In his book On the Origin of Species
, Charles Darwin (1859)
proposed that all organisms on earth evolved from a single proto-organism by descent with modification. He also proposed that the primary force of evolution is natural selection. Most biologists accepted the first proposition almost immediately, but the second proposal was controversial and was criticized by such prominent biologists as Thomas Huxley, Moritz Wagner, and William Bateson. These authors proposed various alternative mechanisms of evolution such as transmutation theory, Lamarckism, geographic isolation, and nonadaptive evolution (see Provine 1986
, chap. 7). Because of these criticisms, Darwin later changed his view of the mechanism of evolution to some extent (Origin of Species
1872, chap. 7). He was a pluralistic man and accepted a weak form of Lamarkism and nonadaptive evolution (see Provine 1986
). Nevertheless, he maintained the view that the natural selection operating on spontaneous variation is the primary factor of evolution. His main interest was in the evolutionary change of morphological or physiological characters and speciation.
Another critic of evolution by natural selection was the post-Mendelian geneticist Thomas Morgan. He rejected Lamarkism and any creative power of natural selection and argued that the most important factor of evolution is the occurrence of advantageous mutations and that natural selection is merely a sieve to save advantageous mutations and eliminate deleterious mutations (Morgan 1925
). For this reason, his view is often called mutationism. However, this view should not be confused with the saltation theory of Bateson (1894)
or the macromutation theory of De Vries (1901–1903)
, in which natural selection plays little role. In Morgan's time the genetic basis of mutation was well established, and his theory of evolution was appealing to many geneticists. The only problem was that most mutations experimentally obtained were deleterious, and this observation hampered the general acceptance of his theory. He also proposed that some part of morphological evolution is caused by neutral mutation. In his 1932 book The Scientific Basis of Evolution
, he stated “If the new mutant is neither more advantageous than the old character, nor less so, it may or may not replace the old character, depending partly on chance; but if the same mutation recurs again and again, it will most probably replace the original character” (p. 132).
However, Morgan's mutation-selection theory or mutationism gradually became unpopular as the neo-Darwinism advocated by Fisher (1930)
, Wright (1931)
, Haldane (1932)
, Dobzhansky (1937
, and others gained support from many investigators in the 1940s. In neo-Darwinism, natural selection is assumed to play a much more important role than mutation, sometimes creating new characters in the presence of genetic recombination. Although there are several reasons for this change (see Nei 1987
, chap. 14), two are particularly important. First, most geneticists at that time believed that the amount of genetic variability contained in natural populations is so large that any genetic change can occur by natural selection without waiting for new mutations. Second, mathematical geneticists showed that the gene frequency change by mutation is much smaller than the change by natural selection. Neo-Darwinism reached its pinnacle in the 1950s and 1960s, and at this time almost every morphological or physiological character was thought to have evolved by natural selection (Dobzhansky 1951
; Mayr 1963
This situation again started to change as molecular data on evolution accumulated in the 1960s. Studying the GC content of the genomes of various organisms, early molecular evolutionists such as Sueoka (1962)
and Freese (1962)
indicated the possibility that the basic process of evolution at the nucleotide level is determined by mutation. Comparative study of amino acid sequences of hemoglobins, cytochrome c, and fibrinopeptides from various organisms also suggested that most amino acid substitutions in a protein do not change the protein function appreciably and are therefore selectively neutral or nearly neutral, as mentioned below. However, this interpretation was immediately challenged by eminent neo-Darwinians such as Simpson (1964)
and Mayr (1965)
, and this initiated a heated controversy over selectionism versus neutralism.
An even more intense controversy on this subject was generated when protein electrophoresis revealed that the extent of genetic variation within populations is much higher than previously thought. At that time, most evolutionists believed that the high degree of genetic variation can be maintained only by some form of balancing selection (Mayr 1963
; Ford 1964
). However, a number of authors argued that this variation can also be explained by neutral mutations. From the beginning of the 1980s, the study of molecular evolution was conducted mainly at the DNA level, but the controversy is still continuing. This longstanding controversy over selectionism versus neutralism indicates that understanding of the mechanism of evolution is fundamental in biology and that the resolution of the problem is extremely complicated. However, some of the controversies were caused by misconceptions of the problems, misinterpretations of empirical observations, faulty statistical analysis, and others.
Because I have been involved in this issue for the last 40 years and have gained some insights, I would like to discuss this controversy with historical perspectives. Obviously, the discussion presented will be based on my experience and knowledge, and therefore it may be biased. In my view, however, we can now reach some consensus and examine what has been solved and what should be done in the future. Needless to say, I shall not be able to cover every subject matter in this short review, and I would like to discuss only fundamental issues.