Mutation and causation in the New Synthesis view

• that mutation is "random" or a matter of "chance"
• that discrete events of mutation are unimportant in evolution (as Darwin had assumed)
• that the direction of evolution is due to selection and cannot be influenced by variation,

1. Treat deleterious mutation like selection, as a "pressure" on allele frequencies that might cause fixation,
2. Demonstrate that in fact, deleterious mutation cannot cause fixation because mutation rates are so low, and
3. Conclude from the above that mutation is not a "cause" or "force" of evolution and cannot influence its direction.

The original Fisher-Haldane argument

Fisher's version of the Fisher-Haldane argument (Ch. 1 of Fisher, 1930; 1958) :

The frequency of individual mutations in Drosophila is certainly seldom greater than one in 100,000 individuals, and we may take this figure to illustrate the inefficacy of any agency, which merely controls the predominant direction of mutation, to determine the predominant direction of evolutionary change.

"Without mutation there would be no gene differences for natural selection to act upon. But the actual evolutionary trend would seem usually to be determined by selection, for the following reason.
A simple calculate shows that recurrent mutation (except of a gene so unstable as to be classifiableas multimutating) can not overcome selection of quite moderate intensity. Consider two phenotypes whose relative fitnesses are in the ratios 1 and 1-k, that is to say, that on the average one leaves (1-k) times as many progeny as the other. Then, if p is the probability that a gene mutates to a less fit allelomorph in the course of a life cycle, it has been shown (Haldane, 1932) that when k is small, the mutant gene will only spread through a small fraction of the population unless p is about as large as k or larger. This is true whether the gene is dominant or recessive."

Later comments on the role of mutation in evolution

Huxley (1964), p. 56:

"For no rate of hereditary change hitherto observed in nature would have any evolutionary effect in the teeth of even the slightest degree of adverse selection. Either mutation-rates many times higher than any as yet detected must be sometimes operative, or else the observed results can be far better accounted for by selection."

Dobzhansky (1955), p. 282:

"The process of mutation supplies the raw materials of evolution, but the tempo of evolution is determined at the populational levels, by natural selection in conjunction with the ecology and the reproductive biology of the group of organisms"

Darlington (1958), p. 231

"Darwin assumed in the Origin of Species that the evolution of living organisms depended on the origin of new forms which varied from old forms by continuous differences in no constant or predictable direction. Crossed together the new and the old showed blending inheritance. To these variations direction was given by a process of natural selection which, like artificial selection, preserved some while it destroyed others. A direction, an adaptive direction, was thus given to variations after they arose. This view was intended by Darwin to supplant the alternative view that direction was given to variations before they arose . . . [Darlington goes on to equate the latter view with neo-Lamarckism, which in my opinion is a mistake]

A later statement by Haldane (1958, p. 17):

"Natural selection, then, may or may not change gene frequencies. But nothing else can do so anything like as fast . . . Mutation is at best slow, and could not usually overcome a selective disadvantage of one in ten thousand.
We are left, I think, with no alternative but to believe that natural seelction has been the main evolutionary agency, and also with surprisingly little evidence for effective selection."

Simpson, 1967, p. 159:

"Adaptation has a known mechanism: natural selection acting on the genetics of populations . . In seeking the orienting factor in evolution we have seen that in some cases this must, by all reasonable inferences, be adaptation and in all, even the most doubtful, it could be adaptation. Thus we have a choice between a concrete factor with a known mechanism and the vagueness of inherent tendencies, vital urges, or cosmic goals, without known mechanism.
With no pretense at having plumbed the whole mystery or excluded all other possibilities, it is concluded that the major (if not the only) nonrandom, orienting facor in the process of evolution is reasonably identified as adaptation." [emphasis mine]

Haldane, 1959, p. 147

"Variation is in some sense random, but natural selection picks out variations in one direction, and not in another."

Mayr, 1963, p. 101

"Mutation as an evolutionary force. In the early days of genetics it was believed that evolutionary trends are directed by mutation, or, as Dobzhansky (1959) recently phrased this view, 'that evolution is due to occasional lucky mutants which happen to be useful rather than harmful.' In contrast, it is held by contemporary geneticists that mutation pressure as such is of small immediate evolutionary consequence in sexual organisms, in view of the relatively far greater contribution of recombination and gene flow to the production of new genotypes and of the overwhelming role of selection in determining the change in the genetic composition of populations from generation to generation."

Mayr, 1963, p. 613.

"It is most important to clear up first some misconceptions still held by a few, not familiar with modern genetics: (1) Evolution is not primarily a genetic event. Mutation merely supplies the gene pool with genetic variation; it is selection that induces evolutionary change."

Stebbins, 1966, p. 29:

"mutations are rarely if ever the direct source of variation upon which evolutionary change is based. Instead, they replenish the supply of variability in the gene pool which is constantly being reduced by selective elimination of unfavorable variants. Because in any one generation the amount of variation contributed to a population by mutation is tiny compared to that brought about by recombination of pre-existing genetic differences, even a doubling or trebling of the mutation rate will have very little effect upon the amount of genetic variability available to the action of natural selection. Consequently, we should not expect to find any relationship between rate of mutation and rate of evolution. There is no evidence that such a relationship exists." [emphasis mine]

Natural selection directs evolution not by accepting or rejecting mutations as they occur, but by sorting new adaptive combinations out of a gene pool of variability which has been built up through the combined action of mutation, gene recombination, and selection over many generations. . . Consequently, the rate of mutation rarely if ever has an influence on the rate of evolution

"If ever it could ahve been thought that mutation is important in the control of evolution, it is impossible to think so now"

Gould (1977), p. 44, defending Darwinism against creationist attack:

"The essense of Darwinism lies in its claim that natural selection creates the fit. Variation is ubiquitous and random in direction. It supplies the raw material only. Natural selection directs the course of evolutionary change."

Dobzhansky, Ayala, Stebbins & Valentine (1977), p. 72:

"The large number of variants arising in each generation by mutation represents only a small fraction of the total amount of genetic variability present in natural populations. ... It follows that rates of evolution are not likely to be closely correlated with rates of mutation. Besides mutation, natural selection and migration help maintain high levels of genetic variation in natural populations. Even if mutation rates would increase by a factor of 10, newly induced mutations would represent only a very small fraction of the variation present at any one time in populations of outcrossing, sexually reproducing organisms." [emphasis mine]

Dobzhansky, Ayala, Stebbins & Valentine (1977), p. 6:

"Each unitary random variation is therefore of little consequence, and may be compared to random movements of molecules within a gas or liquid. Directional movements of air or water can be produced only by forces that act at a much broader level than the movements of individual molecules, e.g., differences in air pressure, which produce wind, or differences in slope, which produce stream currents. In an analogous fashion, the directional force of evolution, natural selection, acts on the basis of conditions existing at the broad level of the environment as it affects populations."

Stebbins, 1982, p. 79:

"The opinion expressed throughout this book, that mutations are most important as a way of replenishing the gene pool as it becomes depleted by natural selection, is now supported by a wealth of experimental and observational evidence. Nevertheless, the old idea that mutations direct evolutionary change is still held by many biologists and is expresssed most often in popular accounts of evolution. "

Stebbins, 1982, p. 160:

"Novelty does not arise because of unique mutations or other genetic changes that appear spontaneously and randomly in populations, regardless of their environment. Selection pressure for it is generated by the appearance of novel challenges presented by the environment and by the ability of certain populations to meet such challenges."

Mayr, 1983, p. 151:

"When one attempts to determine for a given trait whether it is the result of natural selection or of chance (the incidental byproduct of stochastic processes), one is faced by an epistemological dilemma. Almost any change in the course of evolution might have resulted by chance. Can one ever prove this? Probably never. By contrast, can one deduce the probability of causation by selection? [emphasis mine]

Ridley, 1985, p. 25 (and see Chapter 2 in general):

"We can now return to the original problem, of whether heredity alone can produce evolution. Because evolutionary innovations result from mutation and recombination, we should rephrase the question to ask whether mutaion and recombination produce directed or undirected change. The answer is that, like pure Mendelian inheritance, they too are undirected. They do not consistently produce changes in any particular direction. Mutations affecting size are just as likely to produce taller organisms as shorter ones . . . whatever the internal plausibility of these theories [of directed variation], they are in fact wrong. Neither the inheritance of acquired characters, nor any other theory of directed hereditary change (or directed mutation), is the mechanism of evolution."

Mayr (1994), p. 38.

"Those authors who thought that mutations alone supplied the variability on which selection can act, often called natural selection a chance theory. They said that evolution had to wait for the lucky accident of a favorable mutation before natural selection could become active. This is now known to be completely wrong. Recombination provides in every generation abundant variation on which the selection of the relatively better adapted members of a population can work." [emphasis mine].

Freeman and Herron (1998), p. 145, in their excellent textbook:

"In summary, mutation creates the genetic diversity that is the raw material for evolution. In principle, mutation can also produce changes in allele frequencies accross generations. In practice, mutation's role as the source of genetic variation is usually more important than its role as a mechanism of evolution. " [emphasis mine]

Futuyma, et al., 1998, in a white paper sponsored by professional societies (SSE, Soc Am Nat, SMBE, GSA, ESA, SSB, etc):

"For instance, it is possible to say confidently that natural selection exerts so much stronger a force than mutation on many phenotypic characters that the direction and rate of evolution is ordinarily driven by selection even though mutation is ultimately necessary for any evolution to occur." [emphasis mine]

Working Group on Teaching Evolution (U.S. National Academy of Sciences, 1998), from Ch. 2 of their guide to teaching evolution:

"Genetic variation is random, but natural selection is not."

Acknowledgement

References