This is the sixth in a series of postings by guest blogger, Arlin Stoltzfus. You can read the introduction to the series at: Introduction to "The Curious Disconnect". The first part is at: The "Mutationism" Myth I. The Monk's Lost Code and the Great Confusion. The second installment is: Theory vs Theory. The third part is: The Mutationism Myth, II. Revolution. The fourth installment is: The Mutationism Myth: III Foundations of Evolutionary Genetics.
There are many ways in which the so-called "Modern" Synthesis has to be revised and extended. One of them is to reinstate the concept of mutationism which was purged from evolutionary theory in the 1940s. If you want to understand why this is important then these articles are the place to start.
The Curious Disconnect
Last month, we debunked the Mutationism Myth and learned why the discovery of genetics in 1900 led "Mendelians" to reject Darwin's view. These same Mendelians went on to lay the foundations of a genetics-based view of evolution, during a period of rapid innovation from 1900 to 1915. But this begs another question: if the Mendelians invented the 20th-century consensus, and just left it to others to work out the math, why aren't they lauded as "founders" of modern neo-Darwinism, instead of being derided as fools? We'll find out in part 4 (today), and part 5, here on on The Curious Disconnect (credits).
The Mutationism Myth, part 4. Mendelian Heterodoxies
The reader who has been following our story so far may be baffled. As we found out in part 3, the Mendelians understood how to conceptualize a population as a dynamic system of allele and genotype frequencies (the Bateson-Saunders equilibrium), how to see evolutionary change as a probabilistic 2-step process of the introduction and acceptance-or-rejection of mutations, and how to think about selection-driven changes in a quantitative trait.
Why don't the Mendelians get credit for laying the foundations of the 20th-century consensus?
As we will learn today and in part 5, the Mendelian view is not the 20th-century "neo-Darwinian" consensus. The Mendelians combined genetics with selection. By contrast, the 20th-century consensus combines genetics with Darwinism, i.e., the Modern Synthesis invokes the principles of genetics to prop up 19-century doctrines of Darwin and his followers, such as natura non facit salta, the creativity of selection, the idea of evolution as a process of adaptive adjustment initiated by changed conditions, and the notion that the course or direction of evolution is determined by selection but not by "random" variation.
When I mock the Modern Synthesis for its Darwinian excesses, I don't want to give the impression that its wrong for a theory1 to go beyond what is demanded by the facts. All theories1 must go beyond the facts, taking risks. While most theories, it seems, take risks in the service of conceptual simplicity, the Modern Synthesis takes risks in the service of 19th-century Darwinian doctrines. On the basis of these commitments, e.g., its rejection of the "lucky mutant" view necessary to understand molecular evolution, the Modern Synthesis later failed.
But that's getting ahead of ourselves. Our task right now is to begin sorting out why the Modern Synthesis is Darwinian, while the Mendelian view it replaced was not.
"Mutationism" vs the Mendelian "view"
My understanding of the evolutionary views of "Mendelians" is based on the works of Bateson (1894, 1900, 1902, 1909), Johannsen (1903, 1909), de Vries (1905), Morgan (1903, 1916, 1925, 1932), Punnett (1911), Vavilov (1922), Shull (1936) and, with some reservations, Goldschmidt (1940). Every time I research the Mendelians, I find new material and revise my views, e.g., I am resolving more and more to avoid the label "mutationism", which I see increasingly as a pejorative term preferred by opponents rather than supporters.
I also have come to understand more confidently that, while the Mendelians had much to say about evolution— indeed, many of them were motivated to study heredity precisely because of their interest in evolution—, they didn't have a unified "view". With the exception of de Vries, the Mendelians did not propose what we would call "a theory of evolution", i.e., a Grand Unified Theory1 of Evolution (GUTE) that purports to be comprehensive. Instead they argued that we need to rethink how evolution works, and follow the implications of genetics wherever they led— typically away from a more Darwinian view emphasizing infinitesimalism, determinism, and selective control.
Thus, while "Mendelism" (in contrast to "mutationism") does not sound like a very good name for a theory of evolution, that's ok, because it's not: Mendelism is a theory of genetics, and the "Mendelian view of evolution" is simply what the early Mendelian geneticists thought about evolution.
Recognizing the lack of a Mendelian GUTE helps us to appreciate more fully the role of the "Modern Synthesis" in the development of evolutionary thinking, and in the Mutationism Story. In the 19th century, before the discovery of genetics, scientists divided their allegiance among multiple GUTEs, most importantly, Darwinism and Lamarckism. By 1910, it was clear to leading thinkers that genetics had undermined all 19th-century GUTEs (including de Vries's "MutationsTheorie" 1). The geneticists (for whatever reason) did not fill this gap by proposing a new GUTE. Thus, while the Mendelian era from 1900 to 1930 was not a stagnant period, it may be seen as a GUTE-less period that ended with the rise of the Modern Synthesis.2
Initiative
The view that events of mutation initiate evolutionary change contrasts with the view that evolutionary change is a series of adjustments or responses to external stimuli, as in the views of Buffon or Darwin. Punnett writes:
"With the advent of heredity as a definite science we have been led to revise our views as to the nature of variation, and consequently in some respects as to the trend of evolution. Heritable variation has a definite basis in the gamete, and it is to the gamete, therefore, not to the individual, that we must look for the initiation of this process. Somewhere or other in the course of their production is added or removed the factor upon whose removal or addition the new variation owes its existence." (p. 141)
Variation (mutation) is the locale of evolutionary initiative, to the extent that both 1) the possibilities or directions of future evolutionary change are established at the moment of the mutation (i.e., mutation as a source of creativity or direction, as addressed below); and 2) the dynamics of evolutionary change depend on the times of appearance of mutations. This second sense depends somewhat on the "new mutations" conception of evolution as a 2-step process of the introduction of a variant followed by its acceptance or rejection.
In this view, one may expect that the dynamics of evolution (adaptive or not) will depend on mutation rates. In fact, the Mendelians sometimes recognized this kinetic dependence, as when Shull (1936, p. 140) argues, "a gene produced twice by mutation has twice as good a chance to survive as if produced only once" (see also Morgan 1925, p. 142). This non-Darwinian idea that propensities of variation could make an evolutionary change more or less likely was not a new thought (indeed it was understood as the potential mechanistic basis of "orthogenesis"), but now it could be given a more precise interpretation.
The architects of the Modern Synthesis later ridiculed what they called the "lucky mutant" view (Mayr 1963, p. 101), but it was hardly an unsophisticated appeal to chance, as we saw in part 3 with the quotation illustrating Morgan's stunning grasp of the probability of acceptance of new mutations. Punnett made a similar statement in his 1911 book (online source):
"The new variation springs into being by a sudden step, not by a process of gradual and almost imperceptible augmentation. It is not continuous but discontinuous, because it is based upon the presence or absence of some definite factor or factors— upon discontinuity in the gametes from which it sprang. Once formed, its continued existence is subject to the arbitrament of natural selection. If of value in the struggle for existence[,] natural selection will decide that those who possess it shall have a better chance of survival and of leaving offspring than those who do not possess it. If it is harmful to the individual[,] natural selection will soon bring about its elimination. But if the new variation is neither harmful nor useful[,] there seems no reason why it should not persist."
By rejecting this component of the Mendelian view of evolution, the Modern Synthesis disallowed a direct link between the rate of mutation and the rate of evolution, making the theory incompatible with the results of studies of "molecular evolution" that began to emerge a half-century after the insights of Punnett and Morgan.
Discontinuity
To understand the issue of discontinuity or discreteness, again we must distinguish 2 senses. In the passage quoted above from Punnett, it's clear that Punnett is talking about what we might call a "mechanistically" discontinuous change in the sense that the mutant factor comes into existence at a specific point in time, due to an event of mutation, rather than gradually, due to an ongoing process of "imperceptible augmentation".
Mayr and others frequently misinterpret the Mendelian commitment to mechanistic discontinuity as a commitment to dramatic phenotypic saltations, but this is a different issue entirely.
In fact, the Mendelians entertained a range of views on the sizes of evolutionary changes important in evolution, excluding only the Darwinian extreme of relying wholly on "insensible" or "infinitesimal" changes. De Vries adopted an antithetical position emphasizing dramatic changes that create new species (with intra-specific variation and selection playing only a minor role). Bateson challenged
"the crude belief that living beings are plastic conglomerates of miscellaneous attributes . . . and that by Variation any of these attributes may be subtracted or any other attribute added in indefinite proportion" (Bateson 1894, p. 80)
Bateson's view was that, if we wish to understand evolution, we must move beyond speculative reconstructions of past events based on assuming variability and then assuming some adaptive rationale, and start studying what variations actually tend to occur. In pursuit of a less speculative approach to evolution, Bateson traveled the world to catalog 886 cases of discontinuous variation, published in his volume "Materials for the Study of Variation" (Bateson 1894); he planned a second volume on continuous variation but never completed it. Morgan argued that "even the smallest changes that add to or subtract from a part in the smallest measurable degree" may arise by mutation, and these are "the most probable variants that make a theory of evolution possible" (Morgan 1925, p. 129).
Both senses of "discontinuity" represent departures from late-19th-century and 20th-century versions of Darwinism. The mechanistically discretized view of the mutationists clashed with the incipient Modern Synthesis view in Punnett's (1930) Nature review of Fisher's The Genetical Theory of Natural Selection:
Throughout the book one gets the impression that Dr. Fisher views the evolutionary process as a very gradual, almost impalpable one, in spite of the discontinuous basis upon which it works. Perhaps this is because he regards a given population as an entity with its own peculiar properties as such, whereas for the geneticist it is a collection of individuals.
Much of the neo-Darwinian antipathy to "mutationists" was based on a negative reaction to the "saltationism" of de Vries and Goldschmidt, even though their views do not represent a shared commitment of the Mendelians. However, the mere fact that the Mendelians allowed some large changes distinguished them from the Darwinian view that "Natural selection can act only by the preservation and accumulation of infinitesimally small inherited modifications" (Darwin, Ch. 4, Origin of Species).
Creativity
The mutationists held that "the function of natural selection is selection and not creation. It has nothing to do with the formation of new variation" (Punnett 1911). Likewise, Bateson (1909) writes:
"we must relegate Selection to its proper place. Selection permits the viable to continue and decides that the nonviable shall perish; just as the temperature of our atmosphere decides that no liquid carbon shall be found on the face of the earth: but we do not suppose that the form of the diamond has been gradually achieved by a process of Selection. So again, as the course of descent branches in the successive generations, Selection determines along which branch Evolution shall proceed, but it does not decide what novelties that branch shall bring forth."
The creativity of mutation or, more properly, of mutation-and-altered-development (Stoltzfus, 2006), may be illustrated (in the extreme case) by Goldschmidt's concept of a "macromutation", akin to Galton's concept (invoked repeatedly by Bateson, 1894) of a shift between "positions of organic stability". If a variant toad arises with fully formed eyes in the roof of its mouth, such that it must open its mouth to see— as in the actual toad pictured on p. 97 of Dawkins (1996)— this is an extreme yet coordinated change, and a "macromutation" if it is heritable. If such a variant supplants the parental form or becomes a separate species, this is a non-Darwinian, saltational change in which creativity is due largely to mutation-and-altered-development. In the case of less dramatic transformations, the creative role of mutation-and-altered-development is correspondingly less dramatic.
In spite of Goldschmidt's notorious belief that distinctive phenotypic transformations suggested major genetic reorganizations ("systemic mutations"), he insisted that the complexity of the underlying genetic change is not the decisive issue:
It does not make any difference whether a single macroevolutionary step is caused by a major change within the chromosomal pattern, [that is,] a systemic mutation, or by a special kind of gene mutation with generalized effect, if such is imaginable. The decisive point is the single change which affects the entire reaction system of the developing organism simultaneously, as opposed to a slow accumulation of small additive changes. (Goldschmidt 1940, p. 251)
The claim that selection is creative is one of the key claims of Darwinism, advanced and defended by supporters of Darwinism, and rejected by its critics, as Gould (1977) documents extensively. We see this argument arising again and again up to the present day, e.g., the authors of a recent "evo-devo" book echo the century-old rhetoric of Mendelians, claiming that selection is not creative and is merely a "sieve" (Kirschner and Gerhardt, 2005), and in response (in the Nature review of this book), a dyed-in-the-wool Darwinist defends the ancient orthodoxy that selection is creative (Charlesworth, 2005). Later on, we will devote an entire post (probably more than one) to the Darwinian doctrine of selective creativity, and its relation to the Darwinian doctrine known as "gradualism".
Directionality
On a one-dimensional scale of fitness or adaptedness, every change is either "up" (beneficial) or "down" (deleterious), but in a multi-dimensional space of phenotypes, every change has a distinctive direction.
Punnett invoked mutation as a source of direction in considering features such as lepidopteran wing patterns (Punnett 1911, p. 145). A more typical statement was to draw a contrast with the views of Weissman, Fisher, and others who imagine variation in all directions. For instance, in the book review cited earlier, Punnett (1930) chides Fisher for denying to mutations "any importance in determining the direction of evolutionary change"; likewise Shull takes aim at Fisher's view:
"To assert, as Fisher does, that mutation has nothing to do with the direction of evolution is like assuming that a tetrahedron may fall, at different times, with ten or a hundred points uppermost. The ten points and ten opposite sides to fall upon do not exist. How great a restriction is placed upon the course of evolution by the inability of genes to mutate in certain ways it is impossible to tell; but it may easily be much greater than any of us suppose." (Shull, 1936, p. 448)
A clearer Mendelian concept of the influence of mutation emerges in regard to parallel evolution, which was assumed to indicate non-random tendencies of variation, since "it strains one's faith in the laws of chance to imagine that identical changes should crop out again and again if the possibilities are endless and the probabilities equal" (Shull 1935, p. 448). Vavilov noted that the same varieties or polymorphisms often occur in parallel, even in distantly related species in the same genus or family, and he argued for a causal role of this "law of homologous variation" (Vavilov 1922) in parallel evolution. As an example, Vavilov reports that lentils (Ervum lens), a food crop, and vetch (Vicia sativa), a weed, have many homologous variations, and notes that vetches sometimes mimic lentils so closely in cultivated fields that their seeds cannot be separated by mechanical sorters:
the role of natural selection in this case is quite clear. Man unconsciously, year after year, by his sorting machines separated varieties of vetches similar to lentils in size and form of seeds, and ripening simultaneously with lentils. The same varieties certainly existed long before selection itself, and the appearance of their series, irrespective of any selection, was in accordance with the laws of variation. (Vavilov 1922, p. 85)
Darwin preceded Vavilov in recognizing a principle of "analogous variation" due to a similar "inherited constitution", but denied it any influence on evolutionary change:
But characters thus gained [by analogous variation] would probably be of an unimportant nature, for the presence of all important characters will be governed by natural selection, in accordance with the diverse habits of the species, and will not be left to the mutual action of the conditions of life and of a similar inherited constitution. (ch. 5, Darwin 1859)
That is, while we might recognize a kind of dualism in Darwin's view, in the sense that both fluctuation and selection are required for change as opposed to non-change, Darwin insists that selection "governs" the course of evolution, over-ruling variation. Darwin's followers, likewise, emphasize that selection, while not sufficient to cause change by itself, is the proper cause of the manner of change (that is, its directionality, dynamics, creativity, and so on). Darwin's followers have an ideological commitment to giving selection a power to control or dominate "random" mutation, and a commitment to denying internal causes of direction in evolution (if you have these commitments, you are probably a Darwinian; if you don't, you are not— or maybe you're just confused). The Mendelians did not share these ideological commitments.
Nonetheless, the Mendelians were a long way, as we still are, from having a clear view of this issue. Shull once remarked "What the world most needs, then, is not a good five-cent cigar, but a workable— and correct— theory of orthogenesis" (p. 449), "orthogenesis" being the idea of a trend or direction due to intrinsic tendencies of variation. The Mendelians did not develop such a theory. In spite of knowing that some variations occur more often than others, they often spoke as though any conceivable variation were either possible or impossible, which I see— and I see it almost everywhere— as a sign of immature thinking on this topic.
Of course, we are not much better off today. The evo-devo field clearly needs an idea of developmental tendencies in variation as a source of direction, and leading thinkers have called (vaguely) for such an idea for 30 years, but the evo-devo field still has no theory and instead is schlepping around its clunky old "toolbox" metaphor. Apparently, this toolbox contains the tools that selection uses to build structures, revealing that evo-devoists remain Darwinians who personify selection as a craftsman. Elsewhere (Stoltzfus, 2006; Stoltzfus and Yampolsky, 2009; online source), I have argued that we manifestly need a causal theory of orthogenesis, linking tendencies of variation to tendencies of evolution, and I have outlined the conceptual and mechanistic basis for such a theory, including population-genetics modeling.
In a series of later posts, we will take up the issue of "source laws and consequence laws" of variation, i.e., source laws governing the emergence of variation, and consequence laws governing its influence on evolutionary change.
Synopsis
Upon the discovery of genetics in 1900, a new breed of scientists rejected Darwin's theory and began developing a new understanding of evolutionary change based on Mendelian principles. They combined genetics with Darwin's principle of selection, but departed from Darwin's view in arguing that evolutionary change is not composed entirely of infinitesimal increments, and in representing mutation as a source of discontinuity, directionality, creativity and initiative.
Yet, somehow, "Darwinism" returned in the form of the Modern Synthesis. This new view included all the principles of Mendelian genetics, yet rejected all the non-Darwinian innovations of the Mendelians. The restoration of Darwinism in the Modern Synthesis— an accomplishment based more on rhetorical sleight-of-hand than on population genetics theory— will be our topic next time.
References
Bateson, W. 1894. Materials for the Study of Variation, Treated with Especial Regard to Discontinuity in the Origin of Species. Macmillan, London.
Bateson, W. 1900. Problems of Heredity as a Subject for Horticultural Investigation. Journal of the Royal Horticultural Society 25:54-61.
Bateson, W. 1902. Mendel's Principles of Heredity: A Defense. Cambridge University Press, Cambridge.
Bateson, W. 1909. Heredity and Variation in Modern Light. Pp. 85-101 in A. C. Seward, ed. Darwin and Modern Science: Essays in Commemoration of the Centenary of the Birgh of Charles Darwin and of the Fiftieth Anniversary of the publication of the Origin of Species. Cambridge, London.
Bateson, W., and E. R. Saunders. 1902. Experimental Studies in the Physiology of Heredity. Reports to the Evolution Committee. Royal Society.
Charlesworth, B. 2005. On the Origins of Novelty and Variation. Science 310:1619-1620.
Dawkins, R. 1996. Climbing Mount Improbable. W.W. Norton and Company, New York.
De Vries, H. 1905. Species and Varieties: Their Origin by Mutation. The Open Court Publishing Company, Chicago.
Goldschmidt, R. 1940. The Material Basis of Evolution. Yale University Press, New Haven.
Gould, S. J. 1977. Ever Since Darwin. W.W. Norton & Co., New York.
Kirschner, M. W., and J. C. Gerhart. 2005. The Plausibility of Life: Resolving Darwin's Dilemma. Yale University Press, New Haven.
Johannsen, W. L. 1903. Erblichkeit in Populationen und in reinen Linien. Gustav Fischer, Jena.
Mayr, E. 1963. Animal Species and Evolution. Harvard University Press, Cambridge, Massachusetts.
Morgan, T. H. 1903. Evolution and Adaptation. Macmillan, New York.
Morgan, T. H. 1916. A Critique of the Theory of Evolution. Princeton University Press, Princeton, NJ.
Morgan, T. H. 1925. Evolution and Genetics. Princeton University Press, Princeton.
Morgan, T. H. 1932. The Scientific Basis of Evolution. W.W. Norton & Co., New York.
Punnett, R. C. 1911. Mendelism. MacMillan.
Punnett, R. C. 1915. Mimicry in Butterflies.
Punnett, R. C. 1930. Genetics, Mathematics, and Natural Selection. Nature 126:595-597.
Shull, A. F. 1936. Evolution. McGraw-Hill, New York.
Stoltzfus, A. 2006. Mutationism and the Dual Causation of Evolutionary Change. Evol Dev 8:304-317.
Stoltzfus, A., and L. Y. Yampolsky. 2009. Climbing mount probable: mutation as a cause of nonrandomness in evolution. J Hered 100:637-647.
Vavilov, N. I. 1922. The Law of Homologous Series in Variation. J. Heredity 12:47-89
Footnotes
1 Although de Vries continued to promote his "MutationsTheorie" for some years after 1900, it actually was a 19th-century theory of species-selection based on his work on Oenothera varieties, not on his work as one of the 3 re-discoverers of Mendel's principles.
2 The perceived need for a dominant GUTE, and the ideological immunity that develops around a dominant GUTE, are issues that we will address in a future post.
Credits: The Curious Disconnect is the blog of evolutionary biologist Arlin Stoltzfus, available at www.molevol.org/cdblog. An updated version of the post below will be maintained at www.molevol.org/cdblog/mutationism_myth4 (Arlin Stoltzfus, ©2010)
