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.)"
Moreover, it is a curious fact that parasites themselves are often sexual, despite the enormous inconvenience this causes. A bil-harzia 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.
THE POWER OF PARASITES
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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 1 2 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 cen-
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The Red Queen
tered 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. b°
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 inca -
pable 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 THE POWER OF PARASITES
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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."
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."
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."
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 para-
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The Red Queen
sites 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 agaii*t 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."