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Towards a Newer Synthesis of Evolutionary Theory

The notion of "synthesis" presupposes discord, conflict or disintegration. In the original "New Synthesis" or "Modern Synthesis" of evolutionary biology (1930-1950), the conflict was between Darwin's original view of evolution, based on a continuous process of environmentally stimulated phenotypic/genotypic variation, and the new findings of genetics, which revealed a discrete and largely spontaneous process ("mutation") of segregated germline variation. Although it has become fashionable in neo-Darwinian historiography to assert that this conflict was only superficial, this assertion is ridiculous. The birth of genetics was widely accepted as the death of Darwinism. The very real conflicts between the two were not resolved for 50 years. The "New Synthesis" was significant precisely because it purported to resolve this long-standing conflict in a manner that, eventually, was widely accepted.

Today, evolutionary biology is once again in a state of discord. Superficially, at least, it appears that several fundamentally different views of evolution are competing or co-existing in different fields: an "evo-devo" view, a "molecular" view, a "classical" view, maybe even a "systems" view or an "a-life" view. Some authorities tell us that molecular evolution is different from non-molecular evolution. What is the unified theory that provides for both? Familiar icons of neo-Darwinism still write books proclaiming the sufficiency of neo-Darwinism to accomodate new data on molecular evolution and development. Meanwhile, "evo-devo" enthusiasts proclaim a new view that addresses problems "not seen as being soluble by population genetics" (Gilbert, et al., 1996). If population genetics does not provide a unified mathematical framework for addressing evolutionary causes, what body of theory does?

The view argued here is that these apparent differences are real, and that the contemporary discord in evolutionary theory hearkens back to the earlier dispute over mutation and the role of variation in evolution. This connection is elucidated in the next section.

Why not neo-Darwinism?

(Note in passing: readers may be unfamiliar with the sometimes confusing use of the word "theory" in science. If this applies to you, please read a brief description of the distinction as it applies to evolutionary theory.)

Evolutionary biology is in a state of transition, based on a new perception of how the process of variation influences evolutionary change. Evolutionary biologists who understand something of this new view (and not all of them do, yet) disagree among themselves over whether it still should be called "Darwinism". Clearly any new view of evolution will still invoke natural selection in populations, yet just as clearly, it would contradict fundamental propositions of the Darwinism of the 19th century as well as the neo-Darwinism of the mid-20th century (in addition to being different from the crude notion of evolution familiar from popular books, magazines and television).

Darwin assumed that the process of natural selection proceeded from an abundant supply of continuous variation arising each generation by an environmentally stimulated process of phenotypic/genotypic change. However, Darwin had confounded environmental variation and genetic variation, and his view was disqualified at the dawn of the 20th century by the discovery of genetics, and by the acceptance of Weismann's doctrine of germline segregation. For several decades following the demise of Darwin's view, evolutionists debated a new view that would synthesize the new understanding of mutational change as a discrete event that heritably alters a Mendelian factor. Fundamental in this debate were issues such as whether discreteness in the process of variation negated Darwin's assumption of smooth continuous change, whether (contrary to Darwin's belief, based on blending inheritance) evolutionary change could begin with a single event of mutation, and whether novelty and directionality in evolution were due to "external" forces of environmental origin (e.g., selection), or to "internal" forces inherent to the organism (e.g., mutation, development).

The view that subsequently emerged, in 1930-1950, is what we now know as "neo-Darwinism", and is less ambiguously called the "New Synthesis" or "Modern Synthesis" or "Synthetic Theory". The New Synthesis retained Darwin's assumption of abundant "random" variation, but on a mechanistic basis that was more consistent with modern genetics: rampant recombination in a diverse "gene pool" that would produce abundant slight variations every generation. The crucial common feature of both views-- the feature that distinguished "Darwinism" from alternative schools of thought that placed more emphasis on the process of individual variation-- is that the abundance and "randomness" of variation puts natural selection firmly in the driver's seat in evolution: in this view, selection (not mutation) is seen as the creative process in evolution, and the rate and direction of evolution are seen to be dependent on natural selection, not on the process of individual variation. As S.J. Gould has written,

The essence 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.

To the early neo-Darwinians, the notion that the direction of evolution would be influenced by "internal" factors such as mutation and development seemed not merely wrong, but unscientific.

Nevertheless, science advances in ways that are not easily anticipated. As the result of their own research, scientists schooled in the "New Synthesis" tradition have recognized that variation is not inevitably abundant, gradual, and continuous, but may be constrained, abrupt, and discrete; that most living organisms are prokaryotes or asexual eukaryotes that simply lack rampant recombination in a "gene pool"; and-- perhaps most importantly-- that rates and patterns of evolutionary change are manifestly dependent on propensities of variation due to mutation and development. The distinction between the older and newer views is apparent in a variety of statements (many examples can be provided) such as the following:

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.

In addition to showing a continued adherence to Darwin's antique principle that single mutations can not initiate evolutionary change (a conclusion that Darwin based on his assumption of gradualism and his mistaken theory of blending inheritance), the above statement emphasizes the hyper-abundant "gene pool", the importance of recombination, and the conclusion that the rate of evolution does not depend on the rate of mutation. While such a statement might not have raised eyebrows in 1966, no evolutionary biologist would make it today, because of the abundant evidence that the rate of evolution depends on the rate of mutation.

Towards a different synthesis

Evolutionary biologists are not at a loss to accomodate the evidence that the rate of evolution is dependent on the rate of mutation. We now understand that, in a finite world, where variation and time are not infinitely abundant, the non-randomness of variation (long recognized by geneticists) is expected to have a crucial influence on the course of evolution.

Indeed, for several decades, molecular evolutionists have relied on an evolutionary view that abandons the Darwinian presumption of abundant pre-existing variation, assuming instead that the rate of evolution depends directly on the rate of introduction of new alleles by mutation. For instance, highly successful modern methods of phylogenetic inference assume such a dependence implicitly when they implement different rates for transition and transversion changes. Likewise, for two decades, developmental evolutionists have been emphasizing the importance of developmental "constraints" that influence course of evolution via their effects on the generation of variation.

Thus, while there are clearly common threads linking past and present thought in evolutionary biology, the evolutionary theory of today is not that of Darwin, nor even that of Darwin's mid-20th-century successors. This yet-to-be-named new view, with its empirical emphasis on rates and patterns of divergence, and its reliance on, not only natural selection, but also mutation biases and developmental constraints as causes of non-randomness in evolution, has already enjoyed considerable success.

From a historical perspective, this new view is not entirely new. In a sense, we have revisited the dispute between the New Synthesis architects and the "mutationists", and discovered that there is some value in the mutationist position. (to be continued ... )