Evolution by chance

Can natural selection occur by chance or accident? No, with qualifications. Can evolution occur by chance or accident? Yes, definitely.

While tidying up my office I came across an anthology of articles by Richard Dawkins. It included a 2009 review of Jerry Coyne's book Why Evolution Is True (2009) and one of Richard's comments caught my eye because it illustrates the difference between the Dawkins' view of evolution and the current mainstream view that was described by Jerry in his book.

I can illustrate this difference by first quoting from Jerry Coyne's book.

This brings up the most widespread misunderstanding about Darwinism: the idea that, in evolution, "everything happens by chance" (also stated as "everything happens by accident"). This common claim is flatly wrong. No evolutionist—and certainly not Darwin—ever argued that natural selection is based on chance ....

True, the raw materials for evolution—the variations between individuals—are indeed produced by chance mutations. These mutations occur willy-nilly, regardless of whether they are good or bad for the individual. But it is the filitering of that variation by natural selection that produces natural selection, and natural selection is manifestly not random. (p. 119)

It's extremely important to notice that Coyne is referring to NATURAL SELECTION (or Dawinism) in this passage. Natural selection is not random or accidental, according to Coyne. This passage is followed just a few pages later by a section titled "Evolution Without Selection."

Let's take a brief digression here, because it's important to appreciate that natural selection isn't the only process of evolutionary change. Most biologists define evolution as a change in the proportion of alleles (different forms of a gene) in the population.

[Coyne then describes an example of random genetic drift and continues ...] Both drift and selection produce the genetic change that we recognize as evolution. But there's an important difference. Drift is a random process, while selection is the antithesis 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 rid of harmful alleles and raises the frequencies of beneficial ones. (pp. 122-123)

Now let's look at Richard Dawkins' review of Coyne's book as published in the Times Literary Supplement in 2009 and reprinted in Books Do Furnish a Life (2021). I picked out an interesting passage from that review in order to illustrate a point.

Coyne is right to identify the most widespread misunderstanding about Darwinism as 'the idea that, in evolution, 'everything happens by chance' ... This common claim is flatly wrong.' Not only is it flatly wrong, it is obviously wrong, transparently wrong, even to the meanest intelligence (a phrase that has me actively restraining myself). If evolution worked by chance, it obviously couldn't work at all. (p. 427)

That last sentence is jarring to many scientists, including me. I think that the Dawkins' statement is 'obviously wrong' and 'transparently wrong' because, as Coyne pointed out, evolution by random genetic drift can occur by chance. [Let's not quibble about the meanings of 'random' and 'chance." That's a red herring in this context.] Clearly, evolution can work by chance so why does Dawkins say it can't?

It's not because Dawkins is unaware of random genetic drift and Neutral Theory. The explanation (I think) is that Dawkins restricts his definition of evolution to evolution by natural selection. From his perspective, the fixation of alleles by random genetic drift doesn't count as real evolution because it doesn't produce adaptations. That's the view that he described in The Extended Phenotype back in 1982 and the view that he has implicitly supported over the past few decades [Richard Dawkins' View of Random Genetic Drift].

This is one of the reasons why we refer to Dawkins as an adaptationist and it's one of the reasons why so many of today's evolutionary biologists—especially those who study evolution at the molecular level—reject the Dawkins' view of evolution in favor of a more pluralistic approach.

Note: I wrote an earlier version of this post in 2009 [Dawkins on Chance] and I wrote a long essay on Evolution by Accident where I describe many other examples of evolution by chance.

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Testing Natural Selection: Part 2

 
There are several interesting articles about evolution in the Januray 2009 issue of Scientific American. One of the most interesting is an article by H. Allen Orr of the University of Rochester (NY, USA). The magazine title is "Testing Natural Selection"¹ and, as the title implies, the focus is on evolution by natural selection.

Orr's article gives us an opportunity to compare and contrast the views of an adaptationist (Orr) and a pluralistic approach to evolution.

In Testing Natural Selection: Part 1 we discussed two of Orr's opinions: (1) random genetic drift is not as common as most people think, and (2) most (if not all) visible phenotypic change is driven by natural selection.

Here, we discuss Orr's ideas about speciation.

When we say "speciation" we're talking about the biological species concept. Speciation occurs when two formerly compatible populations evolve to the point at which they can no longer interbreed. The key question is what causes this reproductive isolation and how does it evolve?

To contemporary biologists, then, the question of whether natural selection drives the origin of species reduces to the question of whether natural selection drives the origin of reproductive isolation.

For much of the 20th century, many evolutionists thought the answer was no. Instead they believed that genetic drift was the critical factor in speciation. One of the most intriguing findings from recent research on the origin of species is that the genetic drift hypothesis about the origin of species is probably wrong. Rather natural selection plays a major role in speciation.

Orr is correct to point out that random genetic drift is important in speciation. It's the mechanism described in many evolutionary biology textbooks, though it's not the mechanism that most people think about when they think about speciation.

Many biologists have always believed that natural selection plays a much more important role in speciation than random genetic drift. They aren't happy with the textbook description. Orr is one of these biologists. He now claims that the drift explanation is "probably wrong."

Let's think about what has to happen when two species become reproductively isolated. We'll use allopatric speciation as an example.²

We begin with a situation where two populations (races, subspecies) are geographically separated. There is very little gene flow between them so they evolve independently of each other. Over time, they may come to be different because each is adapting to different environments or they may just drift apart by accident. With respect to the actual speciation event, these differences don't matter.

From time to time, individuals from the two subspecies will interbreed to produce fertile offspring. This is responsible for limited gene flow between the subspecies and it proves that speciation has not occurred. If the barrier between the two populations breaks down they will merge back into a single population.

But if the two species have been separated for a long period of time, mutations that prevent interbreeding will accumulate and hybrids will become less and less viable until eventually no fertile hybrids are produced and speciation is complete. There are many ways that this can happen but a common hypothesis involves the build-up of post-zygotic genetic incompatibilities called Dobzhansky-Muller (D-M) incompatibilities.

How are D-M incompatibilites fixed in the population? If they interfere with the matings of individuals from the two populations then how come they don't contribute to infertility when individuals from the same population mate with each other? When the mutation first arises it seems to have a very strange property. It doesn't affect matings between an individual carrying the D-M allele and an individual not carrying that allele from the same population but it does affect matings between the individual carrying the new D-M allele and and an individual from the other population.

In order for this to happen there must already be some genetic differences between the two populations in terms of mating and reproduction. Those differences have accumulated in each of the populations but they must not have an effect on hybrid crosses. Presumably, the new D-M allele is not harmful in one genetic background but it is in the other.

Are these pre-existing potentiators neutral within a population, in which case they become fixed by random genetic drift? Or, are they beneficial in one of the populations, and not in the other, in which case they are fixed by natural selection? The general consensus has been that they are neutral within a population and they accumulate by accident. When enough of them become fixed the cumulative effect is to prevent hybridization. The last allele to arise, the D-M incompatibility allele, is the straw that breaks the camel's back.

Orr believes that the alleles are beneficial in one of the populations. Thus, according to him, reproductive isolation is driven by natural selection. He gives two examples.

The first one is the incomplete speciation in monkeyflower subspecies. I described this in an earlier posting [Speciation in Monkeyflowers], where I pointed out that the role of natural selection was not clear. The differences in flower color and pollinators could have arisen by selection if one postulates changes in the bee population but they could also be due to chance.

For an adaptationist like Allen Orr there's no doubt about what happened.

A good example is the evolutionary history of the two monkeyflower species mentioned earlier. Because their pollinators seldom visit the “wrong” species of monkeyflower, the two species are almost completely isolated reproductively. Even though both species sometimes occur in the same locations in North America, a bumblebee that visits M. lewisii almost never visits M. cardinalis, and a hummingbird that visits M. cardinalis almost never visits M. lewisii. Thus, pollen is rarely transferred between the two species. In fact, Schemske and his colleagues showed that pollinator differences alone account for 98 percent of the total blockage in gene flow between the two species. In this case, then, there can be no doubt that natural selection shaped the plants’ adaptations to distinct pollinators and gave rise to strong reproductive isolation.

This is not a good example of speciation by natural selection. We simply don't know if the flower color mutation spread in one of the populations because it conferred a selective advantage on individuals within that population.

Besides, these two "species" will still form viable hybrids so they're not really species in the first place.

The other example of presumed speciation by natural selection comes from studies on Drosophila There are several example of D-M incompatibility alleles that have been identified. In some of them, there is evidence at the sequence level for rapid fixation. If correct, this is a good indication that the alleles have become fixed by natural selection. The resulting reproductive isolation is an epiphenomenon.³

One example is OdsH in Drosophila mauritiana. It appears to result in an increase in sperm production so it may have been selected in the early population of this species, before it became a species. Presumably, the allele was beneficial in the genetic background that had evolved up to that point and presumably it was detrimental in the genetic background of whatever subspecies it was related to.

The genetic background is obviously part of the speciation event. I suppose that if even one of the D-M alleles is selected then it's fair to say that speciation by natural selection took place.

The question is whether this is common or not. Shucker et al. (2005) looked at post-zygotic reproduction isolation in two populations of grasshopper and provided evidence that all the D-M incompatibilities could be adequately explained by random genetic drift. We'll need to have many more examples in order to decide whether natural selection explains most speciation events.

Personally, I find it easier to understand how reproductive isolation could arise by accidental accumulation of many neutral alleles that eventually lead to reproductive isolation. It's harder to envisage alleles that confer a selective advantage within one population but are extremely detrimental in the other.

Orr doesn't agree.

The studies of the monkeyflower and of hybrid sterility in fruit flies only begin to scratch the surface of a large and growing literature that reveals the hand of natural selection in speciation. Indeed, most biologists now agree that natural selection is the key evolutionary force that drives not only evolutionary change within species but also the origin of new species. Although some laypeople continue to question the cogency or adequacy of natural selection, its status among evolutionary biologists in the past few decades has, perhaps ironically, only grown more secure.

I'm not an expert on speciation and I don't hang out with people who work in the field. However, my general impression from reading the scientific literature is that Orr's statements may be somewhat exaggerated. From what I can see, there are a great many evolutionary biologists who question the hegemony of natural selection. Their numbers seem to be growing, not shrinking.

I don't know where Orr is coming from when he implies that laypeople question the adequacy of natural selection. In my experience laypeople only think about natural selection. They have no idea that there are any other mechanisms of evolution.

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1. The website title is "Testing Natural Selection with Genetics."

2. In allopatric speciation the two diverging populations are geographically separated. That's what makes them distinct populations. In sympatric speciation the two populations may exist in the same geographical and restricted gene flow between them is due to other factors. It's easier to visualize what's happening during allopatric speciation but the logic can apply to sympatric speciation as well.

3. I don't think Orr is actually proposing that there would be selection for reproductive isolation. How would that work?

Shuker, D.M., Underwood, K., King, T.M., and Butlin, R.K. (2005) Patterns of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection. Proc. Roy. Soc. B 272:2491-2497. [DOI: 10.1098/rspb.2005.3242]

Austin Hughes and Neutral Theory

Austin Hughes (1949 - 2015) died a few years ago. He was one of my favorite evolutionary biologists.

Chase Nelson has written a nice summary of Hughes' work at: Austin L. Hughes: The Neutral Theory of Evolution. It's worth reading the first few pages if you aren't clear on the concept. Here's an excerpt ...

When the technology enabling the study of molecular polymorphisms—variations in the sequences of genes and proteins—first arose, a great deal more variability was discovered in natural populations than most evolutionary biologists had expected under natural selection. The neutral theory made the bold claim that these polymorphisms become prevalent through chance alone. It sees polymorphism and long-term evolutionary change as two aspects of the same phenomenon: random changes in the frequencies of alleles. While the neutral theory does not deny that natural selection may be important in adaptive evolutionary change, it does claim that natural selection accounts for a very small fraction of genetic evolution.

A dramatic consequence now follows. Most evolutionary change at the genetic level is not adaptive.

It is difficult to imagine random changes accomplishing so much. But random genetic drift is now widely recognized as one of the most important mechanisms of evolution.

I don't think there's any doubt that this claim is correct as long as you stick to the proper definition of evolution. The vast majority of fixations of alleles are likely due to random genetic drift and not natural selection.

If you don't understand this then you don't understand evolution.

The only quibble I have with the essay is the reference to "Neutral Theory of Evolution" as the antithesis of "Darwinian Evolution" or evolution by natural selection. I think "Neutral Theory" should be restricted to the idea that many alleles are neutral or nearly neutral. These alleles can change in frequency in a population by random genetic drift. The key idea that's anti-Darwinian includes that fact plus two other important facts:

1. New beneficial alleles can be lost by drift before they ever become fixed. In fact, this is the fate of most new beneficial alleles. It's part of the drift-barrier hypothesis.
2. Detrimental alleles can occasionally become fixed in a population due to drift.

In both cases, the alleles are not neutral. The key to understanding the overall process is random genetic drift not the idea of neutral alleles—although that's also important.

Originally proposed by Motoo Kimura, Jack King, and Thomas Jukes, the neutral theory of molecular evolution is inherently non-Darwinian. Darwinism asserts that natural selection is the driving force of evolutionary change. It is the claim of the neutral theory, on the other hand, that the majority of evolutionary change is due to chance.

I would just add that it's Neutral Theory PLUS the other effects of random genetic drift that make evolution much more random than most people believe.

Austin Hughes was a skeptic and a creative thinker who often disagreed with the prevailing dogma in the field of evolutionary biology. He was also very religious, a fact I find very puzzling.

His scientific views were often correct, in my opinion.

In 2013, the ENCODE (Encyclopedia of DNA Elements) Project published results suggesting that eighty per cent of the human genome serves some function. This was considered a rebuttal to the widely held view that a large part of the genome was junk, debris collected over the course of evolution. Hughes sided with his friend Dan Graur in rejecting this point of view. Their argument was simple. Only ten per cent of the human genome shows signs of purifying selection, as opposed to neutrality.

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We Need to Soften the Modern Synthesis

Lately there's been a lot of talk about updating evolutionary theory. Much of the hype has been generated by journalist Susan Mazur who has been drawing attention to a meeting that took place in July. At that meeting there were 16 people interested in evolution. They met at the Konrad Lorenz Institute for Evolution and Cognition Research in Altenberg, Austria. Their goal was to reach a consensus on what needs to be added to evolutionary theory in order to bring it up to date. They've been dubbed the "Altenberg 16."

The current version of evolutionary theory is often referred to as the Modern Synthesis—a term coined by Julian Huxley to describe the consensus reached by evolutionary biologists in the late 1940's. That version of evolutionary theory was appropriately pluralistic, giving prominence to random genetic drift as an important mechanism of evolution.

By the time of the Darwinian centennial celebrations in 1959, the Modern Synthesis had hardened to the point where random genetic drift was barely mentioned. Most prominent evolutionary biologists were confirmed adaptationists—including those who had been more open-minded a decade earlier.

The Altenberg 16 have some interesting ideas but unfortunately, they are also lending their reputations to some ideas that are just plain crazy. Let's see how a prominent science journalist, Elizabeth Pennisi, handles the issue in an article for Science magazine [Modernizing the Modern Synthesis].

That hyperbole has reverberated throughout the evolutionary biology community, putting Pigliucci and the 15 other participants at the forefront of a debate over whether ideas about evolution need updating. The mere mention of the "Altenberg 16," as Mazur dubbed the group, causes some evolutionary biologists to roll their eyes. It's a joke, says Jerry Coyne of the University of Chicago in Illinois. "I don't think there's anything that needs fixing." Mazur's attention, Pigliucci admits, "frankly caused me embarrassment."

That's a pretty accurate commentary on how the Alternberg 16 are viewed by most evolutionary biologists. They don't think the Modern Synthesis needs fixing. But—and this is a big "but"—they are referring to the hardened version of the Modern Synthesis; the version that can be described as ultra-Darwinian. The version that Stephen Jay Gould and others have been trying to change since 1970.

Elizabeth Pennisi seems completely unaware of this controversy in evolution. Here's how she describes modern evolutionary theory ...

Modern tradition

The modern synthesis essentially represents a marriage of the 19th century concept of evolution with Mendelian genetics, which was rediscovered at the beginning of the 20th century; the birth of population genetics in the 1920s added to the intellectual mix. By the 1940s, biologists had worked out a set of ideas that put natural selection and adaptation at evolution's core. Julian Huxley's 1942 book, Evolution: The modern synthesis, brought together this work for a broad audience.

Simply put, the modern synthesis holds that organisms have a repertoire of traits that are passed down through the generations. Mutations in genes alter those traits bit by bit, and if conditions are such that those alterations make an individual more fit, then the altered trait becomes more common over time. This process is called natural selection. In some cases, the new feature can replace an old one; in other instances, natural selection also leads to speciation.

This is definitely not the pluralism promoted by Gould and others and it's not even the original version of the Modern Synthesis published in the 1940's. Two of the key principles of the original Modern Synthesis were ...

5. Evolutionary change is a populational process: it entails, in its most basic form, a change in the relative abundances (proportions or frequencies) or individual organisms with different genotypes (hence, often with different phenotypes) within a population. One genotype may gradually replace other genotypes over the course of generations. Replacement may occur within only certain populations, or in all the populations that make up a species.

6. The rate of mutation is too low for mutation by itself to shift a population from one genotype to another. Instead, the change in genotype proportions within a population can occur by either of two principle processes; random fluctuations in proportions (genetic drift), or nonrandom changes due to the superior survival and/or reproduction of some genotypes with others (i.e., natural selection). Natural selection and random genetic drift can operate simultaneously. (Futuyma, 2005)

The hardened version of the Modern Synthesis only talks about natural selection and random genetic drift barely gets mentioned. It's too bad that Pennisi only interviewed adaptationists and it's too bad that she didn't bother to read an evolution textbook.

The current, most popular view of evolutionary theory needs to be changed. Random genetic drift needs to be restored to its rightful place. At the same time, other points of view should be considered. The problem with the current debate is that the emphasis is on the wrong problem. It's not that we need to incorporate evo-devo; instead. we need to re-incorporate well-established ideas (random genetic drift) that have been known for fifty years!

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Futuyma, D. (2005) Evolution, Sinauer Associates, Inc. Sunderland, MA, USA (p. 10)

An Adaptationist in Piazza San Marco

John Wilkins of Evolving Thoughts is currently in Venice, Italy. He has just visited the Basilica San Marco (St. Mark's Basilica) according to What I am doing on my holidays….

This visit is significant since the Spandrels of San Marco are famous in evolutionary biology. They are part of the attack on adaptationism launched in 1979 by Gould and Lewontin. This is a paper that every student of evolution should read. Here's an online version: The Spandrels of San Marco and the Panglossian Paradigm: A Critique of the Adaptationist Programme.

John has been struggling with adaptationism for almost fifteen years. When he first began studying evolutionary biology he, like many others, was unaware of the importance of random genetic drift and other anti-adaptationist perspectives. He certainly didn't know that random genetic drift is by far the dominant mechanism of evolution in terms of frequency of allele fixation. Over time John has developed an unusual perspective on adaptionism—one that I don't really understand.

Here's how he explains it in his latest posting ...

This is interesting, I think, in the context of Gould’s and Lewontin’s paper. It shows that claims of things being adaptive or not depend crucially on what one counts as the “task” of a structure. Since I think that everything is subjected to selection pressure at all times (sometimes not enough to overcome the noise of statistical properties), counting what is, and what isn’t, adaptive is a bit of a personal call, in the absence of access to the historical processes of particular traits. I am becoming more of an adaptationist these days.

The idea that many alleles might be slightly beneficial or slightly detrimental isn't very controversial. But that's not what John is saying. As I understand him, he's saying there can be no such thing as a truly neutral allele. He seems to be saying that anyone who believes otherwise is making a "personal call." A personal call that he believes is wrong since he thinks (i.e. his personal call) that everything is subject to natural selection.

He's also making a somewhat trivial point that doesn't contribute to the debate, as far as I'm concerned. Many alleles that are slightly beneficial are lost due to random genetic drift and many alleles that are slightly deleterious are fixed by random genetic drift. To me, that says that adaptationism can't explain all of evolutionary biology. To call yourself an adaptationist while knowing that slightly deleterious alleles can be fixed by random genetic drift seems somewhat unsatisfying.

John has a paper in the latest issue of Biology and Philosophy, an issue devoted to Adaptationism. It's not a very enlightening issue, from my perspective. The main problem with adaptationism isn't that it can't explain adaptation and it isn't that some just-so stories are wrong. The main problem is that adaptationists don't even consider any other alternatives to fixation by natural selection. Everything, especially everything with a visible phenotype, is automatically assumed to be adaptive and the arguments proceed from there.

One of the papers I liked was Seven Types of Adaptationism by Tim Lewens (Lewens, 2009). The seven types are:

A Empirical adaptationisms

1. Pan-selectionism–natural selection is the most significant of the evolutionary forces that act on populations.
2. Good-designism–evolutionary processes tend to result in organisms with suites of well-designed traits. Most lineages are highly evolvable.
3. Gradualism–adaptation is always the result of selection acting on gradual
variation.

B Methodological Adaptationisms

4. Weak heuristic adaptationism–those traits that are adaptations are likely to be correctly recognised as such only if we begin by assuming that all traits are adaptations.
5. Strong heuristic adaptationism–only by beginning to think of traits as adaptations can we uncover their true status, whether they are adaptations or not.

C Disciplinary Adaptationism

6. Explanatory adaptationism–an evolutionary biologist’s proper business is the study of adaptations.

D Epistemological Adaptationism

7. Epistemological optimism–investigators have access to the data that reliably discriminate between conflicting evolutionary hypotheses.

There are problems with all seven forms of adaptationism but the nice thing about Lewens' paper is that he effectively refutes #4, #5, and #7. In the case of methodological adaptationism it's just not true that the default assumption has to be adaptation. Evolutionary biology will be just as productive in the long run if drift is the default assumption and adaptation has to be proven.

In explanatory adaptationism, the assumption is that all of the interesting parts of evolution are adaptations and fixation of alleles by random genetic drift is so boring that it might as well not even be evolution. This is the stance taken by many adaptationists, like Richard Dawkins. As you might imagine, it doesn't take much effort to refute that kind of argument. One's personal opinion about what's interesting and what's not interesting should not play a role in determining how everyone else should go about studying evolution.

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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.

Lewens, T. (2009) Seven types of adaptionism. Biol. Philos. 24:161–182. [doi: 10.1007/s10539-008-9145-7]

Evolution by Accident

Evolution by Accident
v1.43 ©2006 Laurence A. Moran
This essay has been transferred here from an old server that has been decommissioned.Modern concepts of evolutionary change are frequently attacked by those who find the notions of randomness, chance, and accident to be highly distasteful. Some of these critics are intelligent design creationists and their objections have been refuted elsewhere. In this essay I'm more concerned about my fellow evolutionists who go to great lengths to eliminate chance and accident from all discussions about the fundamental causes of evolution. This is my attempt to convince them that evolution is not as predictable as they claim. I was originally stimulated to put my ideas down on paper when I read essays by John Wilkins [Evolution and Chance] and Loren Haarsma [Chance from a Theistic Perspective] on the TalkOrigins Archive.

The privilege of living beings is the possession of a structure and of a mechanism which ensures two things: (i) reproduction true to type of the structure itself, and (ii) reproduction equally true to type, of any accident that occurs in the structure. Once you have that, you have evolution, because you have conservation of accidents. Accidents can then be recombined and offered to natural selection to find out if they are of any meaning or not.
Jacques Monod (1974) p.394The main conclusion of this essay is that a large part of ongoing evolution is determined by stochastic events that might as well be called "chance" or "random." Furthermore, a good deal of the past history of life on Earth was the product of chance events, or accidents, that could not have been predicted. When I say "evolution by accident" I'm referring to all these events. This phrase is intended solely to distinguish "accidental" evolution from that which is determined by non-random natural selection. I will argue that evolution is fundamentally a random process, although this should not be interpreted to mean that all of evolution is entirely due to chance or accident. The end result of evolution by accident is modern species that do not look designed.

Dawkins on Chance

 
I know I'm going to be accused of beating a dead horse but as Emile Zucherkandl and Linus Pauling said in 1965 ...

Some beating of dead horses may be ethical, when here and there they display unexpected twitches that look like life.

It is absolutely safe to say that if you meet somebody who claims not to believe in evolution, that person is ignorant, stupid or insane (or wicked, but I’d rather not consider that).

Richard Dawkins
Richard Dawkins has reviewed Jerry Coyne's new book Why Evolution is True in The Times Literary Supplement. The text of the review is posted on RichardDawkins.net [Heat the Hornet].

As you might have guessed, when an adaptationist reviews a book by a fellow adapationist you can expect heaps of praise. Dawkins does not disappoint.

One particular claim caught my eye since Dawkins has made it in the past. I know for a fact that others have pointed out to Dawkins the flaws in this claim. Here's what he says,

Coyne is right to identify the most widespread misunderstanding about Darwinism as the idea that, in evolution, “everything happens by chance”. This common claim is flat wrong – obviously wrong, transparently wrong, even to the meanest intelligence (a phrase that has me actively restraining myself). If evolution worked by chance, it obviously couldn’t work at all.

It's true that to say everything happens by chance is wrong. However, it is not true to say that, "If evolution worked by chance, it obviously couldn’t work at all."

Here's a quotation from the most popular textbook on evolution, Evolution by Douglas J. Futuyma. It's in Chapter 10—a chapter titled Random Genetic Drift: Evolution at Random.

Almost all factors are affected simultaneously by both chance (unpredictable) and nonrandom, or deterministic (predictable), factors.... So it is with evolution. As we will see in the next chapter, natural selection is a deterministic, nonrandom process. But at the same time, there are important random processes in evolution, including mutation and random fluctuations in the frequencies of alleles or haplotypes: the process of random genetic drift.

Genetic drift and natural selection are the two most important causes of allele substitution—that is of evolutionary change—in populations

Futuyma closes the chapter with a summary of the important points. The first two are ...

1. The frequencies of alleles that differ little or not at all in their effect on organisms' fitness (neutral alleles) fluctuate at random. This process, called random genetic drift, reduces genetic variation and leads eventually to the random fixation of one allele and the loss of the other., unless it is countered by other processes, such as gene flow or mutation.
2. Different alleles are fixed by chance in different populations.

Thus, according to the textbook, evolution by chance occurs in spite of the fact that Dawkins says, "If evolution worked by chance, it obviously couldn’t work at all."

Now, the only way to reconcile his statement is to assume that either Dawkins doesn't know about random genetic drift, or he uses a non-standard definition of "evolution" (or he is wicked, but I’d rather not consider that ).

I know that Dawkins has written about random genetic drift so I have to assume that he uses a definition of the word "evolution" that excludes it. Since he is using a non-standard definition of evolution, I think it would be wise of him to make this clear in his writing. He should have written something like ...

In my opinion, the only valid mechanism of evolution is evolution by natural selection and that is definitely not a chance process. If natural selection worked by chance it obviously couldn't work at all.

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Is the high frequency of blood type O in native Americans due to random genetic drift?

The frequency of blood type O is very high in some populations of native Americans. In many North American tribes, for example, the frequency is over 90% and often approaches 100%. A majority of individuals in those populations have blood type O (homozygous for the O allele). [see Theme: ABO Blood Types]

Since there's no solid evidence that blood types are adaptive,¹ the standard explanation is random genetic drift.

Jerry Coyne explains it in Why Evolution Is True.

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.

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.

ASBMB Core Concepts in Biochemistry and Molecular Biology: Evolution

Theme

Better BiochemistryTansey et al. (2013) have described the five core concepts in biochemistry and molecular biology. These are the fundamental concepts that all biochemistry instructors must teach and all biochemistry students must understand.

The five core concept categories are:

1. evolution [ASBMB Core Concepts in Biochemistry and Molecular Biology: Evolution ]
2. matter and energy transformation [ASBMB Core Concepts in Biochemistry and Molecular Biology: Matter and Energy Transformation]
3. homeostasis [ASBMB Core Concepts in Biochemistry and Molecular Biology: Homeostasis]
4. biological information [ASBMB Core Concepts in Biochemistry and Molecular Biology: Biological Information]
5. macromolecular structure and function [ASBMB Core Concepts in Biochemistry and Molecular Biology: Molecular Structure and Function]

Random Genetic Drift and Population Size

One of the most persistent myths of evolutionary biology is that random genetic drift only occurs in small populations. You'll find this myth everywhere you look, even in textbooks that should know better. A few minutes ago I was looking for a simple way to explain this in the comments section of P-ter Accuses Me of Quote Mining when I came across this explanation in Modern Genetic Analysis by Anthony Griffiths, William Gelbart, Jeffrey Miller, and Richard Lewontin (1999 edition). This is the offspring of a textbook that David Suzuki started many years ago [ 17. Population and Evolutionary Genetics].

One result of random sampling is that most new mutations, even if they are not selected against, never succeed in entering the population. Suppose that a single individual is heterozygous for a new mutation. There is some chance that the individual in question will have no offspring at all. Even if it has one offspring, there is a chance of 1/2 that the new mutation will not be transmitted. If the individual has two offspring, the probability that neither offspring will carry the new mutation is 1/4 and so forth. Suppose that the new mutation is successfully transmitted to an offspring. Then the lottery is repeated in the next generation, and again the allele may be lost. In fact, if a population is of size N, the chance that a new mutation is eventually lost by chance is (2N − 1)/2N (For a derivation of this result, which is beyond the scope of this book, see Chapters 2 and 3 of Hartl and Clark, Principles of Population Genetics.) But, if the new mutation is not lost, then the only thing that can happen to it in a finite population is that eventually it will sweep through the population and become fixed. This event has the probability of 1/2N In the absence of selection, then, the history of a population looks like Figure 17-17. For some period of time, it is homozygous; then a new mutation appears. In most cases, the new mutant allele will be lost immediately or very soon after it appears. Occasionally, however, a new mutant allele drifts through the population, and the population becomes homozygous for the new allele. The process then begins again.

Even a new mutation that is slightly favorable selectively will usually be lost in the first few generations after it appears in the population, a victim of genetic drift. If a new mutation has a selective advantage of S in the heterozygote in which it appears, then the chance is only 2S that the mutation will ever succeed in taking over the population. So a mutation that is 1 percent better in fitness than the standard allele in the population will be lost 98 percent of the time by genetic drift.

The fact that occasionally an unselected mutation will, by chance, be incorporated into a population has given rise to a theory of neutral evolution, according to which unselected mutations are being incorporated into populations at a steady rate, which we can calculate. If the mutation rate per locus is μ, and the size of the population is N, so there are 2N copies of each gene, then the absolute number of mutations that will appear in a population per generation at a given locus is 2Nμ. But the probability that any given mutation is eventually incorporated is 1/2N so the absolute number of new mutations that will be incorporated per generation per locus is (2Nµ)(1/2N) = µ If there are k loci mutating, then in each generation there will be kμ newly incorporated mutations in the genome. This is a very powerful result, because it predicts a regular, clocklike rate of evolution that is independent of external circumstances and that depends only on the mutation rate, which we assume to be constant over long periods of time. The total genetic divergence between species should, on this theory, be proportional to the length of time since their separation in evolution. It has been proposed that much of the evolution of amino acid sequences of proteins has been without selection and that evolution of synonymous bases and other DNA that neither encodes proteins nor regulates protein synthesis should behave like a molecular clock with a constant rate over all evolutionary lineages. Different proteins will have different clock rates, depending on what portion of their amino acids is free to be substituted without selection.

This is an important conclusion. It shows that alleles are fixed in large populations by random genetic drift. I'd like it a lot if people would stop saying that drift only occurs in small populations.

Is the Modern Synthesis effectively dead?

The Modern Synthesis is the version of evolutionary theory popularized by Julian Huxley and supported by the leading evolutionary biologists of the 1930s, 40s, and 50s.

The general idea was to merge Dawrin's view of natural selection with the relatively new field of population genetics. Evolution was now defined as a change in allele frequencies in a population and the emphasis was on natural selection as the most important mechanism although, in the original version by Huxley, the fixation of alleles by random genetic drift can occur in small populations. By the early 1960s the most popular vesion of the Modern Synthesis focused almost exclusively on natural selection—an emphasis that's referred to as the hardening of the synthesis. It was this excessively adaptationist view of evolution that led to Gould and Lewontin's paper on "The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme" (Gould and Lewontin, 1979).

Evolutionary biochemistry and the importance of random genetic drift

I urge you to read an important paper that has just been published in PNAS.

Lynch, M., Field, M.C., Goodson, H.V., Malik, H.S., Pereira-Leal, J.B., Roos, D.S., Turkewitz, A.P., and Sazer, S. (2014) Evolutionary cell biology: Two origins, one objective. Proc. Natl. Acad. Sci. (USA) 111:16990–16994. [doi: 10.1073/pnas.1415861111]

Here's the bit on random genetic drift. It will be of interest to readers who have been discussing the importance of drift and natural selection in a previous thread [How to think about evolution].

Do you think Lynch et al. are correct? I do. I think it's important to emphasize the role of random genetic drift and I think it's true that most biochemists and cell biologists are stuck in an adaptationist mode of thinking.

A commonly held but incorrect stance is that essentially all of evolution is a simple consequence of natural selection. Leaving no room for doubt on the process, this narrow view leaves the impression that the only unknowns in evolutionary biology are the identities of the selective agents operating on specific traits. However, population-genetic models make clear that the power of natural selection to promote beneficial mutations and to remove deleterious mutations is strongly influenced by other factors. Most notable among these factors is random genetic drift, which imposes noise in the evolutionary process owing to the finite numbers of individuals and chromosome architecture. Such stochasticity leads to the drift-barrier hypothesis for the evolvable limits to molecular refinement (28, 29), which postulates that the degree to which natural selection can refine any adaptation is defined by the genetic effective population size. One of the most dramatic examples of this principle is the inverse relationship between levels of replication fidelity and the effective population sizes of species across the Tree of Life (30). Reduced effective population sizes also lead to the establishment of weakly harmful embellishments such as introns and mobile element insertions (7). Thus, rather than genome complexity being driven by natural selection, many aspects of the former actually arise as a consequence of inefficient selection.

Indeed, many pathways to greater complexity do not confer a selective fitness advantage at all. For example, due to pervasive duplication of entire genes (7) and their regulatory regions (31) and the promiscuity of many proteins (32), genes commonly acquire multiple modular functions. Subsequent duplication of such genes can then lead to a situation in which each copy loses a complementary subfunction, channeling both down independent evolutionary paths (33). Such dynamics may be responsible for the numerous cases of rewiring of regulatory and metabolic networks noted in the previous section (34, 35). In addition, the effectively neutral acquisition of a protein–protein-binding interaction can facilitate the subsequent accumulation of mutational alterations of interface residues that would be harmful if exposed, thereby rendering what was previously a monomeric structure permanently and irreversibly heteromeric (8, 36–39)¹. Finally, although it has long been assumed that selection virtually always accepts only mutations with immediate positive effects on fitness, it is now known that, in sufficiently large populations, trait modifications involving mutations with individually deleterious effects can become established in large populations when the small subset of maladapted individuals maintained by recurrent mutation acquire complementary secondary mutations that restore or even enhance fitness (40, 41).

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1. Note the brief description of how irreversibly complex structures can evolve. This refutes Michael Behe's main point, which is that irreversibly complex structures can't have arisen by natural processes and must have been designed. We've known this even before Darwin's Black Box was published.

What Is Darwinism?

Over on the thread Close, but no cigar we're having a little discussion about the meaning of the term "Darwinian." I explained it as "evolution by natural selection."

Pete Dunkelberg is one of those people who emphasize natural selection in their discussion of evolution and he didn't like my description of Darwinian evolution. Pete said,

Misbegotten terminology. "darwinian processes" is creationist coinage with no meaning.

Talking of "darwinism" in biology is akin to talking of "newtonism" in physics: a bad idea. Aren't you glad physicists don't use terms like that to make polemics against each other?

wolfwalker asks: Larry, what do people mean by [these unneeded terms]? Larry tells him what Larry means. But the terms have no standard meaning. Larry's official ruling is that Darwin never heard of variable rates of morphological evolution and also thought selection was all.

It is patently untrue that the term "Darwinian" has no meaning in biology. Pete's position is that "Darwinist" refers to evolutionary biologists who no longer exist. He seems to think that everyone has become a pluralist these days. I beg to differ.

Core Darwinism, I shall suggest, is the minimal theory that evolution is guided in adaptively nonrandom directions by the nonrandom survival of small hereditary changes.... Adaptive does not imply that all evolution is adaptive, only that core Darwinism's concern is limited to the part of evolution that is.

Dawkins, R. (2003) The Devil's Chaplain p. 81 In physics, everyone knows that Newtonian physics has been extended in the twentieth century so that it's no longer accurate to refer to oneself as a Newtonian physicist since it implies ignorance of relativity. But this is a bad analogy since there are a great many evolutionary biologists (and even more of the other kinds of biologists) who are proud to call themselves Darwinists. Modern Darwinists place a great deal of emphasis on adaptation and natural selection as the main mechanisms of evolution.

Pete is dead wrong when he claims that, "Larry's official ruling is that Darwin never heard of variable rates of morphological evolution and also thought selection was all." I never said any such thing. I'm well aware of the fact that Darwin considered variable rates of natural selection and I'm well aware of the fact that he accepted other mechanisms of evolution, such as a watered down version of Lamarckism. The problem here seems to be that Pete doesn't understand the meaning of gradualism and he doesn't understand that modern Darwinists do not attribute everything in biology to selection.

As for the standard meaning of "Darwinism," Pete is correct to say that there is no universally accepted definition but that shouldn't be a surprise to anyone. There's hardly anything that all biologists can agree on.

However, there is a considerable group of evolutionary biologists who agree with Ernst Mayr when he says ...

After 1859, that is, during the first Darwinian revolution, Darwinism for almost everybody meant explaining the living world by natural processes. As we will see, during and after the evolutionary synthesis the term "Darwinism" unanimously meant adaptive evolutionary change under the influence of natural selection, and variational instead of transformational evolution. These are the only two meaningful concepts of Darwinism, the one ruling in the nineteenth century (and up to about 1930) and the other ruling in the twentieth century (a consensus having been reached during the evolutionary synthesis). Any other use of the term Darwinism by a moder author is bound to be misleading.

Mayr, E. (1991) What Is Darwinism? in One Long Argument p. 107.

See Why I'm Not a Darwinist for an earlier use of this quotation. The point is that the modern meaning of Darwinism is usually taken to mean an emphasis on natural selection.

Mayr explains the standard adaptationist view of random genetic drift by equating it with Neutral Theory and mischaracterizing the entire controversy. (This seems to be a very common trait among the defenders of strict Darwinism.)

The neutralists are reductionists, and for them the gene—more precisely the base pair—is the target of selection. Hence, any fixation of a "neutral" base pair is a case of neutral evolution. For the Darwinian evolutionists, the individual as a whole is the target of selection, and evolution takes place only if the properties of the individual change. A replacement of neutral genes is considered merely evolutionary noise and irrelevant for phenotypic evolution. (ibid p. 152)

I'm not making this up. I'm trying to do my best to represent the standard—but not universal—description of the adaptationist position. It's quite wrong for Pete Dunkelberg to pretend that the definition of Darwinism and the adaptationists is something that I created. (BTW, most pluralists treat the individual as the unit of evolution. They just believe that populations can fix alleles, even alleles with visible phenotypes, by random genetic drift as well as natural selection.)

Mayr continues,

The Darwinian wonders to what extent it is legitimate to designate as evoluton the changes in gene frequencies caused by nonselected random fixation. In some of the older (particularly nineteenth century) literature on evolution, one finds discussions on how to discriminate between evolution and mere change. There it was pointed out that the continuing changes in weather and climate, the sequences of the seasons of the year, the geomorphological changes of an eroding mountain range or a shifting river bed, and similar changes do not qualify as evolution. Interestingly, the changes in nonselected base pairs and genes are more like those nonevolutionary changes than they are like evolution. Perhaps one should not refer to non-Darwinian evolution but rather to non-Darwinian changes during evolution. (ibid p. 153)

While this position may seem extreme by 2007 standards, I believe that there are many evolutionary biologists who tend to dismiss all nonselected evolutionary change as uninteresting and unimportant. They are Darwinists. The extremists among this group attribute all kinds of things to adaptation, including most animal behavior. They are the ultra-Darwinians.

Many books have been written about the controversy in evolutionary biology between the adaptationists and the pluralists. Michael Ruse, for example, tried to explain it all last year (2006) in Darwinism and Its Discontents. Ruse is a firm believer in Darwinism, which he defines as "natural selection as the chief causal process behind all organisms." This is a common definition as explained above. However, one must read between the lines to see how Darwinists interpret that definition. A key point is what they think about random genetic drift. Here's how the Darwinist Ruse treats Sewall Wright's concept of random genetic drift.

Wright's theory is not very Darwinian. Natural selection does not play an overwhelming role. Genetic drift is a key player in Wright's world. However, although many of these ideas were taken up by later thinkers, especially by Theodosius 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 (Lewontin, 1981). 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.

Michael Ruse is not an evolutionary biologist but he represents the views of Dawkins and, to a lesser extent, E.O. Wilson. They have no use for drift especially when it comes to visible characteristics. That's the hallmark of modern Darwinism.

So, is it true that no evolutionary biologist would want to say that drift is a major player in evolution? Of course not. There are lots of them who say exactly that in spite of what Michale Ruse would have you believe. Does Ruse have an answer to these "discontents?" Yes, he does ...

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

To which I reply, you took the risk and your scholarship has been discredited. I can't speak for God.

What William the Conqueror's Companions Teach Us about Effective Population Size

My mother has been working on genealogy for several decades. She recently gave me a little book called My Ancestors Came with the Conqueror by Anthony J. Camp, first published in 1988. Camp is a professional genealogist. Before discussing this book, I should let you know that the relationship between professional genealogists and the amateur genealogy found on ancestry.com is similar to the relationship between scientists and Intelligent Design Creationism.

It's estimated that half the population of Great Britain claims to have descended from William the Conqueror who defeated King Harold at the Battle of Hastings in 1066. Not all claims meet the rigorous standards of professional genealogists but it's quite reasonable that there are millions of direct descendants of William.

Back in 1400 it was less likely that you were a descendant of William because there were fewer generations and fewer descendants. This was a problem for aspiring nobility and minor landholders so they tended to settle for the next best thing—they claimed descent from one of the companions of William who accompanied him from Normandy and fought at the Battle of Hastings. Gradually the list of companions grew and grew because if you couldn't prove you were related to an existing companion, you just made one up.

Many genealogists and historians have analyzed the various lists of companions. Some lists have over three hundred names but there are only about 20 companions who are definitely known to have been present at the Battle of Hastings in 1066 [William the Conqueror's Companions, The Companions of the Conqueror]. The Order of the Conqueror’s Companions is part of a genealogical society that traces descendants of the companions of William the Conqueror. They list 39 known companions.

Let's assume that there are 20 well-documented companions. Only one of these (William Mallet) has possibly passed on his Y chromosome to the present time and even that male line of descent is disputed. This is fully consistent with our understanding of genetics when you consider that most male lines are likely to die out in a few generations. Those that survive ten generations or so are unlikely to become extinct since there will likely be several male lines at that time.

Only 10 of the companions have descendants who are alive today. This could be due to the fact that genealogists don't have perfect records for all the companions and their families but it's also quite in line with expectations.¹ You don't expect that all 20 families will avoid extinction. What this means is that for a random "population" of 40 individuals (20 companions plus their wives), only 20 of them contributed alleles to the present population after 50 generations.²

The take-home lesson from these genealogical studies is that the actual population size at a given point in time is not the same as the actual number of individuals who contribute to the gene pool over the long term.

This has long been known to population geneticists. They define a new term, N_e, called the "effective population size." In order to understand the definition of effective population size, you have to keep in mind that most of the variation in a given population is due to the presence of nearly neutral alleles whose frequency is fluctuating under the influence of random genetic drift. The parameter of interest, N_e, represents the theoretical number of individual in a population of size N who actually contribute to the variation in a population.

The definition is from Sewell Wright [Effective Population Size] ...

Effective population size is "the number of breeding individuals in an idealized population that would show the same amount of dispersion of allele frequencies under random genetic drift or the same amount of inbreeding as the population under consideration."

The effective population size is always less than the actual population (N_e < N). Sometimes it's a lot less. In most vertebrates, for example, the long-term effective population size is calculated to be about 10,000.

Why is this important? It's important because evolution is important for understanding biology and in order to understand evolution you need to understand population genetics. One of the important lessons from population genetics is that the relative important importance of natural selection and random genetic drift is dependent on effective population size. This is a major theme in Michael Lynch's book The Origins of Genome Architecture.

He argues that the effective population size of most large multicellular animals (e.g. Homo sapiens) was small enough to render natural selection impotent for most alleles that might have been somewhat beneficial in larger populations. This led to loss of such beneficial alleles by random genetic drift and to frequent fixation of mildly deleterious alleles by drift. Thus, even if the accumulation of large amounts of junk DNA, for example, was slightly deleterious, it cannot be eliminated by natural selection when the effective population size is small.

Furthermore, many alleles with small beneficial effects cannot possibly become fixed in such a population so it's silly to construct a model that relies on fixation of alleles with a small advantage. This leads to his theory of the evolution of genome complexity by nonadaptive processes. According to Lynch, the default explanation is random genetic drift and because this accounts for much of genome architecture, there's no reason to invoke natural selection to explain what we observe.

Lynch devotes an entire chapter (Chapter 4) to Why Population Size matters. I'm hoping to get more people interested in this subject by giving them a simple example of the difference between actual population size (N) effective population size (N_e).

This isn't only important in genome evolution. As most of you know, the effective population size is an important consideration in recent human evolution [From genes to numbers: effective population sizes in human evolution] and many other disciplines.

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1. The reason we focus on nobility isn't because they are more important, genealogically, than the 8,000 other soldiers at the battle. It's because we don't have any records of those other potential ancestors.

2. This doesn't mean that all of the alleles in the other 20 individuals were lost because many of them could have been passed down from siblings, aunts, uncles etc.

Kevin Laland's view of "modern" evolutionary theory (again)

Kevin Laland has just published another critique of modern evolutionary theory. This one appears in Aeon [Evolution unleashed]. His criticism is based on a naive and outdated view of modern evolutionary biology. That view has been widely criticized in the past but Laland continues to ignore such criticisms [e.g. Kevin Laland's new view of evolution].

Here's how he describes the state of modern evolutionary biology.

If you are not a biologist, you’d be forgiven for being confused about the state of evolutionary science. Modern evolutionary biology dates back to a synthesis that emerged around the 1940s-60s, which married Charles Darwin’s mechanism of natural selection with Gregor Mendel’s discoveries of how genes are inherited. The traditional, and still dominant, view is that adaptations – from the human brain to the peacock’s tail – are fully and satisfactorily explained by natural selection (and subsequent inheritance). Yet as novel ideas flood in from genomics, epigenetics and developmental biology, most evolutionists agree that their field is in flux. Much of the data implies that evolution is more complex than we once assumed.

Why doesn't natural selection reduce the mutation rate to zero?

All living organisms have developed highly accurate DNA replication complexes and sophisticated mechanisms for repairing DNA damage. The combination results in DNA replication errors that are about 1 per 10 billion base pairs (10^-10 per bp). DNA damage due to other factors is effectively repaired with an error rate of 1 in 100 per base pair (10^-2 per bp).

Mutations can be beneficial, deleterious, or neutral. In organisms with large genomes there are many more neutral mutations than the other two classes but in organisms with smaller genomes a higher percentage of mutations are either beneficial or deleterious. In all cases, there are more deleterious mutations than beneficial ones.

If deleterious mutations are harmful to the individual then natural selection should favor a low mutation rate in order to minimize that effect. This is especially true in large multicellular organisms where somatic cell mutations cause cancer and other problems. It seems logical that the optimal mutation rate should be zero in order to maximize the survival of the individual and its offspring.

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

Michael Lynch
But even though the number of beneficial mutations is low compared to those that are deleterious, this is the stuff of adaptive evolution. In the long run the population will become more fit if beneficial mutations occur and become fixed by natural selection. Eliminating mutations might provide a short-term advantage but eventually the population will go extinct if it can't adapt to new environments. (Neutral and deleterious mutations can also contribute to adaptation over the long term.)

The simplest explanation for this apparent paradox is that there's a trade-off between selection to minimize deleterious mutations and selection for long-term evolutionary advantage. The problem with that explanation is that it is very difficult to show how you can select for the future benefit of mutations to the species (population). It seems as though you have to invoke two bogeymen; group selection and teleology.

Maybe there's a better explanation?

Jerry Coyne recently thought about this problem and posted his analysis under the provocative title: The irony of natural selection. He concludes that there's some constraint that limits the ability of natural selection to achieve a zero mutation rate.

The most probable explanation is that evolution does not produce perfect adaptations. In the case of mutations, though natural selection favors individuals most able to repair any changes in DNA (although a small percentage of these might be adaptive), this level of perfection cannot be achieved because of constraints: the cost of achieving perfection, the fact that all errors are impossible to detect or remove, or that some cells (i.e., sperm or eggs) may not even have DNA-repair mechanisms because of genetic or physiological constraints.

I used to think that this was the best explanation. I taught my students that the accuracy of DNA replication, for example, comes at the cost of speed. The more accurate the polymerization process, the slower it takes. This makes a lot of sense and there's experimental support for the claim. Slowing down the time it takes to replicate the genome will affect the time it takes for cell divisions and that could be harmful ... or so the argument goes.

Unfortunately, I ran into Michael Lynch at an evolution meeting and he quickly destroyed that argument. There's no evidence that the speed of DNA replication is limiting the rate of cell divisions and, besides, there are easy ways for selection to get around such a limitation if it ever occurred. (This is a photo of Michael Lynch looking at me right after setting me straight. He's wondering how I could have been so stupid.)

When you think about it, there doesn't seem to be any biochemical or physiological constraints that could prevent the mutation rate from getting to zero ... or at least a lot closer than it is now.

Michael Lynch has a better answer and he explains it in a paper titled: "The Lower Bound to the Evolution of Mutation Rates" (Lynch, 2011).

As the mutation rate is driven to lower and lower levels by selection, a point must eventually be reached where the advantage of any further increase in replication fidelity is smaller than the power of random genetic drift (Lynch 2008, 2010). The goal here is to evaluate the extent to which such an intrinsic barrier can provide an adequate explanation for the patterns of mutation rates known to have evolved in natural populations.

The main "constraint" is the limited power of natural selection in the presence of random genetic drift. This will depend to some extent of the size of the population.

This idea is called the "drift-barrier hypothesis. It is described in Sung et al. (2012):

... the drift-barrier hypothesis predicts that the level of refinement of molecular attributes, including DNA replication fidelity and repair, that can be accomplished by natural selection will be negatively correlated with the effective population size (N_e) of a species. Under this hypothesis, as natural selection pushes a trait toward perfection, further improvements are expected to have diminishing fitness advantages. Once the point is reached beyond which the effects of subsequent beneficial mutations are unlikely to be large enough to overcome the power of random genetic drift, adaptive progress is expected to come to a standstill. Because selection is generally expected to favor lower mutation rates as a result of the associated load of deleterious mutations, and because the power of drift is inversely proportional to N_e, lower mutation rates are expected in species with larger N_e.

The Lynch lab has produced lots of evidence in support of the hypothesis although there may be some confounding factors in some populations.

The bottom line is that the real irony of natural selection is that it's just not powerful enough to reduce the error rate of replication and repair below the values we currently see.

In a sense, it's the "error rate" of fixation by natural selection in the face of random genetic drift that allows evolution to occur.

The more we learn about biology the more we learn that it's messy and sloppy at every level. Evolution is not a watchmaker and it's not even a blind watchmaker. It's a tinkerer¹ and the "watch" barely keeps time.

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Image Credit: The Mendel's traits image is from Wikispaces Classroom.

1. Jacob, F. (1977) Evolution and tinkering. Science (New York, NY), 196:1161. [PDF]

Lynch, M. (2011) The lower bound to the evolution of mutation rates. Genome Biology and Evolution, 3:1107. [doi: 10.1093/gbe/evr066]

Sung, W., Ackerman, M.S., Miller, S.F., Doak, T.G., and Lynch, M. (2012) Drift-barrier hypothesis and mutation-rate evolution. Proc. Natl. Acad. Sci. (USA) 109:18488-18492. [doi: 10.1073/pnas.1216223109]

Michael Denton and Molecular Clocks

It's easy to construct a phylogenetic tree using cytochrome c sequences (left). The tree shows us that bacteria and eukaryotes form two separate branches just as predicted by evolution. Within the eukaryote branch, we see that plants, fungi, and animals form distinct groups. Again, this is exactly what evolution predicted.

One of the remarkable things about these trees is that the branches have similar lengths. Beginning at the base of the tree, the distance to plants, animals, fungi, and bacteria is about the same. It differs by a factor of two, at most, for any species. This is evidence of a molecular clock—a roughly constant rate of evolutionary change for every lineage over a period of hundreds of millions of years. (Cytochrome c is not the ideal sequence for showing this since it's pretty small as far as proteins go. Substitutions of only a few amino acids can make a big difference to branch lengths. Larger proteins show more regular molecular clocks.)

We know why there's a molecular clock. It's because the vast majority of changes in the amino acid sequences of proteins are due to fixation of neutral, or nearly neutral, mutations by random genetic drift. As with any stochastic process, the law of large numbers produces a predictable pattern. In this case, a relatively constant rate of change over hundreds of millions of years.

As it turns out, the overall rate of fixation of neutral alleles should be close to the mutation rate. This is a conclusion derived from population genetics models and those models are well supported by evidence. Since mutation rates are similar, if not identical, between species this rate becomes roughly constant in each lineage. The branch lengths in the cytochrome c tree reflect this indirectly since they result from a combination of fixation times and mutation rates. Furthermore, they are amino acid sequences so a lot of the underlying mutations at the nucleotide level are hidden.

Michael Denton knows of this population genetics explanation since he mentions it on page 289 of Nature's Destiny: How the Laws of Biology Reveal Purpose in the Universe.

Comparisons of these two rates, the rate of mutation and the evolutionary substitution rate, have revealed the very surprising fact that the two rates are the same. This remarkable finding that the difference between the DNA sequences of different species have been generated by mutation and that other factors such as natural selection could only have played a relatively minor role.

Denton knows that the data supports such an idea because he brings up cytochrome c on the next page.

By comparing sequences a curious pattern was observed. For example, in the case of cytochromes, all the higher organism cytochromes (yeasts, plants, insects, mammals, birds, etc.) exhibit an almost equal degree of sequence divergence from the bacterial cytochrome in Rhodospirillum. This means that all their cytochrome genes have changed to about the same degree—in other words, have evolved at a uniform rate.

The uniform rate of change is what impresses Michael Denton. As I mentioned above, Denton knows that adaptation (selection) is ruled out as an explanation. Unlike many other IDiots, Denton knows that pan-adaptationism (often called Darwinism) is not the prevailing view in evolutionary biology.

Random genetic drift is a perfectly reasonable explanation of the molecular clock but Denton rejects that explanation. He says that,

Explanations of uniform rates of evolution in protein genes in terms of genetic drift of neutral mutations fare no better. The rate of genetic drift in a population is determined by the mutation rate. This is not controversial. Although mutation rates for many organisms are somewhat similar per generation time—10^-6/gene/generation—the problem is that generation times are vastly different, so that the rate of mutation per year in, say, yeast, may be 100,000 times greater than a tree or a mammal such as man or elephant, organisms that have long generation times. (p. 291)

The generation time argument is a bit bogus for several reasons. First, mutation rates are based on changes per cell division (replication) and not generation time. Thus, in mammals such a mouse, there are about 50 cell divisions between zygote and gamete and the organism reproduces in about 100 days. Thus, there is, on average, one mutation-causing replication event every two days. This is no more than the average "generation time" of single-celled organisms such as yeast or bacteria. (Bacteria divide once every few days, at most, contrary to what most people believe.)

The second reason for skepticism is that for most of the history of life the "generation time" of different organisms isn't that much different. Large terrestrial mammals, for example, have only been around for about 15% of the time since single-celled life began.

Molecular biologists and population geneticists have thought about these things. They conclude that the evidence favors the idea that phylogenetic trees are due to fixation of nearly neutral alleles by random genetic drift. This explains the molecular clock.

Denton doesn't buy it. He thinks the molecular clock proves Intelligent Design Creationism.

These twin discoveries—that the mutation rate equals the evolutionary substitution rate, and that the rate of change in many genes is regulated by a clock which seems to tick simultaneously in all branches of the tree of life—may represent the first evidence, albeit indirect, that the mutational processes that are changing the DNA sequences of living things over time are indeed directed by some as yet unknown mechanism, or more likely mechanisms. Of course, these discoveries do not prove directed evolution, but it is far easier to imagine them as the outcome of some sort of direction than the outcome of purely random processes. (p. 292)

In other words, Michael Denton can't imagine how stochastic evolutionary processes might work, so God did it. Another argument from ignorance, albeit an ignorance that's on a much higher level than the ignorance usually on display on creationist websites and blogs. (Michael Denton is by far, the most knowledgeable IDiot when it comes to understanding evolution and molecular biology. Perhaps it's why he's out of favor with the true IDiots.)

The neutralist-selectionist debate in 2024

The neutral theory was first proposed by Mootoo Kimura in 1968 (Kimura, 1968). The following year, a similar idea was published in a seminal paper by Jack King and Thomas Jukes (King and Jukes, 1969). King and Jukes emphasized the importance of non-Darwinian mechanisms of evolution in order to explain protein based phylogenetic trees and the molecular clock. They made it clear that neutral alleles fixed by random genetic drift play an important part in evolution.

There appears to be considerable latitude at the molecular level for random genetic changes that have no effect upon the fitness of the organism. Selectively neutral mutations, if they occur, become passively fixed as evolutionary changes through the action of random genetic drift.

The idea of selectively neutral changes at the molecular level has not been readily accepted by many classical evolutionists, perhaps because of the pervasiveness of Darwinian thought (King and Jukes, 1969).