"The Selfish Gene" turns 40

Richard Dawkins published The Selfish Gene 40 years ago and Matt Ridley notes the anniversary in a Nature article published today (Jan. 28, 2016): In retrospect: The selfish gene.

I don't remember when I first read it—probably the following year when the paperback version came out. I found it quite interesting but I was a bit put off by the emphasis on adaptation (taken from George Williams) and the idea of inclusive fitness (from W.D. Hamilton). I also didn't much like the distinction between vehicles and replicators and the idea that it was the gene, not the individual, that was the unit of selection ("selection" not "evolution").

It is finally time to return to the problem with which we started, to the tension between individual organism and gene as rival candidates for the central role in natural selection...One way of sorting this whole matter out is to use the terms ‘replicator’ and ‘vehicle’. The fundamental units of natural selection, the basic things that survive or fail to survive, that form lineages of identical copies with occasional random mutations, are called replicators. DNA molecules are replicators. They generally, for reasons that we shall come to, gang together into large communal survival machines or ‘vehicles’.

Richard Dawkins

Nevertheless, the book served a useful purpose since it was very popular and it introduced the general public to the idea that evolution is all about genes. The public needed to hear about the gene-centric view.

Matt Ridley thinks there's more to it than that. He says,

Books about science tend to fall into two categories: those that explain it to lay people in the hope of cultivating a wide readership, and those that try to persuade fellow scientists to support a new theory, usually with equations. Books that achieve both — changing science and reaching the public — are rare. Charles Darwin's On the Origin of Species (1859) was one. The Selfish Gene by Richard Dawkins is another. From the moment of its publication 40 years ago, it has been a sparkling best-seller and a scientific game-changer.

That last point is debatable. If the concept really was a "scientific game-changer" then you'd expect it to be covered extensively in the textbooks. It's not. In fact, it barely gets mentioned in most evolutionary biology textbooks.

If you look in the index to Futuyma's Evolution (2nd ed.), for example, there are no references to Dawkins but 11 references to Stephen Jay Gould, 3 references to George Williams, 4 references to Motoo Kimura, 10 references to Ernst Mayr, 7 references to Niles Eldredge, 4 references to W.D. Hamilton, and 5 references to E.O. Wilson. (Darwin gets 17.)

Anyway, I've discussed this issue before and reached the conclusion that the idea of the selfish gene didn't really do much for the science of evolutionary biology [The "selfish gene" is not a good metaphor to describe evolution] [Die, selfish gene, die!].

There's another problem. Most people don't understand Dawkins' use of the term "selfish gene." He's talking about evolution and the fact that beneficial alleles will increase in frequency in an evolving population. It's a metaphor and Richard Dawkins has said that perhaps "immortal gene" would have been better. The gene itself is not selfish, in Dawkins view, because it acts through its effects on phenotype. He explains this much more thoroughly in his next book The Extended Phenotype.

Confusion arises because the term "selfish genes" is used in another context to refer to genes that truly are selfish. Transposons, for example, propagate within genomes because they are good at reproducing themselves and not because they affect the phenotype of the individual they inhabit. There are other examples. They are not the typical selfish genes of Richard Dawkins although he doesn't disown them.

This confusion leads Matt Ridley to say,

As an example of how the book changed science as well as explained it, a throwaway remark by Dawkins led to an entirely new theory in genomics. In the third chapter, he raised the then-new conundrum of excess DNA. It was dawning on molecular biologists that humans possessed 30–50 times more DNA than they needed for protein-coding genes; some species, such as lungfish, had even more. About the usefulness of this “apparently surplus DNA”, Dawkins wrote that “from the point of view of the selfish genes themselves there is no paradox. The true 'purpose' of DNA is to survive, no more and no less. The simplest way to explain the surplus DNA is to suppose that it is a parasite.”

Four years later, two pairs of scientists published papers in Nature formally setting out this theory of “selfish DNA”, and acknowledged Dawkins as their inspiration (L. E. Orgel and F. H. C. Crick Nature 284, 604–607 (1980); W. F. Doolittle and C. Sapienza Nature 284, 601–603; 1980). Since then, Dawkins's speculation has been borne out by the discovery that much surplus DNA consists of reverse transcriptase — a viral enzyme whose job is to spread copies of itself — or simplified versions of transposons dependent on it. Thus, Dawkins's ideas helped to explain what was going on inside genomes, as well as between individuals, even though the book was written long before DNA sequencing became routine. The complexity of the structure of the gene itself has since grown enormously, with the discovery of introns, control sequences, RNA genes, alternative splicing and more. But the essential idea of a gene as a unit of heritable information remains, and Dawkins's synthesis stands to this day.

There were more than just two papers published in 1980. You need to read the entire series before reaching any conclusions [see Selfish genes and transposons].

It's important to note that both Doolittle & Sapienza (1980) and Orgel & Crick (1980) made an effort to distinguish between their views of selfish genes/DNA and those of Richard Dawkins. Doolittle & Sapienza begin their paper with a discussion of the Dawkins view that selfish genes are those that confer a phenotype upon with natural selection acts. They point out that their proposal is a "different kind of explanation" involving genes (transpsosons) that don't confer a phenotype and are invisible to natural selection. Their metaphor refers to parasitic DNA.

Orgel & Crick put their fingers on the exact problem by saying,

The object of this short review is to make widely known the idea of selfish DNA, A pieces of selfish DNA, in its purist form, has two distinctive properties.

1. It arises when a DNA sequence spreads by forming additional copies of itself within a genome.
2. It makes not specific contribution to the phenotype.

This idea is not new. We have not attempted to trace it back to its roots. It is sketched briefly but clearly by Dawkins in his book The Selfish Gene (page 47)....

A brief mention on one page is all the time Dawkins devoted to this particular version of selfish genes. It is not related to the main themes of his book and it is not an original idea.

In one of the follow-up papers (Dover & Doolittle, 1980) the authors take pains to point out the difference between parasitic DNA ("selfish") and selected DNA (also "selfish").

We wish to emphasize, however, that 'ignorant' and 'selfish' self-perpetuation are terms that uniquely apply to these particular DNA processes and cannot be used, meaningfully, to describe changes in frequencies of other elements that are totally dependent on the natural selection of phenotypes. 'Selfish genes' (Dawkins, 1976) and 'replicator selection' are not synonymous terms and the evolutionary processes to which they allude are unknown.

Matt Ridley is greatly exaggerating the role that Richard Dawkins played in understanding how transposons affect genome architecture.

Doolittle, Sapienza, Orgel, and Crick all recognized that selfish transposons could account for the excess DNA in large genomes but there was still a problem in explaining why they weren't eliminated by natural selection. These sequences should not be "selfish" in the sense Dawkins was writing about in most of his book.

Today we know that every one of them was wrong. Only 10% of our genome is functional and I'm including the tiny percentage of parasitic transposons. The rest is junk and none of it is "selfish" DNA in the sense of Doolittle & Sapienza or Orgel & Crick (or Dawkins). A good hunk of our genome (~50%) is bits and pieces of defective (dead) transposons. They are not selfish. They are pseudogenes. Another 40% is junk that has nothing to do with transposons.

We can't account for most of the junk DNA in large genomes by invoking parasites. It may explain the origin of the dead copies but not why they persist. In order to explain junk DNA you need to understand population genetics, neutral alleles, and random genetic drift. The selfish gene ain't gonna help you there.

Matt Ridley is doubly wrong about Richard Dawkins' contribution to our understanding of the genome.

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Doolittle, W.F., and Sapienza, C. (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature, 284(5757), 601-603. [PDF]

Orgel, L.E., and Crick, F.H.C. (1980) Selfish DNA: the ultimate parasite. Nature, 284:604-607. [doi: 10.1038/284604a0]

Dover, G. (1980) Ignorant DNA? Nature, 285:618-619.

Cavalier-Smith, T. (1980) How selfish is DNA? Nature, 285:617-618. [doi: 10.1038/285617a0]

Orgel, L.E., Crick, F.H.C., and Sapienza, C. (1980) Selfish DNA. Nature, 288:645-646. [doi: 10.1038/288645a]

Dover, G., and Doolittle, W.F. (1980) Modes of genome evolution. Nature, 288:646-647.

Jain, H.K. (1980) Incidental DNA. Nature, 288:647-648.