Last December, David Dobbs published a jeremiad in Aeon magazine called “Die, selfish gene, die”. And I criticized it in two posts (here and here), while Richard Dawkins, who of course coined the term “selfish gene,” and Steven Pinker also took issue with it. I’ll summarize Dobb’s original thesis by quoting my initial post on it:
At any rate, Dobb’s goal is several fold. First, he wants to claim that the metaphor of the selfish gene is wrong. Second, he wants to show that it’s wrong because new understanding of gene regulation—how genes turn on and off during development—render the selfish gene metaphor passé. Finally, he claims that a new theory, that of “genetic accommodation,” relegates much of conventional evolutionary theory to the dustbin, for the new theory deposes the centrality of the gene in favor of the centrality of the environment and its non-genetic effects on development.
I won’t reprise my criticisms, except to say that the metaphor of genes acting as if they are “selfish” when subject to natural selection remains perfectly good, whether or not those genes (or any bit of DNA) are part of the genome that makes proteins, regulates other genes, or comprises any bit of DNA that has the ability to get itself replicated more often than its competitors. Second, gene regulation doesn’t do anything to invalidate the “selfish gene” metaphor, for even regulatory genes, if they’re subject to adaptive evolution, behave “selfishly.” Finally, Dobb’s theory of genetic accommodation was incoherent, and, even when construed more coherently as the notion of “genetic assimilation,” is a phenomenon that appears to be very rare in nature—certainly not common enough to make the idea of genes as “selfish” entities passé.
Now, after I thought the dust had settled, Aeon apparently thinks the controversy is worth reviving, and is milking it for web hits by asking five people, Robert Sapolsky, Laura Hercher, Karen James, John Dupré, and David Dobbs himself, to weigh in on the issue: “Dead or alive? Is it time to kill off the idea of the ‘selfish gene’?”
It’s a remarkably unenlightening read—by and large a waste of space—though a few contributors make some good points, and Karen James’s take is well worth reading. I’ll just reprise each person’s main reactions to the question:
Robert Sapolsky, a neuroscientist at Stanford. Sapolsky emphasizes our new knowledge of gene regulation, arguing that perhaps a lot of what we once thought of as “junk” DNA actually has a function in regulating genes. (He does, however, seem to buy into the ENCODE Projects deeply criticized conclusion that a substantial fraction of noncoding DNA has a regulatory function. We don’t really know that yet.) But Sapolsky does narrow in on the huge flaw in Dobb’s argument:
What this implies is that the evolution of genes – selection for changes in the DNA sequences of particular genes – isn’t as important as the extreme gene-centric view suggests. But that doesn’t decrease the importance of the evolution of the genome, the collection of all the DNA (coding for genes, regulatory elements, and whatever other functions haven’t been discovered yet). Why? Because, as noted above, regulatory elements such as promoters are also made of DNA sequences. When there’s a mutational change in the DNA sequence coding for a gene, and that new variant gets selected for, evolution happens. But critically, when there’s a mutational change in the DNA sequence coding for a regulatory element, and that new variant is selected for, evolution also happens. And that can matter – just think of those formerly polygamous mountain voles. By now, it is clear that the evolution of regulatory elements is at least as important as that of the genes themselves.
Dobbs’s point, however, was not to show that we know a lot about how genes are regulated, which would have been fine for a general essay in, say, Scientific American. No, Dobbs wanted to make a big splash by showing that gene regulation and the notion of genetic accommodationism invalidated the idea of the selfish gene. And Sapolsky shows why that’s wrong, for all adaptive changes in the genome, be they in regulatory or coding elements, involve natural selection. And natural selection is precisely what the idea of the “selfish gene” is meant to encapsulate. (And did so brilliantly, in my view). But Sapolsky wants to be a nice guy and not be too hard on Dobbs, even though the paragraph above makes hash of Dobbs’s thesis. Sapolsky ends with a kumbaya moment:
It ultimately makes no sense to ask what a gene does, only what it does in a particular environment; remember what turns grasshoppers into locusts. It is the triumph of context. In proclaiming the importance of gene regulation, Dobbs is de facto proclaiming the genome as more a collaborator with the environment than as the Holy Grail.
Yes, but so what? As we’ve known for over a century (indeed, since Darwin’s time if you count his ignorance of how heredity works), genes have a survival value only in a particular environment. Finches with heavy beaks are advantageous in environments with large seeds, but those beaks are a handicap when seeds are small. Clearly natural selection involves the interaction of genetic variation with an environment, be that environment internal or external. That is old news. Dobbs defends himself later by saying that this stuff, and new findings about gene regulation, may be old news to scientists, but not to the public. Fine. Then let Dobbs write an essay on those new findings. That is not the essay he wrote, for he wanted to make a big splash by overturning the “selfish gene” notion, and did so by dragging in questionable concepts like epigenetics and “genetic accommodation.”
Laura Hercher, an instructor in genetic counseling at Sarah Lawrence college in New York. Hercher’s point seems to be that, as a genetic counselor, she sees that there is no one-to-one relationship between gene and phenotype; things are complex. (Well sometimes they’re not that complex: if you have the gene for Huntington’s chorea or achondroplastic dwarfism, you’re going to show the symptoms.) Like Sapolsky, she lauds Dobbs for emphasizing gene-environment interaction, while largely ignoring his attempt to overturn the selfish gene metaphor. Insofar as she addresses that metaphor, she thinks, mistakenly, that Dawkins equated selfish genes with genetic determinism. Did she read his book? For Dawkins explicitly addresses, and denies, such a connection. Hercher’s essay doesn’t add much to the discussion:
But this emphasis on controversy within the evo-devo universe has obscured what I would consider to be Dobbs’s most significant argument: there is a pressing need to create a language in which to discuss the complex relationship between genes and traits, which is accessible to the non-scientist.
. . . Stories are important to writers. Many of us love the story of The Selfish Gene, which might explain some of the drama in response to Dobbs’s article. But stories are also important to all people as a method of coping, of making predictions about the world, of understanding things that are complicated and frightening. David Dobbs is right that when it comes to genetics in 2014, we need a better story to tell – a less selfish, more inclusive metaphor to offer the wider world.
Really? Do we really need more inclusive metaphors? And why? Did Hercher even read the book, which explains how “selfish genes” can lead to the evolution of cooperation? Does she know that Dawkins considered calling the book The Cooperative Gene instead?
Karen James, a staff scientist at Mount Desert Island Biological Laboratory in Maine. In her essay, “Let’s keep the ‘selfish gene’ lightbulb switched on’,” James shows herself to be the only commenter who seems to understand what Dobbs was getting at, and criticizes it appropriately. She says it all in these excerpts:
Gene expression is important; indeed it is one of the most-studied processes in modern genetics. But it’s not at all clear that gene expression (whether generating environmentally responsive variation within the same species or codified variation among different species) represents an overthrow of the gene-centric view, on which The Selfish Gene rests.
. . .There are some notable exceptions, including cultural transmission of knowledge and behaviour (a concept that Dawkins explores in the final chapter of The Selfish Gene, in which he coins the word ‘meme’), epigenetic changes such as methylation, and epistasis (complex, gene-gene interactions). My major disagreement with Dobbs is not with these, but with the exception that he focuses on at greatest length: genetic assimilation.
Dobbs defines genetic assimilation as ‘an adaptive trait … originally developed through gene expression alone … made more permanent in … descendants by a new gene’. But ‘gene expression alone’ is misleading; gene expression is itself controlled by genes and how they interpret the environment. While it’s true that this interpretation can further modify the organism’s (and the gene’s) environment, and new genetic variations will now be selected in that modified environment, I don’t see this as evidence against the gene-centric view of evolution. I see it as an extension.
. . .In fairness, Dobbs does acknowledge that genetic assimilation is not the norm, nor ‘that it widely replaces conventional gene-driven evolution.’ But if it’s not common, and if it doesn’t replace gene-centric evolution, surely it cannot be a significant threat to the selfish gene.
How does this all connect to a larger view of evolutionary change? Considering the elements of evolution by natural selection – heritability, variation, and differential survival – it becomes clear that rewriting the genome really is the only way to evolve. Heritability is a must for evolution and, with a few exceptions, the aspects of organisms that are stably inherited through the generations are their genes. There are other mechanisms of evolution besides natural selection, such as genetic drift, but those still require heritability.
The answer to Dobbs’s question ‘Why bother rewriting the genome to evolve?’ then is ‘Because there is no other way’. The interactions among genes, and between them and the environment, are indeed far more sophisticated and ramified than what we learnt in high school, but evolution is, and indeed must be, gene-centric.
That summarizes, in just a few short paragraphs, why Dobbs’s article was not only misguided, but misleading. I still maintain that it was, in toto, damaging to the public understanding of science.
John Dupré, a British philosopher of science and director of the Centre for the Study of Life Sciences at Exeter University. Dupré notes that evolution can occur without genetic change (although many of us define “evolution” as a change in the frequencies of different gene forms), and his example is a good one: cultural inheritance, not just in humans but in some nest-parasitic birds like the indigobirds of Africa.
Indigobirds lay their eggs in nests of other species, and are thus freed from babysitting, since the male and female of the “host” species, unable to recognize the alien chick, do all the tending, allowing the parasitic birds to have more offspring. (You can have a lot more chicks if you can farm out their care to others.)
Parasites maintain their fidelity to nests because the fledgling parasitic male chicks learn the song of their foster father, while the parasitic female chicks learn the nest and appearance of their foster parents, and also learn to recognize the calls of their foster father. This keeps the system stable,so that a parasitic female will infest the nest of the same species as did its parents: she will mate with her own male, who emits the recognized call of her foster father, and lays her eggs in the nest of the species of her foster parents.
Occasionally, though, a female makes a mistake and lays an egg in the nest of a different host species. That can trigger a “speciation event,” because such mistakes are rare, and the new parasitic chicks, imprinted on a different host, go on to parasitize the nest of the new species. Parasitic birds infesting the nests of different species, then, can be considered different species themselves, because they don’t mate with each other. As Allen Orr and I discuss in our book “Speciation,” this one of the few forms of nongenetic speciation, effected by a form of cultural inheritance based on imprinting. But even that involves subsequent genetic evolution, because the parasitic chicks go on to evolve markings in their mouths that resemble the markings of the chicks of their foster parents, so as to deceive those parents into feeding the alien parasite birds.
But this nongenetic and cultural form of evolution is rare (most species, and all plants, lack cultural inheritance), and is certainly no reason to overturn the notion of adaptation and speciation based on changes in genes themselves. (We shouldn’t forget, too, that that imprinting of parasitic chicks is the result of natural selection on “selfish genes” to mate properly and maintain nest fidelity.)
Dobbs also brings up genetic assimilation, which is a scenario too complex to explain here (read the Wikipedia article on it). He claims that this also acts to invalidate the selfish gene metaphor.
He’s wrong on two counts: natural selection on genes is still involved in this phenomenon, making the “selfish gene” metaphor still relevant; and examples of adaptations in nature involving genetic assimilation are almost nonexistent. When I wrote my original critique of Dobbs, I didn’t know of any, but now there’s one plausible example involving the reduction of eyes in cave fish. (I give the reference below.) Still, that is only one example out of gazillions of adaptations whose evolutionary basis we understand, and which didn’t involve genetic assimilation.
As for epigenetics, I still know of no examples of adaptations in nature that involved a change in the DNA produced by solely the environment, and which then became inherited in a stable way over many generations. While epigenetics is important, the epigenetic changes involved in evolution have involved modifications of DNA coded by the DNA itself, bringing this evolutionary phenomenon into the bailiwick of “selfish genes.”
David Dobbs, science writer. Dobbs kicked off the whole controversy with his article, but his response to the kerfuffle is lame. It is, in fact, all about tone: we’ve been nasty, and we’ve misunderstood him. There is not a single attempt to address the scientific criticisms that many of us, including Pinker, Dawkins and me, aimed at his article. He claims, in fact, that our criticisms were designed to stifle discussion! But if that was the case, Aeon wouldn’t have run a second piece continuing that discussion! Dobbs’s beef:
My feelings here matter little. What does matter is the effect such attacks have on others looking on, and on open discussions about genetics and evolution at a time when genetics has plentiful reason to regroup and reconsider instead of defend and attack. Such hostility seems designed to quell rather than enrich discussion; to freeze rather than advance understanding; above all, to silence. It worked. While evolutionary researchers who objected to my article rightly felt free to speak up, few scholars who agreed with me felt similarly comfortable. Although many expressed agreement privately, almost no one did so in the open. I can’t blame them; who wants to leap into a bloody shark pool?
Pardon my French, but that’s hogwash. I don’t believe there’s a secret group of evolutionists who are afraid to openly agree with Dobbs. Maybe there are a few such pusillanimous people, but “many”? Of course we’ll never know, for Dobbs can’t name them. They’re scared!
Dobbs goes on to talk about how his intent was to create a multilayered story, and to bring new developments to the eyes of the public. That’s all fine by me, but that wasn’t his sole intent, as is palpably clear to anyone who read his original article. Stung by the criticisms, he retreats to an almost theological stance: the scientific criticisms we raised are ignored, and we should be very concerned with the meaning of the stories:
Dawkins, responding to my article, asked: ‘Does Dobbs really expect me to be surprised [by the power of gene expression]?’
I do not. I was not writing for Dawkins. I was writing, as Dawkins himself writes, for a general audience, and for the same reasons Dawkins does: to share the wonders of genes and evolution with people who might not know of them; to put those wonders into context in a way that might generate new understanding; to share and make memorable not a brand-new fact or finding but a fresh reframing of the story of how evolution works. Like the ideas Dawkins described in The Selfish Gene, the ideas I wrote about had been discussed by scientists for years or decades but had reached few outside academe. And as Dawkins had done originally, I argued that a different characterisation of the gene’s role in evolution – in my case, one emphasizing the gene’s sociability rather than its selfishness – could tell a story about evolution that was still accurate but more layered, exciting, and consistent with recent research.
. . . In the century since it was named, ‘the gene’ has been a thing vague, variable, and often abstract. Is it wise to insist that something so slippery and mutable, so variously conceived, is not just ‘potentially immortal’, as Williams proposed, but literally immortal? Science does not advance by insisting that certain of its stories are immortal. It moves by allowing stories to evolve. And sometimes by letting them die.
There are a lot of new and exciting findings in evolutionary genetics, and plenty of room for responsible journalists like Carl Zimmer or Ed Yong to convey them to the public. But notice that neither Zimmer nor Yong ever resort to hype—to the “Dawkins/Darwin was wrong” trope that sells magazines and brings blog clicks. Dobbs thought he could gain attention by using new findings in genetics to go after a famous man who coined a famous and useful metaphor. It didn’t work, for nothing in science has happened to make that metaphor passé. I hope Dobbs has learned his lesson. Let the science sell itself: you needn’t use it to claim that scientific paradigms are flawed. The “X was wrong” hype may bring attention, but unless it’s supported by solid science, it won’t move people like me, and in the end will only confuse and mislead the public who, claims Dobbs, was the target of his article.
I think the figure below is a readers’ poll, though I’m not sure. I wouldn’t really go by the opinions of nonscientists, many of whom haven’t read Dawkins’s book and aren’t acquainted with evolutionary genetics. Indeed, that’s the case for many scientists as well, so this whole poll seems pretty useless.
Rohner, N., D. F. Jarosz, J. E. Kowalko, M. Yoshizawa, W. R. Jeffery, R. L. Borowsky, S. Lindquist, and C. J. Tabin. 2013. Cryptic Variation in Morphological Evolution: HSP90 as a Capacitor for Loss of Eyes in Cavefish. 10.1126/science.1240276. Science 342:1372-1375.