On the importance of random genetic drift in modern evolutionary theory

The latest issue of New Scientist has a number of articles on evolution. All of them are focused on extending and improving the current theory of evolution, which is described as Darwin's version of natural selection [New Scientist doesn't understand modern evolutionary theory].

Most of the criticisms come from a group who want to extend the evolutionary synthesis (EES proponents). Their main goal is to advertise mechanisms that are presumed to enhance adaptation but that weren't explicitly included in the Modern Synthesis that was put together in the late 1940s.

One of the articles addresses random genetic drift [see Survival of the ... luckiest]. The emphasis in this short article is on the effects of drift in small populations and it gives examples of reduced genetic diversity in small populations.

Misconceptions about Random Genetic Drift

Genetic Drift

Evolutionary change that occurs by random sampling of different alleles from one generation to the next. This causes nonadaptive evolutionary change.

Jerry Coyne
"Why Evolution Is True"There seem to be two important themes in the current pedagogical literature on science education. One of them is about student-centered learning—a concept I think we should all adopt. The other is about student misconceptions and how to deal with them. Much of the literature suggests that misconceptions need to be confronted and corrected. They can't be corrected by simply presenting the "correct" information. You need to actually address the misconception and show why it is wrong. This is a form of "teach the controversy" and that's not going to sit well with many American supporters of evolution.

Here's an interesting paper on "Biology Undergraduates’ Misconceptions about Genetic Drift" (Andrews et al., 2012). The abstract covers all the important points.

Jerry Coyne's View of Random Genetic Drift

Why Evolution Is True by Jerry Coyne is one of the best popular books on evolution. If you can only buy one book this year then this is the one to buy. It contains an excellent explanation of all the basic facts about evolution.

I'm not going to review this book, instead, I'm going to comment on just two things that interest me: how Jerry Coyne treats the mechanisms of evolution (natural selection and random genetic drift); and how he treats speciation—his area of expertise. I'll also discuss Richard Dawkins' treatment of these two topic in his book. (That's four separate postings.)

The first chapter in Why Evolution Is True is "What Is Evolution?" This is an appropriate way to begin and Jerry Coyne starts off nicely by saying that "Darwinism" is the theory of evolution by natural selection. He then proceeds to describe the main tenets of the modern theory of evolution, taking the time to point out that, "the mechanism of most (but not all) of evolutionary change is natural selection."

The sixth tenet of modern evolutionary theory is, "processes other than natural selection can cause evolutionary change." He's talking about random genetic drift although, like most adaptationists, he feels compelled to add a qualifier.

The influence of this process on important evolutionary change, though, is probably minor, because it does not have the moulding power of natural selection. Natural selection remains the only process that can produce adaptation. Nevertheless, we'll see in chapter 5 that genetic drift may play some evolutionary role in small populations and probably accounts for some non-adaptive features of DNA.

Okay, so it's not perfect, but at least he isn't confused about the difference between "evolutionary theory" and "Darwinism". Right?

Wrong. Before the chapter is finished he's talking about the six tenets of "Darwinism" and freely using "Darwinism" and "evolutionary theory" as symptoms. [See Jerry Coyne on Darwinism]

I don't get it. If Darwinism is evolution by natural selection and modern evolutionary theory includes the idea that not all evolution is caused by natural selection, then how can Darwinism be used as a synonym for evolutionary theory? I checked the index for "Darwinism" to see if there was a discussion about this elsewhere in the book. It wasn't much help since the index entry was: "Darwinism, see evolution."

Jerry Coyne is an adaptationist in the sense that he focuses most of his attention on natural selection and gives other mechanisms of evolution short shrift. This does not mean that he ignores them completely as I just showed. He knows about random genetic drift and he described it accurately (see below). The problem is that he tends to forget his lessons when his mind isn't focused on the differences between evolution and natural selection, and Darwinism vs random genetic drift.

In spite of the title of chapter 1, it doesn't really explain what evolution is. It concentrates more on describing evolutionary theory than on actually defining evolution. However, when we get to chapter 5 we to find an adequate definition of evolution. Jerry Coyne says, "Most biologists define evolution as a change in the porportion of alleles (different forms of a gene) in a population."

He then describes how the frequencies of alleles can change in a population by random stochastic means. Using ABO blood types as an example, he describes the typical behavior of alleles in a population of sexually producing organisms. He then says, ...

Such random change in the frequency of genes over time is called genetic drift. It is a legitimate type of evolution, since it involves changes in the frequencies of alleles over time, but it doesn't arise from natural selection. One example of evolution by drift may be the unusual frequencies of blood types (as in the ABO system) in the Old Order Amish and Dunker religious communities in America. These are small, isolated, religious groups whose members intermarry—just the right circumstances for rapid evolution by genetic drift.¹

Accidents of sampling can also happen when a population is founded by just a few immigrants, as occurs when individuals colonize an island or a new area. The almost complete absence of genes producing the B blood type in Native American populations, for example, may reflect the loss of this gene in a small population of humans that colonized North America from Asia around twelve thousand years ago.²

Both drift and natural selection produce genetic change that we recognize as evolution. But there's an important difference. Drift is a random process, while selection is the anti-thesis of randomness. Genetic drift can change the frequencies of alleles regardless of how useful they are to their carrier. Selection, on the other hand, always gets part of harmful alleles and raises the frequencies of beneficial ones.

As a purely random process, genetic drift can't cause the evolution of adaptations. It could never build a wing or an eye. That takes nonrandom natural selection. What drift can do is cause the evolution of features that are neither useful nor harmful to the organism.

This sounds like a typical adaptationist speaking. As a general rule, adaptationists admit to random genetic drift but confine it to small populations. They also make sure you understand that drift can't cause adaptation. Finally they state their opinion that drift only affects neutral alleles.

This is exactly the sort of thing Gould and Lewontin were complaining about in the "Spandrels" paper of 1978.

At this point, some evolutionists will protest that we are caricaturing their view of adaptation. After all, do they not admit genetic drift, allometry, and a variety of reasons for non-adaptive evolution? They do, to be sure, but we make a different point. In natural history, all possible things happen sometimes; you generally do not support your favorite phenomenon by declaring rivals impossible in theory. Rather, you acknowledge the rival, but circumscribe its domain of action so narrowly that it cannot have any importance in the affairs of nature. Then you often congratulate yourself for being such an undogmatic and ecumenical chap. We maintain that alternatives to selection for best overall design have generally been relegated to unimportance by this mode of argument.

This describes the views of many adaptationists but Jerry Coyne does not exactly fall into that mode of thinking—at least not when his attention is focused on the issue.

In fact, genetic drift is not only powerless to create adaptation, but can actually overpower natural selection. Especially in small populations, the sampling effect can be so large that it raises the frequency of harmful genes even though selection is working in the opposite direction. This is almost certainly why we see a high incidence of genetically based diseases in isolated human communities, including Gaucher's disease in northern Swedes, Tay-Sachs in the Cajuns of Louisiana, and in retinitis pigmentosa in the inhabitants in the inhabitants of the island of Tristan da Cunha.

This is very important and Jerry Coyne is one of the few adaptationists who get it. Random genetic drift doesn't just work on neutral alleles. It can also lead to high levels of deleterious alleles. Even their eventual fixation.

It would have been great if he had pointed out that random genetic drift can also lead to the loss of beneficial alleles making natural selection a stochastic process.

Because certain variations in DNA or protein sequence may be, as Darwin puts it "neither useful nor injurious" (or "neutral" as we now call them), such variants are especially liable to evolution by drift. For example, some mutations in a gene don't affect the sequence of the protein that it produces, and so don't change the fitness of its carrier. The same goes for mutations in non-functioning pseudogenes—old wrecks of genes still kicking around in the genome. Any mutations in these genes have no effect on the organism, and therefore can evolve only by genetic drift.

Many aspects of molecular evolution, then, such as certain changes in DNA sequence, may reflect drift rather than selection. It's also possible that many externally visible features of organisms could evolve via drift, especially if they don't affect reproduction. The diverse shapes of leaves of different tree species—like the differences between oaks and maple trees -- were once suggested to be "neutral" traits that evolved by genetic drift. But it's hard to prove that a trait has absolutely no selective advantage. Even a tiny advantage, so small as to be unmeasurable or unobservable by biologists in real time, can lead to important evolutionary changes over eons.

The relative importance of genetic drift versus selection in evolution remains a topic of hot debate among biologists.

It's impressive that Coyne admits to the possibility that externally visible features could be neutral and could evolve by random genetic drift. However, he immediately qualifies the statement by pointing out that it's very difficult to prove whether a trait has absolutely no selective advantage. This is true, but adaptationists usually forget to mention two things about natural selection that weaken this argument. First, they forget to mention that it's often just as difficult to prove that a trait has a selective advantage. Second, traits with small advantages are most often lost before they are fixed. Natural selection is not random but neither is it as much of a sure thing as most people believe.

To my way of thinking, Jerry Coyne clearly falls into the adaptationist camp. But on the continuum from pluralist to adaptationist he lies somewhere close to the middle, albeit still on the adaptationist side.

The fact that he's close to the middle is among the reasons why I think this book is so good.

Hear Coyne talk about his book: Phrasing a Coyne: Jerry Coyne on Why Evolution Is True.

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1. This is technically correct. Individual alleles will be fixed much faster in small populations than in large populations ... if they are fixed. But this does not mean that random genetic drift only fixes genes in small populations.

2. The founder effect is an important feature of evolution by accident.

WIlliam Provine doesn't like random genetic drift

William ("Will") Provine is an emeritus professor of history and of evolution at Cornell University (Ithaca, New YOrk, USA). He is no friend of creationism. Here's what Wikipedia has to say about him ...

Provine is an atheist, philosopher, and critic of intelligent design. He has engaged in prominent debates with theist philosophers and scientists about the existence of God and the viability of intelligent design. He has debated the founder of the intelligent design movement Phillip E. Johnson and the two have a friendly relationship. Provine has stated that he starts his course on evolutionary biology by having his students read Johnson's book "Darwin on Trial."

Provine is a determinist in biology, but not a determinist in physics or chemistry, thus rejecting the idea of free will in humans. Provine believes that there is no evidence for God, there is no life after death, there is no absolute foundation for right and wrong, there is no ultimate meaning for life, and that humans don't have free will.

When someone likes that publishes a book with the title, The 'Random Genetic Drift' Fallacy, I pay attention.

On the difference between Neutral Theory and random genetic drift

PZ Myers posted an interesting article on The state of modern evolutionary theory may not be what you think it is. He makes the point that there's more to evolution than natural selection.

I think this is an important point but I would not explain it the same way as PZ. He focuses attention on Neutral Theory and the fact that neutral, or nearly neutral, mutations are fixed by random genetic drift. Here's how he describes it ...

First thing you have to know: the revolution is over. Neutral and nearly neutral theory won. The neutral theory states that most of the variation found in evolutionary lineages is a product of random genetic drift. Nearly neutral theory is an expansion of that idea that basically says that even slightly advantageous or deleterious mutations will escape selection — they’ll be overwhelmed by effects dependent on population size. This does not in any way imply that selection is unimportant, but only that most molecular differences will not be a product of adaptive, selective changes.

The debate over adaptationism is a debate over mechanisms of evolution. Random genetic drift is a mechanism of evolution that results in fixation or elimination of alleles independently of natural selection. If there was no such thing as neutral mutations then random genetic drift would still be an important mechanism.

Let's say you have a clearly beneficial mutation with a huge selection coefficient of 0.1 (s = 0.1). Population genetics tells us that the probability of fixation is 2s or, in this case, 20%. That means that the allele will be eliminated from the population 80% of the time. That's random genetic drift. Similarly, some fairly deleterious mutations can sometimes be fixed by random genetic drift.

Random genetic drift is a mechanism of evolution that was discovered and described over 30 years before Neutral Theory came on the scene.

What Neutral Theory tells us is that a huge number of mutations are neutral and there are far more neutral mutations fixed by random genetic drift that there are beneficial mutations fixed by natural selection. The conclusion is inescapable. Random genetic drift is, by far, the dominant mechanism of evolution.

Many people seem to equate Neutral Theory with random genetic drift. They think that random genetic drift is only important when the alleles are neutral (or nearly neutral). Then they use this false equivalency as a way of dismissing random genetic drift because it only deals with "background noise" while natural selection is the mechanism for all the interesting parts of evolution. I think we should work toward correcting this idea by separating the mechanisms of evolution (natural selection, random genetic drift, and others) from the quality of alleles being produced by mutation (beneficial, detrimental, neutral).

The revolution is over and strict Darwinism lost. We now know that random genetic drift is an important mechanism of evolution and there's more to evolution than natural selection. Unfortunately, this blatantly obvious fact is not understood by the vast majority of people and teachers. There are even many scientists who don't understand evolution.

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One philosopher's view of random genetic drift

Random genetic drift is the process whereby some allele frequencies change in a population by chance alone. The alleles are not being fixed or eliminated by natural selection. Most of the alleles affected by drift are neutral or nearly neutral with respect to selection. Some are deleterious, in which case they may be accidentally fixed in spite of being selected against. Modern evolutionary theory incorporates random genetic drift as part of population genetics and modern textbooks contain extensive discussions of drift and the influence of population size. The scientific literature has focused recently on the Drift-Barrier Hypothesis, which emphasizes random genetic drift [Learning about modern evolutionary theory: the drift-barrier hypothesis].

Most of the alleles that become fixed in a population are fixed by random genetic drift and not by natural selection. Thus, in a very real sense, drift is the dominant mechanism of evolution. This is especially true in species with large genomes full of junk DNA (like humans) since the majority of alleles occur in junk DNA where they are, by definition, neutral.¹ All of the data documenting drift and confirming its importance was discovered by scientists. All of the hypotheses and theories of modern evolution were, and are, developed by scientists.

Nothing in biology makes sense except in the light of population genetics.

Michael Lynch
You might be wondering why I bother to state the obvious; after all, this is the 21st century and everyone who knows about evolution should know about random genetic drift. Well, as it turns out, there are some people who continue to make silly statements about evolution and I need to set the record straight.

One of those people is Massimo Pigliucci, a former scientist who's currently more interested in the philosophy of science. We've encountered him before on Sandwalk [Massimo Pigliucci tries to defend accommodationism (again): result is predictable] [Does Philosophy Generate Knowledge?] [Proponents of the Extended Evolutionary Synthesis (EES) explain their logic using the Central Dogma as an example]. I looks like Pigliucci doesn't have a firm grip on modern evolutionary theory.

His main beef isn't with evolutionary biology. He's mostly upset about the fact that science as a way of knowing is extraordinarily successful whereas philosophy isn't producing many results. He loves to attack any scientist who points out this obvious fact. He accuses them of "scientism" as though that's all it takes to make up for the lack of success of philosophy. His latest rant appears on the Blog of the American Philosophers Association: The Problem with Scientism.

I'm not going to deal with the main part of his article because it's already been covered many times. However, there was one part that caught my eye. That's the part where he lists questions that science (supposedly) can't answer. The list is interesting. Pigliucci says,

Next to last, comes an attitude that seeks to deploy science to answer questions beyond its scope. It seems to me that it is exceedingly easy to come up with questions that either science is wholly unequipped to answer, or for which it can at best provide a (welcome!) degree of relevant background knowledge. I will leave it to colleagues in other disciplines to arrive at their own list, but as far as philosophy is concerned, the following list is just a start:

• In metaphysics: what is a cause?
• In logic: is modus ponens a type of valid inference?
• In epistemology: is knowledge “justified true belief”?
• In ethics: is abortion permissible once the fetus begins to feel pain?
• In aesthetics: is there a meaningful difference between Mill’s “low” and “high” pleasures?
• In philosophy of science: what role does genetic drift play in the logical structure of evolutionary theory?
• In philosophy of mathematics: what is the ontological status of mathematical objects, such as numbers?

[my emphasis LAM]

Before getting to random genetic drift, I'll just note that my main problem with Pigliucci's argument is that there are other definitions of science that render his discussion meaningless. For example, I prefer the broad definition of science—the one that encompasses several of the Pigliucci's questions [Alan Sokal explains the scientific worldview][Territorial demarcation and the meaning of science]. The second point is that no matter how you define knowledge, philosophers haven't been very successful at adding to our knowledge base. They're good at questions (see above) but not so good at answers. Thus, it's reasonable to claim that science (broad definition) is the only proven method of acquiring knowledge. If that's scientism then I think it's a good working hypothesis.

Now back to random genetic drift. Did you notice that one of the questions that science is "wholly unequiped" to answer is the following: "what role does genetic drift play in the logical structure of evolutionary theory?" Really?

Pigliucci goes on to explain what he means ...

The scientific literature on all the above is basically non-existent, while the philosophical one is huge. None of the above questions admits of answers arising from systematic observations or experiments. While empirical notions may be relevant to some of them (e.g., the one on abortion), it is philosophical arguments that provide the suitable approach.

I hardly know what to say.

How many of you believe that the following statements are true with respect to random genetic drift and evolutionary theory?

1. The scientific literature on all the above is basically non-existent.
2. The philosophical literature is huge.
3. The question does not admit of answers arising from systematic observations or experiments.
4. It is philosophical arguments that provide the suitable approach.

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1. There are some very rare exceptions where a mutation in junk DNA may have detrimental effects.

A philosopher's view of random genetic drift

Random genetic drift is a process that alters allele frequencies within a population. The change is due to "random" events. It differs from natural selection where the change is due to selection for alleles that confer selective advantage on the reproductive success of an individual. Here's one description,

If a population is finite in size (as all populations are) and if a given pair of parents have only a small number of offspring, then even in the absence of all selective forces, the frequency of a gene will not be exactly reproduced in the next generation because of sampling error. If in a population of 1000 individuals the frequency of "a" is 0.5 in one generation, then it may by chance be 0.493 or 0.505 in the next generation because of the chance production of a few more or less progeny of each genotype. In the second generation, there is another sampling error based on the new gene frequency, so the frequency of "a" may go from 0.505 to 0.501 or back to 0.498. This process of random fluctuation continues generation after generation, with no force pushing the frequency back to its initial state because the population has no "genetic memory" of its state many generations ago. Each generation is an independent event. The final result of this random change in allele frequency is that the population eventually drifts to p=1 or p=0. After this point, no further change is possible; the population has become homozygous. A different population, isolated from the first, also undergoes this random genetic drift, but it may become homozygous for allele "A", whereas the first population has become homozygous for allele "a". As time goes on, isolated populations diverge from each other, each losing heterozygosity. The variation originally present within populations now appears as variation between populations.

Suzuki, D.T., Griffiths, A.J.F., Miller, J.H. and Lewontin, R.C.
in An Introduction to Genetic Analysis 4th ed. W.H. Freeman (1989 p.704)

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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15 Answers to Creationist Nonsense

 
The Scientific American website has several articles on Creationism Vs. Evolution.

One of the articles is 15 Answers to Creationist Nonsense from their June 2002 issue. The answers suffer from the same confusion about evolution that I've been addressing for years. It does not distinguish between evolution and natural selection and it fails to mention random genetic drift as a dominant mechanism of evolution. This is most obvious in the response to a question about speciation.

11. Natural selection might explain microevolution, but it cannot explain the origin of new species and higher orders of life.

Evolutionary biologists have written extensively about how natural selection could produce new species. For instance, in the model called allopatry, developed by Ernst Mayr of Harvard University, if a population of organisms were isolated from the rest of its species by geographical boundaries, it might be subjected to different selective pressures. Changes would accumulate in the isolated population. If those changes became so significant that the splinter group could not or routinely would not breed with the original stock, then the splinter group would be reproductively isolated and on its way toward becoming a new species.

Natural selection is the best studied of the evolutionary mechanisms, but biologists are open to other possibilities as well. Biologists are constantly assessing the potential of unusual genetic mechanisms for causing speciation or for producing complex features in organisms. Lynn Margulis of the University of Massachusetts at Amherst and others have persuasively argued that some cellular organelles, such as the energy-generating mitochondria, evolved through the symbiotic merger of ancient organisms. Thus, science welcomes the possibility of evolution resulting from forces beyond natural selection. Yet those forces must be natural; they cannot be attributed to the actions of mysterious creative intelligences whose existence, in scientific terms, is unproved.

One can easily imagine cases where speciation is driven entirely by natural selection but most of the textbooks are more pluralistic. The standard models have two populations diverging in phenotype due to either natural selection or random genetic drift or a combination of the two mechanisms.

The standard models postulate that divergence is initiated when two populations become geographically isolated as described above. If the two locales are different then the population that occupies the new environment might undergo adaptive selection, causing the divergence in morphology. However, if the two locales are similar the populations might just diverge by chance when they become geographically isolated.

Speciation occurs when the two populations have diverged to the point where they can no longer interbreed. At this point they become not only geographically isolated but also reproductively isolated.

There's no obvious way that the evolution of reproductive isolation could be due to natural selection. This would require that one population keep testing itself against the other with lack of cross-fertility providing some benefit to individuals in one of the populations. Instead, it's extremely likely that reproductive isolation is due to chance mutations that become fixed by random genetic drift. John Wilkins, our blogger expert on speciation, described this in a 2006 article that introduces sympatric speciation. Here are the relevant parts concerning the much more common mode of allopatric speciation.

Nobody denies, not even the most ardent antiadaptationist [that's me!], that aspects of organisms are strongly subject to selection, whether during speciation or after it. The critical issue is whether selection is a cause of speciation itself.

The allopatric consensus view allows for local adaptation, of course, when isolated from the parent metapopulation. What it denies is that selection for RI [reproductive isolation] occurs - how could it when speciation is occurring without contact with the reproductively isolated populations? There is selection of RI, of course, since RI on that account is a byproduct of changes in the population that are selectively favoured for ecological reasons. But not selection for RI itself [the selection of and selection for distinction is due to Elliot Sober]. So, argue allopatrists such as Jerry Coyne and Allan Orr, selection is not a cause of speciation in allopatry. And this seems right.

... If we think of speciation as "what makes a species" then we get ecological and other selective processes. If we think of speciation as "what makes it not the same species", then the explanatory focus shifts, and here the answer is, in cases when divergent selection is not going on, populations simply drift away from the reproductive reach of the ancestral population.

The bottom line here is that much of what we call speciation—especially the crucial reproductive isolation—is probably not due to natural selection. Instead, random genetic drift is the culprit. What this meams is that the answer to the question above is somewhat misleading. As it turns out, natural selection cannot account entirely, or even mostly, for all speciation events.

Some of you might recall a discussion I had in July with my colleague Spencer Barrett on this issue. He acted very annoyed when I suggested that random genetic drift might play an important role in speciation [see Species Diversity, Darwinism at the ROM]. This disagreement was made obvious to me today when I took a poll of my students in our class on Scientific Misconceptions. I asked them what they had learned from Professor Barrett in their first year class on evolution and more than 70% of them defined evolution as adaptation and were unable to identify random genetic drift as a mechanism of evolution. This means I'm going to have to explain evolution before we can discuss the evolution vs creationism controversy.

Go back and look at the second paragraph of the Scientific American answer (above). Isn't it strange that they don't even mention random genetic drift when listing other mechanisms of evolution? What's going on here? Do the science writers¹ at scientific American not know about random genetic drift or do they not think that it's a valid mechanism of evolution according to their definition of evolution. I suspect both.

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1. The article was written by John Rennie, a science writer who currently serves as editor in chief of Scientific American.

[Image Credits: The top image comes from webpages on evolution at CUNY Brooklynn (New York). The accompanying text reads, ""In small populations, other forces are at work. When a population is small, the presence or absence of a single individual can have a profound effect on the population gene pool. A sudden reduction in population size can also alter the remaining gene pool. This is the bottleneck effect.

A change in the gene pool brought about by chance is a genetic drift.

An extreme form of genetic drift, combined with the bottleneck effect is called the founder effect, which depends on a small group becoming isolated from the larger group, and can rapidly lead to the creation of a new species."

The bottom image comes from another article by John Wilkins, Explanation, that discusses, among other things, the role of stochastic events, such as random genetic drift, in speciation.]

John Hawks doesn't like random genetic drift

 
The human MYBPC3 gene encodes a muscle protein. A 25 bp deletion in that gene is associated with a large increase the risk of cardiomyopathy ("heart muscle disease"). The most severe problems appear when carriers reach the age of 40.

According to a recent paper by Dhandapany et al. (2009), the overall frequency of the deletion allele is about 4% in India but it ranges from 0% to 7% in different parts of the country. The allele is not present in most other populations outside of India.

The authors conclude that the allele has reached this frequency by random genetic drift beginning with an initial mutation about 30,000 years ago. This increase has occurred in spite of the fact that the allele is deleterious and should decrease overall fitness.

John Hawks disagrees: Could genetic drift really break your heart?.

The issue is not really whether a gene could go from 1 copy to 4 percent in 1200 generations by chance. That wouldn't be so terribly unlikely in Pleistocene humans -- in fact, the mean time for a mutation to go from 1 copy to 4 percent by drift in a population of effective size 10,000 individuals is not 30,000 years, but only around 20,000 years. On the other hand, mtDNA variation today suggests that South Asia experienced early and rapid population growth -- so we're not likely talking about a population of 10,000, but more like a minimum of 100,000 effective individuals through the past 30,000 years at least. It would take genetic drift at least 10 times longer to accomplish the requisite frequency change given that demographic history. Still, a single allele at a single gene locus might be exceptional.

But that scenario, however unlikely, is simply not the situation we have here. Here we have a deletion that must have some disadvantage, because it gives people a fatal disease. This disadvantage is apparently dominant in effect, based on the case-control study. Yet the deletion has managed to persist within the large South Asian populations of the last 10,000 years so that today it is still around 4 percent.

John is an expert on evolution within human populations but he seems to be basing all of his calculations on the idea that the mutation arose in a population of 100,000 individuals and that this population was the effective population (e.g. they all freely interbred). I don't think this is very likely.

The fact that the allele frequency varies within India suggests that there are many subpopulations. Some of them might have been as small as 1000 individuals at vary time over the course of the last 30,000 years. As I'm sure John knows, the populations dynamics of human groups is extremely complex. We only have to think about the allele frequency differences in the Pennsylvania Amish communities or French Canadians to recognize this fact.

And let's not forget that the frequency of Huntington's disease is high around Lake Maracaibo in Venezuela. Over a period of 200 years a single individual with the Huntington's disease allele has left 18,000 descendants.

When we look at modern allele frequencies we don't only think about average rates of change due to random genetic drift in panmitic populations. We also have to consider the unusual events that occur from time to time. These include founder effects, natural disasters, etc. etc. The MYBPC3 is a lottery winner. You can't dismiss evolution by accident just because the probability of any one event is low.

This is why John says that, "Still, a single allele at a single gene locus might be exceptional." But John seems to think that in this case the result is not just "exceptional" but extraordinarily exceptional. He suggests that the deleterious effects of the allele are a recent phenomenon and that explains why it survived in early populations.

I would hypothesize that the disadvantages of the deletion have actually increased over time. The average lifespan increased into the Upper Paleolithic and probably later as well. Meanwhile, as the population grew, larger completed family sizes became more important to fitness. As people became more sedentary, the accumulation and inheritance of possessions and land became an important means of investing in children. The increasing importance of later survival and investment in children should have raised the fitness cost of chronic disease. That would explain a pattern of evolution in which this deletion increased in frequency early in its history, but later remained static or declined.

So, I don't suppose I can say people are crazy for thinking genetic drift could explain this deletion's current high frequency. But considering the powerful effect of weak selection over the many generations involved here, and the very large size of the South Asian population during most of that time, genetic drift seems pretty unlikely.

This makes sense to me. It's consistent with John's idea that the rate of human evolution has changed substantially over the past 30,000 years but I don't see why he objects so much to a random genetic drift explanation. Why does he suggest the the authors of the paper are crazy to suggest drift as an explanation?

It seems to me that his explanation is consistent with an increase in allele frequency due to random genetic drift just as the authors claim.

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Dhandapany, P.S., Sadayappan, S., Xue, Y., Powell, G.T., Rani, D.S., Nallari, P., Rai, T.S., Khullar, M., Soares, P., Bahl, A., Tharkan, J.M., Vaideeswar, P., Rathinavel, A., Narasimhan, C., Ayapati, D.R., Ayub, Q., Mehdi, S.Q., Oppenheimer1, S., Richards, M.B., Price, A.L., Patterson, N., Reich, D., Singh, L., Tyler-Smith, C., and Thangaraj, K. (2009) A common MYBPC3 (cardiac myosin binding protein C) variant associated with cardiomyopathies in South Asia. Nature Genetics, Published online: 18 January 2009 [doi:10.1038/ng.309]

Testing Natural Selection: Part 1

 
The latest issue of Scientific American has an interesting article by H. Allen Orr entitled Testing Natural Selection.

Biologists working with the most sophisticated genetic tools are demonstrating that natural selection plays a greater role in the evolution of genes than even most evolutionists had thought.

Orr is an adaptationist. His perspective on evolution focuses on natural selection as the predominant mechanism. He tends to dismiss all other mechanisms as either uninteresting or unimportant.

I though it might be interesting to compare what a pluralist might say about some of the things in the article. It's one way of highlighting the difference between the two points of view.

Naturally, as a pluralist, I disagree with some statements. My main beef, however, is with the growing tendency to over-emphasize natural selection as we approach the 200th anniversary of Darwin's birth and the 150th anniversary of publication of On the Origin of Species. I think it's possible to describe the differences between evolution in the eighteenth century and evolution in the 21st century without diminishing Darwin's contributions.

Orr begins his article by describing natural selection. He explains that there are several kinds of mutations ...

Most important, we know something about the effects of mutations on fitness. The overwhelming majority of mutations are harmful—that is, they reduce fitness; only a tiny minority are beneficial, increasing fitness.

That's not exactly how I would put it. I would have added that there's a third type of mutation that is neither harmful nor beneficial—neutral mutations.

Furthermore, I would have explained that the frequency of these three different kinds of mutations can vary considerably from one species to the next depending on the organization of the genome. In animals and plants, for example, most of the DNA does not seem to be essential so that the overwhelming majority of mutations are neutral and a smaller number—those that interfere with an essential function—are deleterious. A few mutations can be beneficial.

Orr goes on to say ....

Most mutations are bad for the same reason that most typos in computer code are bad: in finely tuned systems, random tweaks are far more likely to disrupt function than to improve it.

I would not use this analogy because it emphasizes something that I think is false; namely that organisms are "fine tuned systems." I tend to think of them as sloppy Rube Goldberg machines and not as well-tested computer code.

I would say that most mutations in essential regions of the genome are deleterious because random hits in DNA are more likely to make things worse than to make things better. The distinction is subtle, but important. Many adaptationists use language implying that living organisms are almost perfectly adapted to their present environment.

In the next section, Orr describes the advances of population genetics and its influence on how we understand natural selection. I would have described how population genetics led to an understanding of all type of evolution, and not just natural selection. Here's what Orr says,

Population geneticists have also provided insight into natural selection by describing it mathematically. For example, geneticists have shown that the fitter a given type is within a population, the more rapidly it will increase in frequency; indeed, one can calculate just how quickly the increase will occur. Population geneticists have also discovered the surprising fact that natural selection has unimaginably keen “eyes,” which can detect astonishingly small differences in fitness among genetic types. In a population of a million individuals, natural selection can operate on fitness differences as small as one part in a million.

I would have said that the growth of population genetics in the early part of the 20th century led to the recognition of random genetic drift as an important mechanism of evolution. Models were developed to explain how natural selection affected the increase in frequency of a beneficial allele and how neutral alleles could also increase in frequency even though they were invisible to natural selection.

The population geneticists also discovered that harmful alleles could become fixed by accident, although that turns out to be a rare event. More importantly, they discovered that natural selection has a stochastic component. Beneficial alleles will only become fixed part of the time. The probability depends on the fitness advantage. For example, if an allele has a fitness advantage of 10% then it will only become fixed 20% of the time. In 80% of cases when such an allele arises in a population it will be lost by random genetic drift before it becomes fixed.¹

As the fitness advantage diminishes, the probability of fixation becomes lower and lower so that alleles with small fitness advantages (<1%) will hardly ever change the species. That's what population geneticists discovered about natural selection.

The probability of fixation of neutral alleles (or nearly neutral alleles) is very low but since there are so many more of them than beneficial alleles, much of evolution is characterized by changes due to random genetic drift.

The next section is "How Common Is Natural Selection?". This is where Orr asks the key question ...

One of the simplest questions biologists can ask about natural selection has, surprisingly, been one of the hardest to answer: To what degree is it responsible for changes in the overall genetic makeup of a population? No one seriously doubts that natural selection drives the evolution of most physical traits in living creatures—there is no other plausible way to explain such large-scale features as beaks, biceps and brains. But there has been serious doubt about the extent of the role of natural selection in guiding change at the molecular level. Just what proportion of all evolutionary change in DNA is driven, over millions of years, by natural selection—as opposed to some other process?

We've discussed this distinction between molecular changes and physical traits many times. One of the most annoying characteristics of adaptationists is that they insist on relegating other mechanisms of evolution to the level of DNA sequences but refuse to consider anything but natural selection when it comes to visible phenotypes. There is no justification for this assumption. Many physical traits can be neutral or even deleterious. They were not fixed by natural selection.²

What Orr says is simply not true. There are many biologists who seriously doubt that natural selection drives the evolution most physical traits, even though such pluralists readily agree that most adaptions are due to natural selection. Random genetic drift is a plausible way to explain many physical traits.

Until the 1960s biologists had assumed that the answer was “almost all,” but a group of population geneticists led by Japanese investigator Motoo Kimura sharply challenged that view. Kimura argued that molecular evolution is not usually driven by “positive” natural selection—in which the environment increases the frequency of a beneficial type that is initially rare. Rather, he said, nearly all the genetic mutations that persist or reach high frequencies in populations are selectively neutral—they have no appreciable effect on fitness one way or the other. (Of course, harmful mutations continue to appear at a high rate, but they can never reach high frequencies in a population and thus are evolutionary dead ends.) Since neutral mutations are essentially invisible in the present environment, such changes can slip silently through a population, substantially altering its genetic composition over time. The process is called random genetic drift; it is the heart of the neutral theory of molecular evolution.

As I've already pointed out, random genetic drift was discovered in the 1920s and it was incorporated into the first version of the Modern Synthesis in the 1940s. It dropped out of favor when the synthesis hardened at the time of the Darwin centennial in 1959.

Random genetic drift was revived in the late 1960's with the discovery of neutral alleles. Drift is the way in which selectively neutral alleles become fixed in a population. Random genetic drift and neutral theory are not synonyms.

As I indicated above, since the vast majority of animal and plant genomes is non-essential, it stands to reason that the vast majority of alleles will be neutral. Thus at the molecular level, at least, random genetic drift must be the dominant mechanism of evolution.

By the 1980s many evolutionary geneticists had accepted the neutral theory. But the data bearing on it were mostly indirect; more direct, critical tests were lacking. Two developments have helped fix that problem. First, population geneticists have devised simple statistical tests for distinguishing neutral changes in the genome from adaptive ones. Second, new technology has enabled entire genomes from many species to be sequenced, providing voluminous data on which these statistical tests can be applied. The new data suggest that the neutral theory underestimated the importance of natural selection.

Hmmm ... I could see where this was going even before I read it. Orr is about to quote the infamous work of Drosophila geneticists who have devised complicated tests to show that some synonymous mutations might confer a selective advantage in one species but not in another closely related species. Some of the papers claim that many alleles in coding regions are not neutral even thought they don't change the amino acid. There's no question that this is true in some cases.

It's also true that mutations altering the amino acid are sometimes beneficial, and therefore selected. However, if you align the amino acid sequences of a given gene from hundreds of species and map them on to the structure of the protein it becomes readily apparent that most substitutions cannot have a significant effect on the function of the protein. They must be neutral, or nearly neutral. As a matter of fact, in most proteins it is difficult to find any clearly beneficial alleles present in one species and not in the others.

In one study a team led by David J. Begun and Charles H. Langley, both at the University of California, Davis, compared the DNA sequences of two species of fruit fly in the genus Drosophila. They analyzed roughly 6,000 genes in each species, noting which genes had diverged since the two species had split off from a common ancestor. By applying a statistical test, they estimated that they could rule out neutral evolution in at least 19 percent of the 6,000 genes; in other words, natural selection drove the evolutionary divergence of a fifth of all genes studied. (Because the statistical test they employed was conservative, the actual proportion could be much larger.) The result does not suggest that neutral evolution is unimportant—after all, some of the remaining 81 percent of genes may have diverged by genetic drift. But it does prove that natural selection plays a bigger role in the divergence of species than most neutral theorists would have guessed. Similar studies have led most evolutionary geneticists to conclude that natural selection is a common driver of evolutionary change even in the sequences of nucleotides in DNA.

Pluralists disagree. We still think that random genetic drift is by far the dominant mechanism at the molecular level and that it even plays a significant role at the level of visible phenotypes.

In addition, we like to remind adaptationists that most beneficial alleles are eliminated by random genetic drift before they ever become fixed in a population.

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1. Many biologists, and most evolutionary psychologists, do not understand this important point. They think that all they have to do is identify some (real or imagined) benefit and it will automatically take over the population no matter how small the benefit.

2. I know that Orr said "most" physical traits and not "all" physical traits. It's a distinction without meaning since the percentage of non-adaptive changes that adaptationists are willing to admit, grudgingly, is not much different than zero.

Richard Dawkins' View of Random Genetic Drift

The Greatest Show on Earth is Richard Dawkins' latest book. It's his eighth book on evolution: the others are The Selfish Gene (1976), The Extended Phenotype (1982), The Blind Watchmaker (1986), River Out of Eden (1995), Climbing Mount Improbable (1996), Unweaving the Rainbow (1998) and The Ancestors Tale (2004).

I'm interested in the evolution of Richard Dawkins' ideas about evolution; in particular, his ideas about random genetic drift and mechanisms of evolution other than natural selection.

In Chapter 1 Dawkins says, "All reputable biologists go on to agree that natural selection is one of its most important driving forces, although—as some biologists insist more than others—not the only one."

This looks promising. Dawkins is saying— in chapter 1—that there are two mechanisms (driving forces) of evolution. He implies that he accepts random genetic drift as a "driving force" of evolution. (Assuming that random genetic drift is what he has in mind.) It's clear that "some biologists" have influenced him, although it's not clear from the sentence whether those biologists are "reputable"!

Since this is a book about the evidence for evolution, I eagerly anticipated his explanation of random genetic drift. Would it be as good as Jerry Coyne's?¹ In fact, I was so eager that I couldn't wait. I jumped to the index to look under "random."

Nothing. Not to worry. The other important mechanism must be here somewhere. Is it indexed under "genetic"? No. What about "drift"? No, not there either.

What gives? How can you write a book about evolution in the 21st century without mentioning random genetic drift as an important mechanism of evolution? Even the other adaptationist, Jerry Coyne, has it in the index to Why Evolution Is True.

Maybe Dawkins uses another term for the second mechanism of evolution. I recalled that he often gets mixed up about the difference between neutral theory and random genetic drift. Let's see if "Neutral Theory" is in the index. Nope.

What about "Kimura"? Success at last! Check out page 332.

Page 332 is in the middle of a section on The Molecular Clock in Chapter 10. It seems a bit late to begin discussing the second mechanism of evolution, but, as I said before, it's promising that Dawkins even concedes that there is one.

Dawkins explains that the reason why there's a molecular clock is because the majority of changes at the genetic level are neutral and these changes are fixed in a regular, clock-like, albeit stochastic, process. He then goes on to say...

When the neutral theory of molecular evolution was first proposed by, among others, the great Japanese geneticist Motoo Kimura, it was controversial. Some version of it is now widely accepted and, without going into the detailed evidence here, I am going to accept it in this book. Since I have a reputation as an arch-"adaptationist" (allegedly obsessed with natural selection as the major or even only driving force of evolution) you can have some confidence that if even I support the neutral theory it is unlikely that many other biologists will oppose it!

I can't think of any serious biologists who would deny that neutral mutations exist. The essence of Neutral Theory, or Nearly Neutral Theory as it is currently called, is undoubtedly correct. The fact that Richard Dawkins accepts it in this book is not remarkable. What's remarkable is that he has to tell us that he accepts it, especially in a book about the evidence for evolution.

Meanwhile, we are still waiting for the explanation of the "other" mechanism of evolution. The one that was mentioned in Chapter 1 when he said that natural selection does not account for all of evolution. He can't have been thinking about "Neutral Theory" since that's not a mechanism of evolution. And he can't just have been thinking about a mechanism for fixing neutral mutations since he surely knows that the "other" mechanism can result in the loss of beneficial alleles and the fixation of detrimental ones.

Still waiting. What we see in Chapter 10 is an explanation of neutral mutations but no mention of random genetic drift—the mechanism responsible for fixing neutral mutations in a population. He does briefly mention on page 335 that neutral mutations can "go to fixation by chance." I get the impression that he goes out of his way to not name the other mechanism of evolution. You know what I'm referring to, it's the mechanism that gets a whole chapter to itself in all the evolutionary biology textbooks [Evolution: Table of Contents].

Dawkins concedes that the vast majority of the human genome consists of sequences that aren't genes. Here's how he puts it ...

It is a remarkable fact that the greater part (95% in the case of humans) of the genome might as well not be there, for all the difference it makes. The neutral theory applies even to many of the genes in the remaining 5%—the genes that are read and used. It applies even to genes that are totally vital for survival. I must be clear here. We are not saying that a gene to which the neutral theory applies has no effect on the body. What we are saying is that a mutant version of the gene has exactly the same effect as the unmutated version.

In other words, the vast majority of the DNA in our genome is junk. Mutations that occur in junk DNA will become fixed in spite of the fact that they are not seen by natural selection. This is what he means when he says that most mutations are neutral and it's equivalent to saying that the dominant mechanism of evolution, in terms of overall frequency, is random genetic drift and not natural selection. I just wish he'd come right out and say it.

It's a shame that Dawkins does not actually mention the mechanism by which those neutral mutations become fixed but instead continuously refers to neutral theory as the alternate mode of evolution. The general public needs to hear about random genetic drift and Dawkins is—like it or not—the most prominent evolutionist on the planet.

Dawkins has not changed his mind about the existence of these neutral mutations and he has not changed his mind about their importance. While they may exist, they are not important as far as evolution is concerned. He makes this very clear—once again—in this book.

As it happens, it is probably true to say that most mutations are neutral. They are undetectable by natural selection, but detectable by molecular geneticists; and that is an ideal combination for an evolutionary clock.

None of this is to downgrade the all-important tip of the iceberg—the minority of mutations that are not neutral. It is they that are selected, positively or negatively, in the evolution of improvements. They are the ones whose effects we actually see—and natural selection "sees" too. They are the ones whose selection gives living things their breathtaking illusion of design. But it is the rest of the iceberg—the neutral mutations which are in the majority—that concerns us when we are talking about the molecular clock.

As geological time goes by, the genome is subjected to a rain of attrition in the form of mutations. In that small portion of the genome where the mutations really matter for survival, natural selection soon gets rid of the bad ones and favors the good ones. The neutral mutations, on the other hand, simply pile up, unpunished and unnoticed—except by molecular geneticists.

This is the way the adaptationist dismisses non-adaptive evolution. It's not really of interest to real biologists. It's only interesting to molecular geneticists. And we all know that those people are not real evolutionary biologists!

Now we come to one of the most interesting sentences in the entire book; at least as far as I'm concerned. As most Sandwalk readers know, we have long debated whether or not visible mutations can be neutral. Once you have an observed phenotype, can you ever attribute it to neutrality? Many adaptationists argue that you can't.

Here's what Richard Dawkins says in his latest book.

It is also possible (although "ultra-Darwinists" like me incline against the idea) that some mutations really do change the body, but in such a way as to have no effect on survival, one way or the other.

This is progress. Back when he wrote The Extended Phenotype, in 1982, Richard Dawkins said.

The adaptationism controversy is quite different. It is concerned with whether, given that we're 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 behavior are concerned, they are not mutations at all. It was in this spirit that Maynard Smith (1976) 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 differences among phenotypes, he already knows he cannot be dealing with neutrality in the sense of the modern controversy among biochemical geneticists.

Finally, in 2009, Richard Dawkins admits that it is "possible" that visible mutations could be neutral. Hallelujah!

I'm looking forward to book #9.

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1. Jerry Coyne's View of Random Genetic Drift

Darwinism at the ROM

 
Yesterday I attended a symposium on evolution at the Royal Ontario Museum [Darwin Symposium at the ROM]. The emphasis was on Charles Darwin, in line with the Darwin exhibit that is currently running at the ROM.

What I was expecting was a series of lectures that explain how Darwin fits into modern ideas of evolutionary biology. What I got was an adaptationist lovefest.

This was a free public symposium. By the time it started every seat in the auditorium was full and people were standing at the back. There were about 320 people of all ages and all walks of life. I sat beside a high school teacher and talked to retirees from the suburbs.

The first speaker was Michael Ruse. The original title of his talk was Has Darwinism Expired? but he modified it slightly to Is Darwin's Theory Past Its "Sell By" Date. His opening remarks were promising because he mentioned Stephen Jay Gould and Gould's criticism of Darwinism. He said that this was a distorted picture of evolution. It was downhill from that point on.

Ruse never explained why modern evolutionary theory differs from Darwin's evolution by natural selection. Instead he spent close to an hour going over examples of "evolution by natural selection." Most of his examples were, indeed, evidence of evolution but they were not necessarily evidence of evolution by natural selection. It's clear that Micheal Ruse does not distinguish between "evolution" and "natural selection." Evidence for evolution is treated as evidence for natural selection.

By the time he finished, the audience was completely unaware of random genetic drift, or any other mechanism of evolution. Ruse never explained why anyone would even bother to ask the question he asks in the title of his talk. According to Ruse, Darwinism is still the dominant paradigm in evolutionary biology. When examining characteristics of organisms biologists always ask "What is it for?", according to Michale Ruse. The answer will be explained by natural selection. This is the adaptationist fallacy. The correct question should be "Is this "for" anything?"

I know that Ruse is more of an adaptationist than a pluralist. I know that he favors Richard Dawkins and Daniel Dennett over Stephen Jay Gould and the pluralists. That's not the problem. What bothers me most is that when giving a public lecture Ruse does not even present the other side of the issue. What would it have cost him to mention that there are many evolutionary biologists who do not think of themselves as Darwinists? Why couldn't he explain that many of us think random genetic drift—and not natural selection—is the dominant mechanism of evolution? It doesn't diminish the importance of natural selection and adaptation. It doesn't diminish the contribution of Charles Darwin who still remains the greatest scientist who ever lived.

The second talk was by Spencer Barrett of the Department of Ecology & Evolutionary Biology here at the university of Toronto. Spencer Barrett was recently appointed to the rank of University Professor, our highest rank, in recognition of his work on evolution in flowering plants.

The title of his talk was A Darwinian Perspective on the Evolution of Plant Sexual Diversity and that's an accurate reflection of its content. Spencer Barrett is an adaptationist but in terms of his research he's a very successful example of this wordview. He chooses examples from plant evolution that almost certainly are adaptive and can be explained by natural selection. When faced with a strange example of plant sexual organs, Barrett begins by asking "What is the adaptive significance?"

After lunch we were treated to a lecture by Peter and Rosemary Grant on the evolution of Darwin's Finches. Most of you know the story. The Grants have spent 30 years collecting data on finches in the Galapagos. Everything about the evolution of Darwin's finches is explained by natural selection, especially changes in beak size. It has become the dominant example of evolution by natural selection.

The last lecture was delivered by Allan Baker of the Royal Ontario Museum. his title was Modern Darwinism: Natural Selection and Molecular Evolution. Baker works on bird evolution at the molecular level. He is trying to sort out the complicated, and controversial, relationship of bird clades. Baker pointed out that there are many conflicting data sets in the field and he explained how the use of signature sequences—in his case retrotransposon insertions—can be helpful. He noted in passing that he disagrees with the recent Science paper and cautions that bird evolution is still very much up in the air.

The irony here is that Baker was not studying "Darwinian" evolution at all. In spite of his title, it's extremely unlikely that the changes he looks at are due to natural selection. This was another missed opportunity, in my opinion. Baker could have explained to this public audience that molecular evolution is not Darwinian. It is an example of random genetic drift, which, incidentally, is why there's a molecular clock.

In talking to the lecturers afterward, I tried to find out how they thought about evolution. Baker, is well aware of the importance of random genetic drift. Barrett does not agree with me when I say that random genetic drift is the dominant mechanism of evolution at the molecular level and he does not agree that drift plays a role in speciation. Professor Barrett is one of the lecturers in our first year biology course on ecology and evolution. I've pointed out previously that in my second year course the students do not understand or appreciate random genetic drift and they tell me that it is barely mentioned in first year [Freedom in the Classroom]. I really enjoyed talking to Spencer Barrett and I hope we can continue the debate at another time.

The Grants claim that their evidence for natural selection is strong enough to rule out random genetic drift during the years when most of the finch population dies of starvation. The fluctuations in between could be due to drift.

Further reading ...

What Is Darwinism?
A Confused Philosopher
Darwin and Design by Michael Ruse
Why I'm Not a Darwinist
Evolution by Accident
Random Genetic Drift
Visible Mutations and Evolution by Natural Selection
Adaptationomics
Dennett on Adaptationism
The Evolution Poll of Sandwalk Readers

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Branko Kozulic responds

Branko Kozulic has asked me to post his reply to Branko Kozulic has questions about fixation. My policy is to post letters like this without comment. We can discuss it in the comments.

I think it's an excellent example of the difficulties that many creationists will face when they try to come to grips with modern evolutionary biology.

Here's what he wants to say ...

Since Professor Moran has kindly addressed the questions I have raised, I feel obliged to respond here. But I must add that my response will be restricted to one topic only, and therefore this reply should not be construed to have the same purpose as the earlier discussion.

I find only a few minor contentious issues in Professor Moran´s post, so I prefer not to bother the readers with details about them. In my opinion, it is important that we have started to look at the core issue – the average fixation of about 100 mutations per generation, or 22,000,000 in 5,000,000 years, according to the genetic drift model - in terms of close to real-life conditions. Now we see that the simple genetic drift model needs extension, to include population splitting and recombining that leads to the postponement of fixation (I thank Professor Felsenstein for improving the clarity of this point). Furthermore, we see that in expanding populations the fixation rate is lower than the average. Thus, in today´s human population, the fixation rate per generation is close to zero. In order to compensate for the lower than the average fixation rates in some generations, it is necessary to postulate higher than the average fixation rates in other generations, if one wishes to account for the 22,000,000 fixed mutations in 5,000,000 years.

Let us consider the most dramatic case, mentioned in the comments, leading to the maximal fixation rate: the shrinking of a whole population to just a single couple, 2Ne = 2. Today we know that two unrelated human individuals differ in 1 nucleotide per about 1,000 nucleotides, so that each one of us carries about 3,000,000 SNPs. This is the maximal number (actually the maximal number is smaller because a fraction of SNPs is always in the heterozygous state) that can be fixed in this dramatic case. An interesting thing comes out to light now: the average of 100 fixed mutations per generation may result from the values that span a range of over six orders of magnitude, from less than 1, to over 1,000,000.

This raises the question of the meaning of the term “genetic drift model”. Can we maintain to be talking about the genetic drift model if the essential postulate of that model – mutation rate equals fixation rate – does not hold, because while the mutation rate changes little, the fixation rate can vary over six orders of magnitude? I think not. Drastic scenarios, known as “bottlenecks”, do not belong to the genetic drift model, in my opinion.

Now the important question is this: During the 5,000,000 years, what is the number of mutations that would have been “delayed to fix” because of the expansion of the human population, and/or due to the splitting-recombining, so that we must postulate dramatic events (“bottlenecks”) to account for their fixation? In other words, how many mutations were fixed in “bottlenecks” and how many by the ordinary course of genetic drift, in percentage? I doubt anyone can provide a verifiable answer (I kindly ask Professor Felsenstein to correct me if I am wrong). If for a “bottleneck” we take 2Ne significantly larger than 2, then many more “bottlenecks” need to be postulated in order to account for the same number of “delayed to fix” mutations. Is it possible to account for all the fixed synonymous mutations found in the human and chimp genomes by invoking fewer than two “bottlenecks” with 2Ne = 2? So that only 6 Million mutations are fixed in the “bottlenecks”, while 16 Million are fixed by genetic drift? I do not know.

And here is an additional complication. According to Wikipedia (since Professor Moran has relied on that source in his post, I follow suit):

Early humans (before Homo sapiens)

Early members of the Homo genus, i.e. Homo ergaster, Homo erectus and Homo heidelbergensis, migrated from Africa during the Early Pleistocene, possibly as a result of the operation of the Saharan pump, around 1.9 million years ago, and dispersed throughout most of the Old World, reaching as far as Southeast Asia. The date of original dispersal beyond Africa virtually coincides with the appearance of Homo ergaster in the fossil record, and the associated first emergence of full bipedalism, and about half a million years after the appearance of the Homo genus itself and the first stone tools of the Oldowan industry. Key sites for this early migration out of Africa are Riwat in Pakistan (1.9 Mya), Ubeidiya in the Levant (1.5 Mya) and Dmanisi in the Caucasus (1.7 Mya).

If correct, this information means that the time available for fixation of 22,000,000 mutations is reduced by about 2 Million years - to just about 3 Million years - because after migrating out of Africa different human sub-populations fixed different neutral mutations, due to the stochastic nature of the process. All specific human-chimp genetic differences (= all humans have them, no chimp has them, or vice versa) must have been fixed before the out of Africa migration. Is it possible to construct a genetic drift model (without “bottlenecks, with reasonable numbers) able to account for all the fixations, now within 3 Million years? I doubt it, but am willing to review a model that could dispel my doubts.

Let´s suppose that there are indeed 22 Million fixed synonymous mutations between the two genomes. I have no principal problem with that, or any other, experimentally established number. Whatever the exact number may turn out to be, scientists will continue looking for a model that fits the data best. In my opinion, no model should be rejected a priori. In order to contribute more constructively to this discussion, I ask: Why not test a model that uses 2Ne = 2 for the starting human population? With this model, for example, in the first generation 15 Million synonymous mutations might be fixed. Therefore, this model does not require multiple “bottlenecks” (perhaps just one) to account for a large fraction of the fixed mutations; while a smaller fraction - the 7 Million remaining mutations – could then be fixed in many subsequent generations in an expanding and splitting-recombining human population according to the population genetics theory.

One could argue that the starting Ne = 2 model is preferable in view of the principle known as Occham´s razor. But I would be the first one to disagree with such argumentation. Only in view of other experimental data found in the sequenced genomes one should decide which model is the preferred one; if the genome sequence data contradict one of any two models, the bad model should be rejected; and if the data contradict both, both models should be rejected.

I hope the above makes clear my thinking on this topic.

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Learning about modern evolutionary theory: the drift-barrier hypothesis

Many evolutionary biologists are engaged in research that focuses on large organisms that are (presumably) adapting to a local environment. These "field biologists" are mostly concerned with rapid evolutionary changes. Those kind of changes are almost always due to natural selection. Many of these biologists are not interested in molecular evolution and not interested in any process other than natural selection.

Unfortunately, this promotes an adaptationist mentality where all of evolution is viewed through the filter of natural selection. This is the view criticized by Stephen Jay Gould and Richard Lewontin back in 1978 when they presented the Spandrels paper at a Royal Society meeting in London (UK).

Gould, S. J. and Lewontin, R.C. (1979) The Spandrels of San Marco and the Panglossian Paradigm: A Critique of the Adaptationist Programme. Proc. R. Soc. Lond. B 205:581-598. [doi: 10.1098/rspb.1979.0086

I believe there was a substantive change in our view of evolution back in the late 1960s and early 1970s. That's when the results of evolution at the molecular level were first being published. It lead to the development of Neutral Theory, Nearly-Neutral Theory and a growing appreciation of the importance of random genetic drift. Modern population genetics was able to cope easily with this new view of evolution.

The Modern Synthesis

 
Most people do not understand current ideas about evolution. The following is a brief summary of the Modern Synthesis of Genetics and Evolution as put forth by evolutionary biologists in the late 1940s.

The idea that life on Earth has evolved was widely discussed in Europe in the late 1700s and the early part of the 1800s. In 1859 Charles Darwin supplied a mechanism—namely natural selection—that could explain how evolution occurred. Darwin's theory of natural selection helped to convince most people that life has evolved and this point has not been seriously challenged in the past one hundred and fifty years.

It is important to note that Darwin's book The Origin of Species by Means of Natural Selection did two things. It summarized all of the evidence in favor of the idea that organisms have descended with modification from a common ancestor. Darwin built a strong case for evolution. In addition, Darwin advocated natural selection as a mechanism of evolution.

Biologists no longer question whether evolution has occurred or is occurring. That part of Darwin's book is now considered to be so overwhelmingly demonstrated that is is often referred to as the FACT of evolution. However, the MECHANISM of evolution is still debated [Evolution Is a Fact and a Theory].

During the first part of this century the incorporation of genetics and population genetics into studies of evolution led to a Neo-Darwinian theory of evolution that recognized the importance of mutation and variation within a population. Natural selection then became a process that altered the frequency of genes in a population and this came to be the minimal definition evolution [What Is Evolution?].

The earliest version of this essay appears on the TalkOrigins Archive.

A later version is at Evolution by Accident.This point of view held sway for many decades but by the 1940s the classic Neo-Darwinian view was replaced by a new concept that brought together field biology, paleontology, and population genetics. The new version took pains to exclude all mechanisms except natural selection and random genetic drift. This new version was called The Modern Synthesis after the title of a 1942 book by Julian Huxley.

We have learned much since Darwin's time and it is no longer appropriate to claim that natural selection is the only mechanism of evolution. I can understand why this point may not be appreciated by the average non-scientist because natural selection is easy to understand at a superficial level. It has been widely promoted in the popular press and the image of "survival of the fittest" is too powerful and too convenient.

One of the goals of the Modern Synthesis was to reach consensus on the importance of macroevolution. The founders of the Modern Synthesis insisted that macroevolution could be explained by microevolution and no additional mechanisms—such as the bogeyman of saltation—were required.

Ernst Mayr, one of the original founders of the Modern Synthesis, sums it up this way ...

The term "evolutionary synthesis" was introduced by Julian Huxley in Evolution: The Modern Synthesis (1942) to designate the general acceptance of two conclusions: gradual evolution can be explained in terms of small genetic changes ("mutations") and recombination, and the ordering of the genetic variation by natural selection; and the observed evolutionary phenomena, particularly macroevolutonary processes and speciation, can be explained in a manner that is consistent with the known genetic mechanisms.

Ernst Mayr (1980) "Some Thoughts on the History
of the Evolutionary Synthesis" in The Evolutionary Synthesis,
E. Mayr & W.B. Provine eds. Harvard University Press.

The original version of the Modern Synthesis included mechanisms other than natural selection, especially random genetic drift. Later on, there was a hardening of the synthesis so that natural selection became the predominant mechanism and drift was relegated to a bit part (see Mayr quotation, above). The original version is described by Douglas Futuyma as ....

The major tenets of the evolutionary synthesis, then, were that populations contain genetic variation that arises by random (ie. not adaptively directed) mutation and recombination; that populations evolve by changes in gene frequency brought about by random genetic drift, gene flow, and especially natural selection; that most adaptive genetic variants have individually slight phenotypic effects so that phenotypic changes are gradual (although some alleles with discrete effects may be advantageous, as in certain color polymorphisms); that diversification comes about by speciation, which normally entails the gradual evolution of reproductive isolation among populations; and that these processes, continued for sufficiently long, give rise to changes of such great magnitude as to warrant the designation of higher taxonomic levels (genera, families, and so forth).

Futuyma, D.J. in Evolutionary Biology,
Sinauer Associates, 1986; p.12

This description would be incomprehensible to Darwin since he was unaware of genes and genetic drift. The Modern Synthesis differed from Darwinism in four important ways:

1. It defined evolution as a change in the frequency of alleles in a population; an idea based on population genetics.


2. In addition to natural selection, it recognized random genetic drift as an important mechanism of evolution.


3. It recognized that characteristics are inherited as discrete entities called genes. Variation within a population is due to the presence of multiple alleles of a gene. Variation is caused by mutation.


4. It postulated that speciation is (usually) due to the gradual accumulation of small genetic changes. This is equivalent to saying that macroevolution is simply a lot of microevolution.

The Modern Synthesis was a theory about how evolution worked at the level of genes, phenotypes, and populations whereas Darwinism was concerned mainly with organisms, speciation and individuals. This was a major shift in emphasis and those who fail to appreciate it find themselves out of step with the thinking of evolutionary biologists.

The major controversies among evolutionary biologists today concern the validity of points #2 and #4 (above).

Following the centennial celebrations of the publication of Origin in 1959, there was a gradual hardening of the Modern Synthesis. The 1960s version concentrated almost exclusively on natural selection as a mechanism and random genetic drift was pretty much ignored. Today, there is debate about the relative importance of these two mechanisms and some are calling for an updating of the "hardened" Modern Synthesis.

This update would restore random genetic drift as an important mechanism, recognize neutral theory, and incorporate molecular phylogeny (and the molecular clock).

There are many who believe that the fossil record does not show gradual change but instead long periods of stasis followed by rapid speciation. This model is referred to as Punctuated Equilibrium and it is widely accepted as true, at least in some cases. The debate is over the relative contributions of gradual versus punctuated change, the average size of the punctuations, and the mechanism.

The Modern Synthesis is challenged over the emphasis on gradualism and over the claim that microevolution is sufficient to explain macroevolution. Some evolutionary biologists suggest that evolutionary theory be modified to incorporate mechanisms that occur at levels higher than the population (e.g. species sorting). These scientists advocate an extension called hierarchical theory.

There are other challenges to the Modern Synthesis. Some of them are valid and some of them are silly. But I think it's fair to say that the 50-year old version needs some serious updating to incorporate some of the new concepts.

Some scientists continue to refer to modern evolutionary theory as Neo-Darwinian. In some cases these scientists do not understand that the field has changed but in other cases they are referring to what I have called the Modern Synthesis, only they have retained an old name from the early 1900s.

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