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.

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.

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.

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.

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]

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.

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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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.]

A Confused Philosopher

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

The 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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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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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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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]