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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.
SWORDS OR PISTOLS
T
he 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 inside. 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.)
You'll have noticed I've said nothing so far about fighting male wasps. That's because pollinating wasps are generally peaceable types. They are not, however, the only occupants of a fig. As well as having a pollinator species, each fig species has to put up with parasitic wasps—sometimes as many as twenty-five different species. A few are pollinators that have gone bad. They live off the fig, but the pockets they once, long ago, filled with pollen stay empty. Others simply prey on the pollinators. For the most part the biology of these parasites is poorly understood, but we do know that they are often prone to violence.
The difference stems from the way that female parasitic wasps lay their eggs. Rather than crawling into the urn, most of the parasites lay their eggs by drilling through the outside. This means that these females do not have to lay all their eggs in one place as pollinators do but instead can lay a few eggs in many. At the right time of year, you can see speckles on the fig skins from the drilling of different females.
Spreading a brood among several figs will have one of two consequences. In species where population densities are low, males risk finding themselves alone in a fig. So it is not surprising that where this is likely, males have wings so that they can fly off to
search for lovers outside the fig of their birth. But in species—and yours is one—where figs tend to be crowded, males do not fly. Any given fig will probably also be home to mates. The trouble is, of course, it will probably also be home to rivals. Hence the slaughter.
Mortal combat is an effective but risky way of eliminating rivals. Males are not usually interested in fighting to the death unless they have a lot to gain—and little to lose—by doing so. Dying, after all, precludes further reproduction. Thus, lethal fighting is most likely to occur in species like yours that live for only one breeding season. One-shot breeding does not by itself, however, produce routine violence. Two other factors are crucial. First, receptive females must be clumped in space and time such that a fellow's only chance to mate is here, now. Second, fighting must increase the number of females he can mate with: there is no point wasting time fighting if in doing so he is missing out on sex. For example, if females are abundant but they mate only once, then males who copulate will do better than males who fight—a dynamic thought to explain why fighting is virtually unheard of among pollinator wasps.
Only a handful of other creatures have a reputation for extreme violence, and what little we know of them is consistent with this scenario. Take the “annual” fishes of Africa and South America. Their lifestyle is almost magical. They live in puddles, ponds, and ditches that dry up for part of the year. When the puddles dry up, they die. Only their eggs survive, buried under the dried mud, waiting for the next rains. Collect mud, add water—and presto, you get fish! You can see why people believed in spontaneous generation. When the rains come, time is short. As there is no chance to move to a new neighborhood, everyone tries to be the big fish in the small pond: the males of some of
these species are among the most pugnacious fishes known. If I had to bet, I'd predict that the more ephemeral the puddle, the fiercer the fighting.
Or take gladiator frogs. These brown tropical frogs have evolved switchblades: on each hand, just above the thumb, males have a sharp, retractable spine that is shaped like a scythe. Most of the time, they keep it sheathed in folds of flesh. But when two male frogs fight, they rake these spines across each other's faces, aiming for the eyes and eardrums of their opponent. Although we don't know the death toll in the wild, we do know fights can be lethal. As you would expect, competition for mates is fierce. And also consistent with the hypothesis, gladiator frogs have short lives. Even without the fighting, few survive from one breeding season to the next.
Perhaps the strangest example of violence is not from an animal but from a plant, the orchid
Catasetum ochraceum,
and its relations. In these species, female flowers receive pollen from only one pollinator. Immediately after pollination, they swell shut and set about making fruit. Competition between male flowers to be “the one” is therefore fierce. But since they are plants, they can hardly fight it out man to man. Instead, they direct their aggression at a hapless intermediary—a bee. The male flowers assault any bee who ventures inside them, throwing sticky sacks of pollen onto the bees' backs. In one species, the flower throws the pollen at the staggering velocity of 323 centimeters per second. Since the pollen sacs are also large—they can be as much as 23 percent of a bee's weight—the bees don't like this treatment. After one such attack, they avoid all other males, visiting only the gentle female flowers.
But for brutality, nothing rivals wasps in a fig. One scientist I know tried to study fighting in fig wasps—only to find that he was never there in time. Whenever he slit open a fig, there would
be just one male left alive, celebrating his victories by mating with all the females in the fruit. So as you see, there's a reason all the guys you know have such terrifying demeanors—and maybe now that you understand, you can forgive them for being such maniacs.
Dear Dr. Tatiana,
 
Perhaps you can help. I don't know what's happened to me. I'm a twenty-seven-year-old African elephant, and I used to enjoy showering at the water hole and other idle pleasures. But the joy has gone from life. I feel angry all the time—if I see another bull elephant, I want to kill him. And I'm obsessed with sex. Night after night I have erotic dreams, and the sight of a beautiful cow sends me into a frenzy. Worst of all, my penis has turned green. Am I ill?
 
Anxious in Amboseli
Uncontrollable aggression, obsessive lust, morbid anxiety about your sexual health: this all sounds normal for a fellow in his late twenties. It's nothing to worry about. You've just got a case of SINBAD: Single Income, No Babe, Absolutely Desperate. Unfortunately for you, however, you're likely to be in this state for much of the next twenty years. Female elephants prefer older males. Until you're bigger, the cows will run away from you—and their mothers and sisters will bellow for older bulls in the area to come and send you packing.
I'm afraid that females in many species often provoke males into fighting over them. When the mood strikes, they make themselves conspicuous—then stand back and watch the battle, before
mating with the winner. Female northern elephant seals, for example, create a rumpus whenever a male tries to mount them; this has the immediate effect of summoning every other fellow on the beach, even waking those who've been snoozing. The Burmese jungle fowl—the ancestor of the farmyard chicken—gives a loud squawk after laying an egg, an odd thing to do given that it immediately tells hungry predators there are eggs on the menu. But it also, apparently, goads any roosters in the area into fisticuffs over the chance to fertilize her next egg. In my opinion, though, the worst offenders are found in
Zootermopsis nevadensis,
a termite that lives in rotting wood. In this species, males and females usually live together as couples. They meet each other on a suitable log and found a nest. During this initial period, if a male finds he doesn't like his mate, he'll probably leave. But a female will typically invite a new male into the nest, which almost always results in the two males dueling. Between bouts, the female will groom first one and then the other. (On rare occasions, a male will invite a new female into the nest—and will then encourage the girls to fight.) Finally, although female cheetahs do not, as far as I know, goad their admirers into fighting, they do find fights arousing and come into heat shortly after watching one.
Female provocation does not usually lead to a pileup of corpses, however. As the saying goes, “He who fights and runs away lives to mate another day.” There's no point in fighting if you know you're going to lose—especially if by bowing out, you may be able to find another mate elsewhere. That's why even in one-shot breeders, fighting to the death is rare. If a male arrives to discover that another guy got there first, there may be some argy-bargy, but it's more likely to be a show of strength than all-out war. Take two-spotted spider mites. These tiny creatures are agricultural pests: they feed on plant cells, stabbing each cell
with their mouthparts and drinking it dry. Although they are mites, they have the ability to make silk just like their spider cousins. In this species, males hunt for adolescent females—those about to undergo their final molt and become adults—and stand guard, so that they can be first come, first served. A guarding male sits on the female, with his legs draped over her body. If a second male arrives and refuses to leave when threatened, some sort of fight will break out. The two males will wave their front legs and grapple with each other, often trying to trip their opponent by attaching strands of silk to his legs. Fights can end in death, but that's rare. Usually, the smaller male retreats before it comes to that.
Size is crucial in hand-to-hand fighting. In animals from boa constrictors to humans, the larger combatant typically enjoys a large advantage, so smaller males usually back off. As a rule, savage fighting breaks out only when both contestants figure they can win—that is, when they are about the same size. Consequently, many animals have evolved bizarre rituals to assess their opponents. Remember those flies with eyes perched on the ends of long, stiff stalks? Males measure their strength by going head-to-head to compare eye spans. If there isn't a clear difference, they'll fight; otherwise, the male with the smaller eyespan leaves. Thus, you can tell when fighting is important in determining who gets to mate: males will typically have evolved to be big. Male elephants, for example, have evolved to grow throughout their lives rather than stopping after puberty like most mammals. Whereas most mammals cannot grow beyond puberty because their bones fuse together, a male elephant's bones don't fuse until he is middle-aged. That's how male elephants can grow to be more than twice the size of females.
Among elephants, though, it's not only size that matters. Bull elephants, even the largest and oldest of them, feel like fighting
only at certain times of the year, when they are in the grip of a fury known as musth. For young males, a bout of musth lasts only a few days at a time, but for the oldest bulls it can continue for as long as four months. When a bull is in musth, the amount of testosterone in his blood soars to levels fifty times higher than usual. Unsurprisingly, this has profound effects on a fellow's behavior.
BOOK: Dr. Tatiana's Sex Advice to All Creation
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