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-
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.'
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.''
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 pendu-lum, though not necessarily with such regularity:
THE POWER OF PARASITES
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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;
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
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 Hamilton-ian 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:'
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 'mono-lithic confidence ' (in the tangled bank) that infused his book
