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Down with the Selfish Genes!

The Twitter-sphere is abuzz with the talk about David Dobbs recent article in Aeon Magazine, Die, Selfish Gene, Die! Dobbs’ article attacks Richard Dawkins (as is clear from the title). Dawkins responded here and also sent his readers to Jerry Coyne’s more detailed critique (Part I and Part II).

Steven Pinker tweeted Coyne’s blog, and also wrote to Dawkins (quoted from Dawkins’ blog):

Brilliant! This seems to be a congenital problem with science journalists — they think that it’s a profound and revolutionary discovery that genes are regulated, not stopping to think that the alternative would consist of every cell in the body synthesizing all 21,000 proteins around the clock. Part of the blame goes to molecular biologists, who hijacked the term “gene” for protein-coding sequences, confusing everyone.

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I find it quite ironic that Dawkins, Coyne, and Pinker, the three of the most out-spoken opponents of multilevel selection, join forces again, this time to obliterate the hapless David Dobbs. (On the question of group selection, see Steven Pinker on the Edge and Jerry Coyne on his blog; check out also responses by me and colleagues on Social Evolution forum).

In my view, the key passage in the Dobbs article is this one:

For a century, the primary account of evolution has emphasized the gene’s role as architect: a gene creates a trait that either proves advantageous or not, and is thus selected for, changing a species for the better, or not. Thus, a genetic blueprint creates traits and drives evolution.

This gene-centric view, as it is known, is the one you learnt in high school. It’s the one you hear or read of in almost every popular account of how genes create traits and drive evolution. It comes from Gregor Mendel and the work he did with peas in the 1860s. Since then, and especially over the past 50 years, this notion has assumed the weight, solidity, and rootedness of an immovable object.

But a number of biologists argue that we need to replace this gene-centric view with one that more heavily emphasises the role of gene expression — that we need to see the gene less as an architect and more as a member of a collaborative remodelling and maintenance crew.

He then goes on to talk about “genetic accommodation” and describes how it might work during the evolution of running speed in a predator.

All this is interpreted by his critics as an attack on the (neo)evolutionary synthesis. Even the usually astute Razib Khan focuses on this aspect of Dobbs article (see Evolutionary orthodoxy may be boring, but it is probably true).

But I don’t see it as an attack on the evolutionary orthodoxy as much as an attack on a very special, and very limited version of it, the “gene-centric view” of G. C. Williams, popularized by Dawkins in The Selfish Gene. Remember that the main message of The Selfish Gene is that it is not individuals that are selected, but individual genes.

But that is wrong, wrong! Everybody now knows that genes are not independent agents assorting at will in genomes. Quite the opposite. Human genome, in particular, is not a mere collection of genes, it’s a massively integrated network of genes. Most human genes don’t code for proteins, they regulate each other and the small proportion of the genome that actually codes for proteins. We used to think that 98 percent of our genome was ‘junk’, because it did not code for any specific proteins (see, for example, Michael Eisen It’s not Junk blog).

The main point is that selection doesn’t just operate at the level of genes. In fact, most of the action is at the level of integrated networks of genes. And in some species, such as humans, there is an additional level, that of groups of individuals (groups of groups of genes).

Gene-centric view is a huge oversimplification of the way evolution works. And it’s a bad oversimplification. If you want to simplify things, you are better off focusing on individuals, not individual genes. But an even better approach is the multilevel one – considering how selection can act in opposite directions, depending on the level that you are looking.

22 Comments

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22 Comments

  1. Gene Anderson says:

    I get the feeling from Pinker’s comment that he doesn’t understand genetics, or the implications of Dawkins’ work. If Dawkins were right, PInker’s recent book (on violence getting less) couldn’t exist. People wouldn’t cooperate enough to reduce violence or to publish books!
    They all need to read Andrew Bourke’s PRINCIPLES OF SOCIAL EVOLUTION, which explains how you can get from kin selection to true social behavior, and then Gintis, Bowles and their group on how that can make people so social in spite of whatever the genes are up to. One need not go into mystical “group selection” to explain highly prosocial behavior, but one does have to get out of the “selfish” trap.

  2. Peter Fields says:

    In act at multiple levels, in the same direction!

  3. P says:

    But that is wrong, wrong! Everybody now knows that genes are not independent agents assorting at will in genomes. Quite the opposite. Human genome, in particular, is not a mere collection of genes, it’s a massively integrated network of genes. Most human genes don’t code for proteins, they regulate each other and the small proportion of the genome that actually codes for proteins.

    Uh, that’s exactly what Dawkins wrote in his reply, quoting long excerpts from his books explaining that very thing. It seems that you didn’t actually read Dawkins’s (or Coyne’s) response.

    • Peter Turchin says:

      Dawkins agrees that evolution is acting on groups of genes? That’s group selection. He would never agree to it.

      • Peter Fields says:

        Yes, exactly. I can imagine a Daily Show like rundown of this. If only we had the staff!

      • P says:

        The unit of selection is the gene, but other genes are part of each gene’s environment. This is how he puts it:

        Another good alternative to The Selfish Gene would have been The Cooperative Gene. It sounds paradoxically opposite, but a central part of the book argues for a form of cooperation among self-interested genes. This emphatically does not mean that groups of genes prosper at the expense of their members, or at the expense of other groups. Rather, each gene is seen as pursuing its own self-interested agenda against the background of the other genes in the gene pool—the set of candidates for sexual shuffling within a species. Those other genes are part of the environment in which each gene survives, in the same way as the weather, predators and prey, supporting vegetation and soil bacteria are parts of the environment. From each gene’s point of view, the ‘background’ genes are those with which it shares bodies in its journey down the generations. In the short term, that means the other members of the genome. In the long term, it means the other genes in the gene pool of the species. Natural selection therefore sees to it that gangs of mutually compatible—which is almost to say cooperating— genes are favoured in the presence of each other. At no time does this evolution of the ‘cooperative gene’ violate the fundamental principle of the selfish gene.

      • Michael Kehoe says:

        My understanding is that Dawkins considers other genes as part of a single genes environment. An individual gene could be selected in part for how it interacts with or regulated another gene (the rowing team analogy).

  4. Robert Kadar says:

    Peter: btw, genes being what is ultimately selected is not an argument against group selection or multi-level selection. I believe what you wrote can be misinterpreted that way. Dawkin’s main point, I believe, is that genes are the ONLY heredity unit. Individuals, groups, cultures don’t replicate with the same level of fidelity, fecundity and longevity as genes. Henrich, Boyd, and Jablonka argue that Dawkins is wrong. Learning and “cultures” can be selected for. See this paper by Henrich and Boyd: link to www2.psych.ubc.ca

    • Tim Tyler says:

      Re: “Dawkin’s main point, I believe, is that genes are the ONLY heredity unit.”

      For most of the 20th century, genes were the only heredity unit – by definition. A ‘gene’ was just a name for the heritable basis of a trait. Then the molecular biologists came along, people misunderstood what they said – and now we have today’s enormous muddle and confusion over the issue – and we need to have articles like my “Genes are not sections of nucleic-acid”.

  5. Stevie Smith says:

    It really surprises me how people can interpret the ‘selfish gene’ theory as one that presents a solely selfish account of human/animal behaviour. It’s a metaphor, a way of seeing things. I admired P’s elegant attempt to explain the source of confusion.

  6. David Dobbs says:

    Thanks to Peter for writing the post and to all for engaging. Peter’s chose excerpt and post both point to the heart of my argument, which obviously did not come clear in my own article. I’ll be posting a clarification this Wed or Thursday to try to clear up some of the muddle and make more clear the nature of the complaint about the selfish gene picture of genetics and evolution.

    That should show up both at Aeon, where the original article appears (link to aeon.co), and at my blog, http://daviddobbs.net.

    Thanks all for reading and/or discussing.

    David Dobbs

    • Peter Turchin says:

      David, thanks for the interesting article and the link to your response. I can’t understand how people could still seriously refer to the gene-centric view, now that the science of genomics made such huge strides in revealing the massively interconnected gene expression machinery.

      BTW, Aeon is shaping up as a great resource (my article there earlier this year also got a lot of attention).

      • Andron Ocean says:

        I think there are a few reasons people have trouble expanding from the orthodox gene-centric view, perhaps the greatest of which is the complexity of the expression machinery, which David’s article emphasized. In reality, it isn’t machinery at all. It’s nonlinear, not compact, riddled with all sorts of emergent behavior and feedback loops, and being influenced by an organism’s external environment to boot, which means that it is not easily described or visualized by any typical means.

        A lot of people — even excellent scientists — have trouble understanding extremely complex systems because they are so different from what they are used to working with. It’s much easier to focus on the individual agents in the system (in this case, the genes). Given that we understand genes themselves fairly well, that they are the pieces being clearly inherited, and that their role in selection is evident, while the expression system is by comparison a murky, adaptable, uncertain swamp of interactions, the “selfish gene” theory is attractive to many, to the dismay of people like myself who think that, though powerful, it doesn’t tell the whole story. Simplicity talks sweetly, especially in a scientific world ruled by Occam’s Razor.

        • Peter Turchin says:

          Andron, this is absolutely right. Genomes are far from being simply bags of beans (genes). They are extremely complex, massively interconnected systems with complex internal structure. Some aspects of that structure had been known for a long time (chromosomes), others we are seeing dimply only now, as a result of the new science of genomics. Human brains are not equipped to grasp the complexity and understand the dynamics of such systems. The only way forward is to build mathematical models and buttress them with data. Note that Selfish Genes proponents have not done much research that would yield new insights – I mean, in the last decade or two (back in the 1970s it was, for a while, a productive research program).

  7. David Dobbs says:

    PS: Nice cheetah photo.

  8. Tim Tyler says:

    Re: “Everybody now knows that genes are not independent agents assorting at will in genomes. Quite the opposite. Human genome, in particular, is not a mere collection of genes, it’s a massively integrated network of genes.”

    It’s a straw man, though. Nobody believed this in the first place. You should always take care when you paint intellectual opponents as holding views that are stupid – and consider the hypothesis that you didn’t try for a sympathetic reading.

  9. harpend says:

    Peter:

    I have been reading this discussion and I am having a lot of trouble seeing what the controversy is. The focus of much of it, e.g. the title of the Dobbs’ essay, is Dawkins. Dawkins’ Selfish Gene is a brilliant piece of science journalism but it is not science. It is a straightforward elaboration and explanation of Fisher’s view of evolution (as opposed to Sewall Wright’s) with some frosting from Hamilton. The “selfish gene” is, in my naïveté, simply a tautology, like “survival of the fittest”. It is not Dawkins who turned it into a world view (“selfish”), it is journalists as I have read the literature and a the press.

    Gould certainly had a new, deep, even revolutionary insight into evolution but he just couldn’t quite manage to grasp it and get hold of it. It was never clear, perhaps even to him, exactly what that insight was but, he felt, it was out there somewhere. Much of what Dobbs described seem to me like this, something revolutionary that no one could quite get hold of.

    No argument about multi-level selection. Again, in my ignorance, I could never understand and I still cannot understand what the difference between kin selection and group selection (or multi-level selection) is. The models all seem to reduce to kin selection given sufficient care defining what “coefficient of relationship” is. That goes back to the unfortunate use of “r” in Hamilton 1964 since r never was defined very well.

    • Sergio Graziosi says:

      Harpend:
      I have a complete address of what the controversy is about here:
      link to sergiograziosi.wordpress.com
      it does address this specific incident (Dobbs’ article and its revised version – not discussed here) and provides some hints about the role of the selfish gene concept in building more elaborate (and necessary) models.
      Hope you’ll like it.
      In the context of this page, I’m roughly with Dawkins, Coyne, and Pinker:
      proponents of multilevel selections often (erroneously) say that we should leave the selfish gene aside. My opinion is that we need to build on it, leaving it aside will negate the one fundamental and always present mechanism that we can model reliably.
      Enjoy,
      Sergio

    • Tim Tyler says:

      Most of those involved agree these days that there is little or no difference in the predictions made by kin and group selection. However, there *are* still differences. The “kin” enthusiasts make more use of their “weights” than the “group” enthusiasts do. The “kin” folk are most interested in close relatives; the “group” folk often focus on large numbers of more distant relatives. Kin selection has been orthodoxy for some forty years – while group selection has been largely ignored for most of that period. Kin selection is more popular among biologists; group selection is more popular among social scientists… and so on.