This is the eighth 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. Part five is The Mutationism Myth, IV: Mendelian Heterodoxies. The sixth installment was The Mutationism Myth, V: The response to Mendelian heterodoxies.Today on The Curious Disconnect (credits), we wrap up our 6-part series on the Mutationism Myth, and set the stage for the future by locating the primary weakness of the 20th century neo-Darwinian consensus in its theory of variation.
I'd like to thank Larry Moran for hosting this series of posts on Sandwalk. If it still seems like a good idea later in the year, I will continue the Curious Disconnect on my own blog site (to be announced).
The Mutationism Myth, a story about how the discovery of genetics affected evolutionary thought, continues to be part of modern neo-Darwinism's monologue with itself (e.g., Charlesworth and Charlesworth, 2009), being used even by leading thinkers calling for an "Extended" Synthesis (e.g., Pigliucci, 2010 1). Since April, we've been deconstructing the Mutationism Myth by exploring what the early Mendelians actually thought, and how their view was replaced by the Modern Synthesis (MS).
Today we'll take the opportunity to review what we've learned and start unpacking its relevance for the future of evolutionary biology.
In the Mutationism Myth (see part 1 for examples), the founders of genetics misinterpret their discovery, concluding that evolution takes place by large mutational jumps, without selection. The false gospel of these "mutationists" brings on a dark period of confusion and error that lasts until the 1930s, when theoretical population geneticists (Fisher, Haldane and Wright) prove that Mendelian genetics is not only compatible with selection, but provides the missing link that completes Darwin's theory and unites all the biological disciplines. The "Modern Synthesis" combining genetics and selection becomes the foundation for all subsequent evolutionary thought.
As we discovered, the Mutationism Myth isn't very accurate. Heredity is not missing from Darwin's theory; selection is not missing from the Mendelian view. Darwin had a theory of heredity both in the sense of a set of phenomenological laws, and in the sense of a mechanism to account for them (part 2). Both were wrong. The Mendelians synthesized genetics and selection, rejecting Darwin's "Natural Selection" theory due to its dependence on fluctuations or "indefinite variability" (defined by Darwin as the subtle variations that arise anew each generation in response to conditions of life). As we know today, such enrivonment-induced fluctuations are non-heritable.
In part 3, we found that the Mendelians laid the conceptual foundations of evolutionary genetics (later formalized mathematically), while part 4 addressed how their view diverged from Darwinian orthodoxy. The Mendelians assumed that new hereditary variants arise rarely and discretely, by mutations whose effects may be large or small. Each new mutation is likely to be rejected, but it may be accepted by chance, especially if it improves fitness. Because, in this view, change depends on discrete events of mutation, the Mendelians (part 4) considered the process of mutation to be a source of initiative, discontinuity, creativity and direction in evolution (Stoltzfus, 2006). This view expanded the role of variation well beyond the subordinate role of raw materials that Darwin had imagined.
The Mendelians were unable to convince naturalists (the majority of their biologist peers) to accept their new view of evolution, nor even a new view of inheritance. Many naturalists remained wedded to Lamarckian and Darwinian views of "soft inheritance".
As we found out in part 5, the "Modern Synthesis" (modern neo-Darwinism) claimed to reconcile Darwin's own view with genetics, though it quietly ignored Darwin's errors while depicting the Mendelians as foolish "saltationists", dismissing their "lucky mutant" view and their ideas about the role of mutation in evolution. In the MS view, each species has a "gene pool" that automatically soaks up and "maintains" hereditary variation, providing abundant "raw materials" for adaptation. The key innovations of this view were to define "evolution" as "shifting gene frequencies" in the "gene pool", to erase the link between "Darwinism" and Darwin's own theory of soft inheritance, and to develop a theory of causation in terms of population-genetic "forces", in which continuous shifts in allele frequencies are the common currency of causation. The new theory put mutation in a subordinate position of supplying infinitesimal "raw materials" for selection. As a result, the MS created a consensus where the Mendelians had failed: naturalists such as Ernst Mayr found that they could accept Mendelian genetics without giving up adaptationist preconceptions.
The backdrop for this whole discussion (in case you missed it) is that the MS is strikingly wrong in its neo-Darwinian departures from the Mendelian view. I've implied this several times, and perhaps I've waved my hands and pointed vaguely to mountains of molecular evidence contradicting the MS, but I haven't made this point perfectly clear.
In a moment, I will do that, but first I want to make clear what is at stake.
The Mendelians allowed that evolutionary change could be initiated by an event of mutation, and they interpreted this to mean that mutation was (to an unknown degree) a source of initiative, discontinuity, creativity and direction in evolution. The MS represents a very deliberate rejection of this view, and proposes instead that evolution is a complex sorting out of available variation to achieve a new multi-locus equilibrium, literally by "shifting gene frequencies" in the "gene pool". The rate of evolution, in this view, does not depend on mutation, which merely supplies the "gene pool" with variation; evolution is not shaped by mutation, which is the "ultimate" source of variation, but not the proximate source.
When I made this distinction at a 2007 symposium in honor of W. Ford Doolittle, Joe Felsenstein was in the audience and pointed out that, while Fisher may have looked at things in this way, Wright's stochastic view took into account random events, like new mutations. It's true that Wright's "shifting balance" model assigns a prominent role to random genetic drift, while Fisher's view was deterministic. However, these are just two different flavors of the same "shifting gene frequencies" paradigm: neither view incorporates new mutations. The absence of new mutations from Wright's shifting balance process is apparent from the fact that Patrick Phillips (1996) extended it to include a new starting phase ("phase 0") of "waiting for a compensatory mutation".
The fact that contemporary evolutionary biologists, for the most part, don't understand this aspect of their intellectual heritage is not evidence of a cover-up. Scientists don't get much chance to learn history. The history that they absorb is mainly from stories that appear in scientific writings, like the Mutationism Myth and the Essentialism Story, stories that represent Synthesis Historiography (Amundsen, 2005), the discipline of telling history in ways that make things turn out right for the Modern Synthesis. Synthesis Historiography teaches us that "saltationism" (Mayr's pejorative term for the Mendelian view) and other alternatives to neo-Darwinism are nonsensical, "doomed rivals", supported only by "typologists", creationists, vitalists and other crazies. That is, Synthesis Historiography teaches the TINA doctrine: There Is No Alternative.
As contemporary research drifts away from the "gene pool" theory and the Darwinian doctrines of the MS, each evolutionary biologist remains confident that, due to the TINA doctrine, his own view must be "neo-Darwinian". In reality, alternatives are being explored with increasing vigor in molecular evolution, evo-devo, and evolutionary genetics.
A few folks today are in the reverse situation of being familiar with MS orthodoxy, but not with recent research. Dawkins (2007) stakes his critique of a book by "intelligent design" creationist Michael Behe entirely on his faith in the gene pool theory. Behe claims, in effect, that there was not sufficient time for all the mutations needed to account for evolution. Dawkins responds by attacking the premise that evolutionary rates depend on mutation rates:
"If correct, Behe's calculations would at a stroke confound generations of mathematical geneticists, who have repeatedly shown that evolutionary rates are not limited by mutation. Single-handedly, Behe is taking on Ronald Fisher, Sewall Wright, J.B.S. Haldane, Theodosius Dobzhansky, Richard Lewontin, John Maynard Smith and hundreds of their talented co-workers and intellectual descendants. Notwithstanding the inconvenient existence of dogs, cabbages and pouter pigeons, the entire corpus of mathematical genetics, from 1930 to today, is flat wrong. Michael Behe, the disowned biochemist of Lehigh University, is the only one who has done his sums right. You think? The best way to find out is for Behe to submit a mathematical paper to The Journal of Theoretical Biology, say, or The American Naturalist, whose editors would send it to qualified referees."
With his signature over-the-top rhetoric, Dawkins insists that "mathematical genetics" has proven that evolutionary rates are not limited by mutation. Allowing for some exaggeration, this is an accurate representation of MS orthodoxy ca. 1959, the approximate vintage of Dawkins's views. If Mayr had been alive, he might have said the same thing.
Meanwhile, no one who has been active in evolutionary genetics research in the past 15 years would represent the current state of knowledge in this way. If you want to know what a contemporary researcher would say, take a look at the most recent issue of Evolution in which the article by Douglas Futuyma (famous for his evolution textbook) gives many examples of how evolutionists (including himself) repeated the doctrine that mutation does not "limit" evolution, but argues that we are no longer making this dubious assumption. Another example would be the piece by Ronny Woodruff and James Thompson (1998) that introduces their symposium volume on Mutation and Evolution.2
Yet the MS and its "gene pool" theory have left their mark on evolutionary biology, even if the MS itself has largely disappeared from the collective memory of researchers. One indelible mark is what Gillespie calls "The Great Obsession" of population genetics to understand the "maintenance of variation", but that's a story for another day.
Another indelible mark is the long absence of mutationist models of "adaptation", a topic that has blossomed just in the last dozen years. Allen Orr has achieved well deserved fame for his innovations in this area, and we'll discuss his work briefly in the next section. For now, let us note how other researchers have pointed out the absence of such models:
"Almost every theoretical model in population genetics can be classified into one of two major types. In one type of model, mutations with stipulated selective effects are assumed to be present in the population as an initial condition . . . The second major type of models does allow mutations to occur at random intervals of time, but the mutations are assumed to be selectively neutral or nearly neutral." (Hartl & Taubes, 1998)
"The process of adaptation occurs on two timescales. In the short term, natural selection merely sorts the variation already present in a population, whereas in the longer term genotypes quite different from any that were initially present evolve through the cumulation of new mutations. The first process is described by the mathematical theory of population genetics. However, this theory begins by defining a fixed set of genotypes and cannot provide a satisfactory analysis of the second process because it does not permit any genuinely new type to arise. " (Yedid and Bell, 2002)
These authors are not trying to make a point about history or about the Modern Synthesis: they are simply claiming the novelty of their own models of adaptation that incorporate new mutations. And what they are saying is that the paradigm of 20th-century population genetics is "shifting gene frequencies": overwhelmingly, it's a body of theory about what happens to the variation that is present in a population as an initial condition, not about a larger-scale process in which there are new beneficial mutations.3
The actual role of mutation in evolution is not what is theorized in the MS. Many arguments could be made to support this contention, but I'm going to make just one argument drawing on one source, namely Rokyta, et al., 2005. I choose this argument because it is particularly compelling and concise. My argument addresses the lucky mutant view of initiative or (to put it another way) dynamics.
Rokyta, et al. is a study of parallel evolution in an experimental population of the bacteriophage phiX174, published in Nature Genetics. It was hailed as "the first empirical test of an evolutionary theory" (Bull & Otto, 2005), where the theory in question is Orr's (2002) ingenious extension of Gillespie's (1984) "mutational landscape" model to take into account predictions of extreme value theory.4
In spite of the fancy name, the "mutational landscape" model of sequence evolution is simple. Rather than considering all conceivable evolutionary changes from a starting sequence, we simplify the problem by considering only changes that occur via 1-bp mutations. That set of possibilities, by definition, is the "mutational landscape" or (my preferred term) the "evolutionary horizon". Each change will shift the evolutionary horizon, but it's easy to recompute the horizon, because it's easy to enumerate (theoretically) all the alternative sequences.
We are going to make this a model of beneficial changes ("adaptation"). A beneficial mutation is introduced into the population of N individuals at some total rate Nu, and faces acceptance with a probability of 2s, based on the classic formula p = 2s for the probability of fixation of a new beneficial mutation.5 For beneficial substitution i with selection coefficient si, the probability6 is just Nu*2si. If we divide an individual Nu*2si by the sum of all such values on the horizon, we get a normalized probability: the probability that the next step in our evolving system is step i. The factor Nu*2 is the same for every step, so it cancels out: only the si values matter. To evolve our sequence, we just sample from this probability distribution of possible steps, then recompute the new evolutionary horizon in preparation for the next step. Easy! 7
From past experiments, Rokyta, et al. know which steps on the horizon are beneficial, and they even know the selection coefficients. They know that sometimes, the same evolutionary steps happen in parallel, in replicate phage populations. They can compare the observed pattern of parallel evolution with the pattern predicted from theory.
Now, the preceding description suggests something fascinating: the cutting edge of evolutionary genetics today, with papers that get published in Nature Genetics with commentaries, uses experimental systems to explore the "lucky mutant" view of parallel evolution.
But the story gets even better. Rokyta, et al actually reject Orr's model, in its original version. They find more parallel evolution than expected. Why? Because the model treats all mutation rates equally. Note above that we canceled out mutation rates on the grounds that they are all the same. But that's not realistic. Some mutations are more likely than others, and this will affect the rate at which they are introduced into the population and subjected to acceptance or rejection. The more heterogeneity in rates of mutation, the more parallel evolution. Rokyta, et al. found that if they revised the model to take into account transition:transversion bias (I think it's about 5-or 6-fold under the experimental conditions), then the predicted amount of parallelism matched the observed amount.
Just let that soak in for a moment. We have an experimental study and a precise model. Evolution in this model is characterized by origin-fixation dynamics, dependent on the rate of mutational introduction of new alleles, and on their probability of fixation. Both factors affect the outcome of evolution; both factors affect the chance of parallelism. The experimental study eliminates (statistically) a model that lacks mutational bias in the introduction of new alleles. Thus the study clearly illustrates the dual causation of evolutionary change, in regard to its dynamics.
The MS is wrong, and not in a small way: it's wrong because reality just looks too much like the antithesis of the MS, i.e., the mutationist view. For instance, as we found out in part 4, Vavilov (1922; see Stoltzfus, 2006) understood the dual causation of parallel evolution, including the role of parallel variation. By contrast, Mayr famously said that the search for homologous genes or homologous mutations was foolish.
This mistaken prediction is repeated ad nauseam in the evo-devo literature. If you have been following along, you now understand why Mayr would make such a prediction. The MS makes substantive claims about evolution, among which are the claim that, while mutation is ultimately necessary to keep the "gene pool" from drying up, selection doesn't need to wait for a new mutation, but draws together a multi-locus optimum from the abundance of raw materials in the gene pool; "evolution" is so far removed from the process of mutation, with so many complex dynamic processes interceding, that the outcome of evolution does not depend on specific events of mutation. If evolution really were like that, parallel mutation would be unimportant. That is, Mayr's prediction accurately reflects the logic of the MS. But as the Rokyta, et al study (and many others) show, the prediction is not fulfilled.
According to Dawkins, "the entire corpus of mathematical genetics" from 1930 to "today" (i.e., about 1959, for Dawkins) would be "flat wrong" if one accepts the premise that evolution depends on new mutations, or that it is limited by the mutation rate. While this view is not often defended, that isn't because it's Dawkins's own personal opinion. Dawkins is accurately characterizing a theory that makes substantive claims about the world, a theory that most of us have forgotten. One of these claims is that "evolution" can be represented mathematically as a process of shifting the frequencies of alleles already present in an initial population, without new mutation; sometimes this doctrine is invoked by saying that "macroevolution" can be extrapolated from "microevolution".
If evolution actually worked like this, then evolutionary change would not exhibit a dependence on the rate of mutation, and Dawkins would be right in his criticism of Behe. But this is wrong. In fact, the dependence is so sensitive that effects of only a few-fold are noticeable, as the Rokyta, et al study (and many others) shows.
I'm not going to mince words. The MS is wrong, and not in a small way: reality looks too much like the mutationist view that we (the scientific community) rejected when we bought into the MS. We need another theory1, perhaps several others.
What's wrong about the MS, and what its replacement(s) must replace, is its theory of the role of variation in evolution. In future posts on the Curious Disconnect, I intend to focus on this issue. The Mutationism Myth suggests a lesson about how to develop (or rather, how not to develop) a theory of variation.
Darwin knew that hereditary variation played a vital role in evolution. He studied the subject intensely. He found that organisms vary in many different ways, and on many scales, but the evidence on heredity was bewildering and inconclusive. Lacking the means to derive a mechanism of evolution by reasoning upward from genetics, Darwin reasoned downwards from his premises that 1) organisms are exquisitely and pervasively adapted to their niches, 2) selection must have played some role in this, and 3) Mother Nature never makes a jump. Gould argues that Darwin's willingness to posit precise restrictions on variation was a stroke of genius.8 Darwin knew that discrete "sports" (mutants) could be heritable, but he discounted them: they could not make his theory work as desired. Instead, he staked his "natural selection" theory on the heritability of fluctuations, because they were infinitesimal, indefinite (unbiased), and "everywhere present", being induced in abundance whenever organisms encountered altered "conditions of life". Inferring the heritability of fluctuations completed his theory and made it work.
But it was wrong: the fluctuations that made Darwin's theory work are non-heritable, as the Mendelians discovered.
The architects of the MS tried again, with advantages unavailable to Darwin. Not only did they know genetics, they had some mathematical tools to work out unforeseeable implications of genetic concepts. However, they didn't have the knowledge to distinguish among different, genetically consistent modes of evolution. They had to fill in this gap somehow. Their downwards Darwinian reasoning and their upwards Mendelian reasoning met in the middle with the "gene pool": a theory of population genetics that would supply abundant, infinitesimal, "random" variations, in order to rationalize their commitment to the same premises Darwin accepted. That was the genius of the MS.
But again, it was wrong.
If we look at Darwinism in Popperian terms, as a theory1 that takes risks and generates potentially falsifiable claims, then (counterintuitively) it is largely a theory of the role of variation in evolution. The claims that selection is "important", and that it has some inalienable role in adaptation, carry little risk and have been widely accepted for 150 years. By contrast, the restrictions that Darwinism places on variation, in order to make it a subordinate factor that supplies "raw material" to selection, are risky and controversial, e.g., the claim that variation is random with respect to the direction of evolution, or that the rate of evolution does not depend on the rate of mutation, or the "gradualist" claim that variation is not a source of discontinuity. The architects of the MS invested the "gene pool" with nearly magical properties in order to improve the prospects for adaptation. Problematic claims about the role of variation are, and have been for 150 years, the overwhelming basis for scientific criticism of Darwinism.
And this problematic view of variation is based on reasoning from the premise that organisms are exquisitely and pervasively adapted to their niches, to the conclusion that variation must play just the right role of supplying abundant raw materials to make this possible. I believe that there is something fundamentally wrong with this mode of reasoning. Perhaps it betrays a kind of subconscious Panglossian agenda. Every time I give a lecture on mutation-biased evolution, someone suggests that perhaps the mutation biases themselves are adaptive, as though this inference could restore one's faith that everything turns out for the best, and that "the ultimate source of explanation in biology is the principle of natural selection" (Ayala, 1970). Remarkably, the evo-devo-inspired view that seems destined for inclusion in the emerging "Extended Synthesis" is headed down much the same path, with a focus on the idea that the process of variation has been jiggered to make things turn out right for adaptation. What's revealing about this new view is how little attention its proponents have paid to understanding precisely, in terms of population-genetic causation, how the process of variation shapes evolution, before jumping ahead to the shadowy inference that the process of variation itself was shaped by selection for this very role.
We are not going to go down that same road here on the Curious Disconnect, which should make things all the more interesting.
Ayala, F. J. 1970. Teleological Explanations in Evolutionary Biology. Philosophy of Science 37:1-15.
Bull, J. J., and S. P. Otto. 2005. The first steps in adaptive evolution. Nat Genet 37:342-343.
Charlesworth, B., and D. Charlesworth. 2009. Darwin and genetics. Genetics 183:757-766.
Dawkins, R. 2007. Review: The Edge of Evolution. Pp. 2. International Herald Tribune, Paris.
Gould, S. J. 2002. The Structure of Evolutionary Theory. Harvard University Press, Cambridge, Massachusetts.
Hartl, D. L., and C. H. Taubes. 1998. Towards a theory of evolutionary adaptation. Genetica 103:525-533.
Medawar, P. B. 1967. The Art of the Soluble. Methuen and Co., London.
Nei, M. 2007. The new mutation theory of phenotypic evolution. Proc Natl Acad Sci U S A 104:12235-12242.
Orr, H. A. 2002. The population genetics of adaptation: the adaptation of DNA sequences. Evolution Int J Org Evolution 56:1317-1330.
Phillips, P.C. 1996. Waiting for a compensatory mutation: phase zero of the shifting-balance process. Genetical Research, Cambridge 67:271-283.
Rokyta, D. R., P. Joyce, S. B. Caudle, and H. A. Wichman. 2005. An empirical test of the mutational landscape model of adaptation using a single-stranded DNA virus. Nat Genet 37:441-444.
Woodruff, R. C., and J. D. Thompson. 1998. Preface in R. C. Woodruff, and J. D. Thompson, eds. Mutation and Evolution. Kluwer, Dordrecht, The Netherlands.
Yedid, G., and G. Bell. 2002. Macroevolution simulated with autonomously replicating computer programs. Nature 420:810-812.
1 Pigliucci, along with Gerd Muller, edited a book on "the extended Synthesis" with papers from a select group of thinkers who were invited in July, 2008 to a special meeting in Altenberg, Austria. The book is now available in paperback: http://www.amazon.com/Evolution-Extended-Synthesis-Massimo-Pigliucci/dp/0262513676
2 from p. 1 "Although mutation is a key parameter in the genetics of populations, the role of mutation as an evolutionary factor has been debated since the time of Darwin. Early geneticists, who held to the 'classical' view of the genome as being homogeneous with occasional mutant alleles, saw new mutation as a major determining force in adaptive change. When the classical view was replaced with the 'balance' view of the genome, i.e., highly heterogeneous, pre-existing variation became more important as the resource on which selection would act. Many, therefore, began to disregard new mutation as a significant force in evolution, since the level of genetic diversity is already so high that new mutants would generally be expected to add little to that resource . . . Mechanisms responsible for maintaining levels of genetic diversity became the focus of attention, and mutation pressure is now thought by many to have only minor significance, especially when compared to selection, recombination, gene flow, and similar factors. We think this position, like the classical view, is too extreme. While there can be little doubt that mutation per se is not the principle driving force it was once believed to be for phenotypic evolution, we see growing evidence that its role is under-appreciated in important situations. The rate and pattern of mutation can be influenctial variables in adaptive responses, and the role of mutation in evolution deserves to be reexamined."
3 Orr (2002) notes the absence of such models by making a far more sweeping claim that population genetics has ignored, not just new-mutations models of adaptation, but all models of adaptation, and instead has focused on neutral and deleterious alleles. That is an odd thing to say, given that the quantitative genetics of adaptation have been a topic for a long time. In any case, here is what Orr says: "Evolutionary biologists are nearly unanimous in thinking that adaptation by natural selection explains most phenotypic evolution within species as well as most morphological, physiological, and behavioral differences between species. But until recently, the mathematical theory of population genetics has had suprisingly little to say about adaptation. Instead, population genetics has, for both historical and technical resasons, focussed on the fates of neutral and deleterious alleles. The result is a curious disconnect between the verbal theory that sits at the heart of neo-Darwinism and the mathematical content of most evolutionary genetics. "
4 Also known as the theory of records—"record" in the sense of "pinnacle of achievement". Given a series of records, such as the world record in the long-jump, what's the interval of time to the next record, and by how much will it break the previous record? The theory of records addresses such questions. Can you see how this would be useful to make a predictive theory of adaptation?
5 Rokyta, et al. used a different formula for the probability of fixation, because the classic approximation only works for s << 1, whereas the phiX174 populations experience very large s, sometimes s > 1.
6 Formally Nu*2si is not a probability but a steady-state rate (e.g., for an infinite-alleles model). If we treat it as an instantaneous rate, and then compare it to all other instantaneous rates, this makes it a relative probability of choosing step i over a short interval.
7 For our present purposes, we don't need to explain Orr's addition to this model, which was a theory of the distribution of the favorable s values under generalized assumptions (oddly, the commentators on Rokyta, et al. did not mention that Orr's theory wasn't really needed, and that the study really was a test of the mutational landscape model itself).
8 Gould (2002, p. 140) is not endorsing Darwin's error about fluctuation. Darwin's followers think of that mistake as a trivial detail. Instead Gould is endorsing a more general inference. Here is what he writes. "Darwin reasoned that natural selection can only play such a role [as exclusive source of creativity and direction] if evolution obeys two crucial conditions: (1) if nothing about the provision of raw materials—that is, the sources of variation—imparts direction to evolutionary change; and (2) if change occurs by a long and insensible series of intermediary steps, each superintended by natural selection—so that "creativity" or "direction" can arise by the summation of increments.
Under these provisos, variation becomes raw material only—an isotropic sphere of potential about the modal form of a species. Natural selection, by superintending the differential preservation of a biased region from this sphere in each generation, and by summing up (over countless repetitions) the tiny changes thus produced in each episode, can manufacture substantial, directional change. What else but natural selection could be called 'creative,' or direction-giving, in such a process? As long as variation only supplies raw material; as long as change accretes in an insensibly gradual manner; and as long as the reproductive advantages of certain individuals provide the statistical source of change; then natural selection must be construed as the directional cause of evolutionary modification.
These conditions are stringent; and they cannot be construed as vague, unconstraining, or too far in the distance to matter. In fact, I would argue that the single most brilliant (and daring) stroke in Darwin's entire theory lay in his willingness to assert a set of precise and stringent requirements for variation—all in complete ignorance of the mechanics of heredity. Darwin understood that if any of these claims failed, natural selection could not be a creative force, and the theory of natural selection would collapse. "
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_myth6 (Arlin Stoltzfus, ©2010)
This is the seventh 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. Part five is The Mutationism Myth, IV: Mendelian Heterodoxies."evolution is not primarily a genetic event. Mutation merely supplies the gene pool with genetic variation; it is selection that induces evolutionary change" (Mayr 1963, p. 613).Rates and propensities of mutation are rendered irrelevant, because the "gene pool" serves as a dynamic buffer that insulates evolution from mutational effects:
"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 . . . . 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." (Stebbins, 1966, p. 29)
"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 introduced mutations would represent only a very small fraction of the variation present at any one time in populations of outcrossing, sexually reproducing organisms." (Dobzhansky, et al., 1977, p. 72) 2
"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." (Mayr, 1994, p. 38)Thus, Darwin's view of a process initiated by a change in conditions is restored: the source of initiative is not the occurrence of mutations, which are individually insignificant (Dobzhansky et al. 1977, p. 72) and merely "replenish the supply of variability in the gene pool" (Stebbins 1966, p. 29), but the change in conditions that brings on selection of variation already present (e.g., Dobzhansky 1955, p. 282; Dobzhansky et al. 1977, p. 6; e.g., Stebbins 1982, p. 160).
If it could be demonstrated that any complex organ existed, which could not possibly have been formed by numerous, successive, slight modifications, my theory would absolutely break down. (Darwin, Ch. 6, Origin)The "saltationist" alternative typically offered to this doctrine, as stated by Huxley in his 1860 review of the Origin of Species (online source), is merely that evolution takes some jumps:
Mr. Darwin's position might, we think, have been even stronger than it is if he had not embarrassed himself with the aphorism, "Natura non facit saltum," which turns up so often in his pages. We believe, as we have said above, that Nature does make jumps now and then, and a recognition of the fact is of no small importance in disposing of many minor objections to the doctrine of transmutation.As we found out in part 4, the Mendelians sided with Huxley on this issue, and did not share Darwin's commitment to infinitesimalism.
"The high frequency of mutations producing small changes in the phenotype raises a strong presumption in favor of supposing that such mutations play a greater role in evolutionary processes than mutations with grosser effects. Fisher (1930) has given an interesting mathematical argument in favor of this view. These considerations agree very well with the results of the genetic analysis of the interracial and interspecific differences (Chapter III), showing these differences to be caused in a majority of cases by cooperation of numerous genes, each of which taken separately has only slight effects on the phenotype." (p. 26)I think this aspect of the MS is familiar and uncontroversial, so I won't bore the reader with more quotations from original sources, several of which are given in the review by Orr and Coyne (1992). In general, the architects of the MS emphasized the importance of "slight" or "small" differences, and they claimed that this position was borne out by theoretical considerations, as well as by experimental studies.
"But why was natural selection compared to a composer by Dobzhansky; to a poet by Simpson; to a sculptor by Mayr; and to, of all people, Mr. Shakespeare by Julian Huxley? I won't defend the choice of metaphors, but I will uphold the intent, namely, to illustrate the essence of Darwinism— the creativity of natural selection. Natural selection has a place in all anti-Darwinian theories that I know. It is cast in a negative role as an executioner, a headsman for the unfit . . . 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. It preserves favorable variants and builds fitness gradually. In fact, since artists fashion their creations from the raw material of notes, words, and stone, the metaphors do not strike me as inappropriate."Dobzhansky also invokes the same "raw materials" metaphor, but in the context of a factory rather than an artist:
"the objection [that natural selection cannot be the guiding agent in evolution because it produces nothing new] became invalid in the light of modern biological knowledge . . .We should clearly distinguish the two basic evolutionary processes: that of the origin of the raw materials from which evolutionary changes can be constructed, and that of building and perfecting the organic form and function. Evolution can be compared to a factory: any factory needs a supply of raw materials to work with, but when the materials are available they must be transformed into a finished product by means of some manufacturing process. " (Dobzhansky, 1955, p. 131)That is, selection is understood to be the builder or artist or manufacturing process, while mutation supplies "raw" materials. Note that Gould ultimately endorses the creativity claim precisely on the grounds that variation supplies raw material only. It might seem surprising that the metaphor of "raw materials" should play such an important role in evolutionary reasoning.
"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, 1958, p. 231)
"The idea that evolution comes about from the interaction of a stochastic and a directed process was the essence of Darwin's theory. The stochastic process that he invoked was the occurrence of small random variations which he supposed, provided the raw material for natural selection, a process directed by the requirements of the environment and one that builds up, step by step, changes that would be inconceivably improbable at a single step . . .The meaning of 'random' . . . is that the variations are, as a group, not correlated with the course subsequently taken by evolution (which is determined by selection)." (Wright, 1967, p. 117)As noted in part 4, the Mendelians were ready to challenge this assumption, though their alternative view was not well developed. Some Mendelians noted that the repeated occurrence of a mutation improved its chance of being established in evolution (part 4), and that "in the deal out of mutations, the cards are stacked" (Shull, 1936). Vavilov (1922) applied this line of thinking at length in his explication of a possible role for parallel variations in parallel evolution.
"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." (Dobzhansky, et al., 1977, p. 6)Note that Dobzhansky uses an analogy with statistical physics to argue that selection's unique role is due to its status as a high-level "force", whereas a "random variation" is not a force, but is like the movement of a single particle.
"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" (p. 31 Stebbins, 1966, Processes of Organic Evolution)Finally, given this position, its not surprising that Vavilov's hypothesis about the role of parallel variation in parallel evolution was not taken seriously. Given the abundance of variation in the "gene pool", and the ability of selection to shape this gene pool to fit circumstances, it was not safe to assume that shared characters had a shared genetic basis, as Mayr (1963) argued in one of his more famous erroneous claims 8:
"In the early days of Mendelism there was much search for homologous genes that would account for such similarities. Much that has been learned about gene physiology makes it evident that the search for homologous genes is quite futile except in very close relatives (Dobzhansky, 1955). If there is only one efficient solution for a certain functional demand, very different gene complexes will come up with the same solution, no matter how different the pathway by which it is achieved." (p. 609)
"The theory of evolution by natural selection is a theory that relates the variation between individuals within a population to variation of populations in time and space. The theory amounts, in short, to the realization that intrapopulation variation is converted into spatial and temporal differentiation. The process of this conversion is the process of evolution." (Lewontin, 1965, p. 67)That is, "the process of evolution" ("evolution by natural selection") literally does not include the introduction of new alleles, but instead corresponds to the sorting out of available variation.
"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" (Dobzhansky, 1955, p. 282)
"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." (p. 101 of Mayr, 1963)In this way, following the arguments of Fisher (1930), population genetics was believed to undermine any and all non-Darwinian theories of "evolution worked by mutation".
The genetic work of the last four decades has refuted mutationism (saltationism) so thoroughly that it is not necessary to repeat once more all the genetic evidence against it. (Mayr 1960, p. 355)
if ever it could have been thought that mutation is important in the control of evolution, it is impossible to think so now (Ford 1971, p. 361)
As late as 1932 T.H. Morgan was asserting that 'natural selection does not play the role of a creative principle in evolution', but ten years later all but a very few biologists were agreed on an evolutionary theory based firmly on Darwin's own ideas knitted with subsequent developments in genetics. (Berry 1982, p. 14)
for simplicity we speak of mutation as the first stage in the Darwinian process, natural selection as the second stage. But this is misleading if it suggests that natural selection hangs about waiting for a mutation which is then either rejected or snapped up and the waiting begins again. It could have been like that: natural selection of that kind would probably work, and maybe does work somewhere in the universe. But as a matter of fact on this planet it usually isn't like that. (Dawkins 1996, p. 87)
Adaptation is a two-step process: (i) alleles having different effects on fitness arise by mutation and (ii) those alleles that improve fitness tend to increase in frequency by natural selection.thus directly contradicting what Dawkins says (above) about evolution "on this planet" (which, I suppose, raises a question about where Dawkins was when he wrote that statement).
References
Beatty, J. 2010. Reconsidering the Importance of Chance Variation in M. Pigliucci, and G. MŸller, eds. Evolution: The Extended Synthesis.
Berry, R. J. 1982. Neo-Darwinism. Edward Arnold, Ltd., London.
Charlesworth, B. 2005. On the Origins of Novelty and Variation. Science 310:1619-1620.
Chetverikov, S. S. 1997. On Certain Aspects of the Evolutionary Process from the Standpoint of Modern Genetics. Genetics Heritage Press, Placitas, New Mexico.
Darlington, C. D. 1958. The Evolution of Genetic Systems. Basic Books, New York.
Dawkins, R. 1996. Climbing Mount Improbable. W.W. Norton and Company, New York.
Dobzhansky, T. 1937. Genetics and the Origin of Species. Columbia University Press, New York.
Dobzhansky, T. 1955. Genetics and the Origin of Species. Wiley & Sons, Inc., New York.
Dobzhansky, T., F. J. Ayala, G. L. Stebbins, and J. W. Valentine. 1977. Evolution. W.H. Freeman.
Fisher, R. A. 1930. The Genetical Theory of Natural Selection. Oxford University Press, London.
Ford, E. B. 1971. Ecological Genetics. Chapman & Hall, London.
Gould, S. J. 2002. The Structure of Evolutionary Theory. Harvard University Press, Cambridge, Massachusetts.
Gould, S. J. 1977. Ever Since Darwin. W.W. Norton & Co., New York.
Huxley, J. S. 1942. Evolution: The Modern Synthesis. George Allen & Unwin, London.
Kirschner, M. W., and J. C. Gerhart. 2005. The Plausibility of Life: Resolving Darwin's Dilemma. Yale University Press, New Haven.
Lewontin, R. C. 1965. The Gene and Evolution. Pp. 67-75 in R. M. Nardone, ed. Mendel Centenary: Genetics, Development and Evolution. Catholic University of America Press, Washington, DC.
Lewontin, R. C., and K. Kojima. 1960. The evolutionary dynamics of complex polymorphisms. Evolution 14:458-472.
MacBride, E. W. 1930. Embryology and Evolution. Nature 126:918-919.
Maynard Smith, J. 1976. What determines the rate of evolution? American Naturalist 110:331-338.
Mayr, E. 1963. Animal Species and Evolution. Harvard University Press, Cambridge, Massachusetts.
Mayr, E. 1980. Some Thoughts on the History of the Evolutionary Synthesis. Pp. 1-48 in E. Mayr, and W. Provine, eds. The Evolutionary Synthesis. Harvard University Mayr, E. 1994. The Resistance to Darwinism and the Misconceptions on which it was Based. Pp. 35-46 in J. H. Campbell, and J. W. Schopf, eds. Creative Evolution?! Jones & Bartlett, Inc., London.
Orr, H. A. 2003. The distribution of fitness effects among beneficial mutations. Genetics 163:1519-1526.
Orr, H. A., and J. A. Coyne. 1992. The Genetics of Adaptation: A Reassessment. American Naturalist 140:725-742.
Rokyta, D. R., P. Joyce, S. B. Caudle, and H. A. Wichman. 2005. An empirical test of the mutational landscape model of adaptation using a single-stranded DNA virus. Nat Genet 37:441-444.
Shull, A. F. 1936. Evolution. McGraw-Hill, New York.
Stebbins, G. L. 1966. Processes of Organic Evolution. Prentice Hall, Englewood Cliffs, NJ.
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.
Wright, S. 1967. Comments on the preliminary working papers of Eden and Waddington. Pp. 117-120 in P. S. Moorehead, and M. M. Kaplan, eds. Mathematical challenges to the neo-Darwinian interpretation of evolution. Wistar Institutional Press, Philadelphia.
Yampolsky, L. Y., and A. Stoltzfus. 2001. Bias in the introduction of variation as an orienting factor in evolution. Evol Dev 3:73-83.
Notes
1 The point of this comment is that I don't claim to be presenting the MS in a comprehensive way. This view of the MS is one view. In particular, it represents a kind of dialectic perspective on the MS as a response to Mendelism, focusing on what seems to be a characteristically Darwinian view of the role of variation, and focusing on evolutionary causation.
2 Note that Dobzhansky, in particular, started out as a bit of a heretic on the importance of mutation. In his 1937 book he speculated that different rates of mutation might explain different rates of evolution (p. 37), an idea that later was mocked by Simpson and others, lending credence to Gould's idea of a "hardening" of the Synthesis.
3 Orr and Coyne write "the micromutational view of Darwin, Fisher and others is clear: adaptations arise by allelic substitutions of slight effect at many loci, and no single substitution constitutes a major portion of an adaptation." I think they are right about Fisher and Darwin (ignoring the flagrant anachronism linking Darwin to a position on "allelic substitutions"), but who are the "others"? I can't put Dobzhansky in the same category. He only emphasizes that "small" or "slight" differences predominate in "the majority of cases".
4 Some present-day biologists have an adverse reaction to the term "creativity". Perhaps this is similar to my own adverse reaction to "design": I'd rather that biologists not use the term "design", which smacks of teleology. A similar objection might be made to the term "creativity". Nevertheless, in some sense, a theory of evolution must explain how new things come into existence (creativity) and how they appear to be adapted (design). So, if you are having an adverse reaction to "creativity", then please bear in mind the possibility that there might be ways to re-frame the issues at stake, but that for now, we are going to continue to use the old language of "creativity" because that is what's historically important.
5 This distinction is from Aristotle. His 4-fold taxonomy of causes includes material, efficient, formal (plans, archetypes), and final (goals, intentions) causes.
6 Its hardly ever clear what "random" means in such contexts. This is a topic that we will take up in a future post. The definition that is perhaps the most defensible historically is the one given by Wright, which also corresponds to Darwin's view as discussed in Beatty, 2010. By this definition, "randomness" is not a property of mutation per se, but of its role in evolution.
7 In passing, note how this argument obscures where "new" things come from. In reality, new combinations of pre-existing alleles arise by sexual mixis, by the reassortment of chromosomes, and by intra-chromosomal recombination. These processes, and not future selection, bring the new combinations into existence (and may break it apart again).
8 This passage has been singled out by Gould, 2002 and others. Amundsen (2005) gives a brief explanation of the thinking that underlies this (in his Ch. 11).
9 The "opposing pressures" argument is analyzed in more detail in Yampolsky and Stoltzfus (2001).
10 In the genesis of the MS, this doctrine had no clear basis in theory or experiment. It was not considered in a rigorous way until Maynard Smith tried (and, in my opinion, failed) to justify it in 1976, long after it had become an established orthodoxy.
11 This is explained in more detail in Stoltzfus (2009; see also Yampolsky and Stoltzfus, 2001).
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_myth5 (Arlin Stoltzfus, ©2010)
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.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.
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
"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.
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).
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".
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.
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.
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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)
