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In 1988, the American microbiologist John Cairns and his colleagues dropped a small bombshell on the biological community.1 For more than fifty years, right from the early days of the Modern Synthesis, biologists had accepted almost without question the dogma that all new heritable variation is the result of accidental and random genetic changes. The idea that new genetic variants—mutations—might be produced particularly when and where they were needed had been dismissed as a heretical Lamarckian notion. In reality, however, there was little evidence against it. The rate at which new mutations are produced is very low, so detecting them at all required a lot of searching among large numbers of animals or plants; deciding whether or not mutations were produced randomly was effectively impossible. Only for bacteria were there techniques that allowed vast numbers of organisms to be screened relatively easily, and it was these organisms that had provided the main evidence that mutation is random. Experiments carried out in the 1940s and 1950s seemed to show that for bacteria the conditions of life had no effect on the production of new mutations. It was this conclusion that John Cairns and his associates challenged in 1988. They argued that the earlier experiments had been overinterpreted. Their own experiments suggested that some mutations in bacteria are produced in response to the conditions of life and the needs of the organism. The generation of mutations is therefore not an entirely random process. This was not the first time that experimental evidence suggesting nonrandom mutation had been reported, but the scientific stature of John Cairns, and the publication of his group’s findings in Nature, the leading British science journal, meant it could no longer be ignored. The Nature article led to a spate of responses and comments in both the scientific and popular press. The idea of nonrandom mutation was seen by many as a challenge to the well-established neo-Darwinian theory of evolution, and although some 3 Genetic Variation: Blind, Directed, Interpretive? 80 Chapter 3 people’s reaction was to suggest mechanisms that might underlie the production of induced mutations, others were extremely reluctant to accept that they could occur at all. They offered alternative interpretations of the experimental results—interpretations that did not require that mutations were formed in response to the environmental conditions. The upshot of all the arguments was that it was quickly realized that there was really no good evidence of any kind to show that all mutations are random accidents . It was equally clear, however, that a lot more experimental work was needed before it could be firmly concluded that some mutations are formed in response to environmental challenges. We don’t want to go into the details of all the claims and counterclaims that resulted from the work following up the 1988 Nature paper. On balance we think that the experimental evidence that is now available suggests that Cairns and his colleagues were probably wrong; they were not dealing with mutations that were produced in direct response to the environmental challenge they imposed. However, what emerged from the work their paper stimulated and subsequent molecular studies is important, because it has resulted in a far less simplistic view of the nature of mutations and mutational processes. There is now good experimental evidence, as well as theoretical reasons, for thinking that the generation of mutations and other types of genetic variation is not a totally unregulated process. In this chapter we want to look at the whole question of where the variation that underlies the genetic dimension of evolution comes from. Essentially , it has two sources: one is mutation, which creates new variations in genes; the other is sex, through which preexisting gene variations are shuffled to produce new combinations. We shall focus mainly on mutation, particularly on nonrandom mutation, but first we want to say something about the variation generated through sexual reproduction, and how this process has been shaped by natural selection. Genetic Variation through Sex Sexual reproduction is the most obvious source of genetic variation. In animals like ourselves, it creates enormous diversity by producing new combinations of the genes existing in parents. From personal experience we know how very different the children in a human family can be, and how the kittens in a litter are often totally dissimilar, even on the rare occasions when we are quite sure only one father was involved. This variation, which is the outcome of sexual reproduction, is not adaptively linked...


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