The Mutationism Myth, VI: Back to the Future

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.

This is Arlin's last contribution. The entire series has been an excellent introduction to the history of evolutionary theory and the concept of mutationism. 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.

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The Curious Disconnect

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, part 6. Back to the Future

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.

Review

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.

A bright line

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

One small step for a phage, one giant leap for evolutionary biology

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 s_i, the probability⁶ is just Nu*2s_i. If we divide an individual Nu*2s_i 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 s_i 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.

Back to the future

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.

The road less traveled

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.

References

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.

Notes

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*2s_i 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. "

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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_myth6 (Arlin Stoltzfus, ©2010)

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Molecular Evolution Exam - April 2015

Here's the final exam in my course. Students have to answer the first two questions and three of the next five questions. How would you do?

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1. Choose a subtopic from your essay and explain it better than you did in your essay and/or rebut the comments and criticisms made by the marker/grader.


2. Michael Lynch says in The Origins of Genome Architecture ....
   

   Nothing in Evolution Makes Sense Except in the Light of Population Genetics
   Evolution is a population genetic process governed by four fundamental forces, which jointly dictate the relative abilities of genotype variants to expand through a species. Darwin articulated a clear but informal description of one of those forces, selection (including natural and sexual selection), whose central role in the evolution of complex phenotypic traits is universally accepted, and for which an elaborate formal theory in terms of changing genotype frequencies now exists. The remaining three evolutionary forces, however, are non-adaptive in the sense that they are not the function of the fitness properties of individuals: mutation (broadly including insertions, deletions, and duplications) is the fundamental source of variation on which natural selection acts; recombination (including crossing-over and gene conversion) assorts variation within and among chromosomes; and random genetic drift insures that gene frequencies deviate a bit from generation to generation independently of other forces. Given the century of theoretical and empirical work devoted to the study of evolution, the only logical conclusion is that these four broad classes of mechanisms are, in fact, the only fundamental forces of evolution. Their relative intensity, directionality, and variation over time define the way in which evolution proceeds in a particular context.

   Do you agree with Lynch that “Nothing in Evolution Makes Sense Except in the Light of Population Genetics”? If so, why isn’t population genetics taught in introductory biology courses? If not, why not?


3. Imagine that identical female twins were born to a woman in 1000 AD. Imagine that you could find a direct descendant of each twin in 2015. If you sequence the complete genomes of the descendants, approximately how many differences would you expect to find? How do these compare to the differences between any two randomly selected individuals from the same part of the world? Explain your reasoning and describe any assumptions you make. Think carefully before you answer. The second question is the most important one. (Human mutation rate = 130 mutations per generation. Haploid genome size = 3.2 × 10⁹ bp.)


4. Why do some scientists think that there is no unique tree of life?


5. Many people believe that recombination evolved because it increases genetic variation in a population and this provided a selective advantage over species that didn’t have recombination. Do you agree with this explanation for the evolution of recombination? Why, or why not? What are the other possibilities?


6. What is “evolvability ”and why could it be important in evolution? Why are some scientists skeptical of this claim?


7. Richard Dawkins once wrote,
   

   Even the most ardent neutralist is quite happy to agree that natural selection is responsible for all adaptation. All he is saying is that most evolutionary change is not adaptation. He may well be right, although one school of geneticists would not agree. From the sidelines, my own hope is that the neutralists will win, because this will make it so much easier to work out evolutionary relationships and rates of evolution. Everybody on both sides agrees that neutral evolution cannot lead to adaptive improvement, for the simple reason that neutral evolution is, by definition, random, and adaptive improvement is, by definition, non-random. Once again, we have failed to find any alternative to Darwinian selection, as an explanation for the feature of life that distinguishes it from non-life, namely adaptive complexity.
   
   Richard Dawkins (1986) The Blind Watchmaker. p. 304

   Can you describe situations in Richard Lenski’s ongoing evolution experiment where neutral or deleterious alleles were essential for adaptive change?

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P-ter Accuses Me of Quote Mining

 
There are many adaptationists who recognize that random genetic drift exists. They will, when pressed, admit that neutral alleles can be fixed in a population. However, these adapationists pften maintain that visible phenotypes cannot be neutral with respect to survivability. Thus all visible phenotypes, with rare exceptions, are adaptations.

Several people have expressed this point of view in the comments on Sandwalk but the most prominent proponent is Richard Dawkins. I often use a quotation from The Extended Phenotype to demonstrate how Dawkins thinks about this issue. It comes from a chapter titled Constraints on Perfection. Here's the complete paragraph; I often use just the part that begins "The biochemical controversy ....[Richard Dawkins on Visible Changes and Adaptationism].

I have tried to show that adapatationism can have virtues as well as faults. But this chapter's main purpose is to list and classify constraints on perfection, to list the main reasons why a student of adaptation should proceed with caution. Before coming to my list of six constraints on perfection, I should deal with three others that have been proposed, but which I find less persuasive. Taking first, the modern controversy among biochemical geneticists about "neutral mutations", repeatedly cited in critiques of adaptationism, it is simply irrelevant. If there are neutral mutations in the biochemist's sense, what this means is that any change in polypeptide structure which they induce has no effect on the enzymatic activity of the protein. This means that the neutral mutations will not change the course of embryonic development, will have no phenotypic effect at all, as a whole-organism biologist would understand phenotypic effect. The biochemical controversy over neutralism is concerned with the interesting and important question of whether all gene substitutions have phenotypic effects. The adaptationism controversy is quite different. It is concerned with whether, given that we are dealing with a phenotypic effect big enough to see and ask questions about, we should assume that it is the product of natural selection. The biochemist's 'neutral mutations' are more than neutral. As far as those of us who look at gross morphology, physiology and behaviour are concerned, they are not mutations at all. It was in this spirit that Maynard Smith (1976b) wrote: "I interpret 'rate of evolution' as a rate of adaptive change. In this sense, the substitution of a neutral allele would not constitute evolution ..." If a whole-organism biologist sees a genetically determined difference among phenotypes, he already knows he cannot be dealing with neutrality in the sense of the modern controversy among biochemical geneticists.

Natural selection is the only explanation we know for the functional beauty and apparently "designed" complexity of living things. But if there are any changes that have no visible effect—changes that pass right under natural selection's radar—they can accumulate in the gene pool with impunity and may supply just what we need for an evolutionary clock.

Richard Dawkins
The Extended Phenotype (2005)I have discussed this quotation with Richard Dawkins and I am convinced that it fairly represents his viewpoint. The only quibble would be that Dawkins would probably admit of one or two exceptions where neutral alleles might produce a phenotypic effect. In other words, his statement above is perhaps an example of hyperbole but that's how I always read it anyway. Almost all popular science writers make generalizations of this sort and it's not a great crime.

The bottom line is that Dawkins thinks that neutral mutations cannot have an effect on embryonic development; therefore, they cannot result in a visible phenotype. Dawkins believes that almost all visible mutations will have either a beneficial or a detrimental effect on the survivability of an organism and that neutral mutations are a phenomenon that's confined to the molecular level where they may not even count as evolution.

P-ter thinks that I misrepresent Dawkins by quote mining [Larry Moran caught quote mining]. Here's what P-ter says,

This certainly seems to place Dawkins as an "adaptationist", one who thinks that all differences in phenotypes are adaptations. I was a little surprised by this, but the quote seemed clear, and I wasn't going to take the time to find my original.

Luckily, another commenter pointed out that The Extended Phenotype is searchable at Google Books [The Extended Phenotype]. And funny, the very next line after Moran stops quoting is possibly relevant:

The next lines P-ter is referring to is the beginning of a new paragraph ...

He might, nevertheless, be dealing with a neutral character in the sense of an earlier controversy (Fisher & Ford 1950; Wright 1951). A genetic difference could show itself at the phenotypic level, yet still be selectively neutral.

P-ter then continues with ...

Dawkins goes on to express some skepticism about some arguments for evolution by drift, but he's certainly not an "adaptationist" in the Moran sense.

I suppose I'm somewhat naive: distorting someone's argument through selective quotation is a classic creationist tactic, and Moran has written a bit about the propaganda techniques used by that crowd. Little did I know his familiarity is not of an entirely academic sort.

[1] As opposed to "pluralists", as he likes to call himself. For someone who (rightfully, in my opinion) is disdainful of "framing" (the view that scientists need to spin their results in order to resonate better with the public), he certainly knows how to frame.

This is a very serious charge. I'm accused of deliberately distorting Dawkins' position by selective quotation. According to P-ter, Dawkins does not believe what he says in the quoted paragraph. (And elswhere, I might add.) According to P-ter Dawkins believes that mutations with a visible phenotype can be neutral. (We're not talking about one or two exceptions here, we're talking about the generality that applies to a significant percentage of mutations.)

P-ter's evidence of the crime of quote mining is the first two sentences of a paragraph that appears on the bottom of page 32. You can read it for yourself but it seems obvious to me that Dawkins is raising a possible objection to his claim and then dismissing it. Here are the first few (not just two) sentences of that paragraph: I think they convey the correct intent.

He might, nevertheless, be dealing with a neutral character in the sense of an earlier controversy (Fisher & Ford 1950; Wright 1951). A genetic difference could show itself at the phenotypic level, yet still be selectively neutral. But mathematical calculations such as those of Fisher (1930b) and Haldane (1932a) show how unreliable human subjective judgement can be on the "obviously trivial" nature of some biological characters. Haldane, for example, showed that, with plausible assumptions about a typical population, a selection pressure as weak as 1 in a 1000 would take only a few thousand generations to push an initially rare mutation to fixation, a small time by geological standards. It appears that in the controversy referred to above, Wright was misunderstood (see below) ...

A careful reading of Dawkins shows that the objection to his claim doesn't stand because people misunderstood Wright. Thus, according to Dawkins, characters that appear to be neutral really aren't.

I maintain that my original characterization of the Dawkins' position is accurate and his words reflect his true beliefs. I resent P-ter's accusation that I deliberately tried to misrepresent Dawkins by quoting that passage.

Incidentally, P-ter puts words in my mouth. I recognize several different kinds of adaptationist. The worst of them are those who think every visible phenotype is an adaptation of some sort but there are many who do not hold this extreme position. It's simply not true that I say every adaptationist must deny the fixation of neutral alleles with a visible phenotype. Some are easier to mock than others, but it's pretty easy to get most of them going whenever I point out that Dawkins is an adaptationist.

What would happen if Intelligent Design Creationists understood evolution?

There's an interesting phenomenon taking place over on one of the main Intelligent Design Creationist websites. It started when a philosphopher, Vincent Torley, tried to understand how the sequences differences between chimpanzees and humans could be explained by evolution. In the beginning, he was skeptical of the explanation I offered and he was supported by a biochemist creationist named Branko Kozulic. Kozilic assured him that his skpeticism was justified and the population geneticists were wrong.

Then an amazing thing happened. Salvador Cordova, another well-known creationist, posted a comment on one of Torley's blog posts. You can see it as comment #39 on Branko Kozulic responds to Professor Moran. Cordova was responding to comments posted by Nick Matzke and "WD400" on that same post. Here's what Sal Cordova said,

Michael Lynch on modern evolutionary theory

Of the Five Things You Should Know if You Want to Participate in the Junk DNA Debate, the most difficult to explain is "Modern Evolutionary Theory." Most scientists think they understand evolution well enough to engage in the debate about junk DNA. However, sooner or later they will mention that junk DNA should have been deleted by selection if it ever existed. You can see that their worldview leads them to believe that everything in biology has an adaptive function.

It's been a few years since I posted Michael Lynch's scathing comments on panadaptationism and how it applies to understanding genomes [Michael Lynch on Adaptationism and A New View of Evolution]. You're in for a treat today.

Here's what you need to know about evolution in order to discuss junk DNA. The first quotation is from the preface to The Origins of Genome Architecture (pages xiii-xiv). The second quotations are from the last chapter (page 366 and pages 368-369.

Contrary to popular belief, evolution is not driven by natural selection alone. Many aspects of evolutionary change are indeed facilitated by natural selection, but all populations are influenced by nonadaptive forces of mutation, recombination, and random genetic drift. These additional forces are not simple embellishments around a primary axis of selection, but are quite the opposite—they dictate what natural selection can and cannot do. Although this basic principle has been known for a long time, it is quite remarkable that most biologists continue to interpret nearly aspect of biodiversity as an outcome of adaptive processes. This blind acceptance of natural selection as the only force relevant to evolution has led to a lot of sloppy thinking, and is probably the primary reason why evolution is viewed as a soft science by much of society.

A central point to be explained in this book is that most aspects of evolution at the genome level cannot be fully explained in adaptive terms, and moreover, that many features could not have emerged without a near-complete disengagement of the power of natural selection. This contention is supported by a wide array of comparative data, as well as by well-established principles of population genetics. However, even if such support did not exist, there is an important reason for pursuing nonadaptive (neutral) models of evolution. If one wants to confidently invoke a specific adaptive scenario to explain an observed pattern of comparative data, then an ability to reject a hypothesis based entirely on the nonadaptive forces of evolution is critical.

The blind worship of natural selection is not evolutionary biology. It is arguably not even science.

Michael Lynch

Despite the tremendous theoretical and physical resources now available, the field of evolutionary biology continues to be widely perceived as a soft science. Here I am referring not to the problems associated with those pushing the view that life was created by an intelligent designer, but to a more significant internal issue: a subset of academics who consider themselves strong advocates of evolution but who see no compelling reason to probe the substantial knowledge base of the field. Although this is a heavy charge, it is easy to document. For example, in his 2001 presidential address to the Society for the Study of Evolution, Nick Barton presented a survey that demonstrated that about half of the recent literature devoted to evolutionary issues is far removed from mainstream evolutionary biology.

With the possible exception of behavior, evolutionary biology is treated unlike any other science. Philosophers, sociologists, and ethicists expound on the central role of evolutionary theory in understanding our place in the world. Physicists excited about biocomplexity and computer scientists enamored with genetic algorithms promise a bold new understanding of evolution, and similar claims are made in the emerging field of evolutionary psychology (and its derivatives in political science, economics, and even the humanities). Numerous popularizers of evolution, some with careers focused on defending the teaching of evolution in public schools, are entirely satisfied that a blind adherence to the Darwinian concept of natural selection is a license for such activities. A commonality among all these groups is the near-absence of an appreciation of the most fundamental principles of evolution. Unfortunately, this list extends deep within the life sciences.

....

... the uncritical acceptance of natural selection as an explanatory force for all aspects of biodiversity (without any direct evidence) is not much different than invoking an intelligent designer (without any direct evidence). True, we have actually seen natural selection in action in a number of well-documented cases of phenotypic evolution (Endler 1986; Kingsolver et al. 2001), but it is a leap to assume that selection accounts for all evolutionary change, particularly at the molecular and cellular levels. The blind worship of natural selection is not evolutionary biology. It is arguably not even science. Natural selection is just one of several evolutionary mechanisms, and the failure to realize this is probably the most significant impediment to a fruitful integration of evolutionary theory with molecular, cellular, and developmental biology.

Natural selection is just one of several evolutionary mechanisms, and the failure to realize this is probably the most significant impediment to a fruitful integration of evolutionary theory with molecular, cellular, and developmental biology.It should be emphasized here that the sins of panselectionism are by no means restricted to developmental biology, but simply follow the tradition embraced by many areas of evolutionary biology itself, including paleontology and evolutionary ecology (as cogently articulated by Gould and Lewontin in 1979). The vast majority of evolutionary biologists studying morphological, physiological, and or behavioral traits almost always interpret the results in terms of adaptive mechanisms, and they are so convinced of the validity of this approach that virtually no attention is given to the null hypothesis of neutral evolution, despite the availability of methods to do so (Lande 1976; Lynch and Hill 1986; Lynch 1994). For example, in a substantial series of books addressed to the general public, Dawkins (e,g., 1976, 1986, 1996, 2004) has deftly explained a bewildering array of observations in terms of hypothetical selection scenarios. Dawkins's effort to spread the gospel of the awesome power of natural selection has been quite successful, but it has come at the expense of reference to any other mechanisms, and because more people have probably read Dawkins than Darwin, his words have in some ways been profoundly misleading. To his credit, Gould, who is also widely read by the general public, frequently railed against adaptive storytelling, but it can be difficult to understand what alternative mechanisms of evolution Gould had in mind.

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A Confused Philosopher

Darwinism and Its Discontents, by Michael Ruse, Cambridge University Press (2006)

Ruse defines Darwinism as the idea that natural selection is the chief causal process behind all organisms (p.2). He identifies a whole list of people who oppose Darwinism. Some of these are creationists—this book is not about them.

The main "discontents," according to Ruse, are misguided social scientists with their irrational fear of genetic determinism; philosophers who "can't handle the awful truth;" and evolutionary biologists whose objections "cannot be grounded purely in theory or evidence" (p.3). Many of discontent evolutionary biologists are (gasp!) Marxists.

I am one of those scientists who question Darwinism, so this book is all about me.

What does Michael Ruse have to say about us "discontents?"

At the risk of damning myself in the eyes of sound scholarship and of God, let me be categorical. All of the critics of Darwinism are deeply mistaken.

Wrong. It is Michael Ruse who is mistaken and this damn book is full of sloppy scholarship.

Chapters 1-4 cover the basic facts of evolution. Ruse establishes the important contribution of Darwin in discovering natural selection. He points out that natural selection is the "single best idea anyone ever had" (Dennett, 195). I agree.

The "fact" of evolution is explained and the history of life is briefly described. None of this is controversial as far as scientists are concerned but Ruse is setting the stage for the most important part of the book.

Before continuing, it's worth pointing out one of the major failings of the book: the lack of any solid definition of evolution. It seems clear that Ruse is confused about the difference between evolution and one of the main mechanisms of evolution, namely, natural selection. This confusion haunts the last part of the book and makes it very difficult for Ruse to come to grips with the ideas of the "discontents."

Chapter 5 ("The Cause of Evolution") is all about natural selection. Ruse builds the case for natural selection using all the old examples that we are familiar with. Only in Chapter 6 ("Limitations and Restrictions") does he begin to address the objections to classical Darwinism.

First in the dock is adaptationism as a flawed strategy. The adaptationist fallacy is a direct frontal attack on old-fashioned Darwinian thinking. The attack was first launched by Gould and Lewontin in the famous Spandrels of San Marco paper (1979). What does Ruse have to say about this?

Now, what is to be said by the Darwinian in response to this charge? Simply this: whoever doubted the point that Gould and Lewontin are making? It has always been recognized by evolutionists—certainly from the "Origin of Species" on—that however common or ubiquitous adaptation may be, it is only part of the story. (p.135)

Bravo! In two sentences Michael Ruse admits there's more to evolution than natural selection and, therefore, the discontents have a good case. Now let's see if he understands what these other things are and why they are important. (Don't hold your breath.)

Several examples follow. In all of them, Ruse makes the case that adaptation isn't necessarily optimal. Sometimes there just hasn't been enough time for adaptation to succeed, this is why some bird species haven't yet adjusted to being parasitized by cuckoos. Sometimes natural selection has done a good, but not perfect, job; as in the circuitous route followed by mammalian sperm ducts that loop over the ureter. Sometimes natural selection is even maladaptive, as in the large antlers of the extinct Irish Elk. All of these examples are intended to show that Gould and Lewontin were wrong.

What about group selection? That's a major challenge to Darwinism and natural selection. Not a problem. Hamilton solved it by coming up with kin selection. Kin selection has been the greatest gift to adaptationist thinking since natural selection itself.

What about random genetic drift? Now, that's a real issue since there's very little doubt about its importance. (It's by far the main mechanism of evolution, properly defined.) Does Ruse agree? Nope. Ruse notes that random genetic drift was first proposed by Sewall Wright back in 1931 and expanded by Moto Kimura in 1968. But after some initial excitement Ruse concludes,

Wright's theory is not very Darwinian. Natural selection does not play an overwhelming role. Genetic drift is the key player in Wright's world. However, although many of these ideas were taken up by later thinkers, especially by Theodosuis Dobzhansky in the first edition of his influential "Genetics and the Origin of Species," drift soon fell right out of fashion, thanks to discoveries that showed that many features formerly considered just random are in fact under tight control of selection. Today no one would want to say that drift (at the physical level) is a major direct player, although in America particularly, there has always been a lingering fondness for it. (p.150)

There you have it. One of the most decisive and well studied alternatives to natural selection is dismissed as a fad. This is sloppy scholarship. Ruse clearly does not know what he's talking about. He's probably read too much of Richard Dawkins and his fellow philosopher Daniel Dennett, and not enough evolutionary biology textbooks.

Now we turn to punctuated equilibria. If Ruse is an opponent of Gould you would expect to see the standard references to saltation in this part of the book. You won't be disappointed. Although saltation and hopeful monsters have nothing to do with punctuated equilibria—and certainly nothing to do with the challenge to Darwinism—they are obligatory strawmen whenever you want to discredit Stephen Jay Gould. It's another indicator of poor scholarship.

Species selection, the real hierarchical challenge to Darwinism, isn't even mentioned. This omission is all the more remarkable since Ruse recognizes that in order to make a case for evolution at higher levels a non-Darwinian mechanism is needed; one that will decouple macroevolution and microevolution.

[Gould proposes] that at upper levels there are other mechanisms that the microevolutionists miss. Which of course might be so, but until some convincing alternatives are supplied, Darwinians continue to argue that in important respects macroevolution is microevolution writ large. Natural selection working on random mutation is the key to evolutionary change, long term as well as short term. (p.159)

What a remarkably crude way of dismissing all the work done by a large number of paleontologists, not to mention a 1433 page book called The Structure of Evolutionary Theory. Ruse may have good reason for rejecting species selection but we'll never know. Sloppy scholarship, Ruse should be ashamed.

Chapter 6 is the most important chapter since it covers the main objections of the discontented. Ruse fails to meet any of those objections; indeed, he fails to understand most of them. The rest of the book doesn't get any better.

I'll finish this off by quoting from the concluding paragraph of Chapter 6.

What is our end point? It is just plain silly to say that Darwinism is an exhausted paradigm or that selection is a trivial cause of change—or even that it calls for significant revision or augmentation. It is a powerful mechanism and has proven its worth time and time again. It is not all-powerful. Natural selection has its limits—limits that have been recognized since the time of Darwin (he himself noted many of them)—but taken as a whole, it is the key to understanding the organic world. There is no call for theory change yet, nor is there any prospect of such change in the near future. (p.165)

Speaking for the discontents, I beg to differ. Random genetic drift is by far the most common mechanism of evolution and modern evolutionary theory fully acknowledges this fact. Darwinism (natural selection) is important but it ain't the only game in town. Darwin knew nothing about random genetic drift. That's why it's wrong to describe modern evolutionary theory as Darwinism.

Gould and his colleagues have proposed a hierarchical theory of evolution in which natural selection is only one mechanism and it operates at only one level (individuals within a population). Hierarchical theory may not be correct but you'll never know from reading this damn book.

The "Null Hypothesis" in Evolution

There's been a lot of discussion about the proper way to engage in thinking about evolution. When faced with a new problem, some people think that it's proper to begin by investigating adaptationist explanations. Others think that the proper way to begin is by assuming that the character in question is mostly influenced by random genetic drift. We are having a lively debate about this at Dawkins, Darwin, Drift, and Neutral Theory.

Part of the discussion boils down to a debate about the proper "null hypothesis" in evolutionary theory.

Here are some explanations from the textbooks that may help explain the "null hypothesis."

The most widely used methods for measuring selection are based on comparisons with the neutral theory, in which variation is shaped by the interaction between mutation and random genetic drift (Chapter 15). The neutral theory serves as a well-understood null hypothesis, and deviations from it may be caused by various kinds of selection. In the following sections, we examine ways of detecting and measuring selection by comparison with neutral theory.

EVOLUTION by Nicholas H. Barton, Derek E.G. Briggs, Jonathan A. Eisen, David B. Goldstein, and Nipam H. Patel, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2007 (p. 530)

The first step in a statistical test is to specify the null hypothesis. This is the hypothesis that there is actually no difference between the groups. In our example, the null hypothesis is that the presence or absence of wing markings does not effect the way jumping spiders respond to flies. According to this hypothesis, the true frequency of attack is the same for flies with markings on their wings as for flies without markings on their wings.

The second step is to calculate a value called a test statistic....

The third step is to determine the probability that chance alone could have made the test statistic as large as it is. In other words, if the null hypothesis were true, and we did the same experiment many times, how often would we get a value for the test statistic that is larger than the one we actually got?

EVOLUTIONARY ANALYSIS by Scott Freeman and Jon C. Herron, Prentice Hall, Upper Saddle River, New York 1998 (p. 73)

Genetic drift and natural selection are the two most important causes of allele substitution—that is, of evolutionary change—in populations. Genetic drift occurs in all natural populations because, unlike ideal populations at Hardy Weinberg equilibrium, natural populations are finite in size. Random fluctuations in allele frequencies can result in the replacement of old alleles by new ones, resulting in non-adaptive evolution. That is, while natural selection results in adaptation, genetic drift does not—so this process is not responsible for those anatomical, physiological, and behavioral features of organisms that equip them for survival and reproduction. Genetic drift nevertheless has many important consequences, especially at the molecular genetic level: it appears to account for much of the differences in DNA sequences among species.

Because all populations are finite, alleles at all loci are potentially subject to random genetic drift—but all are not necessarily subject to natural selection. For this reason, and because the expected effects of genetic drift can be mathematically described with some precision, some evolutionary geneticists hold the opinion that genetic drift should be the "null hypothesis" used to explain an evolutionary observation unless there is positive evidence of natural selection or some other factor. This perspective is analogous to the "null hypothesis" in statistics: the hypothesis that the data does not depart from those expected on the basis of chance alone. According to this view, we should not assume that a characteristic, or a difference between populations or species, is adaptive or has evolved by natural selection unless there is evidence for this conclusion.

EVOLUTION by Douglas Futuyma, Sinauer Associates Inc., Sunderland, MA, USA 2009 (p. 256)

Here are some papers from the scientific literature that illustrate how one goes about using the null hypothesis to ask questions about evolution.

Duret, L. and Galtier, N. (2007) Adaptation or biased gene conversion? Extending the null hypothesis of molecular evolution. Trends in Genetics 23:273-27 [doi:10.1016/j.tig.2007.03.011]

Orr, H.A. (1998) Testing Natural Selection vs. Genetic Drift in Phenotypic Evolution Using Quantitative Trait Locus Data. Genetics 149:2099-2104. [Abstract]

Brown, G.B. and Silk, J.B. (2002) Reconsidering the null hypothesis: Is maternal rank associated with birth sex ratios in primate groups? Proc. Natl. Acd. Sci. (USA) 99:11252-11255. [doi: 10.1073/pnas.162360599]

Nachman, M.W., Boyer, S.N., and Aquadro, C.F. (1994) Nonneutral evolution at the mitochondrial NADH dehydrogenase subunit 3 gene in mice. Proc. Natl. Acd. Sci. (USA) 91:6364-6368. [Abstract]

Fincke, O.M. (1994) Female colour polymorphism in damselflies: failure to reject the null hypothesis. Anìm. Behav. 47:1249-1266. [PDF]

Roff, D. (2000) The evolution of the G matrix: selection or drift? Heredity 84:135–142. [doi:10.1046/j.1365-2540.2000.00695.x]

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A New View of Evolution

There have been lots of new books about evolution in the past decade or so. I tend to divide them into three categories:

1. The Standard View: These are books that basically support the Modern Synthesis with some small tweaks here and there. They do not advocate major shifts in the way we look at evolution. Books by Richard Dawkins (The Greatest Show on Earth: The Evidence for Evolution), Jerry Coyne (Why Evolution Is True), Sean B. Carroll (Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom, The Making of the Fittest: DNA and the Ultimate Forensic Record of Evolution), and Ken Miller (Only a Theory) fall into this category.
2. The New View: Some books make the case for a new way of looking at evolution. I'll call it the "New View." Many of Stephen Jay Gould's books fall into this category (The Structure of Evolutionary Theory). He refers to it as extending the modern synthesis. Most of the "extension" is based on a pluralist, rather than an adaptationist approach but other modifications are important. Two recent books by Michael Lynch (Origins of Genome Architecture) and Eugene Koonin (The Logic of Chance: The Nature and Origin of Biological Evolution) fall into this category. It's a view that I share.
3. The Radical View: Some books advocate a more-or-less complete overthrow of the Modern Synthesis, replacing it with the author's pet theory. Examples are: Marc Kirschner, and John Gerhart (The Plausibility of Life: Resolving Darwin's Dilemma), James Shapiro (Evolution: A View from the 21st Century), Lynn Margulis and Dorion Sagan (Acquiring Genomes: A Theory Of the Origin Of Species), Massimo Pigliucci and Gerd B. Müllerand (editors) (Evolution - the Extended Synthesis), many others.

Darwin and Design by Michael Ruse

 
In Darwin and Design Michael Ruse tackles a tough problem; namely "Does evolution have a purpose?" Unfortunately the correct answer is "no" but Ruse muddles, misdirects, and misunderstands so thoroughly that by the time you reach the end of the book you just want to throw it against the wall.

The main theme of the book is teleological thinking or the idea that things happen in order to achieve a goal. We are familiar with this way of thinking in religion. Ruse spends some time describing the history, culminating in the natural theology of William Paley.

Paley and others argued that the presence of design in nature demanded a God who was the designer. The teleological part of this argument is the recognition that designed species, especially humans, represent a clear goal that needs an explanation. Life has meaning and purpose, according to believers, and it is God who gave it to us.

A teleological argument, or argument from design, is an argument for the existence of God or a creator based on perceived evidence of order, purpose, design and/or direction in nature. The word "teleological" is derived from the Greek word telos, meaning end or purpose. Teleology is the supposition that there is purpose or directive principle in the works and processes of nature.
"Teleological Argument" WikipediaCharles Darwin explained how life could appear to be designed by invoking natural selection, thus removing God from the equation. Nevertheless, teleology remains an important part of science, according to Ruse, because nature is designed by natural selection. It is quite appropriate, he says, to argue from design (the eye for example) to cause (adaptation).

This then is the paradox to which Darwin and Design is directed. Darwin seems to have expelled design from biology, and yet we still go on using and seemingly needing this way of thinking. We still talk in terms appropriate to conscious intention, whether or not we believe in God. In biology we still use forward-looking language of a kind that would not be deemed appropriate in physics or chemistry. Why is this?

Ruse seems to be at his best when describing the history of philosophy—as long as that history pre-dates Charles Darwin. His book is worth reading if you want a good summary of the design argument up to 1859. From that point on things begin to fall apart because Ruse does not understand modern evolution and he does not understand the controversies over evolutionary theory that persist to this day. Consequently, all of his history from Darwin on is biased and wrong.

The essence of Ruse's argument is as follows. Life evolves by natural selection. This leads to species and characteristics that are well-adapted. These characteristics have the appearance of design because they are, in fact, designed by natural selection. Because we know that everything is an adaptation it's perfectly legitimate to look at a species or an organ and assume that it as been designed by natural selection. While this adaptationist program may seem teleological because it assumes a purpose, it is, in fact a very legitimate way to do biology because design is a fundamental part of biology.

There are times when one thinks that Michael Ruse must have slept through the last half of the twentieth century. Has he never heard of Gould & Lewontin and The spandrels of San Marco? Is he unaware of the controversy over the validity of the adaptationist program?

Yes and no. He's heard of the controversy but he just wasn't listening. Everyone else who has addressed this question recognizes that the Gould & Lewontin challenge is not going to go away. They attempt to deal with it—usually not very successfully.

To his credit, Ruse seems to have picked up on the rumors that something important was going on so he does mention the spandrels paper and the attack on the adaptationist program. It's right there on pages 234-239. Five pages on structural constraints as introduced by Gould & Lewontin in their famous 1979 paper. Structural constraints? Surely there's more to the argument than that? Yes, there is but Ruse can easily dismiss it,

The point is whether they [Gould & Lewontin] introduce a whole new dimension into the discussion, by showing that much in the organic world is fundamentally nonadaptive. Darwinians have failed to see this and still continue not to see it.

That's it. Ruse is blind to modern evolutionary theory and quite proud of it. According to Ruse everything is an adaptation and "Darwinism" and "evolution" are synonyms.

The rest of the five pages on Gould & Lewontin are no more enlightening. Lest you think I'm being too harsh on Ruse, I assure you I'm not. He really doesn't get it. There are two pages devoted to random genetic drift. Two pages! After acknowledging that drift can sometimes cause evolution he dismisses it out of hand with,

Over time, however, random drift would be expected to average out more smoothly than differences due to the ever-changing forces of selection. For this reason the hypothesis that most molecular difference is due to drift has not been well received. Time and time again, measurements have shown that molecular differences are not what we would expect were drift the sole or main cause of change. In fruit flies, we see how random drift was ruled out as a significant factor in changing levels of the Adh gene.(p. 201)

Having summarily dismissed all objections to the ubiquity of adaption, Ruse can defend the argument from design by invoking adaptation as the sole driving force of evolution. In a chapter on "Design as Metaphor" he outlines his version of the adaptationist program. It's not only appropriate to attribute design to living things but it's a very productive way of advancing scientific knowledge.

Organisms produced by natural selection, have adaptations, and these give the appearance of being designed. This is not a chance thing or a miracle. If organisms did not seem to be designed, they would not work and hence would not survive and reproduce. But organisms do work, they do seem to be designed, and hence the design metaphor, with all the values and forward-looking, causal perspective it entails, seems appropriate.(p. 276)

Critics of the adaptationist program—I am one—argue that it begs the question. When you see something in nature it is reasonable to assume that it arose by evolution. The question we want to answer is what kind of evolution gave rise to that particular characteristic?

Take the fact that some people can roll their tongue as a simple example. We know there is a genetic basis to tongue-rolling. Some people have the allele that allows it, and some don't. We want to know why tongue-rolling exists.

     Once you have the metaphor of design in play, then of course you can ask questions about borderline instances and extensions and so forth. The real question, though, is whether, in the first place, the metaphor itself is an appropriate one. The question is not whether metaphors should be used at all but whether the specific metaphor of design should be used to explain evolution.

     Darwinians argue strenuously that it must be used. Richard Dawkins speaks to precisely this issue, asking what job we expect an evolutionary theory to perform. ... Dawkins agrees with John Maynard Smith that the "main task of any theory of evolution is to explain adaptive complexity, i.e. to explain the same set of facts which Paley used as evidence of a Creator."
Michael Ruse p. 278If you are a modern evolutionary biologist then you are aware of several possibilities. It could be just an accident that has no great significance at all. Maybe tongue-rollers and non-tongue-rollers have an equal chance of leaving offspring and the alleles will be fixed or eliminated by random genetic drift. Or maybe one of these groups has a selective advantage. Maybe tongue-rollers are more successful at having children and that's why the allele persists in the population. Eventually everyone will be a tongue-roller because natural selection is operating.

If you are a committed adaptationist then you begin by assuming that the ability to roll your tongue is designed. Your task is then to explain how this design arose and you have only one choice—evolution by natural selection. Thus, your choice of the design metaphor has blinded you to the possibility that tongue-rolling may not be an adaptation at all. This is a very restrictive research program because the question pre-supposes the answer. In other words, by imposing design and purpose on the natural world—albeit natural and not divine purpose—Ruse and his colleagues are avoiding the very question they should be asking; namely, "is this an adaptation?" This bias leads to fanciful just-so stories as the adaptationists struggle to come up with imaginary ways of explaining the design that they think they see in nature.

Does Ruse have an answer to this objection? Yes he does,

The critic might respond that one has here a circular situation: Darwinians make searching for adaptation central to their program, and then when they find the adaptations they so fervently seek, they use them as support for Darwinism. But a better term than "circularity" might be "self-reinforcement." Darwinism is a successful theory—our scientific examples show that—and at the moment (and for the foreseeable future, whatever the qualifications) it is the only game in town, on its own merits. Fruit flies, dunnocks, dinosaurs, fig wasps—this is a theory on a roll. It has earned the right to set the agenda. (p. 280)

As far as I'm concerned this is dead wrong. Darwinism is not the only game in town and we've known that for almost fifty years. At the very least you have to consider fixation of alleles by random genetic drift. If this is how a character actually evolved then there is no design. The metaphor is inappropriate. The program is useless. (There are other non-Darwinian processes.)

The entire thrust of Ruse's argument for design and purpose in evolution is absolutely dependent on one critical assumption: that natural selection is the only significant mechanism of evolution. If this isn't true then his whole argument falls apart. It isn't true.

I accept Ruse's challenge when he says,

Of course, Lewontin and his school do not care for many of the findings of the adaptationists. But to say that we should not play the game at all, or that we should count all as equal, requires some persuasive arguments. Better than arguments would be examples. Let those who worry about explanatory adaptationism show their dunnnocks and dinosaurs and fig wasps. When they demonstrate that they can do science which explains and predicts without invoking adaptation even implicitly, then we can start taking their position seriously. (p. 281)

There are literally dozens of examples of non-adaptive evolution that have been widely discussed in the scientific literature. It is more than "silly" of Ruse to issue a challenge like this. It's just plain ignorant.

Scientists who study junk DNA, for example, are doing very legitimate science when they predict that junk DNA sequences will not be conserved between species. Scientists who study blood type in humans are doing real science when they test the null hypothesis by asking whether the alleles conform to the Hardy-Weinberg distribution. (They do, suggesting strongly that they are not under selection.) Scientists who study speciation in birds ask whether the founder effect is real. (It is, and this shows that morphological changes during speciation are not due to adaptation.) The late Stephen Jay Gould and his colleagues have done good science by developing theories of punctuated equilibria and species sorting without assuming that natural selection and adaptation are essential. Ruse needs to take their position seriously. Meanwhile Ruse has demonstrated that we don't need to take him seriously.

The entire field of molecular evolution is based largely on explanations and predictions that rely on random genetic drift of neutral alleles. As far as I know, the people who work in that field are good evolutionary biologists even though they don't assume design when constructing their phylogenies.

And lets not forget about one of Lewontin's favorite examples. The African rhinoceros has two horns while the Indian rhinoceros has only one. Why? If you accept the modern theory of evolution then your choices of explanation can range from adaptive to accidental. If you restrict yourself to Darwinism then you must assume design and your explanation has to invoke natural selection. Somehow you have to come up with ways to explain why African rhinos were better off with two horns while Indian rhinos were better off with only one.

Using the metaphor of design and purpose forces you to assume the answer to the very question you are asking. It forces you to reject known evolutionary mechanisms such as random genetic drift. This may be good philosophy but it's not good science.

Getting back to the title of the book. Is nature designed? Partly, but there are lots of things that don't look designed and are not the end product of natural selection. Our genome is a good example. It's more like a Rube Goldberg apparatus than a well-tuned machine. It is not particularly helpful to say that living things are designed, or even that they have the appearance of design. If we stop saying that everything is designed then we will be better prepared to consider other possibilities, like evolution by accident.

Species Diversity

 
Some of you might recall my series of postings last year on the top Science questions. One of them was What Causes Species Diversity?. This is an important unanswered question in evolutionary biology even if it's conflated with speciation. We don't really have a good handle on what causes speciation.

That doesn't mean that we are completely ignorant. There are several candidates that, singly or in combination, account for much of what we understand about speciation and diversity. I'd like to quote Richard Dawkins from Unweaving the Rainbow since, as an admitted adaptationist, his view carries much more weight than that of a pluralist. (The reason will become apparent.) Here's how Dawkins describes the problem ...

The standard neo-Darwinian view of the evolution of diversity is that a species splits into two when two populations become sufficiently unalike that they can no longer interbreed. Often the populations begin diverging when they chance to be geographically separated. The separation means that they no longer mix their genes sexually and this permits them to evolve in different directions. The divergent evolution might be driven by natural selection (which is likely to push in different direction because of different conditions in the two geographical areas). Or it might consist of random evolutionary drift (since the two populations are not genetically held together by sexual mixing, there is nothing to stop them drifting apart). In either case, when they have evolved sufficiently far apart that they no longer interbreed even if they were geographically united again, they are defined as belonging to separate species.

Either, or both, of the two main mechanisms of evolution—natural selection and random genetic drift—can lead to speciation and diversity.

One could also argue that diversity depends ultimately on mutation. In this case, the main role of natural selection and random genetic drift is to reduce diversity by eliminating unfit and neutral alleles.

This has always been similar to my understanding of speciation and diversity. I was surprised, therefore to learn that one of my colleagues at the University of Toronto, Spencer Barrett, doesn't think random genetic drift plays a role in speciation [see Darwinism at the ROM]. Barrett is one of the featured presenters in a video at the Darwin exhibit at the Royal Ontario Museum.

In a display on the evolution/creation controversy, I copied down the following statement ...

Darwin's Theory of Evolution by Natural Selection is the only scientific explanation for the spectacular diversity of life on Earth.

So, here's the question of the day. Do you agree with that statement? Do you agree that natural selection is the only scientific explanation of diversity? Spencer Barrett seems to agree. Richard Dawkins would not agree. What do you think?¹

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1. If you disagree with the statement then please try and explain why it is featured so prominently in the Darwin exhibit. Is this an example of framing, or ignorance?

Good Science Writers: Douglas J. Futuyma

 
Douglas J. Futuyma is Distinguished Professor in the Department of Ecology and Evolution at the State University of New York at Stony Brook [Douglas Futuyma]. He is best known for his textbooks on evolution, Evolutionary Biology, beginning with the first edition in 1979. The latest version is a shorter textbook entitled Evolution (2005).

Futuyma has also published a trade book on the evolution/creation controversy. The first edition of Science on Trial: The Case for Evolution was published in 1983 and the second edition was published in 1995. Since Futuyma is a professional scientist, he meets all the qualifications for inclusion in Richard Dawkins' book: The Oxford Book of Modern Science Writing. But he is not there.

Douglas Futuyma is a brilliant textbook author. This kind of science writing is not usually recognized, but it should be. Futuyma's ability to accurately explain complex ideas is head-and-shoulders above that of most other textbook authors—no matter what their subject. I've chosen two excerpts from Evolution (2005) to illustrate this ability. You may find them familiar—that's because they have been widely quoted and paraphrased to the point where they seem trivial. Let's not forget that it is Futuyma who first began to explain evolution in this manner.

What Is Evolution?
The word evolution comes from the Latin evolvere, "to unfold or unroll"—to reveal or manifest hidden potentialities. Today "evolution" has come to mean, simply, "change." It is sometimes used to describe changes in individual objects such as stars. Biological (or organic) evolution, however, is change in the properties of groups or organisms over the course of generations. The development or ONTOGENY, or individual organisms is not considered evolution: individual organisms do not evolve. Groups of organisms, which we may call populations, undergo descent with modification. Populations may become subdivided, so that several populations are derived from a common ancestral population. If different changes transpire in the several populations, the populations diverge.

The changes in populations that are considered evolutionary are those that are passed via the genetic material from one generation to the next. Biological evolution may be slight or substantial: it embraces everything from slight changes in the proportions of different forms of a gene within a population to the alterations that led from the earliest organism to dinosaurs, bees, oaks, and humans. (p. 2)

Good Science Writers

Good Science Writing
David Suzuki
Helena Curtis
David Raup
Niles Eldridge
Richard Lewontin
Steven Vogel
Jacques Monod
G. Brent Dalrymple
Eugenie Scott
Sean B. Carroll
Richard Dawkins

Evolution as Fact and Theory
In The Origin of Species, Darwin propounded two major hypotheses: that organisms have descended, with modification, from common ancestors; and that the chief cause of modification is natural selection acting on hereditary variation. Darwin provided abundant evidence for descent with modification, and hundreds of thousands of observations from paleontology, geographic distributions of species, comparative anatomy, embryology, genetics, biochemistry, and molecular biology have confirmed this hypothesis since Darwin's time. Thus the hypothesis of descent with modification from common ancestors has long had the status of a scientific fact.

The explanation of how modification occurs and how ancestors gave rise to diverse descendants constitutes the theory of evolution. We now know that Darwin's hypothesis of natural selection on hereditary variation was correct, but we also know that there are more causes of evolution than Darwin realized, and that natural selection and hereditary variation themselves are more complex than he imagined. A body of ideas about the causes of evolution, including mutation, recombination, gene flow, isolation, random genetic drift, the many forms of natural selection, and other factors, constitute our current theory of evolution or "evolutionary theory." Like all theories in science, it is incomplete, for we do not yet know the causes of all of evolution, and some details may turn out to be wrong. But the main tenets of the theory are well supported, and most biologists accept them with confidence. (pp. 13-14)

I've also chosen an excerpt from Science on Trial (1995). In order to appreciate it, you will need a bit of background. The passage below comes from a chapter on "Chance and Mutation." The chapter opens with a brief description of a play by Tom Stoppard celled Rosencrantz and Guildenstern Are Dead. For those of you not intimately familiar with Shakespeare's Hamlet, Rosencrantz and Guildenstern are two minor characters who are tricked by Hamlet and end up sailing to England where, contrary to their expectations, they will be executed. Stoppard's play is about fate and inevitability.

But just as gravity and Brownian movement may both affect the motion of an airborne particle, chance and natural selection often work simultaneously, and certain evolutionary phenomena can be understood only if we take both into account. Many populations of houseflies throughout the world have evolved a resistance to DDT—an adaptation that has come about by natural selection. In some populations, however, the adaptation is provided by a dominant gene; in some by a recessive gene; in some by a number of genes, each with a small effect. The physiological mechanism by which the genes act also varies: flies can be resistant, for example, either by having developed an enzyme that degrades DDT or by having altered the cell membrane so that DDT is less able to penetrate the tissues. These are alternative adaptive mechanisms. Which one developed in a particular population must have depended on which mutations happened to be present in the population when it became exposed to DDT—and this is very much a matter of chance. Thus, chance initially determines what genetic variations will be acted on by natural selection to develop an adaptation.

When we extrapolate this principle of indeterminacy to long-term evolution, we can understand why different organisms have evolved different "solutions" to similar adaptive "problems." By chance, they had different genetic raw materials to work with. It is doubtless adaptive for male frogs to have a vocal sac that enables them to produce resonant calls that attract females. But whether a frog developed a single sac in the middle of the throat, as in the bullfrog, or a pair of sacs on either side, as in the leopard frog, may have been affected by what mutations first occurred by chance in the ancestor of each species.

If chance is a name for the unpredictable, them almost any historical event is affected by chance. Would Hamlet's mother, watching him stab Polonius through the arras, have predicted that this would be one in a chain of events leading to the death of Rosencrantz and Guildenstern? If you had been on the island of Mauritius in the mid-Tertiary, would you have predicted that the pigeons there would evolve into flightless dodos and then become extinct in the seventeenth century because they were easy prey for sailors? If you had seen a bipedal ape on the plains of Africa in the Pliocene, could you have predicted that this feature would prove crucial in the evolution of a larger brain and the development of human culture? Probably not; for in all such instances, the event that we recognize in hindsight as a "cause" might have been followed by other events leading to a different outcome. All of evolution, like all of history, seems to involve chance, in that very little of what has happened was determined from the beginning.

The mind that cannot abide uncertainty is troubled by the idea that the human species developed by "chance." But whether we evolved by chance or not depends on what the word means. We did not arise by a fortuitous aggregation of molecules, but rather by a nonrandom process—natural selection favoring some genes over others. But we are indeed a product of chance in that we were not predestined, from the beginning of the world, to come into existence. Like the extinction of the dodo, the death of Rosencrantz and Guildenstern, or the outbreak of World War I, we are a product of a history that might have been different. (pp. 146-147)

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