I can vividly remember reading The Selfish Gene in my local library as a teenager: it was both a page-turner and something of a conversion experience. Richard Dawkins’s explanation of the unsparing reality of evolution blew like a cold, refreshing wind through everything I thought I knew about human nature, and is one of the great pieces of scientific writing from the last century. I was hardly surprised then, that David Dobbs’s essay ‘Die Selfish Gene’ provoked a fierce and prolonged debate when we published it in Aeon last December. But now it’s time to take stock: is the ‘selfish gene’ idea still a useful way to explain evolution? We invited four experts, and the writer himself, to respond to this question. And we invite you to join the conversation by taking our quick survey at the bottom of the page. What do you think: is it time to get rid of the ‘selfish gene’ or is it here to stay?

Brigid Hains, Editor

It makes no sense to ask what a particular gene does

Robert Sapolsky, neuroscientist

This is a time of feverish belief in the importance of genes, as an ever greater number of genomes are sequenced at ever faster rates. The premise of this excitement is that DNA is the centre of the universe of life, the Code of Codes, the holy grail, the source of information and commands that run every cell.

David Dobbs’s provocative and timely piece argues against the importance of the gears of evolution working through selection for genes. Instead, he emphasises the critical role of gene regulation. When, where and how much a gene is expressed – the crux of gene regulation – can be more important than the gene itself. Differences in gene regulation explain why your neurons and your big-toe cells can contain the same genes yet be so different. It explains how caterpillars turn into butterflies. And, sometimes, how one species can split into two. Therefore, Dobbs concludes, the traditional ‘gene-centric’ obsession with selection for genes, and of the hegemony of the selfish gene, should be scrapped.

Naturally, Dobbs is both right and wrong. To see why, it helps to translate this level of description into a more molecular one. How, on a simplified nuts and bolts level, does gene regulation actually work?

Each of our 20,000 or so genes specifies the construction of a specific protein; proteins shape the structure and function of cells, the communication between them, and their collectivity as organisms. Scientists once thought that, starting at the beginning of a chromosome, there’d be a stretch of DNA coding for gene A, which directed the construction of protein A. Immediately after that would be the DNA coding for gene B, specifying for protein B, followed by gene C, and so on.

But this turned out to be wrong. Between the stretches of DNA coding for two genes came a stretch of ‘non-coding’ DNA, once pejoratively called ‘junk DNA’, of no obvious use. Then came the astonishing discovery that approximately 95 per cent of DNA is non-coding. It can’t be that nearly all of DNA is junk; instead, much of that 95 per cent is the instruction manual for using genes. More specifically, these ‘regulatory elements’ are the on-off switches determining when and how much a particular gene is transcribed (ie, prodded into instigating the construction of its protein). Just before the start of the DNA coding for a gene is a stretch of regulatory DNA constituting that gene’s ‘promoter’. If a particular ‘transcription factor’ comes floating over from somewhere in the cell and binds to that promoter, this triggers transcription of that gene.

Thus, genes code for what protein is made; regulatory elements code for when/where/how much. Many genes can have the same promoter, and be regulated as a coordinated network; one gene can have multiple promoters, and be regulated as part of multiple networks. A wonderful example of the importance of regulatory elements concerns two species of voles and the gene coding for the receptor for a hormone called vasopressin. Mountain voles and prairie voles have identical DNA sequences for that gene. But they have different sequences for the promoter, and as a result, the receptor occurs in different parts of the brain in the two species. And this makes a big difference – it’s why mountain voles are polygamous and prairie voles are monogamous. If you do some molecular engineering wizardry and turn the promoter in a male mountain vole into the version in prairie voles, he becomes monogamous.

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. For example, a disproportionate percentage of the genomic differences between humans and chimps are in the sequences of regulatory elements, and in the genes that code for the transcription factors that activate regulatory elements.

So Dobbs is right in emphasising the importance of gene regulation, and therefore of evolution most consequentially working on the genome, rather than on genes per se. Hooray for gene regulation. But time to explore the implications of the molecular biology of such gene regulation. Recall Dobbs’s iconic example of gene regulation, the transformation of a grasshopper into a locust. What started that drama? Crowding and/or food shortage. Let’s restate that question and answer: what triggered the frenzy of transcription factors that caused that metamorphosis by regulating gene transcription in virtually every cell of that organism? The environment. Dobbs correctly de-emphasises genes as the Code of Code. But in doing so, he incorrectly turns the genome into that instead; he remains trapped in the gravitational pull of DNA, rather than recognising what regulates the gene regulators.

The environment can be the local cellular environment. Suppose oxygen radicals are accumulating in a cell, not a good thing. Scattered throughout the cell are copies of a class of sentinel transcription factors that are activated by oxygen radicals. Once activated, they head off to the DNA. There are a number of genes that code for antioxidants that mop up oxygen radicals, and just before the start of each is a promoter regulated by that transcription factor. So in this scenario, the genome inside this cell mobilises antioxidant defences in response to signals from the cellular environment.

The environment can be the environment of the body. Suppose a woman is secreting oestrogen from her ovaries during the latter half of her reproductive cycle. After coursing through the bloodstream, oestrogen will enter the uterine cells and bind to an oestrogen receptor. And this activated receptor now acts as… yes, a transcription factor. It binds to promoters ‘upstream’ of genes related to cell division. And as a result, new cells proliferate, the uterus thickens, preparing it for implantation of a fertilised egg. In this scenario, the genome inside this cell causes it to divide in response to a signal from a distant organ.

And the environment can be environment with a capital ‘E’, the outside world. Suppose a male antelope smells the pheromones of a threatening competitor. Through steps leading from the nose to the testes, he secretes testosterone. Which makes its way to a muscle cell, binds to a testosterone receptor, which acts as a transcription factor and activates genes related to cell growth, contributing to increased muscle mass. And thus in this scenario, the much-vaunted genome inside that cell is being regulated by some other guy’s pee.

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.

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We need better genetic explanations for patients and parents

Laura Hercher, genetic counsellor

Genetics is new, but genetic determinism is old. The idea that you cannot escape your destiny lurks in ancient stories, making a monster of Oedipus and a fool of Macbeth. In the 16th century, the theologian John Calvin convinced multitudes that God had determined before birth who was to be damned, and who was to be saved. A secular, molecular Calvinism was neither invented nor endorsed by Richard Dawkins in The Selfish Gene. And yet the book – brilliant, subtle, even poetic – has persuaded many of its readers that the gene exists in isolation, the engineer of traits, constructing the organism as a mere vehicle to carry itself one step further through evolutionary time. Humans are ‘survival machines’, Dawkins wrote, ‘robot vehicles blindly programmed to preserve the selfish molecules known as genes’. Taken literally and reductively, it presents a caricature of genetic determinism: you, as the temporary manifestation of genes in search of their own immortality.

In ‘Die, Selfish Gene, Die’, David Dobbs takes aim not at the book, which he calls ‘one of the most thrilling stretches of explanatory writing ever penned’ – but at the story, the take-home message that ate all the other take-home messages. Dobbs’s argument is that gene-centric explanations aren’t wrong so much as incomplete – but incomplete in a way that fundamentally clouds our general understanding of how genetics works.

Much of the reaction to the essay has focussed on whether the critique of Dawkins was fair; how one defines a ‘gene’; and some spluttering about the incorrect characterisation of William Hamilton as a statistician. The science was ‘old news’, scoffed some reviewers, speaking on behalf of those for whom epigenetics and epistasis are familiar words. 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.

In retrospect, Mr Dobbs, you might have reconsidered the title.

Genes affect traits – not in simple ways, but in complicated ways. This complexity makes the science interesting, but it makes clinical practice very hard. As a genetic counsellor, I am often called upon to explain to worried patients and their family members concepts such as incomplete penetrance, which sounds like a sexual problem but actually denotes the likelihood that someone with a gene for a condition will remain unaffected. Or variable expressivity, which describes the range of outcomes associated with a given genetic disease.

It turns out to be very difficult to make predictions about the effect that a given gene variant will have on traits and behaviours. Even in those exceptional situations where there is a well-characterised relationship between the gene and the disease, my colleagues and I often have a hard time predicting who will get sick and how sick they will be. In the clinic, we call these genotype-phenotype correlations, and they are notoriously inexact. For example, the gene for cystic fibrosis (CF) was identified in 1989. We know how and why the changes in the gene create symptoms of the disease. Does that mean we can predict the course of the disease in individuals? No, it does not. Even siblings with CF can have very different outcomes. This is the frustrating reality for a couple with a foetus diagnosed prenatally. And these are the easy cases, the Mendelian diseases, the ones that pass down through families in predictable patterns of inheritance, like Gregor Mendel’s peas.

Complexity is very hard to communicate, in part because people are primed to believe that genes are powerful (which they are) and determinative (which they are not). It might not be news to geneticists or science writers or professors of evolutionary biology at Oxford that identical DNA can produce both grasshoppers and locusts. But the case for plasticity has not been made in a manner accessible to the general population. Shifting the popular emphasis from genes to gene expression, Dobbs suggests, will allow people to understand how environment and other mediators of gene expression affect the development of traits and behaviours at the same fundamental level as DNA sequence.

This is such an important discussion to have right now, as we embark on a grand experiment, using DNA to personalise treatment and prognosis, to predict who is at risk for heart disease, cancer, diabetes, mental illness, etc. What should you, as an individual, do with that information?

Understanding that your genes are not destiny is the difference between paralysis and empowerment. Understanding that environment has a hand in gene expression means that intervention is not just a fancy name for pills you take when you are already sick. Sometimes, as with Alzheimer’s disease, we in the genetics community have debated the ethics of informing people about their genetic risk factors, because it is hard to get comfortable with the idea of looking someone in the eye and telling them that this is likely their future, unless – unless! – you can also give them some hope. And slowly, we are getting to a point where we have some hope to give them – treatments, risk-reducing strategies, preventive measures.

In September last year, the National Institute of Health in the US announced a grant of $25 million to examine the impact of DNA sequencing in newborns. Some of those parents are going to get results that suggest that the little bundle they are bringing home from the hospital is at risk for cancer, heart disease, autism. How important is it for parents to understand the limitations of the test? We have a minute, two minutes, maybe a year, to think about that question before we start talking about pre-natal DNA sequencing.

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.

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Let’s keep the ‘selfish gene’ lightbulb switched on

Karen James, biologist

I was an 18-year-old creationist when I first read The Selfish Gene by Richard Dawkins. A freshman, pre-vet major at Colorado State University, I found myself in Bernard Rollin’s honours biology course. As well as Dawkins’s book, he assigned Thomas Kuhn’s The Structure of Scientific Revolutions (1962), James Watson’s The Double Helix (1968), and Farley Mowat’s Never Cry Wolf (1963).

All of those books were mind-expanding, but The Selfish Gene finally taught me evolution (my creationist high-school biology teacher had omitted the subject). The idea that my body is a vehicle for my genes was not only a personal and intellectual challenge, it was part of a larger ‘it’s not all about me’ revelation of the sort that happens to college students.

The Selfish Gene started me on a number of paths: away from creationism, away from teenage narcissism and towards biology as my chosen field. I lost interest in becoming a veterinarian, and decided that research in genetics, cell biology, and developmental biology was for me. So when David Dobbs’s essay, provocatively titled ‘Die, Selfish Gene, Die’ triggered an energetic debate, I found myself in the ‘both liked it and objected to it’ camp.

‘Die, Selfish Gene, Die’ is a splendidly written, carefully researched and constructed piece. As a scientist and an educator, I was delighted to read clean, compelling descriptions of complex processes such as environmentally responsive gene expression and epistasis, and to imagine others – especially students and non-scientists – reading them. On the other hand, as a geneticist who has done research in some of these areas, I also objected to the portrayal of The Selfish Gene book (and the selfish gene concept described therein) as outdated, wrong, and even harmful to scientific progress.

Dobbs begins his essay by telling the story of how grasshoppers morph into locusts and back again, not through a change in the grasshoppers’ genes, but in how those genes are read (gene expression). He cites other examples as well – such as honeybees becoming either workers, guards or scouts – and could have called on hundreds more if he had wanted. 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.

It’s important to realise that there are two quite distinct meanings of the ‘gene-centric view’. One is the view that the gene – not the cell, the organism, the group, or the species – is the unit of natural selection. This is the meaning that is typically used in discussions of evolution, especially where the selfish gene is concerned. Although it remains controversial – there is vigorous debate about whether and how selection acts at different levels of the hierarchy of life – it’s not the focus of Dobbs’s essay.

Dobbs defines the gene-centric view as ‘the one you learnt in high school … the one you hear or read of in almost every popular account of how genes create traits and drive evolution’, or, quoting the Berkeley geneticist Michael Eisen: ‘a gene changes, and therefore the organism changes’. In a blog post responding to Dobbs, Richard Dawkins describes this definition of the gene-centric view as a ‘deterministic, one-to-one, atomistic causal relationship between a gene and an object of phenotype … an extension of a deep principle of embryonic differentiation’.

I agree with Dobbs that this gene-centric view of development is commonly oversimplified. Genetics involves ‘more fluid, environmentally dependent factors such as gene expression and intra-genome complexity’, and we need to do a better job communicating this.

Even so, such complexity is still encoded in, and inherited through, genes (defined broadly as biologically relevant stretches of DNA). All of these variations, including those triggered by the organism’s environmental context, the cell’s cellular context, or the gene’s genomic context, are a function of genes. The ability of an individual organism or a species to change can come from changes in gene expression, but those changes are controlled by the products of other genes. Variation via gene expression is still gene-centric.

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.

This does not mean that the selfish gene is entirely safe from attack. Another important aspect of Dobbs’s argument is about metaphor and story, not just the technical account of genetics – in particular how metaphors and stories percolate into the public imagination. My sense is that the regulation of gene expression is indeed an under-communicated phenomenon. Supporting this argument, a commenter on the essay wrote:

As a complete layperson, [I thought:] Wow, evolution makes sense now! … I was taught that … genes randomly mutate and the most favourable carry on through survival and reproduction … To find out that evolution has … the mechanism that changes the locust and bees without changing the gene first, that just blew my mind! The whole thing … explains much better how such complexity and specialisation could arise, through interaction with the environment

If ‘Die, Selfish Gene, Die’ had this effect, then I am delighted.

Perhaps we do need a new meme that expresses the complexity of gene-gene and gene-environment interactions (and their role in evolution). The ideal metaphor would avoid the rhetorical pitfall of ‘selfish’ and include, or at least hint at, a greater complexity than is conveyed by ‘gene’. Dobbs suggests ‘the social genome’. Suggestions floated on Twitter include ‘DNA soirée’, ‘copy co-op’, ‘genome-environmental complex’, ‘thrifty genes’, and ‘the interactive genome’. Many of these seem to me to address only development, not evolution, or else fail to convey what I think of as the ‘lightbulb’ idea that we are vehicles for our genes. Those that refer to the ‘genome’ are problematic, as the genome is not inherited intact in sexually reproducing species. The heritable unit is the ‘haplotype’, a stretch of DNA much smaller than the genome that is statistically indivisible by genetic recombination, a process that occurs every generation. Unfortunately, ‘selfish haplotype’ is way too technical to become popular. My favourite by far is the ‘Allele Olympics’, suggested by the American science writer Emily Willingham on Twitter. ‘Some compete alone. Some in teams’ she elaborated. ‘And genome = national contingent eg Team USA,’ I added.

But is ‘the selfish gene’ really such a bad metaphor? We simply do not know what its real influence on lay audiences and students might be. Willingham posted a public question to her Facebook profile: ‘Non-scientist friends: have you heard of the selfish gene? What do you think that means? (no googling!)’ and the responses revealed ignorance and confusion about the concept rather than something akin to the gene-centric view (of development) that worries Dobbs (and me).

Some outstanding questions prompted by this discussion include: what contributes to the overuse of the ‘gene for x’ rhetoric, that is, the portrayal of genes acting in relative isolation to produce phenotypes? Is the selfish gene meme part of the problem and, if so, how? What other factors might contribute?

On my wish list for 2014 are answers to these questions and more, and further explorations of alternatives to the selfish gene that both highlight the complexity of gene-gene and gene-environment interactions while keeping the selfish gene ‘lightbulb’ switched on.

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Why should evolution require something immortal at its heart?

John Dupré, philosopher of science

Should we bury the selfish gene metaphor? I believe we should. In his Aeon essay, David Dobbs surveys many of the recent developments in biology that have rightly been seen as putting pressure on this metaphor, but the effect is somewhat scattergun, and it is not easy to see where exactly the fatal damage has been done.

As Richard Dawkins and Jerry Coyne made clear in their responses to Dobbs’s essay, the existence and importance of many regulatory genes, even the realisation that most genes are regulatory, is not an immediate problem for the selfish gene theory. A regulatory gene can fit Dawkins’s account of selfishness just as well as a structural gene.

The so-called ‘Baldwin effect’, that is, the process by which genetic assimilation gradually takes over changes produced by phenotypic adaptation (such as the development of larger muscles from particular uses) is not a fatal problem for the selfish gene either. In fact, genetic assimilation can readily exemplify the thinking that all evolutionary processes must ultimately involve genetic change. What is more radical is the argument that evolutionary change can occur without genetic involvement at all. Here, I think, we glimpse the dogma at the heart of the gene selfishness metaphor that needs to be abandoned. This is a dogma about the nature of evolution itself.

All evolutionary processes consist of countless cycles of reproduction and development. Each individual cycle varies in generally minor ways, and some are more successful than others. These are selected, that is they are successful in passing on to new cycles those changes that are spun off in a process of reproduction. Selfish gene theory says that the only changes that satisfy this condition are changes in gene sequence but this is an article of faith that has outgrown its usefulness. Stronger leg muscles can be passed on if they are the result of different genes, but they might also be passed on if parents ‘train’ their offspring to chase faster prey. In both cases, there are traits that contribute to differential rates of reproductive success, but in only one case are they genetically encoded.

Coyne disagrees. Consider his response to Dobbs, in which he argues that:

‘All heritable differences between species, in fact, must reside in the DNA; we know of no cases in which they don’t. Where else could they be?’

This is a remarkably narrow view and, surely, false. In the human species, wealth and education, for instance, are highly heritable, but certainly not because of DNA. Dobbs’s pig-hunting predators pass on the developed leg muscles to their offspring by encouraging them to chase the juicy little pigs. These cases illustrate what is often broadly referred to as cultural inheritance.

The cultural inheritance of learnt behaviour is one alternative to genes as a basis for inheritance, but not the only one. Behavioural changes in a particular organism that are passed on to their offspring by other means can even initiate a process of speciation. African Indigobirds are brood parasites – like cuckoos, they lay their eggs in the nests of their host species. As the biologist Michael Sorenson of Boston University has shown, if a particular female lays her eggs in a nest belonging to a different host species, her offspring will grow up imprinted on that host species and even learn its songs. A process of sympatric speciation whereby two populations diverge, in spite of continuing to live in the same place, has been observed to have started with this behavioural change. The rosehip fruit fly lays eggs on a number of host plants: a change in the choice of host plant can cause far-reaching metabolic and behavioural changes in a population that are not necessarily accompanied by genetic changes, but are stabilised over time and can also represent the beginning of a speciation process.

It is becoming increasingly clear that some trans-generational epigenetic inheritance does occur. Experiments by the neurologist Michael Meaney and colleagues at McGill University in Montreal have shown that when mother rats lick their pups this produces epigenetic changes affecting gene expression in the brains of the pups, the upshot of which is that the pups develop into adults less susceptible to stress. One of the consequences of this for developing females is that they are more likely to lick their own pups properly, thus transmitting the behaviour across generations, without any genetic mechanism. The real relevance of the complexity of gene expression and regulation systems, as well as epigenetic inheritance, is that these provide multiple possible ways in which changes to the system might be stabilised without involving changes in DNA sequence.

These examples call into question a remarkable and insufficiently discussed idea in The Selfish Gene, the idea that DNA forms immortal coils. Dawkins argues that only genes replicate with sufficient fidelity to stabilise an evolutionary process. But why should evolution, a process of change, require something immortal at its heart? A more modest assumption is that without highly durable change, the lineage will revert to its previous state. But why should this be? Within an evolving lineage there are many possible sources of phenotypic variation and many sources of stabilisation.

The dogma of DNA as the only means of inheritance is reinforced by the idea of a genetic bottleneck. Many multicellular organisms pass through a single-celled stage in their life cycle, the zygote, or fertilised egg with a novel genome constructed from parts of those of its parents. No doubt this generation of new genomes is important for evolution. But of course there is much more to even the single cell than its genetic sequence. This exists in a massively complex chemical and structural environment, and the genome itself is shaped (literally and functionally) by epigenetic changes. Moreover, the bottleneck does not occur in all species. Many plants, for instance, reproduce vegetatively, and there is no conceptual reason why evolution should not take place within these vegetatively reproducing processes.

A far better way of understanding evolution is to see it as a sequence of life cycles. There is a common tendency of thought to see the world as composed of things, and therefore to see evolution as a sequence of subtly different things – genes, genomes, or organisms. But if we hold on to the life cycle perspective, keeping in mind that evolution is a process composed of processes, evolution should be seen as a series of perturbations and re-stabilisations of these processes, some of which lead to more robust and reproductively fecund parts of the process. From this perspective, it is easy to see that there can be many sources of perturbation and, provided there are effective stabilisations of these perturbed processes, they might all have evolutionary consequences. The importance of the complex systems of gene regulation and of the interaction of these with epigenetic effects is of providing biological systems with a diverse range of sources of both change and stability.

Science moves by allowing its stories to evolve

David Dobbs, science writer

In ‘Die, Selfish Gene, Die’, I argued that Richard Dawkins’s ‘selfish-gene’ model of evolution threatens to blind us to richer emerging views of genetics and evolution. The essay generated responses ranging from enthusiastic agreement to objections both civil and savage. I naturally drew pleasure from the excited agreement, which came from both laypeople and scientists. And I was truly heartened by the constructive criticism from scientists and others who took issue with the idea of retiring the selfish-gene meme. Their challenge expanded my thinking, helped me to improve the essay in a revised form, and, best of all, spurred a wide-ranging, open-minded discussion full of mutual inquiry, reconsideration, and great humour.

Alas, a more vitriolic line of objection also arose. I first ran into it in the form of a tweet from the Harvard psychologist Steven Pinker, describing me as ‘another confused journalist who hates genetic evolution but doesn’t understand it’. I remain puzzled that Pinker concluded I hate genetic evolution, whose wonders and riddles I have written about for several years.

In another tweet Pinker asked:

Why do sci journalists think it’s profound that genes are switched on/off? Do they think that all cells produce all proteins all the time?

Which leads me to ask:

Why does Steven Pinker think it’s shallow when science writers tell readers about things that scientists know but others do not?

As a writer and teacher, surely Pinker is in the business of sharing knowledge and ideas. Why should I not do the same? Gene expression might be old hat to scientists. But the power of this most essential biological dynamic strikes many other curious and intelligent people as something new and, as the responses to my essay made clear, deeply exciting. In his blog, population geneticist Jerry Coyne also accused me of trying to sell old things as new. And Dawkins, after graciously acknowledging that I ‘made scarcely a single point’ that he would not have been glad to make himself, rather less graciously accused me of writing about well-established facts, ideas, and dynamics as a way of ‘manufacturing controversy’.

It soon became apparent that some people are willing to defend the selfish gene idea as if guarding a holy kingdom. The rhetoric was astounding. Coyne averred that ‘if [Dobbs] were an honest man’, I would apologise for my story, ‘but we know that won’t happen!’ His followers accused me of bringing ‘other agendas’; of tabloid-style sensationalism, intentional distortion, and intellectual dishonesty; of being a journalistic buffoon; of being cheap, shoddy, and crass; of writing in the pay of creationists. One commenter said that rather than question him, I should behold Richard Dawkins and cower.

I suppose I can see how people might write such stuff if they’ve spent too much time defending science from attacks from creationists or others hostile to empirical endeavour. But it’s an odd way to respond to ideas submitted in good faith.

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?

On the upside, some people did object to this noise. Many, including people I’d never heard from before, wrote to me privately to say they thought the Pinker-Coyne-Dawkins response was sclerotic and counterproductive. And a few protested publicly. One commenter at my blog, a reader named Agga, expressed his dismay this way:

As a complete layperson, my interpretation of the Aeon article was this. Wow, evolution makes sense now! Before, as someone who has only taken high-school biology and an undergrad short module in heritability, I was taught that evolution worked in this manner: genes randomly mutate and the most favourable carry on through survival and reproduction.… This extremely simplified view is what is being taught, and what is implied from the common narrative of evolution. To find out that evolution has these mechanisms such as epigenetics and the mechanism that changes the locust and bees without changing the gene first, that just blew my mind! The whole thing is so much more intuitive; and explains much better how such complexity and specialisation could arise, through interaction with the environment in this way.

Agga also took issue with the complaint about gene expression being old hat:

[P]erhaps all you PhDs should remember that you do not know what the layman’s view is, what the common narrative or the [selfish gene] metaphor actually does, how it is interpreted. You don’t know this because you already know about the complexity. I never knew, until now. Isn’t that a shame?

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 emphasising 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.

For Agga and others, including many scientists, this worked. The article stirred in them, if I might borrow the title of Dawkins’s newest book, an appetite for wonder.

Some might object that science is not about stories but facts. But science is always a story about facts. That’s why scientific papers have discussion sections. And there are always different stories to tell about any given set of facts. That’s why people offer various and overlapping hypotheses and theories. Science’s true job and modus operandi is to find and articulate the most compelling story consistent with the facts. Naturally, scientists must revise and replace these stories as research reveals new facts.

Dawkins knows this, and in The Selfish Gene he tells one hell of a compelling story. But in an age when research is showing the genome’s conversation with the outside world, and with itself, to be far more complex than we ever supposed, does the selfish-gene story remain the most compelling one we can offer about genetics and evolution?

That’s my question. Many of Dawkins’s defenders dismiss it by insisting that Dawkins’s selfish gene is not merely a meme or a metaphor, but a parsimonious statement of fact that deserves the status of a fact itself. But it’s not a fact. It’s a story about facts.

In truth, we can hardly even agree on what a gene is. George Williams himself, the biologist who was the selfish gene’s true father, clearly recognised this. In Adaptation and Natural Selection, his pivotal 1966 book that laid out the gene-centric theory which Dawkins would popularise a decade later, Williams noted that our DNA is passed on in repeatedly, continuously ‘dissociated fragments’, and that the ‘potentially immortal’ object of selection – ‘the gene’ that Dawkins would soon call selfish – was an abstraction that could be defined in any number of ways. Williams emphasised this by citing no less than four definitions of ‘the gene’ (as he himself framed it, in quotes) in the very paragraph in which he called it potentially immortal. He defined the gene as ‘“the gene” that is treated in the abstract discussions of population genetics’; as a rare ‘segment or chromosome’, protected from common forces of recombination, ‘[that] behaves in a way that approximates the population genetics of a single gene’; as ‘that which segregates and recombines with appreciable frequency’, and which is ‘potentially immortal’; and finally and most broadly, as ‘any hereditary information’ for which there is selection.

That was 48 years ago. As the Yale geneticist Mark Gerstein and others demonstrate in the article ‘What Is a Gene?’ (2012), the ensuing half-century has added only more definitions to Williams’s conservative list.

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.