The selfish gene vs the lucky allele

The Selfish Gene was published forty-one years ago (1976) and last year there was a bit of a celebration. I think we can all appreciate the impact that the book had at the time but I'm not sure it's as profound and lasting as most people believe ["The Selfish Gene" turns 40] [The "selfish gene" is not a good metaphor to describe evolution] [Die, selfish gene, die!].

The main criticisms fall into two categories: (1) the primary unit of selection is the individual organism, not the gene, and (2) the book placed too much emphasis on adaptation (Darwinism). I think modern evolutionary theory is based on 21st century population genetics and that view puts a great deal of emphasis on the power of random genetic drift. The evolution of a population involves the survival of individuals within the population and that, in turn, depends on the variation that exists in the population. Thus, evolution is characterized by changes in the frequencies of alleles in a population.

Some alleles confer a beneficial effect on the individuals that carry them but whether those alleles become fixed will depend on a number of features (i.e. population size). Most of them will be lost before they ever become fixed unless the beneficial effect (selection coefficient) is very high. Thus, even beneficial alleles are often more "lucky" than "selfish." In addition, a large number of alleles are effectively neutral and changes in their frequencies are more due to luck than anything else.

No metaphor will accurately describe all of evolution but I would argue that in communicating to the general public (and other scientists) the term "lucky allele" is just as appropriate as "selfish gene." I would also argue that Gould's hierarchical view of evolution as a process occurring at a number of levels (gene, organism, population, species) is better than Dawkins' view where all the emphasis is evolution at the gene level.

It's interesting to see how Richard Dawkins has responded to all the criticism over the years. He published a new edition in 1989 where he stated (p. x) that, "In the dozen years since The Selfish Gene was published its central message has become textbook orthodoxy."

I don't think that's correct. I have pointed out on many occasions that the book is rarely mentioned in modern textbooks and the central messages—evolution at the gene level and adaptationism—are not really textbook orthodoxy.

In the 1989 edition, Dawkins makes sure that readers understand his view of evolution.

The selfish gene theory is Darwin's theory, expressed in a way that Darwin did not choose but whose aptness, I should like to think, he would instantly have recognized and delighted in. It is in fact a logical outgrowth of orthodox neo-Darwinism, but expressed as a novel image. Rather than focus on the individual organism, it takes a gene's-eye view of nature. It is a different way of seeing, not a different theory.

I don't think this way of seeing (gene's-eye view) has become textbook orthodoxy. I think the main emphasis in evolutionary biology textbooks is on the individual as the unit of selection. I also don't think that Darwin's Theory of Natural Selection is seen today as the only way to explain evolution—yet that's the view you get from reading The Selfish Gene. I think Dawkins is correct to say that his book is based on orthodox neo-Darwinism but by the 1980s evolutionary theory had moved beyond that view (Gould and Lewontin, 1979).

Richard Dawkins has just published an article in The Skeptical Inquirer outlining his current view of evolution and how it relates to The Selfish Gene [The Selfish Gene Revisited]. Let's look at it to see if his views have changed over the years. He begins with a defense of the word "gene."

In some ways I would quite like to find ways to recant the central message of The Selfish Gene. So many exciting things are fast happening in the world of genomics, it would seem almost inevitable—even tantalizing—that a book with the word "gene" in the title would, forty years on, need drastic revision if not outright discarding. This might indeed be so, were it not that "gene" in this book is used in a special sense, tailored to evolution rather than embryology. My definition is the population geneticists’ definition adopted by George C. Williams, one of the acknowledged heroes of the book, now lost to us along with John Maynard Smith and Bill Hamilton: "A gene is defined as any portion of chromosomal material that potentially lasts for enough generations to serve as a unit of natural selection." I pushed it to a somewhat facetious conclusion: "To be strict, this book should be called . . . The slightly selfish big bit of chromosome and the even more selfish little bit of chromosome." As opposed to the embryologist’s concern with how genes affect phenotypes, we have here the neo-Darwinist’s concern with changes in frequencies of entities in populations. Those entities are genes in the Williams sense (Williams later called that sense the “codex”). Genes can be counted and their frequency is the measure of their success.

This is complicated. It's perfectly understandable that Dawkins is using the term "selfish gene" as a metaphor but what I don't understand is why today, forty-one years later, he still avoids using the word "allele." And I can understand the word "selfish" as a metaphor to emphasize the power of natural selection but why does Dawkins continue to emphasize the connection between "gene" and "the unit of natural selection" when he knows full well that many "genes" (alleles) survive by luck and not by selfishness? Surely he knows of dozens of "genes" (alleles) that are invisible to natural selection?

A gene achieves its numerical success in the population by virtue of its (phenotypic) effects on individual bodies. A successful gene is represented in many bodies over a long period of time. It helps those bodies to survive long enough to reproduce in the environment. But the environment means not just the external environment of the body—trees, water, predators, etc.—but also the internal environment, and especially the other genes with which the selfish gene shares a succession of bodies through the population and down the generations. It follows that natural selection favours genes that flourish in the company of other genes in the breeding population. Genes are indeed "selfish" in the sense promoted in this book.

Nobody questions the idea that the "selfish" description applies metaphorically to some "genes" (alleles). But it would be nice to see Richard acknowledge two ideas that really are part of textbook orthodoxy: (1) many alleles have no observable phenotype, and (2) many alleles survive (become fixed) by luck and not by selection. I'm puzzled by the fact he didn't take advantage of forty-one years of criticism to acknowledge that the selfish gene metaphor is not a universal description of evolutionary theory.

The next part of his article is a defense of inclusive fitness. Dawkins is an ethologist and he makes it very clear in the original 1976 edition that the book is about animal behavior (p. vi).

I am an ethologist, and this is a book about animal behavior. My debt to the ethological tradition in which I was trained will be obvious.

Fair enough. The Selfish Gene is a book about evolution as it applies to animal behavior so it's not a surprise that Hamilton's views on inclusive fitness would play a prominent role. The problem it is that a generation of readers have assumed that the book is about evolution in general and not a particular aspect of it that happens to interest Richard Dawkins. Dawkins concedes that his view of evolutionary theory only applies to sexually reproducing organisms, thus ruling out the majority of organisms on the planet, but he doesn't really respond to criticisms of his ethological perspective and how inclusive fitness applies to most changes in allele frequencies in a population. All he does is admit this bias, "A central point of the book is the one developed by my friend the great Bill Hamilton, whose death I still mourn. Animals are expected to look after not only their own children but other genetic relatives."

The last part of his recent essay is about coalescence and the dating of allele divergences. In this section he mentions alleles once but then uses the word "genes" to describe two alleles. I don't know why he does this. He explains how you can date the origin of different alleles using coalescence theory and how it can lead to estimates of population size in the past. Then he says,

To summarize, the gene’s eye view of life, the central theme of this book, illuminates not just the evolution of altruism and selfishness, as expounded in previous editions. It also illuminates the deep past, in ways of which I had no inkling when I first wrote 
The Selfish Gene and which are expounded more fully in relevant passages (largely written by Yan, my co-author) of the second edition (2016) of The Ancestor’s Tale. So powerful is the gene’s eye view, the genome of a single individual is sufficient to make quantitatively detailed inferences about historical demography.

I don't understand coalescent theory even though I have access to textbooks by Dan Graur and Joe Felsenstein. However, my readings suggest that it owes very little to the concept of a selfish gene and to orthodox Darwinism. It seems to me that you need a deep understanding of random genetic drift and the effect of population sizes in order to explain coalescence. Here's how Douglas Futuyma explains it in the second edition (2009) of his textbook Evolution.

Earlier in this chapter, we introduced the principle of genetic drift by showing that because gene lineages within a population become extinct by chance over the course of time, all gene copies in a population today are descended from one gene copy that existed at some time in the past. The genealogical history of genes in populations is the basis of COALESCENT THEORY.

I didn't get such an understanding of drift and effective population sizes from reading The Selfish Gene. Surely this is a place where Dawkins could have mentioned the limitations of his forty-year-old gene's-eye view of evolution and how modern evolutionary theory has advanced beyond it in the 21st century?

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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. Proceedings of the Royal Society of London. Series B. Biological Sciences, 205:581-598. [doi: 10.1098/rspb.1979.0086]