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Authors: Olivia Judson

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Both the runaway process and the good genes theory make sense in principle. As usual, though, it's difficult to work out what Mother Nature's been up to in any particular case. Let me give you a couple of examples.
When biologists study wild birds, they often put little colored bracelets on the birds' legs so that they can tell who's who from far away. Evidently, bracelets are not a characteristic that can be inherited. Yet it turns out that female zebra finches find a male sporting red bracelets to be extremely sexy. So sexy, indeed, that they will lay him an extra clutch of eggs. Green bracelets, however, have no such charm. Perhaps females find that green clashes with a fellow's orange legs; in any case, males wearing green bracelets have no luck with the girls.
But although this preference shows females can pick a mate based on sex appeal alone—the basic requirement for a runaway process—in more natural situations it is often exceedingly hard to tell whether females are mating because they find the males
sexy or because they're hoping for good genes. An example of the difficulties comes from peacocks. Peachicks sired by males with fancier tails survive at a higher rate than those fathered by more humdrum-looking males—which at first glance supports the good genes hypothesis. The trouble is, there's always the possibility that the effect appears simply because females who mate with sexy males take more trouble over their offspring. Among mallards, a duck who mates with the sexiest drake lays larger eggs than she does for an ugly fellow. Big eggs are a crucial factor in a chick's early survival. But it turns out that a drake's genes have no bearing on the size of the eggs. The difference in bigness can be explained entirely by the mother's tender loving care. So why does she bother? Who knows. Perhaps it's Fisher coming through the back door: perhaps ducks with sexy mates put more effort into their offspring because they know their ducklings will grow up to be sexy too. Is something like this also going on in peacocks? We don't know. Although peahens don't alter the size of their eggs, they could be making more subtle adjustments. Female zebra finches mated to attractive males, for example, increase the testosterone composition of their eggs—thus accelerating the speed at which the chicks grow.
Your situation is similarly complex, my stalky friend. When females mate with you, are they after good genes or sexy sons? There is evidence that if the larval environment is harsh, only a few males have the genes to grow great stalks. Again, at first glance, this supports the good genes idea: females select the males most able to cope with a tough environment. Alas, without information on whether these males have offspring who are more likely to survive than the offspring of other males, we cannot arbitrate. In picking males with the longest eyestalks, the females also increase the odds that their sons will be sexy too.
Dear Dr. Tatiana,
 
I'm a harlequin-beetle-riding pseudoscorpion. At least, I should be. But when I found a beetle to ride, I wasn't allowed on board. Some big thug of a pseudoscorpion helped my girlfriend on but pushed me away as the beetle took off. ,She went with him happily, and I just know she's having sex with him, the tramp. Meanwhile, here I am marooned, a stuck-on-a-rotting-log pseudoscorpion. I've tried waving my pincers at harlequin beetles flying overhead, but none has landed. How can I get off this log and find a girl who will be true?
Stranded in Panama
Boy, have you got a bundle of problems. Let's start with the most pressing one—getting you off that log. You won't get anywhere by waving your pincers, I'm afraid. Here's the scoop. Harlequin-beetle-riding pseudoscorpions live on rotting logs—the fallen branches of fig trees, preferably. The only problem with this otherwise excellent arrangement is that sooner or later a given log will decay completely; when it does, anyone in residence will perish. So, how can you escape from the log before it has rotted to nothing? Enter the harlequin beetle.
Harlequin beetles are magnificent, their jet-black wing covers decorated with jagged red stripes. More germane than their looks, however, is where they make their homes—in rotting logs. The cycle begins when a female harlequin beetle lays her eggs in a freshly fallen fig tree. Her children develop in the wood; after several months, they emerge fully grown. This is your moment. Pseudoscorpions are tiny—far smaller than proper
scorpions (although the real distinction is that you have no sting). This means that you can stow away under a harlequin beetle's wing covers and fly off to a new home when the harlequin beetle flies to fresh logs to find mates and lay eggs.
But as you found out, space under the wings is limited. Even on a large beetle, no more than about thirty pseudoscorpions can clamber on board. Worse, a big male pseudoscorpion can easily defend this space from rivals. With bogus gallantry, he lets females on and keeps other males off. Then, when they take to the skies, he will have sex with as many of his companions as possible. Right now, just as you feared, your girlfriend is probably squatting over a packet of sperm that the “big thug” has deposited for her on the harlequin beetle's back. Sorry about that. And I'm afraid I have some other bad news. Harlequin beetles already out in the world are not attracted to old logs, so there will be no casual passersby. If you can't find and board another beetle as it emerges, you'll be marooned forever, a helpless member of a doomed population.
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
BOOK: Dr. Tatiana's Sex Advice to All Creation
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