Neo-Darwinism is a theory based on genes, G.C. Williams (1966) states explicitly, “. . . In explaining adaptation, one should assume the adequacy of the simplest form of natural selection, that of alternative alleles in Mendelian populations.” (p.4) Natural selection on alternative alleles can only be a valid description of reality when the following abstractions of the genetic paradigm are assumed to be true: (a) genes determine characters in a straightforward and additive way, (b) they are stable and, except for rare random mutations, are passed on unchanged to the next generation, and (c) there is no feedback from the environment to the organism’s genes. All three assumptions have been demonstrated to be false.
Assumption (a) was known to be false since the beginning of the neo-Darwinian synthesis, and to some of the most prominent ‘architects’ of the grand synthesis such as Sewell Wright (1969; 1978) and Ernst Mayr (1963). Wright argues that selection relates to the organism as a whole, or to the social group, not to single genes except as a net resultant. He saw that the major source of variability is in the recombination of already existing genes into a great number of different genotypes, many of which would occupy equivalent “adaptive peaks” in a “fitness landscape”. Mayr, on the other hand, insists that natural selection acts on “co-adapted gene complexes” as a whole, and remains highly critical of ‘beanbag [population] genetics’ such as that of R.A. Fisher (1930) and J.B.S. Haldane (1932), which deals with selection of single genes. However, that still leaves both the “fitness landscape” and the “co-adaptive gene complex” undefined, and with little impact on the study of evolution in the mainstream, where it is customary to identify a character, then assume there is a hypothetical gene (or set of genes) responsible for it, which may be selected in isolation from everything else.
Critics point out that the mapping between genes and the organisms’ characters (phenotype) in development is nonlinear and non-additive (as it would already be when one takes Wright and Mayr seriously), and that the organism as a dynamical system is subject to universal generative principles not immediately dependent on the genes. Neo-Darwinists counter that these are only “developmental constraints” which limit, to some extent, the action of natural selection, but that natural selection still plays the creative role in evolution (Bonner, 1982).
There have been serious attempts to use developmental findings to trace phylogenetic relationships (Humphries, 1988 ; Wake, 1990 ; D.B. Wake, 1991 ) although the theoretical relationship between ontogeny and phylogeny is still not adequately understood by most systematists (Ho, 1988a; Wake, 1994).
Assumptions (b) and (c) effectively separate the organism from the environment, which has the role of the ‘selector’. Of course, most people accept that the environment also interacts with the organism, causing changes in its characteristics. However, it is supposed that the environment as ‘interactor’ can be neatly separated from the environment that selects, for so long as the germline genes are stable, and do not change ith the environment, then it is irrelevant how the rest of the body is affected. As only the genes are passed on in evolution, it also means that evolution is separate from development. Maynard Smith and Holliday ( 1979 ) have indeed declared that the gift of Weismannism to evolutionary (i.e., neo-Darwinian) theory is that development can be safely ignored. As we shall see, these assumptions are no longer tenable.
Mae Wan Ho, Evolution, in Comparative Psychology, a Handbook, (G. Greenberg and M. M. Haraway, eds.), pp. 107-119, Garland Publishing, 1998.