The chessboard is the world; the pieces are the phenomena of the universe; the rules of the game are what we call the laws of Nature. The player on the other side is hidden from us. We know that his play is always fair, just, and patient. But also we know, to our cost, that he never overlooks a mistake or makes the smallest allowance for ignorance.
—Thomas Henry Huxley
Even for microscopic animals, the bdelloid rotifers are peculiar. They live in any kind of fresh water, from puddles in your gutter to hot springs by the Dead Sea and ephemeral ponds on the Antarctic continent. They look like animated commas driven by what appear to be small waterwheels at the front of the body, and when their watery home dries up or freezes, they adopt the shape of an apostrophe and go to sleep. This apostrophe is known as a “tun,” and it is astonishingly resistant to abuse. You can boil it for an hour or freeze it to within I degree of absolute zero—that is, to -272 degrees Centigrade—for a whole hour. Not only does it fail to disintegrate, it does not even die. Tuns blow about the globe as dust so easily that rotifers are thought to travel regularly between Africa and America. Once thawed out, the tun quickly turns back into a rotifer, paddles its way about the pond with its bow wheels, eating bacteria as it goes, and within a few hours starts producing eggs that hatch into other rotifers. A bdelloid rotifer can fill a medium-sized lake with its progeny in just two months.
But there is another odd thing about bdelloids besides their feats of endurance and fecundity. No male bdelloid rotifer has ever been seen. As far as biologists can tell, every single member of every one of all five hundred species of bdelloid in the world is a female. Sex is simply not in the bdelloid repertoire.
It is possible that bdelloid rotifers mix others’ genes with their own by eating their dead comrades and absorbing some of their genes, or something bizarre like that,1 but recent research by Matthew Meselson and David Welch suggests that they just never do have sex. They have found that the same gene in two different individuals can be up to 30 percent different at points that do not affect its function—a level of difference that implies bdelloids gave up sex between 40 million and 80 million years ago.2
There are many other species in the world that never have sex, from dandelions and lizards to bacteria and amoebas, but the bdelloids are the only example of a whole order of animal that entirely lacks the sexual habit. Perhaps as a result the bdelloids all look rather alike, whereas their relatives, the monogonont rotifers, tend to be much more varied; they cover the whole range of shapes of punctuation marks. Nonetheless, the bdelloids are a living rebuke to the conventional wisdom of biology textbooks—that without sex, evolution can barely happen and species cannot adapt to change. The existence of the bdelloid rotifers is, in the words of John Maynard Smith, “an evolutionary scandal.”3
THE ART OF BEING SLIGHTLY DIFFERENT
Unless a genetic mistake happens, a baby bdelloid rotifer is identical to its mother. A human baby is not identical to its mother. That is the first consequence of sex. Indeed, according to most ecologists, it is the purpose of sex.
In 1966, George Williams exposed the logical flaw at the heart of the textbook explanation of sex. He showed how it required animals to ignore short-term self-interest in order to further the survival and evolution of their species, a form of self-restraint that could have evolved only under very peculiar circumstances. He was very unsure what to put in its place. But he noticed that sex and dispersal often seem to be linked. Thus, grass grows asexual runners to propagate locally but commits its sexually produced seeds to the wind to travel farther. Sexual aphids grow wings; asexual ones do not. The suggestion that immediately follows is that if your young are going to have to travel abroad, then it is better that they vary because abroad may not be like home.4
Elaborating on that idea was the main activity throughout the 1970s of ecologists interested in sex. In 1971, in his first attack on the problem, John Maynard Smith suggested that sex was needed for those cases in which two different creatures migrate into a new habitat in which it helps to combine both their characters.5 Two years later Williams returned to the fray and suggested that if most of the young are going to die, as most who try their luck as travelers will, then it may be the very fittest ones that will survive. It therefore matters not one bit how many young of average quality a creature has. What counts is having a handful of young that are exceptional. If you want your son to become pope, the best way to achieve this is not to have lots of identical sons but to have lots of different sons in the hope that one is good, clever, and religious enough.6
The common analogy for what Williams was describing is a lottery. Breeding asexually is like having lots of lottery tickets all with the same number. To stand a chance of winning the lottery, you need lots of different tickets. Therefore, sex is useful to the individual rather than the species when the offspring are likely to face changed or unusual conditions.
Williams was especially intrigued by creatures such as aphids and monogonont rotifers, which have sex only once every few generations. Aphids multiply during the summer on a rosebush, and monogonont rotifers multiply in a street puddle. But when the summer comes to an end, the last generation of aphids or of monogonont rotifers is entirely sexual: It produces males and females that seek each other out, mate, and produce tough little young that spend the winter or the drought as hardened cysts awaiting the return of better conditions. To Williams this looked like the operation of his lottery. While conditions were favorable and predictable, it paid to reproduce as fast as possible—asexually. When the little world came to an end and the next generation of aphid or rotifer faced the uncertainty of finding a new home or waited for the old one to reappear, then it paid to produce a variety of different young in the hope that one would prove ideal.
Williams contrasted the “aphid-rotifer model” with two others: the strawberry-coral model and the elm-oyster model. Strawberry plants and the animals that build coral reefs sit in the same place all their lives, but they send out runners or coral branches so that the individual and its clones gradually spread over the surrounding space. However, when they want to send their young much farther away, in search of a new, pristine habitat, the strawberries produce sexual seeds and the corals produce sexual larvae called “planulae.” The seeds are carried away by birds; the planulae drift for many days on the ocean currents. To Williams, this looked like a spatial version of the lottery: Those who travel farthest are most likely to encounter different conditions, so it is best that they vary in the hope that one or two of them will suit the place they reach. Elm trees and oysters, which are sexual, produce millions of tiny young that drift on breezes or ocean currents until a few are lucky enough to land in a suitable place and begin a new life. Why do they do this? Because, said Williams, both elms and oysters have saturated their living space already. There are few clearings in an elm forest and few vacancies on an oyster bed. Each vacancy will attract many thousands of applicants in the form of new seeds or larvae. Therefore, it does not matter that your young are good enough to survive. What matters is whether they are the very best. Sex gives variety, so sex makes a few of your offspring exceptional and a few abysmal, whereas asex makes them all average.7
THE TANGLED BANK
Williams’s proposition has reappeared in many guises over the years, under many names and with many ingenious twists. In general, however, the mathematical models suggest that these lottery models only work if the prize that rewards the right lottery ticket is indeed a huge jackpot. Only if a very few of the dispersers survive and do spectacularly well does sex pay its way. In other cases, it does not.8
Because of this limitation, and because most species are not necessarily producing young that will migrate elsewhere, few ecologists wholeheartedly adopted lottery theories. But it was not until Graham Bell in Montreal asked, like the apocryphal king and the goldfish, to see the actual evidence for the pattern the lottery model was designed to explain that the whole edifice tumbled down. Bell set out to catalog species according to their ecology and their sexuality. He was trying to find the correlation between ecological uncertainty and sexuality that Williams and Maynard Smith had more or less assumed existed. So he expected to find that animals and plants were more likely to be sexual at higher latitudes and altitudes (where weather is more variable and conditions harsher); in fresh water rather than the sea (because fresh water varies all the time, flooding, drying up, heating up in summer, freezing in winter, and so on, whereas the sea is predictable); among weeds that live in disturbed habitats; and in small creatures rather than large ones. He found exactly the opposite. Asexual species tend to be small and live at high latitudes and high altitudes, in fresh water or disturbed ground. They live in unsaturated habitats where harsh, unpredictable conditions keep populations from reaching full capacity. Indeed, even the association between sex and hard times in aphids and rotifers turns out to be a myth. Aphids and monogonont rotifers both turn sexual not when winter or drought threaten but when overcrowding affects the food supply. You can make them turn sexual in the laboratory just by letting them get too crowded.
Bell’s verdict on the lottery model was scathing: “Accepted, at least as a conceptual foundation, by the best minds which have contemplated the function of sexuality, it seems utterly to fail the test of comparative analysis.”9
Lottery models predict that sex should be most common where in fact it is rarest—among highly fecund, small creatures in changeable environments. On the contrary, here sex is the exception; but in big, long-lived, slow-breeding creatures in stable environments sex is the rule.
This was a bit unfair toward Williams, whose “elm-oyster model” had at least predicted that fierce competition between saplings for space was the reason elms were sexual. Michael Ghiselin developed this idea further in 1974 and made some telling analogies with economic trends. As Ghiselin put it, “In a saturated economy, it pays to diversify.” Ghiselin suggested that most creatures compete with their brothers and sisters, so if everybody is a little different from their brothers and sisters, then more can survive. The fact that your parents thrived doing one thing means that it will probably pay to do something else because the local habitat might well be full already with your parents’ friends or relatives doing their thing.10
Graham Bell has called this the “tangled bank” theory, after the famous last paragraph of Charles Darwin’s Origin of Species: “It is interesting to contemplate an entangled bank, clothed with many plants of many kinds, with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other and dependent upon each other in so complex a manner, have all been produced by laws acting around us.”11
Bell used the analogy of a button maker who has no competitors and has already supplied buttons to most of the local market. What does he do? He could either continue selling replacements for buttons or he could diversify the range of his buttons and try to expand the market by encouraging his customers to buy all sorts of different kinds of buttons. Likewise, sexual organisms in saturated environments, rather than churning out more of the same offspring, would be better off varying them a bit in the hope of producing offspring that could avoid the competition by adapting to a new niche. Bell concluded from his exhaustive survey of sex and asex in the animal kingdom that the tangled bank was the most promising of the ecological theories for sex.12
The tangled bankers had some circumstantial evidence for their idea, which came from crops of wheat and barley. Mixtures of different varieties generally yield more than a single variety does; plants transplanted to different sites generally do worse than in their home patches, as if genetically suited to their home ground; if allowed to compete with one another in a new site, plants derived from cuttings or tillers generally do worse than plants derived from sexual seed, as if sex provides some sort of variable advantage.13
The trouble is, all these results are also predicted by rival theories just as plausibly. Williams wrote: “Fortune will be benevolent indeed if the inference from one theory contradicts that of another.”14 This is an especially acute problem in the debate. One scientist gives the analogy of somebody trying to decide what makes his driveway wet: rain, lawn sprinklers, or flooding from the local river. It is no good turning on the sprinkler and observing that it wets the drive or watching rain fall and seeing that it wets the drive.15 To conclude anything from such observations would be to fall into the trap that philosophers call “the fallacy of affirming the consequent.” Because sprinklers can wet the drive does not prove that they did wet the drive. Because the tangled bank is consistent with the facts does not prove it is the cause of the facts.
It is hard to find dedicated enthusiasts of tangled banks these days. Their main trouble is a familiar one: If it ain’t broke, why does sex need to fix it? An oyster that has grown large enough to breed is a great success, in oyster terms. Most of its siblings are dead. If, as tangled bankers assume, the genes had something to do with that, then why must we automatically assume that the combination of genes that won in this generation will be a flop in the next? There are ways around this difficulty for tangled bankers, but they sound a bit like special pleading. It is easy enough to identify an individual case where sex would have some advantage, but to raise it to a general principle for every habitat of every mammal and bird, for every coniferous tree, a principle that can give a big enough advantage to overcome the fact that asex is twice as fecund as sex—nobody can quite bring himself to do that.
There is a more empirical objection to the tangled bank theory. Tangled banks predict a greater interest in sex in those animals and plants that have many small offspring that then compete with one another than among the plants and animals that have few large young. Superficially, the effort devoted to sex has little to do with how small the offspring are. Blue whales, the biggest animals, have huge young—each may weigh five tons or more. Giant sequoias, the biggest plants, have tiny seeds, so small that the ratio of their weight to the weight of the tree is the same as the ratio of the tree to the planet Earth.16 Yet both are sexual creatures. By contrast, an amoeba, which splits in half when it breeds, has an enormous “young” as big as “itself.” Yet it never has sex.
A student of Graham Bell’s named Austin Burt went out and looked at the real world to see if the tangled bank fitted the facts. He looked not at whether mammals have sex but at how much recombination goes on among their genes. He measured this quite easily by counting the number of “crossovers” on a chromosome. These are spots where, quite literally, one chromosome swaps genes with another. What Burt found was that among mammals the amount of recombination bears no relation to the number of young, little relation to body size, and close relation to age at maturity. In other words, long-lived, late-maturing mammals do more genetic mixing regardless of their size or fecundity than short-lived, early maturing mammals. By Burt’s measure, man has thirty crossovers, rabbits ten, and mice three. Tangled-bank theories would predict the opposite.17
The tangled bank also conflicted with the evidence from fossils. In the 1970s evolutionary biologists realized that species do not change much. They stay exactly the same for thousands of generations, to be suddenly replaced by other forms of life. The tangled bank is a gradualist idea. If tangled banks were true, then species would gradually drift through the adaptive landscape, changing a little in every generation, instead of remaining true to type for millions of generations. A gradual drifting away of a species from its previous form happens on small islands or in tiny populations precisely because of effects somewhat analogous to Muller’s ratchet: the chance extinction of some forms and the chance prosperity of other, mutated forms. In larger populations the process that hinders this is sex itself, for an innovation is donated to the rest of the species and quickly lost in the crowd. In island populations sex cannot do this precisely because the population is so inbred.18
It was Williams who first pointed out that a huge false assumption lay, and indeed still lies, at the core of most popular treatments of evolution. The old concept of the ladder of progress still lingers on in the form of a teleology: Evolution is good for species, and so they strive to make it go faster. Yet it is stasis, not change, that is the hallmark of evolution. Sex and gene repair and the sophisticated screening mechanisms of higher animals to ensure that only defect-free eggs and sperm contribute to the next generation—all these are ways of preventing change. The coelacanth, not the human, is the triumph of genetic systems because it has remained faithfully true to type for millions of generations despite endless assaults on the chemicals that carry its heredity. The old “Vicar of Bray” model of sex, in which sex is an aid to faster evolution, implies that organisms would prefer to keep their mutation rate fairly high—since mutation is the source of all variety—and then do a good job of sieving out the bad ones. But, as Williams put it, there is no evidence yet found that any creature ever does anything other than try to keep its mutation rate as low as possible. It strives for a mutation rate of zero. Evolution depends on the fact that it fails.19
Tangled banks work mathematically only if there is a sufficient advantage in being odd. The gamble is that what paid off in one generation will not pay off in the next and that the longer the generation, the more this is so—which implies that conditions keep changing.
THE RED QUEEN
Enter, running, the Red Queen. This peculiar monarch became part of biological theory twenty years ago and has been growing ever more important in the years since then. Follow me if you will into a dark labyrinth of stacked shelves in an office at the University of Chicago, past ziggurats of balanced books and three-foot Babels of paper. Squeeze between two filing cabinets and emerge into a Stygian space the size of a broom cupboard, where sits an oldish man in a checked shirt and with a gray beard that is longer than God’s but not so long as Charles Darwin’s. This is the Red Queen’s first prophet, Leigh Van Valen, a single-minded student of evolution. One day in 1973, before his beard was so gray, Van Valen was searching his capacious mind for a phrase to express a new discovery he had made while studying marine fossils. The discovery was that the probability a family of animals would become extinct does not depend on how long that family has already existed. In other words, species do not get better at surviving (nor do they grow feeble with age, as individuals do). Their chances of extinction are random.
The significance of this discovery had not escaped Van Valen, for it represented a vital truth about evolution that Darwin had not wholly appreciated. The struggle for existence never gets easier. However well a species may adapt to its environment, it can never relax, because its competitors and its enemies are also adapting to their niches. Survival is a zero-sum game. Success only makes one species a more tempting target for a rival species. Van Valen’s mind went back to his childhood and lit upon the living chess pieces that Alice encountered beyond the looking glass. The Red Queen is a formidable woman who runs like the wind but never seems to get anywhere:
“Well, in our country,” said Alice, still panting a little, “you’d generally get to somewhere else—if you ran very fast for a long time as we’ve been doing.”
“A slow sort of country!” said the Queen. “Now, here, you see, it takes all the running you can do to keep in the same place. If you want to get to somewhere else, you must run at least twice as fast as that!”20
“A new evolutionary law,” wrote Van Valen, who sent a manuscript to each of the most prestigious scientific journals, only to see it rejected. Yet his claim was justified. The Red Queen has become a great personage in the biological court. And nowhere has she won a greater reputation than in theories of sex.21
Red Queen theories hold that the world is competitive to the death. It does keep changing. But did we not just hear that species are static for many generations and do not change? Yes. The point about the Red Queen is that she runs but stays in the same place. The world keeps coming back to where it started; there is change but not progress.
Sex, according to the Red Queen theory, has nothing to do with adapting to the inanimate world—becoming bigger or better camouflaged or more tolerant of cold or better at flying—but is all about combating the enemy that fights back.
Biologists have persistently overestimated the importance of physical causes of premature death rather than biological ones. In virtually any account of evolution, drought, frost, wind, or starvation looms large as the enemy of life. The great struggle, we are told, is to adapt to these conditions. Marvels of physical adaptation—the camel’s hump, the polar bear’s fur, the rotifer’s boil-resistant tun—are held to be among evolution’s greatest achievements. The first ecological theories of sex were all directed at explaining this adaptability to the physical environment. But with the tangled bank, a different theme has begun to be heard, and in the Red Queen’s march it is the dominant tune. The things that kill animals or prevent them from reproducing are only rarely physical factors. Far more often other creatures are involved—parasites, predators, and competitors. A water flea that is starving in a crowded pond is the victim not of food shortage but of competition. Predators and parasites probably cause most of the world’s deaths, directly or indirectly. When a tree falls in the forest, it has usually been weakened by a fungus. When a herring meets its end, it is usually in the mouth of a bigger fish or a in a net. What killed your ancestors two centuries or more ago? Smallpox, tuberculosis, influenza, pneumonia, plague, scarlet fever, diarrhea. Starvation or accidents may have weakened people, but infection killed them. A few of the wealthier ones died of old age or cancer or heart attacks, but not many.22
The “great war” of 1914-18 killed 25 million people in four years. The influenza epidemic that followed killed 25 million in four months.23 It was merely the latest in a series of devastating plagues to hit the human species after the dawn of civilization. Europe was laid waste by measles after A.D. 165, by smallpox after A.D. 251, by bubonic plague after 1348, by syphilis after 1492, and by tuberculosis after 1800.24 And those are just the epidemics. Endemic diseases carried away additional vast numbers of people. Just as every plant is perpetually under attack from insects, so every animal is a seething mass of hungry bacteria waiting for an opening. There may be more bacterial than human cells in the object you proudly call “your” body. There may be more bacteria in and on you as you read this than there are human beings in the whole world.
Again and again in recent years evolutionary biologists have found themselves returning to the theme of parasites. As Richard Dawkins put it in a recent paper: “Eavesdrop [over] morning coffee at any major centre of evolutionary theory today, and you will find ‘parasite’ to be one of the commonest words in the language. Parasites are touted as the prime movers in the evolution of sex, promising a final solution to that problem of problems.”25
Parasites have a deadlier effect than predators for two reasons. One is that there are more of them. Human beings have no predators except great white sharks and one another, but they have lots of parasites. Even rabbits, which are eaten by stoats, weasels, foxes, buzzards, dogs, and people, are host to far more fleas, lice, ticks, mosquitoes, tapeworms, and uncounted varieties of protozoa, bacteria, fungi, and viruses. The myxomatosis virus has killed far more rabbits than have foxes. The second reason, which is the cause of the first, is that parasites are usually smaller than their hosts, while predators are usually larger. This means that the parasites live shorter lives and pass through more generations in a given time than their hosts. The bacteria in your gut pass through six times as many generations during your lifetime as people have passed through since they were apes.26 As a consequence, they can multiply faster than their hosts and control or reduce the host population. The predator merely follows the abundance of its prey.
Parasites and their hosts are locked in a close evolutionary embrace. The more successful the parasite’s attack (the more hosts it infects or the more resources it gets from each), the more the host’s chances of survival will depend on whether it can invent a defense. The better the host defends, the more natural selection will promote the parasites that can overcome the defense. So the advantage will always be swinging from one to the other: The more dire the emergency for one, the better it will fight. This is truly the world of the Red Queen, where you never win, you only gain a temporary respite.
BATTLES OF WIT
It is also the inconstant world of sex. Parasites provide exactly the incentive to change genes every generation that sex seems to demand. The success of the genes that defended you so well in the last generation may be the best of reasons to abandon these same gene combinations in the next. By the time the next generation comes around, the parasites will have surely evolved an answer to the defense that worked best in the last generation. It is a bit like sport. In chess or in football, the tactic that proves most effective is soon the one that people learn to block easily. Every innovation in attack is soon countered by another in defense.
But of course the usual analogy is an arms race. America builds an atom bomb, so Russia does, too. America builds missiles; so must Russia. Tank after tank, helicopter after helicopter, bomber after bomber, submarine after submarine, the two countries run against each other, yet stay in the same place. Weapons that would have been invincible twenty years before are now vulnerable and obsolete. The bigger the lead of one superpower, the harder the other tries to catch up. Neither dares step off the treadmill while it can afford to stay in the race. Only when the economy of Russia collapses does the arms race cease (or pause).27
These arms race analogies should not be taken too seriously, but they do lead to some interesting insights. Richard Dawkins and John Krebs raised one argument derived from arms races to the level of a “principle”: the “life-dinner principle.” A rabbit running from a fox is running for its life, so it has the greater evolutionary incentive to be fast. The fox is merely after its dinner. True enough, but what about a gazelle running from a cheetah? Whereas foxes eat things other than rabbits, cheetahs eat only gazelles. A slow gazelle might never be unlucky enough to meet a cheetah, but a slow cheetah that never catches anything dies. So the downside is greater for the cheetah. As Dawkins and Krebs put it, the specialist will usually win the race.28
Parasites are supreme specialists, but arms race analogies are less reliable for them. The flea that lives in the cheetah’s ear has what economists call an “identity of interest” with the cheetah: If the cheetah dies, the flea dies. Gary Larson once drew a cartoon of a flea walking through the hairs on a dog’s back carrying a placard that read: THE END OF THE DOG IS NEAR. The death of the dog is bad news for the flea, even if the flea hastened it. The question of whether parasites benefit from harming their hosts has vexed parasitologists for many years. When a parasite first encounters a new host (myxomatosis in European rabbits, AIDS in human beings, plague in fourteenth-century Europeans) it usually starts off as extremely virulent and gradually becomes less so. But some diseases remain fatal, while others quickly become almost harmless. The explanation is simple: The more contagious the disease, and the fewer resistant hosts there are around, the easier it will be to find a new host. So contagious diseases in unresistant populations need not worry about killing their hosts, because they have already moved on. But when most potential hosts are already infected or resistant, and the parasite has difficulty moving from host to host, it must take care not to kill its own livelihood. In the same way an industrial boss who pleads with his workers, “Please don’t strike or the company will go bust,” is likely to be more persuasive if unemployment is high than if the workers already have other job offers. Yet, even where virulence declines, the host is still being hurt by the parasite and is still under pressure to improve its defenses, while the parasite is continually trying to get around those defenses and sequester more resources to itself at the host’s expense.29
ARTIFICIAL VIRUSES
Startling proof of the fact that parasites and hosts are locked in evolutionary arms races has come from a surprising source: the innards of computers. In the late 1980s evolutionary biologists began to notice a new discipline growing among their more computer-adept colleagues called artificial life. Artificial life is a hubristic name for computer programs that are designed to evolve through the same process of replication, competition, and selection as real life. They are, in a sense, the ultimate proof that life is just a matter of information and that complexity can result from directionless competition, design from randomness.
If life is information and life is riddled with parasites, then information, too, should be vulnerable to parasites. When the history of computers comes to be written, it is possible that the first program to earn the appellation “artificially alive” will be a deceptively simple little two-hundred-line program written in 1983 by Fred Cohen, a graduate student at the California Institute of Technology. The program was a “virus” that would insinuate copies of itself into other programs in the same way a real virus insinuates copies of itself into other hosts. Computer viruses have since become a worldwide problem. It begins to look as if parasites are inevitable in any system of life.30
But Cohen’s virus and its pesky successors were created by people. It was not until Thomas Ray, a biologist at the University of Delaware, conceived an interest in artificial life that computer parasites first appeared spontaneously. Ray designed a system called Tierra that consisted of competing programs that were constantly being filled by mutation with small errors. Successful programs would thrive at one another’s expense.
The effect was astonishing. Within Tierra, programs began to evolve into shorter versions of themselves. Programs that were seventy-nine instructions long began to replace the original eighty-instruction programs. But then suddenly there appeared versions of the program just forty-five instructions long: They borrowed half of the code they needed from longer programs. These were true parasites. Soon a few of the longer programs evolved what Ray called immunity to parasites. One program became impregnable to the attentions of one parasite by concealing part of itself. But the parasites were not beaten. A mutant parasite appeared in the soup that could find the concealed lines.31
And so the arms race escalated. Sometimes when he ran the computer, Ray was confronted with spontaneously appearing hyperparasites, social hyperparasites, and cheating hyper-hyperparasites—all within an evolving system of (initially) ridiculous simplicity. He had discovered that the notion of a host-parasite arms race is one of the most basic and unavoidable consequences of evolution.32
Arms race analogies are flawed, though. In a real arms race, an old weapon rarely regains its advantage. The day of the longbow will not come again. In the contest between a parasite and its host, it is the old weapons, against which the antagonist has forgotten how to defend, that may well be the most effective. So the Red Queen may not stay in the same place so much as end up where she started from, like Sisyphus, the fellow condemned to spend eternity rolling a stone up a hill in Hades only to see it roll down again.
There are three ways for animals to defend their bodies against parasites. One is to grow and divide fast enough to leave them behind. This is well known to plant breeders, for example: The tip of the growing shoot into which the plant is putting all its resources is generally free of parasites. Indeed, one ingenious theory holds that sperm are small specifically so they have no room to carry bacteria with them to infect eggs.33 A human embryo indulges in a frenzy of cell division soon after it is fertilized, perhaps to leave behind any viruses and bacteria stuck in one of the compartments. The second defense is sex, of which more anon. The third is an immune system, used only by the descendants of reptiles. Plants and many insects and amphibians have an additional method: chemical defense. They produce chemicals that are toxic to their pests. Some species of pests then evolve ways of breaking down the toxins, and so on. An arms race has begun.
Antibiotics are chemicals produced naturally by fungi to kill their rivals: bacteria. But when man began to use antibiotics, he found that, with disappointing speed, the bacteria were evolving the ability to resist the antibiotics. There were two startling things about antibiotic resistance in pathogenic bacteria. One, the genes for resistance seemed to jump from one species to another, from harmless gut bacteria to pathogens, by a form of gene transfer not unlike sex. And two, many of the bugs seemed to have the resistance genes already on their chromosomes; it was just a matter of reinventing the trick of switching them on. The arms race between bacteria and fungi has left many bacteria with the ability to fight antibiotics, an ability they no longer “thought they would need” when inside a human gut.
Because they are so short-lived compared with their hosts, parasites can be quicker to evolve and adapt. In about ten years, the genes of the AIDS virus change as much as human genes change in 10 million years. For bacteria, thirty minutes can be a lifetime. Human beings, whose generations are an eternal thirty years long, are evolutionary tortoises.
PICKING DNA’S LOCKS
Evolutionary tortoises nonetheless do more genetic mixing than evolutionary hares. Austin Burt’s discovery of a correlation between generation length and amount of recombination is evidence of the Red Queen at work. The longer your generation time, the more genetic mixing you need to combat your parasites.34 Bell and Burt also discovered that the mere presence of a rogue parasitic chromosome called a “B-chromosome” is enough to induce extra recombination (more genetic mixing) in a species.35 Sex seems to be an essential part of combating parasites. But how?
Leaving aside for the moment such things as fleas and mosquitoes, let us concentrate on viruses, bacteria, and fungi, the causes of most diseases. They specialize in breaking into cells—either to eat them, as fungi and bacteria do, or, like viruses, to subvert their genetic machinery for the purpose of making new viruses. Either way, they must get into cells. To do that they employ protein molecules that fit into other molecules on cell surfaces; in the jargon, they “bind.” The arms races between parasites and their hosts are all about these binding proteins. Parasites invent new keys; hosts change the locks. There is an obvious group-selectionist argument here for sex: At any one time a sexual species will have lots of different locks; members of an asexual one will all have the same locks. So a parasite with the right key will quickly exterminate the asexual species but not the sexual one. Hence, the well-known fact: By turning our fields over to monocultures of increasingly inbred strains of wheat and maize, we are inviting the very epidemics of disease that can only be fought by the pesticides we are forced to use in ever larger quantities.36
The Red Queen’s case is both subtler and stronger than that, though. It is that an individual, by having sex, can produce offspring more likely to survive than an individual that produces clones of itself. The advantage of sex can appear in a single generation. This is because whatever lock is common in one generation will produce among the parasites the key that fits it. So you can be sure that it is the very lock not to have a few generations later, for by then the key that fits it will be common. Rarity is at a premium.
Sexual species can call on a sort of library of locks that is unavailable to asexual species. This library is known by two long words that mean roughly the same thing: heterozygosity and polymorphism. They are the things that animals lose when their lineage becomes inbred. What they mean is that in the population at large (polymorphism) and in each individual as well (heterozygosity) there are different versions of the same gene at any one time. The “polymorphic” blue and brown eyes of Westerners are a good example: Many brown-eyed people carry the recessive gene for blue eyes as well; they are heterozygous. Such polymorphisms are almost as puzzling as sex to true Darwinists because they imply that one gene is as good as the other. Surely, if brown eyes were marginally better than blue (or, more to the point, if normal genes were better than sickle-cell-anemia genes), then one would gradually have driven the other extinct. So why on earth are we stuffed full of so many different versions of genes? Why is there so much heterozygosity? In the case of sickle-cell anemia it is because the sickle gene helps to defeat malaria, so the heterozygotes (those with one normal gene and one sickle gene) are better off than those with normal genes where malaria is common, whereas the homozygotes (those with two normal genes or two sickle genes) suffer from malaria and anemia respectively.37
This example is so well worn from overuse in biology textbooks that it is hard to realize it is not just another anecdote but an example of a common theme. It transpires that many of the most notoriously polymorphic genes, such as the blood groups, the histocompatibility antigens and the like, are the very genes that affect resistance to disease—the genes for locks. Moreover, some of these polymorphisms are astonishingly ancient; they have persisted for geological eons. For example, there are genes that have several versions in mankind, and the equivalent genes in cows also have several versions. But what is bizarre is that the cows have the very same versions of the genes as mankind. This means that you might have a gene that is more like the gene of a certain cow than it is like the equivalent gene in your spouse. This is considerably more astonishing than it would be to discover that the word for, say, “meat” was viande in France, fleisch in Germany, viande again in one uncontacted Stone Age village in New Guinea, and fleisch in a neighboring village. Some very powerful force is at work ensuring that most versions of each gene survive and that no version changes very much.38
That force is almost certainly disease. As soon as a lock gene becomes rare, the parasite key gene that fits it becomes rare, so that lock gains an advantage. In a case where rarity is at a premium, the advantage is always swinging from one gene to another, and no gene is ever allowed to become extinct. To be sure, there are other mechanisms that can favor polymorphism: anything that gives rare genes a selective advantage over common genes. Predators often give rare genes a selective advantage by overlooking rare forms and picking out common forms. Give a bird in a cage some concealed pieces of food, most of which are painted red but a few painted green; it will quickly get the idea that red things are edible and will initially overlook green things. J. B. S Haldane was the first to realize that parasitism, even more than predation, could help to maintain polymorphism, especially if the parasite’s increased success in attacking a new variety of host goes with reduced success against an old variety—which would be the case with keys and locks.39
The key and lock metaphor deserves closer scrutiny. In flax, for example, there are twenty-seven versions of five different genes that confer resistance to a rust fungus: twenty-seven versions of five locks. Each lock is fitted by several versions of one key gene in the rust. The virulence of the rust fungus attack is determined by how well its five keys fit the flax’s five locks. It is not quite like real keys and locks because there are partial fits: The rust does not have to open every lock before it can infect the flax. But the more locks it opens, the more virulent its effects.40
THE SIMILARITY BETWEEN SEX AND VACCINATION
At this point the alert know-it-alls among you will be seething with impatience at my neglect of the immune system. The normal way to fight a disease, you may point out, is not to have sex but to produce antibodies, by vaccination or whatever. The immune system is a fairly recent invention in geological terms. It started in the reptiles perhaps 300 million years ago. Frogs, fish, insects, lobsters, snails, and water fleas do not have immune systems. Even so, there is now an ingenious theory that marries the immune system with sex in an overarching Red Queen hypothesis. Hans Bremermann of the University of California at Berkeley is its author, and he makes a fascinating case for the interdependence of the two. The immune system, he points out, would not work without sex.41
The immune system consists of white blood cells that come in about 10 million different types. Each type has a protein lock on it called an “antibody,” which corresponds to a key carried by a bacterium called an “antigen.” If a key enters that lock, the white cell starts multiplying ferociously in order to produce an army of white cells to gobble up the key-carrying invader, be it a flu virus, a tuberculosis bacterium, or even the cells of a transplanted heart. But the body has a problem. It cannot keep armies of each antibody-lock ready to immobilize all types of keys because there is simply no room for millions of different types, each represented by millions of individual cells. So it keeps only a few copies of each white cell. As soon as one type of white cell meets the antigen that fits its locks, it begins multiplying. Hence the delay between the onset of flu and the immune response that cures it.
Each lock is generated by a sort of random assembly device that tries to maintain as broad a library of kinds of lock as it can, even if some of the keys that fit them have not yet been found in parasites. This is because the parasites are continually changing their keys to try to find ones that fit the host’s changing locks. The immune system is therefore prepared. But this randomness means that the host is bound to produce white cells that are designed to attack its own cells among the many types it invents. To get around this, the host’s own cells are equipped with a password, which is known as a major histocompatibility antigen. This stops the attack. (Please excuse the mixed metaphor—keys and locks and passwords; it does not get any more mixed.)
To win, then, the parasite must do one of the following: infect somebody else by the time the immune response hits (as flu does), conceal itself inside host cells (as the AIDS virus does), change its own keys frequently (as malaria does), or try to imitate whatever password the host’s own cells carry that enable them to escape attention. Bilharzia parasites, for example, grab password molecules from host cells and stick them all over their bodies to camouflage themselves from passing white cells. Trypanosomes, which cause sleeping sickness, keep changing their keys by switching on one gene after another. The AIDS virus is craftiest of all. According to one theory, it seems to keep mutating so that each generation has different keys. Time after time the host has locks that fit the keys and the virus gets suppressed. But eventually, after perhaps ten years, the virus’s random mutation hits upon a key that the host does not have a lock for. At that point the virus has won. It has found the gap in the repertoire of the immune system’s locks and runs riot. In essence, according to this theory, the AIDS virus evolves until it finds a chink in the body’s immune armor.42
Other parasites try to mimic the passwords carried by the host. The selective pressure is on all pathogens to mimic the passwords of their hosts. The selective pressure is on all hosts to keep changing the password. This, according to Bremermann, is where sex comes in.
The histocompatibility genes, which determine more than the passwords but are themselves responsible for susceptibility to disease, are richly polymorphic. There are over one hundred versions of each histocompatibility gene in the average population of mice, and even more in human beings. Every person carries a unique combination, which is why transplants between people other than identical twins are rejected unless special drugs are taken. And without sexual outbreeding, it is impossible to maintain that polymorphism.
Is this conjecture or is there proof? In 1991, Adrian Hill and his colleagues at Oxford University produced the first good evidence that the variability of histocompatibility genes is driven by disease. They found that one kind of histocompatibility gene, HLA-Bw53, is frequent where malaria is common and very rare elsewhere. Moreover, children ill with malaria generally do not have HLA-Bw53. That may be why they are ill.43 And in an extraordinary discovery made by Wayne Potts of the University of Florida at Gainesville, house mice appear to choose as mates only those house mice that have different histocompatibility genes from their own. They do this by smell. This preference maximizes the variety of genes in mice and makes the young mice more disease-resistant.44
WILLIAM HAMILTON AND PARASITE POWER
That sex, polymorphism, and parasites have something to do with one another is an idea with many fathers. With characteristic prescience, J. B. S. Haldane got most of the way there: “I wish to suggest that [heterozygosity] may play a part in disease resistance, a particular race of bacteria or virus being adapted to individuals of a certain range of biochemical constitutions, while the other constitutions are relatively resistant.” Haldane wrote that in 1949, four years before the structure of DNA was elucidated.45 An Indian colleague of Haldane’s, Suresh Jayakar, got even closer a few years latter.46 Then the idea lay dormant for many years, until the late 1970s when five people came up with the same notion independently of one another within the space of a few years, John Jaenike of Rochester, Graham Bell of Montreal, Hans Bremermann of Berkeley, John Tooby of Harvard, and Bill Hamilton of Oxford.47
But it was Hamilton who pursued the connection between sex and disease most doggedly and became most associated with it. In appearance, Hamilton was an almost implausibly perfect example of the absentminded professor as he stalked through the streets of Oxford, deep in thought, his spectacles attached umbilically to a string around his neck, his eyes fixed on the ground in front of him. His unassuming manner and relaxed style of writing and storytelling were deceptive. Hamilton had a habit of being at the right place in biology at the right time. In the 1960s he molded the theory of kin selection—the idea that much of animal cooperation and altruism is explained by the success of genes that cause animals to look after close relatives because they share many of the same genes. Then in 1967 he stumbled on the bizarre internecine warfare of the genes that we shall meet in chapter 4. By the 1980s he was anticipating most of his colleagues in pronouncing reciprocity as the key to human cooperation. Again and again in this book we will find we are treading in Hamilton’s footsteps.48
With the help of two colleagues from the University of Michigan, Hamilton built a computer model of sex and disease, a slice of artificial life. It began with an imaginary population of two hundred creatures. They happened to be rather like humans—each began breeding at fourteen, continued until thirty-five or so, and had one offspring every year. But the computer then made some of them sexual—meaning two parents had to produce and rear each child—and some of them asexual. Death was random. As expected, the sexual race quickly became extinct every time they ran the computer. In a game between sex and asex, asex always won, other things being equal.49
Next, they introduced several species of parasites, two hundred of each, whose power depended on “virulence genes” matched by “resistance genes” in the hosts. The least resistant hosts and the least virulent parasites were killed in each generation. Now the asexual race no longer had an automatic advantage. Sex often won the game, mostly if there were lots of genes that determined resistance and virulence in each creature.
What kept happening in the model, as expected, was that resistance genes that worked got more common, then virulence genes that undid those resistance genes got more common in turn, so those resistance genes grew rare again, followed by the virulence genes. As Hamilton put it, “Antiparasite adaptations are in constant obsolescence.” But instead of the unfavored genes being driven to extinction, as happened to the asexual species, once rare, they stopped getting rarer; they could therefore be brought back. “The essence of sex in our theory,” wrote Hamilton, “is that it stores genes that are currently bad but have promise for reuse. It continually tries them in combination, waiting for the time when the focus of disadvantage has moved elsewhere.” There is no permanent ideal of disease resistance, merely the shifting sands of impermanent obsolescence.50
When it runs the simulations, Hamilton’s computer screen fills with a red transparent cube inside which two lines, one green and one blue, chase each other like fireworks on a slow-exposure photograph. What is happening is that the parasite is pursuing the host through genetic “space,” or, to put it more precisely, each axis of the cube represents different versions of the same gene, and the host and the parasite keep changing their gene combinations. About half the time the host eventually ends up in one corner of the cube, having run out of variety in its genes, and stays there. Mutation mistakes are especially good at preventing it from doing that, but even without them it will do so spontaneously. What happens is entirely unpredictable even though the starting conditions are ruthlessly “deterministic”—there is no element of chance. Sometimes the two lines pursue each other on exactly the same steady course around the edge of the cube, gradually changing one gene for fifty generations, then another, and so on. Sometimes strange waves and cycles appear. Sometimes there is pure chaos: The two lines just fill the cube with colored spaghetti. It is strangely alive.51
Of course the model is hardly the real world; it no more clinches the argument than building a model of a battleship proves that a real battleship will float. But it helps identify the conditions under which the Red Queen is running forever: A hugely simplified version of a human being and a grotesquely simplified version of a parasite will continually change their genes in cyclical and random ways, never settling, always running, but never going anywhere, eventually coming back to where they started—as long as they both have sex.52
SEX AT ALTITUDE
Hamilton’s disease theory makes many of the same predictions as Alexey Kondrashov’s mutation theory, which we met in the last chapter. To return to the analogy of the lawn sprinkler and the rainstorm, both can explain how the driveway got wet. But which is correct? In recent years ecological evidence has begun to tip the scales Hamilton’s way. In certain habitats, mutation is common and diseases rare—mountaintops, for example, where there is much more ultraviolet light of the type that damages genes and causes mutations. So if Kondrashov is right, sex should be more common on mountaintops. It is not. Alpine flowers are often among the most asexual of flowers. In some groups of flowers, the ones that live near the tops of mountains are asexual, while those that live lower down are sexual. In five species of Townsendia, the alpine daisy, the asexuals are all found at higher altitudes than the sexuals. In Townsendia condensata, which lives only at very high altitudes, only one sexual population has ever been found, and that was the one nearest sea level.53
There are all sorts of explanations of this that have little to do with parasites, of course: The higher you go, the colder it gets, and the less you can rely on insects to pollinate a sexual flower. But if Kondrashov were right, such factors should be overwhelmed by the need to fight mutation. And the altitude effect is mirrored by a latitude effect. In the words of one textbook: “There are ticks and lice, bugs and flies, moths, beetles, grasshoppers, millipedes, and more, in all of which males disappear as one moves from the tropics toward the poles.”54
Another trend that fits the parasite theory is that most asexual plants are short-lived annuals. Long-lived trees face a particular problem because their parasites have time to adapt to their genetic defenses—to evolve. For example, among Douglas firs infested by scale insects (which are amorphous blobs of insectness that barely even look like animals), the older trees are more heavily infested than the younger ones. By transplanting scale insects from one tree to another, two scientists were able to show that this is an effect of better-adapted insects, not weaker old trees. Such trees would do their offspring no favors by having identical young, on whom the well-adapted insects would immediately descend. Instead, the trees are sexual and have different young.55
Disease might almost put a sort of limit on longevity: There is little point in living much longer than it takes your parasites to adapt to you. How yew trees, bristlecone pines, and giant sequoias get away with living for thousands of years is not clear, but what is clear is that, by virtue of chemicals in their bark and wood, they are remarkably resistant to decay. In the Sierra Nevada mountains of California lie the trunks of fallen sequoias, partly covered by the roots of huge pine trees that are hundreds of years old, yet the wood of the sequoia stumps is hard and true.56
In the same vein it is tempting to speculate that the peculiar synchronized flowering of bamboo might have something to do with sex and disease. Some bamboos flower only once every 121 years, and they do so at exactly the same moment all over the world, then die. This gives their young all sorts of advantages: They do not have living parents to compete with, and the parasites are wiped out when the bamboo parent plants die. (Their predators have problems, too; flowering causes a crisis for pandas.)57
Moreover, it is a curious fact that parasites themselves are often sexual, despite the enormous inconvenience this causes. A bilharzia worm inside a human vein cannot travel abroad to seek a mate, but if it encounters a genetically different worm, infected on a separate occasion, they have sex. To compete with their sexual hosts, parasites, too, need sex.
SEXLESS SNAILS
But these are all hints from natural history, not careful scientific experiments. There is also a small amount of more direct evidence in favor of the parasite theory of sex. By far the most thorough study of the Red Queen was done in New Zealand by a soft-spoken American biologist named Curtis Lively who became intrigued by the evolution of sex when told to write an essay on the subject as a student. He soon abandoned his other research, determined to solve the problem of sex. He went to New Zealand and examined water snails from streams and lakes and found that in many populations there are no males and the females give birth as virgins, but in other populations the females mate with males and produce sexual offspring. So he was able to sample the snails, count the males, and get a rough measure of the predominance of sex. His prediction was that if the Vicar of Bray was right and snails needed sex to adjust to changes, he would find more males in streams than in lakes because streams are changeable habitats; if the tangled bank was right and competition between snails was the cause of sex, he would find more males in lakes than in streams because lakes are stable, crowded habitats; if the Red Queen was right, he would find more males where there were more parasites.58
There were more males in lakes. About 12 percent of snails in the average lake are male, compared to 2 percent in the average stream. So the Vicar of Bray is ruled out. But there are also more parasites in lakes, so the Red Queen is not ruled out. Indeed, the closer he looked, the more promising the Red Queen seemed to be. There were no highly sexual populations without parasites.59
But Lively could not rule out the tangled bank, so he returned to New Zealand and repeated his survey, this time intent on finding out whether the snails and their parasites were genetically adapted to each other. He took parasites from one lake and tried to infect snails from another lake on the other side of the Southern Alps. In every case the parasites were better at infecting snails from their own lake. At first this sounds like bad news for the Red Queen, but Lively realized it was not. It is a very host centered view to expect greater resistance in the home lake. The parasite is constantly trying to outwit the snail’s defenses, so it is likely to be only one molecular step behind the snail in changing its keys to suit the snail’s locks. Snails from another lake have altogether different locks. But since the parasite in question, a little creature called Microphallus, actually castrates the snail, it grants enormous relative success to the snails with new locks. Lively is now doing the crucial experiment in the laboratory—to see whether the presence of parasites actually prevents an asexual snail from displacing a sexual one.60
The case of the New Zealand snails has done much to satisfy critics of the Red Queen, but they have been even more impressed by another of Lively’s studies—of a little fish in Mexico called the topminnow. The topminnow sometimes hybridizes with a similar fish to produce a triploid hybrid (that is, a fish that stores its genes in triplicate, like a bureaucrat). The hybrid fish are incapable of sexual reproduction, but each female will as a virgin produce clones of herself as long as she receives sperm from a normal fish. Lively and Robert Vrijenhoek of Rutgers University in New Jersey caught topminnows in each of three different pools and counted the number of cysts caused by black spot disease, a form of worm infection. The bigger the fish, the more black spots. But in the first pool, Log pool, the hybrids had far more spots than the sexual topminnows, especially when large. In the second pool, Sandal pool, where two different asexual clones coexisted, those from the more common clone were the more parasitized; the rarer clones and the sexual topminnows were largely immune. This was what Lively had predicted, reasoning that the worms would adjust their keys to the most common locks in the pond, which would be those of the most common clone. Why? Because a worm would always have a greater chance of encountering the most common lock than any other lock. The rare clone would be safe, as would the sexual topminnows, each of which had a different lock.
But even more intriguing was the third pool, Heart pool. This pool had dried up in a drought in 1976 and had been recolonized two years later by just a few topminnows. By 1983 all the topminnows there were highly inbred, and the sexual ones were more susceptible to black spots than the clones in the same pool. Soon more than 95 percent of the topminnows in Heart pool were asexual clones. This, too, fits the Red Queen theory, for sex is no good if there is no genetic variety: It’s no good changing the locks if there is only one type of lock available. Lively and Vrijenhoek introduced some more sexual female topminnows into the pool as a source of new kinds of lock. Within two years the sexual topminnows had become virtually immune to black spot, which had now switched to attacking the hybrid clones. More than 80 percent of the topminnows in the pool were sexual again. So all it took for sex to overcome its twofold disadvantage was a little bit of genetic variety.61
The topminnow study beautifully illustrates the way in which sex enables hosts to impale their parasites on the horns of a dilemma. As John Tooby has pointed out, parasites simply cannot keep their options open. They must always “choose.” In competition with one another they must be continually chasing the most common kind of host and so poisoning their own well by encouraging the less common type of host. The better their keys fit the locks of the host, the quicker the host is induced to change its locks.62
Sex keeps the parasite guessing. In Chile, where introduced European bramble plants became a pest, rust fungus was introduced to control them. It worked against an asexual species of bramble and failed against a sexual species. And when mixtures of different varieties of barley or wheat do better than pure stands of one variety (as they do), roughly two-thirds of the advantage can be accounted for by the fact that mildew spreads less easily through the mixture than through a pure stand.63
THE SEARCH FOR INSTABILITY
The history of the Red Queen explanation of sex is an excellent example of how science works by synthesizing different approaches to a problem. Hamilton and others did not pluck the idea of parasites and sex from thin air. They are the beneficiaries of three separate lines of research that have only now converged. The first was the discovery that parasites can control populations and cause them to go in cycles. This was hinted at by Alfred Lotka and Vito Volterra in the 1920s and fleshed out by Robert May and Roy Anderson in London in the 1970s. The second was the discovery by J. B. S. Haldane and others in the 1940s of abundant polymorphism, the curious phenomenon that for almost every gene there seemed to be several different versions, and something was keeping one from driving out all the others. The third was the discovery by Walter Bodmer and other medical scientists of how defense against parasites works—the notion of genes for resistance providing a sort of lock-and-key system. Hamilton put all three lines of inquiry together and said: Parasites are in a constant battle with hosts, a battle that is fought by switching from one resistance gene to another; hence the battery of different versions of genes. None of this would work without sex.64
In all three fields the breakthrough was to abandon notions of stability. Lotka and Volterra were interested in knowing whether parasites could stably control populations of hosts; Haldane was interested in what kept polymorphisms stable for so long. Hamilton was different. “Where others seem to want stability I always hope to find, for the benefit of my idea of sex, as much change and motion…as I can get.”65
The main weakness of the theory remains the fact that it requires some kind of cycles of susceptibility and resistance; the advantage should always be swinging back and forth like a pendulum, though not necessarily with such regularity.66 There are some examples of regular cycles in nature: Lemmings and other rodents often grow abundant every three years and rare in between. Grouse on Scottish moors go through regular cycles of abundance and scarcity, with about four years between peaks, and this is caused by a parasitic worm. But chaotic surges, such as locust plagues, or much more steady growth or decline, such as in human beings, are more normal. It remains possible that versions of the genes for resistance to disease do indeed show cycles of abundance and scarcity. But nobody has looked.67
THE RIDDLE OF THE ROTIFER
Having explained why sex exists, I must now return to the case of the bdelloid rotifers, the tiny freshwater creatures that never have sex at all—a fact that John Maynard Smith called a “scandal.” For the Red Queen theory to be right, the bdelloids must in some manner be immune from disease; they must have an alternative antiparasite mechanism to sex. That way they could be exceptions that prove the rule rather than embarrass it.
As it happens, the rotifer scandal may be on the verge of a solution. But in the best traditions of the science of sex, it could still go either way. Two new theories to explain the sexlessness of bdelloid rotifers point to two different explanations.
The first is Matthew Meselson’s. He thinks that genetic insertions—jumping genes that insert copies of themselves into parts of the genome where they do not belong—are for some reason not a problem for rotifers. They do not need sex to purge them from their genes. It’s a Kondrashov-like explanation, though with a touch of Hamilton. (Meselson calls insertions a form of venereal genetic infection.)68 The second is a more conventional Hamiltonian idea. Richard Ladle of Oxford University noticed that there are groups of animals capable of drying out altogether without dying—losing about 90 percent of their water content. This requires remarkable biochemical skill. And none of them have sex. They are tardigrades, nematodes, and bdelloid rotifers. Some rotifers, remember, dry themselves out into little “tuns” and blow around the world in dust. This is something sexual monogonont rotifers cannot do (although their eggs can). Ladle thinks that drying yourself out may be an effective antiparasite strategy, a way of purging the parasites from your body. He cannot yet explain exactly why the parasites mind being dried out more than their hosts do; viruses are little more than molecular particles, in any case, and so could surely survive a good drying. But he seems to be on to something. Those nematode or tardigrade species that do not dry out are sexual. Those that can dry out are all female.69
The Red Queen has by no means conquered all her rivals. Pockets of resistance remain. Genetic repair diehards hold out in places like Arizona, Wisconsin, and Texas. Kondrashov’s banner still attracts fresh followers. A few lonely tangled bankers snipe from their laboratories. John Maynard Smith pointedly calls himself a pluralist still. Graham Bell says he has abandoned the “monolithic confidence” (in the tangled bank) that infused his book The Masterpiece of Nature, but has not become an undoubting Red Queener. George Williams still hankers after his notion that sex is a historical accident that we are stuck with. Joe Felsenstein maintains that the whole argument was misconceived, like a discussion of why goldfish do not add to the weight of the water when added to a bowl. Austin Burt takes the surprising view that the Red Queen and the Kondrashov mutation theory are merely detailed vindications of Weismann’s original idea that sex supports the variation needed to speed up evolution—that we have come full circle. Even Bill Hamilton concedes that the pure Red Queen probably needs some variation in space as well as time to make her work. Hamilton and Kondrashov met for the first time in Ohio in July 1992 and agreed convivially to differ until more evidence was in. But scientists always say that: Advocates never concede defeat. I believe that a century hence biologists will look back and declare that the Vicar of Bray fell down a tangled bank and was slain by the Red Queen.70
Sex is about disease. It is used to combat the threat from parasites. Organisms need sex to keep their genes one step ahead of their parasites. Men are not redundant after all; they are woman’s insurance policy against her children being wiped out by influenza and smallpox (if that is a consolation). Women add sperm to their eggs because if they did not, the resulting babies would be identically vulnerable to the first parasite that picked their genetic locks.
Yet before men begin to celebrate their new role, before the fireside drum-beating sessions incorporate songs about pathogens, let them tremble before a new threat to the purpose of their existence. Let them consider the fungus. Many fungi are sexual, but they do not have males. They have tens of thousands of different sexes, all physically identical, all capable of mating on equal terms, but all incapable of mating with themselves.71 Even among animals there are many, such as the earthworm, that are hermaphrodites. To be sexual does not necessarily imply the need for sexes, let alone for just two sexes, let alone for two sexes as different as men and women. Indeed, at first sight, the most foolish system of all is two sexes because it means that fully 50 percent of the people you meet are incompatible as breeding partners. If we were hermaphrodites, everybody would be a potential partner. If we had ten thousand sexes, as does the average toadstool, 99 percent of those we meet would be potential partners. If we had three sexes, two-thirds would be available. It turns out that the Red Queen’s solution to the problem of why people are sexual is only the beginning of a long story.