Graham Bell of McGill University has disinterred a curious debate that raged among biologists at the turn of the century about whether sex had a rejuvenating effect. What intrigued these early biologists was if and why a population of protozoa kept in a tank with sufficient food but given no chance to have sex inevitably fell into a gradual decline in vigor, size, and rate of (asexual) reproduction. Reanalyzing the experiments, Bell found some clear examples of Muller 's ratchet at work. Bad mutations gradually accumulated in the protozoa deprived of sex. The process was accelerated by the habit of this one group of protozoa, the ciliates, of keeping its germ-line genes in one place and keeping copies of them elsewhere for everyday use. The method of reproducing the copies is hasty and inaccurate, so defects accumulate especially fast there. During sex, one of the things the creatures do is throw away their copies THE ENIGMA
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and create new ones from the germ-line originals. Bell compares it with a chair maker who copies the last chair he made, errors and all, and returns to his original design only occasionally. Sex therefore does indeed have a rejuvenating effect: It enables these little animals to drop all the accumulated errors of an especially fast asexual ratchet whenever they have sex."
Bell's conclusion was a curious one. If a population is small (less than 10 billion) or the number of genes in the creature is very large, the ratchet has a severe effect on an asexual lineage. This is because it is easier to lose the defect-free class in a smaller population. So those creatures with larger genomes and relatively smaller populations (10 billion is twice as many people as there are on Earth) will be ratcheted into trouble fairly quickly. But those with few genes and vast populations are all right. Bell reckons that being sexual was a prerequisite for being big (and therefore few), or, con-versely, sex is unnecessary if you stay small. 38
Bell calculated the amount of sex—or, rather, of recombination—that is needed to halt the ratchet; for smaller creatures, less sex is necessary. Water fleas need to have sex only once every several generations. Human beings need to have sex in every generation: Moreover, as James Crow at the University of Wisconsin in Madison has suggested, Muller's ratchet may explain why budding is a relatively rare way of reproducing—especially among animals. Most asexual species still go to the trouble of growing their offspring from single cells (eggs). Why? Crow suggests it is because defects that would be fatal in a single cell can be easily smuggled into a bud. 39
If the ratchet is a problem only for big creatures, why do so many small ones have sex? Besides, to halt the ratchet requires only occasional episodes of sex; it does not require so many animals to abandon asexual reproduction altogether: Aware of these difficulties, in 1982 Alexey Kondrashov of the Research Computer Center in Poschino, near Moscow, came up with a theory that is a sort of reverse Muller 's ratchet. He argued that in an asexual population, every time a creature dies because of a mutation it gets rid of that mutation but no more. In a sexual population some of the creatures born have lots of mutations and some have few: If the ones with
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The Red Queen
lots of mutations die, then sex keeps throwing the ratchet into reverse, purging mutations: Since most mutations are harmful, this gives sex a great advantage.'°
But why purge mutations in this way rather than correct more of them by better proofreading? Kondrashov has an ingenious explanation of why this makes sense: The cost of making proofreading mechanisms perfect gets rapidly higher as you get nearer to perfection; in other words, it is like the law of diminishing returns: Allowing some mistakes through but having sex to purge them out may be cheaper:
Matthew Meselson, a distinguished molecular biologist, has come up with another explanation that expands on Kondrashov 's idea: Meselson suggests that "ordinary " mutations that change one letter for another in the genetic code are fairly innocuous because they can be repaired, but insertions—whole chunks of DNA that jump into the middle of genes—cannot be reversed so easily: These "selfish " insertions tend to spread like an infection, but sex defeats them, since sex segregates them into certain individuals whose deaths purge them from the population:"
Kondrashov is prepared to stand by an empirical test of his idea: He says that if the rate of deleterious mutations turns out to be more than one per individual per generation, then he is happy; if it proves to be less than one, then his idea is in trouble: The evidence so far is that the deleterious mutation rate teeters on the edge: It is about one per individual per generation in most creatures: But even supposing it is high enough, all that proves is that sex can perhaps play a role in purging mutations: It does not say that is why sex persists.' Z
Meanwhile, there are defects in the theory: It fails to explain how bacteria—of which some species rarely have sex and others not at all—nonetheless suffer from mutation at a low rate and make fewer proofreading mistakes when copying DNA: As one of Kondrashov 's critics put it, sex is "a cumbersome strange tool to have evolved for a housekeeping role: ""
And Kondrashov 's theory suffers from the same flaw as all genetic-repair theories and the Vicar of Bray himself: It works too THE ENIGMA
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slowly. Pitted against a clone of asexual individuals, a sexual population must inevitably be driven extinct by the clone 's greater productivity unless the clone 's genetic drawbacks can appear in time. It is a race against time. For how long? Curtis Lively of the University of Indiana has calculated that for every tenfold increase in population size, the advantage of sex is granted six more generations to show its effects or sex will lose the game. If there are a million individuals, sex has forty generations before it goes extinct; if a billion, it has eighty. Yet the genetic repair theories all require thousands of generations to do their work. Kondrashov's is certainly the fastest theory, but it is probably not fast enough."
There is still no purely genetic theory to explain sex that attracts wide support. An increasing number of students of evolution believe that the solution to the great enigma of sex lies in ecology, not genetics.
Chapter 3
THE POWER OF
PARASITES
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 small-est 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 dis-integrate, 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.