Thursday, January 28, 2016

"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.

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.


  1. Are there any references to the idea of selfish DNA before Dawkins 1976 - to support the claim that "it is not an original idea"?

    1. I don't know about the phrase "selfish DNA", but the idea of genes that spread by rigging Mendelian segregation in their own favor was very clear in the work on Segregation Distortion in Drosophila melanogaster since about 1959 by Larry Sandler, Yuichiro Hiraizumi, and Iris Sandler. Cases where sex chromosomes segregated selfishly in organisms like Drosophila were known since the mid-1920s.

    2. Previous work on segregation distorters was covered in "The Selfish Gene", IIRC. Dawkins was talking about something a bit different, I think. He was offering selfish DNA as an explanation for the reams of junk DNA found in many large organisms. The suggestion subsequently panned out - more or less as described by Ridley - with the numerous reverse transcriptase copies.

    3. The suggestion subsequently panned out - more or less as described by Ridley - with the numerous reverse transcriptase copies.

      No, it did not pan out. Only a tiny percentage of the genome is selfish.

    4. The segregation-distorter locus in Drosphila was discussed in both the Doolittle & Sapienza paper and the Orgel & Crick paper. This is not the kind of gene Dawkins was discussing in most of his book.

    5. Mammals are around 45% transposons. Wheat is 68% transposons. Those are substantial percentages, not 'tiny' ones.

    6. @Tim Tyler

      You are referring to fragments of ancient transposons not active transposons. They are pseudogenes or junk DNA. They are not selfish genes that can propagate in the genome although they are derived from such genes that were once active 10-100 million years ago.

    7. Over 40% of our DNA is derived from the remnants of viruses. Dawkins used the term 'parasite'. It turns out that historical virus infections that remained active in the host genome account for a bit less than half of the gene sequences in mammal genomes and more than half of the genome of many plants. I think that it is reasonable to regard this subsequent discovery as a vindication of Dawkins' pioneering idea about the origin of junk DNA.

    8. Unfortunately for Tim, Larry, and Joe, it seems they can't get past the idea that it was the 'organism' actively incorporating foreign material (endosymbiosis, viruses) into its genome, utilizing its benefits.

      There is nothing non-teleological, step-wise, selfish, purposeless about any of it.

      The selfish gene is a silly idea, simply put forth to keep bishops outta management positions in science departments, as if that was a real possibility.

      Moreover, it's mindboggling that purportedly smart cookies would go out of their way to kill the cookie chef.

    9. @Steve: That is a total mischaracterization of what Tim Tyler and I said. Neither of us talked about (or thought about) "the 'organism' actively incorporating" anything.

  2. As a creationist I'm on the outside looking in.
    However I would understand the "selfish gene", as a metaphor also. in fact its a good phrase for what is being hypothesized.
    Its just to teach scholars and the public that evolution results are from the survival of genes and so affecting populations.
    So the gene's survival is the priority and it is about selfishness.
    Not a purpose, of coarse, but a result of gene survival.
    Its just punch home evolution is the result of selection forces on genes.
    (genetic drift aside for the moment)
    Evolution is not the result of selection on finished life forms.
    Its about genes prevailing in populations and not the populations of some creature surviving.
    The public would misunderstand this.
    I don't know it changed things in evolutionary biology but it was teach and did gain a great audience.

  3. The evolutionary meme that promotes such wrong-headed thinking is that the organism is a bit player, having no control over what happens to its DNA, like being hijacked, kidnapped, then enslaved by rogue DNA.

    Its all a silly attempt to avoid talking about the elephant in the room- namely that life has been intelligent from the get-go.

    And Larry wants to keep it that way by numbing us all with this junk DNA mantra.

    Truth is Larry only understands 10% of genes. He just doesn't want you to know that he doesn't have to tools or more probably the desire to do research on the other 90%.

    Guess I can't blame him. I mean what could possibly come out of researching bits and pieces of DNA floating around??!!

    Right? Right!.

    1. 'Interesting' delusions there Steve !

      Examination of REALITY shows that organisms have no intentional control over their DNA; you have something other than your gibbering ignorance and willful incredulity to show otherwise ?

      Researchers have the tools and the desire to research the other 90% of the genome - THEY SEQUENCED THE WHOLE HUMAN GENOME YEARS AGO, TWIT !

      That's who we KNOW that most of it is transposons, dead transposons, repeated elements, etc.

      And how much of the genome do creationuts, IDiots and theoloons understand again ?

      Oh right - ZERO PERCENT (but have the delusion that they have 100% understanding simply because they believe that a Magical Sky Pixie somehow did something sometime in the past for some reason.)

    2. @Steve
      I should know better than to respond to this, but since segregation distorters have been brought up, I am really curious what you make of them.

      Let's take a well-known example: the mouse t-complex:
      A male mouse carrying a normal and a t-allele (heterozygote) will (nearly) always transmit the t-allele. A little programming in Excel will show that t-complex alleles should rapidly sweep through a population because of their distorting effect, and displace the wildtype allele. The reason this doesn't happen is that male mice carrying two copies of the t-allele (homozygotes) are either inviable or sterile!

      To me it surely seems that "the organism is enslaved by a piece of rogue DNA", as inviability and sterility are clearly bad news to the organism. What sort of intelligence do you see in such a system? (Not trying to convince you here, just really curious)

  4. I first read it in 81 or 82. Maybe I didn't understand what he was trying to say but I interpreted it more as a different way to visualize evolution than as a new theory.

    Much like the Necker cube (I think Dawkins used this as an example) the idea of the selfish gene was just a suggestion to look at evolution from a different perspective.

    I am sure that Dawkins perceived his idea as profound, but I simply didn't read that into it.

    1. I also read The Selfish Gene about that time. As I remember, it was about shifting the level of organization we think about in evolution from the individual to the gene. The argument was (IIRC) that evolution isn't about the survival or reproduction of individuals but of the reproduction of genes. Individuals are merely temporary homes for the genes. Each gene is "successful" if it gets passed on. Genes that make individuals healthier and longer-lived may be selected for, but in other cases genes that make individuals very short-lived may be selected for. It's about genes, not individuals. Transposons are just extreme examples of selfish genes, but all genes are selfish.

    2. bwilson295
      Yes thats what I tried to say. you put it more articulate.
      its about genes surviving and not individuals or populations. The genes surviving just to create new populations that survive.

  5. The most astonishing thing about The Selfish Gene is the book reviews it spurred from religious people who did everything in their power to not understand what it was about. That one particular letter Dawkins received, from a person blaming the book for his depression and existential angst, really opened my eyes to the rational poverty of the average human psyche.

    1. If you want to see just how much religion is a crutch to people, read those reviews.

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

    The problem is Doolittle, Orgel, etc. were talking about *actual* selfish genes that could actually be experimentally detected. Dawkins was talking about metaphorical genes that owe more to Mendelian factors than anything that exists physically. As someone who has done work on transposons, basically nothing in the metaphorical genes that Dawkins was talking about is of interest to actual molecular evolution. It's more useful (for better or worse) to making selectionist stories about behaviors rather than "gene level evolution" in any meaningful sense.

  7. Matt Ridley writing biased and misleading things that are informed by his own particlar prejudices, does not come as a huge surprise.

  8. Dawkins was the first to bring the one locus model of selection (from Wright 1931 or so) to the attention of the general public, because he left out the math, spruced it up with the then hot topic of DNA, and had much schwung in his writing style. Dawkins made the theoretical alleles of the one-locus model pieces of DNA, and suddenly the model caught on.

    1. Dawkins certainly brought kin selection to "the attention of the general public", but Hamilton's work on kin selection had been increasingly "catching on" among evolutionary biologists since Hamilton's papers of 1964, with a boost from E.O. Wilson's book Sociobiology in 1975.

  9. I also read "The Selfish Gene" within a year or two of its publication. Unlike other commentators I knew nothing of biology and had never come across an accessible book explaining evolution. For someone like me it was a revelation. Whatever the professional quibbles I think Dawkins did an enormously valuable job by enlightening the ignorant in a language they could understand. "The Selfish Gene" is the reason I am reading Larry's blog, forty years later.

  10. @Larry Moran

    It strikes me as odd that you claim Dawkins was wrong about selfish genes (or others about selfish DNA for that matter) because a big portion of the genome is made up of broken transposons and viral DNA, that is, junk. To me, this move seems analogous to saying that Darwin was wrong, because fossils are not alive any more.

  11. When you say Dawkins is not referenced in text books, my guess is that's because Dawkins didn't do the research he discusses in his books. Text book authors, if inspired by Dawkins' books, will cite the researchers Dawkins wrote about, not Dawkins himself.