females mate with a number of males, each subsequent suitor will sire a larger proportion of her children if his sperm are the ones that do the trick. A male who can stimulate his mate to take up more of his sperm, or who can somehow get rid of the sperm of his rivals, will spread more of his genes than less artful fellows. Thus, the first consequence of female promiscuity is that males are under great pressure to outdo one another in all aspects of love. For this task, the penis is an important tool.
Consider damselflies. These insects, close relations of dragonflies, look sweet and innocent as they flit along the riverbanks on a sultry summer day. But they have evolved some of the fanciest penises around. A typical damselfly penis has a balloon--aninflatable bulb--and two horns at the tip, plus long bristles down the sides. In the black-winged damselfly, Calopteryx maculata, the male uses this device to scour sperm from inside a female before depositing his own. But in the related Calopteryx haemorrhoidalis asturica, he uses his penis as an instrument of persuasion: by stimulating her in the proper manner, he can induce her to eject sperm from previous lovers. Meanwhile, the moth Olceclostera seraphica has genitals that resemble a musical instrument: the male rubs one part of his privates against another, producing vibrations with which to thrill his mate. In contrast, among termites the female typically mates with only one male--and male termites have plain, unadorned genitalia that do not differ much from one species to the next.
A penis is not the only way to outdo other males, of course. Take the ghost spider crab Inachus phalangium, a creature that lives under the protective tentacles of sea anemones. The male makes a special jelly to seal the sperm of previous males into a corner of the female's reproductive tract so it won't be able to mingle with his own. Or consider the dunnock, a bird that looks like a sparrow that has fluffed its feathers in ashes. Most male birds--swans, ducks, and ostriches being exceptions--do not have penises. Instead, males and females copulate by quickly pressing their genital openings together. Hardly satisfactory. But even without a penis, male dunnocks have found a way to get rid of rival sperm. Before sex, the male pecks the nether regions of his mate; sometimes this encourages her to dump any sperm she's collected. Even more exotic: the red-billed buffalo weaver, an African bird that lives in small communities. The female is wildly promiscuous. Apparently in response, the male has evolved a pseudophallus--a rod of tissue that cannot transfer sperm. During sex, he rubs this rod against the female's genitalia for about half an hour--at which point he ejaculates from his genital openingand appears to have an intense orgasm. The male who provides the most vigorous stimulation is presumably the most successful at persuading a female to use his sperm.
All of this provides a clue as to why your friend's penis looks so alarming. Among primates as among insects, it is a rule of thumb that in species where females consort with one male at a time, penises are small and uninteresting. I mean, take the gorilla--a huge guy with a little teeny weenie. A male gorilla can weigh 210 kilos (460 pounds), but his penis is a measly five centimeters (two inches) long and entirely devoid of knobs and spikes. The Argentine lake duck puts him to shame. The duck is small, but his penis, which rivals that of the ostrich, is twenty centimeters (eight inches) long--and it has spines. But then, a male gorilla generally presides over a small group and does not often have to worry about other fellows' sperm. If I were a girl gorilla, though, I'd feel I was missing out: as far as anyone can tell, the females of more promiscuous primate species are more capable of orgasm. So I'd guess your mate's penis is gloriously bespined because female golden pottos sometimes sleep around. But whether the spines have evolved because you like them or whether they are more for scrubbing--well, why don't you find out?
Dear Dr. Tatiana,
I'm a queen bee, and I'm worried. All my lovers leave their genitals inside me and then drop dead. Is this normal?
Perplexed in Cloverhill
For your lovers, this is the way the world ends--with a bang, not a whimper. When a male honeybee reaches his climax, heexplodes, 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 losinghalf 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 queenfrom 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 removethe 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.
Copyright © 2002 by Olivia Judson