Die, selfish gene, die

For decades, the selfish gene metaphor let us view evolution with new clarity. Is it now blinding us?

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Grasshopper (Acrididae), Barbilla National Park, Costa Rica. Photo by Piotr Naskrecki/Minden Pictures/Corbis

Grasshopper (Acrididae), Barbilla National Park, Costa Rica. Photo by Piotr Naskrecki/Minden Pictures/Corbis

David Dobbs has written for The New York Times, National Geographic, NewYorker.com and Slate. His next book, working title The Orchid and the Dandelion, is due in 2015. He lives in Vermont.

A couple of years ago, at a massive conference of neuroscientists — 35,000 attendees, scores of sessions going at any given time — I wandered into a talk that I thought would be about consciousness but proved (wrong room) to be about grasshoppers and locusts. At the front of the room, a bug-obsessed neuroscientist named Steve Rogers was describing these two creatures — one elegant, modest, and well-mannered, the other a soccer hooligan.

The grasshopper, he noted, sports long legs and wings, walks low and slow, and dines discreetly in solitude. The locust scurries hurriedly and hoggishly on short, crooked legs and joins hungrily with others to form swarms that darken the sky and descend to chew the farmer’s fields bare.

Related, yes, just as grasshoppers and crickets are. But even someone as insect-ignorant as I could see that the hopper and the locust were radically different animals — different species, doubtless, possibly different genera. So I was quite amazed when Rogers told us that grasshopper and locust are in fact the same species, even the same animal, and that, as Jekyll is Hyde, one can morph into the other at alarmingly short notice.

Not all grasshopper species, he explained (there are some 11,000), possess this morphing power; some always remain grasshoppers. But every locust was, and technically still is, a grasshopper — not a different species or subspecies, but a sort of hopper gone mad. If faced with clues that food might be scarce, such as hunger or crowding, certain grasshopper species can transform within days or even hours from their solitudinous hopper states to become part of a maniacally social locust scourge. They can also return quickly to their original form.

In the most infamous species, Schistocerca gregaria, the desert locust of Africa, the Middle East and Asia, these phase changes (as this morphing process is called) occur when crowding spurs a temporary spike in serotonin levels, which causes changes in gene expression so widespread and powerful they alter not just the hopper’s behaviour but its appearance and form. Legs and wings shrink. Subtle camo colouring turns conspicuously garish. The brain grows to manage the animal’s newly complicated social world, which includes the fact that, if a locust moves too slowly amid its million cousins, the cousins directly behind might eat it.

How does this happen? Does something happen to their genes? Yes, but — and here was the point of Rogers’s talk — their genes don’t actually change. That is, they don’t mutate or in any way alter the genetic sequence or DNA. Nothing gets rewritten. Instead, this bug’s DNA — the genetic book with millions of letters that form the instructions for building and operating a grasshopper — gets reread so that the very same book becomes the instructions for operating a locust. Even as one animal becomes the other, as Jekyll becomes Hyde, its genome stays unchanged. Same genome, same individual, but, I think we can all agree, quite a different beast.

Why?

Transforming the hopper is gene expression — a change in how the hopper’s genes are ‘expressed’, or read out. Gene expression is what makes a gene meaningful, and it’s vital for distinguishing one species from another. We humans, for instance, share more than half our genomes with flatworms; about 60 per cent with fruit flies and chickens; 80 per cent with cows; and 99 per cent with chimps. Those genetic distinctions aren’t enough to create all our differences from those animals — what biologists call our particular phenotype, which is essentially the recognisable thing a genotype builds. This means that we are human, rather than wormlike, flylike, chickenlike, feline, bovine, or excessively simian, less because we carry different genes from those other species than because our cells read differently our remarkably similar genomes as we develop from zygote to adult. The writing varies — but hardly as much as the reading.

This raises a question: if merely reading a genome differently can change organisms so wildly, why bother rewriting the genome to evolve? How vital, really, are actual changes in the genetic code? Do we always need DNA changes to adapt to new environments? Are there other ways to get the job done? Is the importance of the gene as the driver of evolution being overplayed?

You’ve probably noticed that these questions are not gracing the cover of Time or haunting Oprah, Letterman, or even TED talks. Yet for more than two decades they have been stirring a heated argument among geneticists and other evolutionary theorists. As evidence of the power of rapid gene expression and other complex genomic dynamics mounts, these questions might (or might not, for pesky reasons we’ll get to) begin to change not only mainstream evolutionary theory but our more everyday understanding of evolution.

Twenty years ago, phase changes such as those that turn grasshopper to locust were relatively unknown, and, outside of botany anyway, rarely viewed as changes in gene expression. Now, notes Mary Jane West-Eberhard, a wasp researcher at the Smithsonian Tropical Research Institute in Panama, sharp phenotype changes due to gene expression are ‘everywhere’. They show up in gene-expression studies of plants, microbes, fish, wasps, bees, birds, and even people. The genome is continually surprising biologists with how fast and fluidly it can change gene expression — and thus phenotype.

These discoveries closely follow the recognition, during the 1980s, that gene-expression changes during very early development — such as in embryos or sprouting plant seeds — help to create differences between species. At around the same time, genome sequencing began to reveal the startling overlaps mentioned above between the genomes of starkly different creatures. (To repeat: you are 80 per cent cow.)

Shapeshifter; The Locust. Photo by Ocean/Corbis Shapeshifter: the locust. Photo by Ocean/Corbis

Gregory Wray, a biologist at Duke University in North Carolina who studies fruit flies, sees this flexibility of genomic interpretation as a short path to adaptive flexibility. When one game plan written in the book can’t provide enough flexibility, fast changes in gene expression — a change in the book’s reading — can provide another plan that better matches the prevailing environment.

‘Different groups of animals succeed for different reasons,’ says Wray. ‘Primates, including humans, have succeeded because they’re especially flexible. You could even say flexibility is the essence of being a primate.’

According to Wray, West-Eberhard and many others, this recognition of gene expression’s power, along with other dynamics and processes unanticipated by mainstream genetic theory through the middle of last century, requires that we rethink and expand the way we view genes and evolution. For a century, the primary account of evolution has emphasised the gene’s role as architect: a gene (or gene variant) 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 more fluid, environmentally dependent factors such as gene expression and intra-genome complexity — that we need to see the gene less as an architect and more as a member of a collaborative remodelling and maintenance crew.

‘We have a more complicated understanding of football than we do genetics and evolution. Nobody thinks just the quarterback wins the game’

They ask for something like the rejection a century ago of the Victorian-era ‘Great Man’ model of history. This revolt among historians recast leaders not as masters of history, as Tolstoy put it, but as servants. Thus the Russian Revolution exploded not because Marx and Lenin were so clever, but because fed-up peasants created an impatience and an agenda that Marx articulated and Lenin ultimately hijacked. Likewise, D-Day succeeded not because Eisenhower was brilliant but because US and British soldiers repeatedly improvised their way out of disastrously fluid situations. Wray, West-Eberhard and company want to depose genes likewise. They want to cast genes not as the instigators of change, but as agents that institutionalise change rising from more dispersed and fluid forces.

This matters like hell to people like West-Eberhard and Wray. Need it concern the rest of us?

It should. We are rapidly entering a genomic age. A couple of years ago, for instance, I became one of what is now almost a half-million 23andMe customers, paying the genetic-profiling company to identify hundreds of genetic variants that I carry. I now know ‘genes of interest’ that reveal my ancestry and help determine my health. Do I know how to make sense of them? Do they even make sense? Sometimes; sometimes not. They tell me, for instance, that I’m slightly more likely than most to develop Alzheimer’s disease, which allows me to manage my health accordingly. But those genes also tell me I should expect to be short and bald, when in fact I’m 6’3” with a good head of hair.

Soon, it will be practical to buy my entire genome. Will it tell me more? Will it make sense? Millions of people will face this puzzle. Along with our doctors, we’ll draw on this information to decide everything from what drugs to take to whether to have kids, including kids a few days past conception — a true make-or-break decision.

Yet we enter this genomic age with a view of genetics that, were we to apply it, say, to basketball, would reduce that complicated team sport to a game of one-on-one. A view like that can be worse than no view. It tempts you to think you understand the game when you don’t. We need something more complex.

‘And it’s not as if people can’t handle things more complex,’ says Wray. ‘Educated people handle ideas more complex than this all the time. We have a more complicated understanding of football than we do genetics and evolution. Nobody thinks just the quarterback wins the game.

‘We’re stuck in an outmoded way of thinking that should have fallen long ago.’

This outmoded thinking grew from seeds planted 150 years ago by Gregor Mendel, the monk who studied peas. Mendel spent seven years breeding peas in a five-acre monastery garden in the town of Brno, now part of the Czech Republic. He crossed plants bearing wrinkled peas with those bearing smooth peas, producing 29,000 plants altogether. When he was done and he had run the numbers, he had exposed the gene.

This was the Holy Shit! moment that launched genetics’ Holy Shit! century

Mendel didn’t expose the physical gene, of course (that would come a century later), but the conceptual gene. And this conceptual gene, revealed in the tables and calculations of this math-friendly monk, seemed an agent of mathematical neatness. Mendel’s thousands of crossings showed that the traits he studied — smooth skin versus wrinkled, for instance, or purple flower versus white — appeared or disappeared in consistent ratios dictated by clear mathematical formulas. Inheritance appeared to work like algebra. Anything so math-friendly had to be driven by discrete integers.

It was beautiful work. Yet when Mendel first published his findings in 1866, just seven years after Charles Darwin’s On the Origin of Species, no one noticed. Starting in 1900, however, biologists rediscovering his work began to see that these units of heredity he’d discovered — dubbed genes in 1909 — filled a crucial gap in Darwin’s theory of evolution. This recognition was the Holy Shit! moment that launched genetics’ Holy Shit! century. It seemed to explain everything. And it saved Darwin.

Darwin had legitimised evolution by proposing for it a viable mechanism — natural selection, in which organisms with the most favourable traits survive and multiply at higher rates than do others. But he could not explain what created or altered traits.

Mendel could. Genes created traits, and both would spread through a population if a gene created a trait that survived selection.

That much was clear by 1935. Naturally, some kinks remained, but more math-friendly biologists soon straightened those out. This took most of the middle part of the 20th century. Biologists now call this decades-long project the modern evolutionary synthesis. And it was all about maths.

The first vital calculations were run in the 1930s, when Ronald Fisher, J B S Haldane and Sewall Wright, two Brits and an American working more or less separately, worked out how Mendel’s rather binary genetic model could create not just binary differences such as smooth versus wrinkled peas but the gradual evolutionary change of the sort that Darwin described. Fisher, Haldane and Wright, working the complicated maths of how multiple genes interacted through time in a large population, showed that significant evolutionary change often revealed itself as many small changes yielded a large effect, just as a series of small nested equations within a long algebra equation could.

The second kink was tougher. If organisms prospered by out-competing others, why did humans and some other animals help one another? This might seem a non-mathy problem. Yet in the 1960s, British biologist William Hamilton and American geneticist George Price, who was working in London at the time, solved it too with maths, devising formulas quantifying precisely how altruism could be selected for. Some animals act generously, they explained, because doing so can aid others, such as their children, parents, siblings, cousins, grandchildren, or tribal mates, who share or might share some of their genes. The closer the kin, the kinder the behaviour. Thus, as Haldane once allegedly quipped, ‘I would lay down my life for two brothers or eight cousins.’

Thus maths reconciled Mendel and Darwin and made modern genetics and evolutionary theory a coherent whole. Watson and Crick’s 1953 discovery of the structure of DNA simply iced the cake: now we knew the structure that performed the maths.

Finally, also in the 1960s, Hamilton and American George Williams upped the ante on the gene’s primacy. With fancy maths, they argued that we should view any organism, including any human, as merely a sort of courier for genes and their traits. This flipped the usual thinking. It made the gene vital and the organism expendable. Our genes did not exist for us. We existed for them. We served only to carry these chemical codes forward through time, like those messengers in old sword-and-sandal war movies who run non-stop for days to deliver data and then drop dead. A radical idea. Yet it merely extended the logic of kin selection, in which any gene-courier — say, a mom watching her children’s canoe overturn — would risk her life to let her kin carry forth her DNA.

This notion of the gene as the unit selected, and the organism as a kludged-up cart for carrying it through time, placed the gene smack at the centre of things. It granted the gene something like agency.

At first, not even many academics paid this any heed. This might be partly because people resist seeing themselves as donkey carts. Another reason was that neither Hamilton nor Williams were masterly communicators.

But 15 years after Hamilton and Williams kited this idea, it was embraced and polished into gleaming form by one of the best communicators science has ever produced: the biologist Richard Dawkins. In his magnificent book The Selfish Gene (1976), Dawkins gathered all the threads of the modern synthesis — Mendel, Fisher, Haldane, Wright, Watson, Crick, Hamilton, and Williams — into a single shimmering magic carpet.

These days, Dawkins makes the news so often for things like pointing out that a single college in Cambridge has won more Nobel Prizes than the entire Muslim world, that some might wonder how he ever became so celebrated. The Selfish Gene is how. To read The Selfish Gene is to be amazed, entertained, transported. For instance, when Dawkins describes how life might have begun — how a randomly generated strand of chemicals pulled from the ether could happen to become a ‘replicator’, a little machine that starts to build other strands like itself, and then generates organisms to carry it — he creates one of the most thrilling stretches of explanatory writing ever penned. It’s breathtaking.

Dawkins reveals the gene as not just the centre of the cell but the centre of all life, agency, and behaviour

Dawkins assembles genetics’ dry materials and abstract maths into a rich but orderly landscape through which he guides you with grace, charm, urbanity, and humour. He replicates in prose the process he describes. He gives agency to chemical chains, logic to confounding behaviour. He takes an impossibly complex idea and makes it almost impossible to misunderstand. He reveals the gene as not just the centre of the cell but the centre of all life, agency, and behaviour. By the time you’ve finished his book, or well before that, Dawkins has made of the tiny gene — this replicator, this strip of chemicals little more than an abstraction — a huge, relentlessly turning gearwheel of steel, its teeth driving smaller cogs to make all of life happen.

It’s a gorgeous story. Along with its beauty and other advantageous traits, it is amenable to maths and, at its core, wonderfully simple. It has inspired countless biologists and geneticists to plumb the gene’s wonders and do brilliant work. Unfortunately, say Wray, West-Eberhard and many others, the selfish-gene story is so focused on the gene’s singular role in natural selection that in an age when it’s ever more clear that evolution works in ways far more clever and complex than we realise, the selfish-gene model increasingly impoverishes both scientific and popular views of genetics and evolution. As both conceptual framework and metaphor, the selfish-gene has helped us see the gene as it revealed itself over the 20th century. But as a new age and new tools reveal a more complicated genome, the selfish-gene is blinding us.

For over two decades, Wray, West-Eberhard and other evolutionary theorists — such as Massimo Pigliucci, professor of philosophy at the City University of New York; Eva Jablonka, a geneticist and historian of science at Tel Aviv University, London; Stuart Kauffman, professor of biochemistry and mathematics at the University of Vermont; Stuart A Newman, professor of cell biology and anatomy at the New York Medical College; and the late Stephen Jay Gould, to name a few — have been calling for an ‘extended modern synthesis’ to replace the gene-centric view of evolution with something richer. They do so even though they agree with most of what Dawkins says a gene does. They agree, in essence, that the gene is a big cog, but would argue that the biggest cog doesn’t necessarily always drive the other cogs. In many cases, the other cogs drive the gene. The gene, in short, just happens to be the biggest, most obvious part of the trait-making inheritance and evolutionary machine. But not the driver.

Another way to put it: Mendel stumbled over the wrong chunk of gold.

Mendel ran experiments that happened to reveal strong single-gene dynamics whose effects — flower colour, skin texture — can seem far more significant than they really are. Many plant experiments since then, for instance, have shown that environmental factors such as temperature changes can spur gene-expression changes that alter a plant far more than Mendel’s gene variants do. As with grasshoppers, a new environment can quickly turn a plant into something almost unrecognisable from its original form. If Mendel had owned an RNA sequencing machine and was in the habit of tracking gene expression changes, he might have spotted these. But sequencers didn’t exist, so he crossed plants instead, and saw just one particularly obvious way that an organism can change.

The gene-centric view is thus ‘an artefact of history’, says Michael Eisen, an evolutionary biologist who researches fruit flies at the University of California, Berkeley. ‘It rose simply because it was easier to identify individual genes as something that shaped evolution. But that’s about opportunity and convenience rather than accuracy. People confuse the fact that we can more easily study it with the idea that it’s more important.’

The gene’s power to create traits, says Eisen, is just one of many evolutionary mechanisms. ‘Evolution is not even that simple. Anyone who’s worked on systems sees that natural selection takes advantage of the most bizarre aspects of biology. When something has so many parts, evolution will act on all of them.

‘It’s not that genes don’t sometimes drive evolutionary change. It’s that this mutational model — a gene changes, therefore the organism changes — is just one way to get the job done. Other ways may actually do more.’

Like what other ways? What significant and plausible evolutionary dynamics stand in tension with a single-gene-centred model? What gets obscured by the insistence that a ‘selfish gene’, a coherent, solitary replicator, is the irreducible and ever-present driver of evolution?

A shortlist of such dynamics would include some of the evolutionary dynamics being proposed by anthropologists, such as cultural transmission of knowledge and behaviour that allow social species ranging from bees to humans to adapt to changing environments without genetic alterations; and culture-gene evolution, a related idea, in which culture is not the ‘handmaiden’ of genes, but another source of transmissible adaptive information whose elements co-evolves with genes, each affecting the other.

Also in tension with the selfish-gene model are epigenetic changes suggested by recent research, such as methylation and other alterations to chemical wrappings around DNA, that can modulate DNA’s expression without changing its sequence. Such epigenetic changes may provide a way to pass heritable traits down through at least a few generations without changing any actual genes. To be sure, this research is still unproven as a significant evolutionary force. But while it is clearly important enough to pursue, many defenders of the selfish-gene model dismiss it out of hand.

Finally, the selfish-gene model is in tension with various ‘interesting evolutionary phenomena’, as Gregory Wray puts it in Evolution: The Extended Synthesis, ‘that are apparent only at the scale of hundreds or thousands of genes’ — a scale only made viewable during the past decade or so, as we’ve learnt to rapidly sequence entire genomes.

Of these genomic dynamics, perhaps the most challenging to the selfish-gene story are epistatic or gene-gene interactions. Epistasis refers to the fact that the presence of some genes (or their variants) can have profound and unpredictable influences on the activity and effects generated by other genes. To put it another way, a gene’s effect can vary wildly depending on which combination of other genes it finds itself with. (Think Jerry Garcia playing with different musical partners.)

Epistasis is hardly a new concept. In fact, geneticists have been arguing about its importance ever since R.A. Fisher and Sewall Wright bickered about it in the 1920s. Dawkins acknowledges a role for gene-gene interactions in The Selfish Gene, noting that ‘the effect of any one gene depends on interaction with many others.’ But research since then show that these interactions take place in non-linear, non-additive ways of a complexity impossible to understand at the time Dawkins wrote his book. Casey Greene and Jason Moore of Dartmouth, for instance, recently found that in some cases epistatic interactions seem to warp conventional gene-trait relationships so profoundly that they can often negate the gene as a trait’s reliable carrier.

Individual bees morph from worker to guard to scout by gene expression alone, depending on the needs of the hive

This is not merely a matter of one gene muffling or amplifying another, though both these things happen. And it’s not a matter of additive effects, such as four ‘tall’ genes making you taller than would two. Rather, these multi-gene epistatic interactions can create endless possible combinations of mutual influence in which any given gene’s contribution seems to rise less from its inherent trait-making power than from what company that gene finds itself keeping. To draw on P.Z. Myers' apt analogy, epistasis means that single genes often carry little more inherent significance than individual playing cards do in poker. In a poker hand, the significance and effect of a two of hearts — its ‘trait’ — depend so heavily on the other cards you’re holding that it’s almost meaningless to say the card has any replicable power on its own. It’s replicable in that it’s a two of hearts every time it’s dealt. But it can deliver the same effect in subsequent generations only if it’s dealt not just into the exact same handful of cards, but into a round in which all the other players at the table also hold the same cards as before — and happen to bet, hold, and fold in exactly the same way. Not something to count on.

And a two of hearts is a far more coherent thing than is a gene. One of the peskiest problems of leaning too heavily on a gene-centric model these days is that the definition of the word ‘gene’ gets ever more various and slippery.

Even as a technical term, the word carries at least a half-dozen meanings, and more are added as science finds new tools for exploring the genome. This alone makes it either a poor candidate for a popular meme — or, if you value flexibility over exactitude, perhaps a perfect one, since its meaning can be defended or reshaped or expanded to suit the occasion. If you expand the meaning to be ‘the thing essential to all true heredity and selection’, you can then give the gene primary credit for any discovered or proposed evolutionary force in which the gene seems to be involved — and reject outright any proposed evolutionary force that doesn’t seem to involve genes.

But the gene’s definition is not just semantically vague. As geneticists explore the genome’s previously uncharted stretches, they’re finding that a lot of the work conventionally attributed to ‘genes’ (in the sense of consistent, reasonably well defined clusters of DNA) appears to be done instead by networks of genes and strange DNA elements that doubly defy the selfish-gene model.

These regulatory networks challenge the selfish-gene model first because they include DNA elements not conventionally defined as genes. More important, some researchers believe these networks challenge the selfish-gene model because they often seem to behave not like selfish entities balancing their separate agendas, in selfish-gene style, but like managerial teams regulating the behaviour of individual genes for the interest of the organism. The chromosome’s three-dimensional nature brings those regulatory chunks into contact with individual genes in highly unpredictable ways. With each gene ‘surrounded by an ocean’ of such regulatory elements, as molecular biophysicist Joe Dekker told WIRED, each gene ‘can touch and interact with a whole collection of them’. Yale geneticist Mark Gerstein found that the genes in these networks sometimes seem to get selected for even if they don’t have important effects on their own. In other cases they seem to have effects but be exempt from selection pressure.

These regulatory elements now appear to grossly outnumber the actual genes, possibly by as much as 50 to 1. As Yale geneticist Mark Gerstein politely notes, the complexity of these regulatory networks, along with their ad hoc management-team nature, raise the question of what’s being selected: individual genes, as the selfish-gene model proposes, or the management team, by some process still hidden amid all this complexity. Others, such as Cold Spring Harbor geneticist Thomas Gingeras, question outright whether the transcript (the marching orders a gene issues to begin gene expression) should replace the gene as the genome’s functional unit. These issues are not merely academic; resolving them could help solve mysteries about cancer and other diseases.

Such dynamics have emerged only in the last decade or so, as researchers have been able to examine the genome more closely. Yet even though we so far ‘have only a dim idea of how all this works’, as Gregory Wray wrote in 2010, it ‘is clear … that these kinds of assumption-violating exceptions are not rare.’

Wray’s language here is crucial: he’s not saying these findings refute the details of the gene-centric model. He’s saying they violate the model’s assumptions.

And this is the crux of this entire dispute: The point is not whether the findings of a genomic age or of anthropology refute the selfish-gene model, invalidate its theoretical details, or debunk the modern synthesis. Mostly they don’t. The selfish-gene model is roomy enough to host many of these findings. It has shown a uncanny ability to do so. But as time passes it does so ever more uncomfortably, for both host and guests. Some findings or ideas must be almost forced in. Others get prematurely locked out.

The selfish-gene model and metaphor can probably be stretched even more to account for some of these things. But in an age when assumption-violating ideas from genomic studies, anthropology, and other fields are flourishing, does the selfish gene story remain the best way to account for them? Does it make sense to attach these proliferating findings and ideas on to the selfish-gene story as appendices? Or is it time to find another story? It may be that the gene is always a player. But it is rarely the only player. And — may I speak metaphorically? — it may (or may not) be that the gene always behaves as if it were selfish. But that doesn't mean it always gets its way.

One of the assumption-violating exceptions Wray refers to is gene expression’s breadth of power. In the social wasps that Mary Jane West-Eberhard has been studying in Panama since 1979, many of the most important distinctions among a colony’s individuals rise not from differences in their genomes, which vary little, but from the plasticity born of gene expression. This starts with the queen, who is genetically identical to her thousands of sisters yet whose gene expression makes her not only larger, but singles her out as the colony’s reproductive unit. Likewise with most honeybees. In social honeybees, the differences between workers, guards, and scouts all arise from gene expression, not gene sequence. Individual bees morph from one form to another — worker to guard to scout — by gene expression alone, depending on the needs of the hive.

As described above, the questionable coherence of genes seems to apply especially to gene regulation — as do epistatic networks that further undermine the gene’s primacy. So while it’s clear that DNA plays a key role in regulating gene expression, it is not clear that all these ‘regulatory genes’ are the selfish genes of the Dawkins model.

This is but one reason why West-Eberhard, among others, has been long trying to cure the ‘cyclic amnesia’ that she says has ignored 150 years of evidence that the gene’s centrality is overplayed. West-Eberhard is a particularly articulate advocate. Yet she’s frustrated at how little she’s been able to change things.

As a David to Dawkins’s Goliath, West-Eberhard faces distinct challenges. For starters, she’s a she while Dawkins is a he, which should not matter but does. And while Dawkins holds forth from Oxford, one of the most prestigious universities on earth, and deploys from London an entire foundation in his name, West-Eberhard studies and writes from a remote outpost in Central America. Dawkins commands locust-sized audiences any time he speaks and probably turns down enough speaking engagements to fill five calendars; West-Eberhard speaks mainly to insect-crazed colleagues at small conferences. Dawkins wrote a delicious 300-page book that has sold tens of millions of copies; West-Eberhard has written a bunch of fine obscure papers and an 800-page tome, Developmental Plasticity and Evolution (2003), which, though not without its sweet parts, is generally consumed as a meal of obligation.

She does have her pithy moments. There are times, she says, when ‘the gene does not lead. It follows.’

Massimo Piglucci and Gerd Muller use the same language in Evolution: The Extended Synthesis. By ‘the gene follows’, they mean that in complex organisms particularly, dynamics other than gene alterations, ranging from gene expression to complex gene regulation to developmental pathways formed by culture, can create heritable adaptations that either remain on their own or later become ‘fixed’ or locked in by genes.

One way in which the gene follows is through genetic assimilation — a clunky term for a graceful process. This can look Lamarckian, but it is not. It’s the development of a heritable change through flexible gene-expression responses that later get ‘fixed,' or locked in, by a change in genotype. It takes a moment to explain. But let’s give it a run.

Genetic assimilation involves a three-step process.

First, an organism adapts to a changing environment by altering its gene expression to change its phenotype — its form or behaviour. Second, a gene emerges that locks in that phenotypic change. Finally, the gene spreads through the population.

For example, suppose you’re a predator. You live with others of your ilk in dense forest. Your kind hunts by stealth: you hide among trees, then jump out and snag your meat. You needn’t be fast, just sneaky and quick off the mark.

They didn’t inherit your speed in any Lamarckian way. Rather, like you, they simply developed it through gene expression driven by running so much

Then a big event — maybe a forest fire, or a plague that kills all your normal prey — forces you into a new environment. This new place is more open, which nixes your jump-and-grab tactic, but contains juicy little wild pigs that you can outrun if you sprint really hard. You start running down these critters. As you do, certain genes ramp up expression to build more muscle and fire the muscles more quickly. You get faster. You're becoming a different animal.

You mate with another hunter. Your kids grow up to hunt with you. Since they hunt and practice hunting from early on, they too become fast — maybe faster than you, since they started younger. They didn’t inherit your speed in any Lamarckian way. Rather, like you, they simply developed it through gene expression driven by running so much. The same thing happens with their children: they run early, so they’re fast. Their speed is environmentally dependent. Your descendants keep this greater speed (greater, that is, than your ancestors’) for as long as they’re running down little pigs. The hunt makes them faster. But if they could get meals without sprinting, their speed would fade.

Now comes the second step: Several generations down the line, a beneficial mutation occurs in one of your descendants. Most mutations are neutral and many are bad. But this one’s good: It creates faster muscle fibres that let this descendant of yours — let’s call her Diana — easily run faster than her fastest siblings and cousins ever could. She flies.

Finally comes the third step: Diana’s children inherit the gene, as do some of theirs, and because their speed wows their mating prospects, Diana’s descendants mate early and often, bearing many kids. Thus this runner’s gene spreads through the generations until it becomes fixed in the population.

Now the thing is complete. An adaptive trait you originally developed through gene expression alone is made more permanent in your descendants by a new gene. Had the gene showed up back when you lived in the forest and speed didn’t mean anything, it would have given no advantage, and instead of being selected for, that speed gene would have disappeared or remained present but uncommon. But because hunting gave the gene value, the population took it in and spread it wide. The gene didn’t drive the train; it hopped aboard.

This isn’t the gene-centric world in which genotype creates phenotype. It’s a phenotype accommodating a new genotype by making it valuable.

Genetic assimilation was recognised as a possibility in the 1940s, but as Massimo Pigliucci and Courtney Murren put it, it was ‘attacked as of minor importance during the ‘hardening’ of the neo-Darwinian synthesis and … relegated to a secondary role for decades’. Interest has surged lately as gene expression becomes more apparent, and biologists are starting to spot the process in the field. No one proposes that genetic assimilation happens all the time or even commonly, or that it widely replaces conventional gene-driven evolution. But its existence suggests how gene expression’s fluidity can combine with conventional genetic dynamics to broaden evolution’s reach.

Gene Robinson, an entomologist who studies honeybees at the University of Illinois, says genetic assimilation could well have helped to create African honeybees, the ‘killer bee’ subspecies that is genetically distinct from the sweeter European honeybees that most beekeepers keep. Honeybee hives in certain parts of Africa, he says, were and are raided by predators more often than hives elsewhere, so their inhabitants had to react more sharply to attacks. This encouraged gene-expression changes that made the African bees respond more aggressively to threat. When new genes showed up that reinforced this aggression, those genes would have been selected for and spread through the population. This, Robinson says, is quite likely how African bees became genetically distinct from their European honeybee cousins. And they’d have been led there not by a gene, but by gene expression.

After several weeks of reading and talking to this phenotypic plasticity crowd, I phoned Richard Dawkins to see what he thought of all this. Did genes follow rather than lead? I asked him specifically about whether processes such as gene assimilation might lead instead. He said that genetic assimilation doesn’t really change anything, because since the gene ends up locking in the change and carrying it forward, it all comes back to the gene anyway.

‘This doesn’t modify the gene-centric model at all,’ he said. ‘The gene-centric model is all about the gene being the unit in the hierarchy of life that is selected. That remains the gene.’

‘He’s backfilling,’ said West-Eberhard. ‘He and others have long been arguing for the primacy of an individual gene that creates a trait that either survives or doesn’t.’

Yet West-Eberhard understands why many biologists stick to the gene-centric model. ‘It makes it easier to explain evolution,’ she says. ‘I’ve seen people who work in gene expression who understand all of this. But when they get asked about evolution, they go straight to Mendel. Because people understand it more easily.’ It’s easy to see why: even though life is a zillion bits of biology repeatedly rearranging themselves in a webwork of constantly modulated feedback loops, the selfish-gene model offers a step-by-step account as neat as a three-step flow chart. Gene, trait, phenotype, done.

In other words, the gene-centric model survives because simplicity is a hugely advantageous trait for an idea to possess. People will select a simple idea over a complex idea almost every time. This holds especially in a hostile environment, like, say, a sceptical crowd. For example, Sean B Carroll, professor of molecular biology and genetics at the University of Wisconsin, spends much of his time studying gene expression, but usually uses gene-centric explanations, because when talking to the public, he finds a simple story is a damned good thing to have.

Which drives West-Eberhard nuts.

‘Dawkins understands very well that gene expression is powerful,’ she says. ‘He sees things are more complex than a selfish gene. He could turn on its head the whole language.’

Yet Dawkins, and with him much of pop science, sticks to the selfish gene. The gene explains all. So far it has worked. The extended synthesis crowd has published scores of papers, quite a few books, and held meetings galore. They have changed the way many biologists think about evolution. But they have scarcely touched the public’s understanding. And they have not found a way to displace a meme so powerful as the selfish gene.

This meme, methinks, forms the true bone of contention and the true obstacle to progress. It’s one of the odd beauties of this whole mess that Dawkins himself coined the term meme, and did so in The Selfish Gene. He defined it as a big idea that competes for dominance in a tough environment — an idea that, like a catchy tune or a good joke, ‘propagates itself by leaping from brain to brain’. The selfish-gene meme has done just that. It has made of evolutionary theory a vehicle for its replication. The selfish gene has become a selfish meme.

If you’re West-Eberhard or of like mind, what are you to replace it with? The slave-ish gene? Not likely to leap from brain to brain. The co-operative gene? Dawkins himself considered this but rejected it and I agree that it lacks sufficient bling. And as West-Eberhard notes, any phrase with ‘gene’ in it still encourages a focus on single genes. And ‘evolution is not about single genes,’ she says. ‘It’s about genes working together.’

Perhaps better then to speak not of genes but the genome — all your genes together. And not the genome as a unitary actor, but the genome in conversation with itself, with other genomes, and with the outside environment. If grasshoppers becoming locusts, sweet bees becoming killers, and genetic assimilation are to be believed it’s those conversations that define the organism and drive the evolution of new traits and species. It’s not a selfish gene or a solitary genome. It’s a social genome.

What would Mendel think of that? Let’s play this out.

Mendel actually studied bees as a boy, and he studied them again for a couple years after he finished his pea-plant studies. In crossbreeding two species at the monastery, he accidentally created a strain of bees so vicious that he couldn’t work with them. If he’d had an RNA sequencer, he, like Gene Robinson, could have studied how much of the bees’ aggression rose from changes in the genetic code or how much rose from gene expression in response to the environment. If he had, the father of genetics might have seen right then that traits change and species evolve not just when genes change, when a creature and its genome and hive mates respond to an environment. He might have discovered not just genes, but genetic assimilation. Not the selfish gene, but the social genome.

Alas, no such equipment existed, and Mendel worked in a monastery in the middle of town. His vicious bees promised not a research opportunity but trouble. So he killed them. He would found genetics not through a complex story told by morphing bees, but through a simple tale told by one pea wrinkled and one pea smooth.

This is a revised version of the essay ‘Die, selfish gene, die’. It replaced the original on 13 December, 2013. Reader comments posted before that date were responding to the original version. A post at the author's blog explains the revision and includes some other resources.

Read more essays on evolution and life sciences

Comments

  • Adrian Grom

    Once upon a time lord Kelvin (the lord Kelvin) said that a young scientist has a wide horizon but, as he grew old, the horizon will shrink to a point, from there referred as his point of view! (himself was a victim of this :d ) . It is the problem that we love discrete unites of measurement instead of fuzzy logic. If you go to the bottom of gene you got a strand of bases. They are discrete. That is quite obvious. We know now that genes aren't fixed and they change by mutations or by adding genome from viruses or even by self modifying. However their expression is not discrete but fuzzy. It's like quantum physics: light is made of photons, we could see individual ones (well, at least 7 are required to trigger a signal to brain) but in every day we do not see individual but a continuum of light. So is the gene expression. It is a continuum. And is modulated by other genes... Like oxytocin. Great for love but also great for lactating. Provided by same gene but with different results according to the pool of genes around AND their carrier (a bonded male will respond different from a single one).
    It is only fit to think that gene expression is related to environment. If only the mutation will be the only mechanism than it wouldn't react quick enough to a fast pace modification of environment (like an asteroid hitting the earth...). Accommodation is a good explanation for those genes that a natural selection cleaver should have taken out from genome but...they are there. Just in case. They do not cost much but they do keep a reserve for desperate situation. For bigger organisms. At bacterial level you can't have that luxury but you do have quick multiplications - that will do for a bigger chance to have the numbers needed for that mutations which will save the line from doom..
    Even Dawkins mentioned in his books that a single gene is not enough to measure the fitness. He explained that a carnivore gene, stranded in a herbivore genome, will be awkward so the complex genome is the unit... I guess he just forgotten his own idea... :P Not that a carnivore gene couldn't stay quiet in the herbivore genome, waiting for the chance to express itself (like going from an strictly herbivore diet to an omnivore one than to a meat based one).
    Returning to the first mentioned lord Kelvin... Maybe Dawkins just reached his point of view and is just human to dismiss anything that might endanger his projects (atheism, activism evolution, etc) which are based on his status and reputation. All built on selfish genes... And he is not so young...as in seventies.. :D .
    All in one...is just a point of view. Frequency of genes respond to environment pressure... Mutation never was considered to be the only way to evolve but it is the only way to create new genes. The old ones die hard...and are reused.. It is complex and this take time to understand.

  • Adam Marples

    I feel like either I'm missing something here or the author is.

    The main point seems to be that an organism with one set of genes can express those genes in different ways depending on the environment it's in. But what controls that expression? Other genes, right? This seems like a victory for genes which can control the expression of other genes in adaptive ways. It's another layer of complexity, and perhaps they are exponentially more influential than other genes.

    It seems from reading this that it is it those gene-expression-controlling genes that are able to quickly adapt the organism to environmental changes and consequently are being selected for.

    • Mark

      I think you have hit the nail on the head.

    • Brent Tater

      Agreed. I think that the author's argument would be valid if he could prove that changes in gene expression could somehow lead directly to permanent changes in the genome itself. Lacking this evidence, the article seems to argue that the existence of epigenetics somehow disproves the selfish gene theory

    • Lexi

      Pretty sure they're not to be understated, but to be held in perspective as making the whole system *work*. They make a link between environment and genetic expression modification, and they have to -- because DNA's the stable molecule and embodies the permanence of the organism. This is no reason to declare it the origin of change; in a system that's full of cyclical action, once you have an epigenetic system in place, change can in principle come from anywhere in the cycle.

      I believe I read that the promoters of the "new way" are emphasizing how insignificant changes that originate from DNA alteration might be in the overall scheme of things. This isn't to say that such changes never happen, or are never significant, which is what I took from "Wray and West-Eberhard don’t say that Dawkins is dead wrong" in the article (though sadly it was not explained).

      • Adam Marples

        I don't think anyone is saying that genes drive change, the environment of course drives change.

        But if a stretch of DNA, finding itself in two different environments, produces two different kinds of protein, and those proteins are both useful in their respective environments, then that bit of DNA is useful to have around, and will probably survive.

        And that stretch of DNA is called a gene.

        • Lexi

          Pretty sure one of The Extended Phenotype's main points is that genes affect the environment. So, in that respect, genes will change other genes through their effects on the environment.

          And then you have gene interaction networks. They too could be said to be genes changing genes, in a more direct fashion.

          And in a similar fashion the environment alters the environment...

          Put whatever terms you want on it, it's ultimately a feedback loop, and everything "drives" everything. Singling out genes is useful only for establishing the obvious -- that they're stable in a system full of change -- and there's nothing wrong with looking at it in other ways.

          • Adam Marples

            Good points, and I definitely need to get the extended phenotype off my amazon wishlist and into my hands!

          • Joachim D.

            And then you may want to skip the first ten chapters and go straight to the core chapters 11, 12, and 13. They are brilliant - wonder why they've never been published on their own as an extract of The Extended Phenotype. The antecedent chapters are discussions with Gould and other long dead issues that potentially put readers off from ever reaching the core chapters.

    • Guest

      "But what controls that expression?"

      Environment (including all other surrounding organisms/plant life/etc.) and microbiome. If you want to argue, "well, those are made of genes too!", then you're broadening the scope to the point of meaninglessness. You might as well call it the "selfish atom."

    • Hominid

      You have it right. Moreover, the range of adaptability due to differential gene expression is severely limited. The most likely result of drastic environmental change has always been extinction. This is because, while gene expression is indeed regulated and responsive to the environment, the genome is fixed (unless there is a lucky mutation). That is to say, different species have different books that can be read-out in somewhat different styles, but the words of the book - the story - remain constant. The scenario the author describes about a complex organism undergoing rapid, extreme, and heritable transformations is sci-fi puffery. Accommodation theory is full of holes. Dawkins thesis is far closer to reality.

      • Manuel Cruz

        Mosquitoes grows larger under higher concentrations of oxygen, certain fish species can switch sex if there's a lack of members of the opposite sex. In other words, there are mechanisms that allow species to adapt and survive sudden, drastic changes to the environment so they live long enough to have an offspring.

        Of course, this could just mean that these species evolved to include "different books" to use under different external conditions. Dawkins avoids the question by suggesting that the information is probably stored in the genotype somewhere, so it still can only be passed from one generation to the next one through sexual reproduction and mutations.

        Another reasonable theory is that the traits caused by environment aren't "explicitly" stored in the genome. It's just that the genome behaves differently under different environment conditions. Just like people behave differently if they consume alcohol or drugs, the genome doesn't normally tell the individual to display a certain trait, but it will do so if the environment is weird enough. So, the environment "implicitly" tells the individual to choose one interpretation of the genome over another.

        For example, a small mosquito couple moves to an area with bigger mosquitoes and they have a baby mosquito. This baby mosquito grows big like the other mosquitoes in the area, regardless of the size of its parents mosquitoes. That's because the "size" was determined by the environment, the environment affected how the genotype was read.

        • Hominid

          Duh! Did anyone deny that genes can be regulated in response to environmental factors? Try to focus on the issue.

    • http://neuroautomaton.com/ Zachary Stansfield

      You are essentially correct. Moreover, even though we recognize that environmental influences can affect gene expression as well, there is no mechanism to produce heritable changes in the organism (grist for the evolutionary mill), without genetic change.

      What's unclear here is why "gene accommodation" provides a unique perspective on this model. Nobody denies that organisms need to adapt to new environments in order to survive before major genetic shifts can occur. In fact, this is entirely consistent with the prevailing evolutionary model.

      Where is the controversy here?

  • Archies_Boy

    Thank you for this fascinating article! (It explains a lot about my ex-mother-in-law)

  • Peter Fields

    Sewall Wright was an American geneticist.

  • Dan Jones

    A fascinating and elegant essay (although I’m not entirely unfamiliar with
    the extended evolutionary synthesis and moves to go beyond gene-centric
    models). Here is my two cents' worth (well, two criticisms' worth).

    First, at one point, Dawkins is lauded for taking “an
    impossibly complex idea” – the selfish gene theory — and making it “almost
    impossible to misunderstand”. Later, selfish gene thinking is criticized – or at
    least its popularity explained – because it simplifies evolution: “the
    gene-centric model survives because simplicity is a hugely advantageous trait
    for an idea to possess.” I would suggest that the idea of the selfish gene is,
    on the face of it, very simple, but beneath that simplicity lies a wealth of
    complexity when you get into the real, messy details of biology. That
    complexity, in and of itself, does not, however, refute selfish gene thinking —
    just as the existence of epigenetic mechanisms affecting gene expression does
    not undermine the theory (even if it does require adding in some extra details*).

    Second, the idea that the unit of selection is the “social
    genome” rather than the selfish gene is hard to cash out. (David didn't phrase it as "unit of selection" in the essay, but if you're displacing the idea of the selfish gene, which is an argument about the units of selection, then what you replace it with will have to work as a unit of selection too.) My genome is a unique,
    one-off creation, and will disappear with me when I die. My son, for better or
    worse, has inherited half his genes from me, but his genome is his own, and likewise
    totally unique. As much as I wish it wasn't the case, his genome won’t last for
    ever either. So how can the ephemeral genome be a unit of selection if it’s
    destroyed every generation? This is perhaps the core message of the selfish
    gene: that which evolution selects must persist for sufficient time, and be
    replicated with sufficient fidelity, that its fortunes can change over time.
    Genomes don’t fit the bill. Nor do individuals (which also come to end
    generation after generation). The gene, however, is potentially immortal, and
    is copied with high fidelity, making it a candidate unit of selection in a way
    that individuals, or their genomes, never can be.

    *This, obviously, is the debatable point! But over the many
    years I've followed these debates, including the ideas of niche construction,
    gene-culture co-evolution, developmental systems theory, I’ve never been
    convinced that the idea of the selfish gene is wrong in the way that critics
    say it is. Sometimes, there’s an air of straw men in these arguments. For
    example, criticizing the selfish gene theory because it turns out that other
    processes beyond gene selection – or natural selection more broadly – are important for understanding the evolutionary history of the planet is besides the point.

    Of course not everything of interest about the evolution of life on earth can
    be explained through gene selection. Sixty-five million years ago a meteorite hit
    the earth and wiped out the dinosaurs, opening up new niches for small mammals
    that eventually gave rise to the primates, and us. A meteorite strike cannot be
    explained in terms of gene selection, and yet it was very important for
    evolution on this planet! Acknowledging that there’s more to evolution than
    selection of gene variants does not mean that genes are not the unit of
    selection, nor that natural selection (which must be distinguished from
    evolution per se) operates on something other than the gene.

    • stevenjohnson2

      Isn't the real problem that so little about the organism can be explained by gene selection?

      And, I'm sorry, given the discovery of phenotype selection prior to genetic change is not a "propter hoc, ergo post hoc" fallacy. It indicates a serious problem in gene selection as causal agent, no matter how you spin it. You're advocating "post hoc, ergo propter hoc," which is beyond wrong, into obstuse.

      • Dan Jones

        Actually, quite a lot about the organism can be explained by gene selection. You should check out some textbooks on behavioural ecology. And the fact that we disagree does not make me obtuse.

        • stevenjohnson2

          It's true that ignorance of the facts will mislead. Textbooks on behavioral ecology are not available. But if it's true that there is quite a bit explained, then I've admitted I was wrong.

          However phenotypes, unlike specific genomes, do persist over time and are potential units of selection even by tendentious standards. The gene selection view is that mutant genes increase fitness of the organism and are propagated through the population by natural selection and that this is evolution. But the evidence indicates that the phenotypes appear first, then the genes are selected. You don't even seem to see the problem.

          More broadly, natural selection usually acts to conserve the phenotype in the face of inevitable genetic change. The selfish gene approach doesn't even seem to notice that problem either.

          I didn't mean to get insulting, sorry. Ignoring those problems while asserting we don't understand comes across pretty badly too.

  • rabrav

    I can see how the title 'The Selfish Gene' could be misunderstood, especially by those philosophers who prefer to read a book by title only, omitting the rather extensive footnote which is the book itself.

    - Richard Dawkins

    • Dan Jones

      I forget, was this a reply to Mary Midgley's monumentally silly review of TSG?

      • John Thomas

        Yes.

    • Guest

      I can see how this article could be misunderstood, especially by those commentators who prefer to read it by title only, omitting the rather extensive footnote which is the article itself.

  • http://stephenjones2013.wordpress.com/ Stephen Jones

    was that good! Last year I read Dawkin's book "The Selfish Gene" for the first time, and will now have to read it again to reconcile it with "gene expression" modeling... hmmm!

  • Tom

    As is quite common, this essay misunderstands the idea behind the "selfish gene" metaphor.

    The idea is that the gene is the unit of selection. Not that it is at the "centre" of evolution, but that it is the smallest persistent, indivisible organic unit that is reproduced in the process of natural selection.

    The fact that a gene, or complex of genes, can have a wide range of phenotypic expressions—the phenotypic plasticity about which the article harps—says nothing to counteract this perspective.

    In this view, the how and why of the expression (or irrelevance) of genetic material in a whole organism, group of organisms, or ecosystem of complex, differing organisms, and how the mechanisms of its expression in the organism contribute to reproductive likelihood, is deemphasised—it's the mere fact of the reproduction and survival of the genetic material that is emphasised.

    The article even captures this insight: "The gene didn't drive the train—it merely hopped aboard." That's it. That's the selfish gene. It doesn't care how it survives, it just does—the trick is to work out the many noble, ignoble, complex, multimodal simple and improbable ways that it phenotypically does.

    • stevenjohnson2

      Differential reproduction is a key part of natural selection, and that is due to phenotype differences, not genotype differences. In that vital, real world sense, the unit of selection is indeed the phenotype. The discovery that genes can be irrelevant junk may show that genes mindlessly replicate (are "selfish,") but they also show that genetic determinism is a dubious proposition indeed, that organisms are not just the genes writ large. And the existence of junk DNA demonstrates the inability of natural selection to directly select genes. As said above, the gene doesn't drive the train.

      It might be objected that none of this contradicts the fact that the gene is mechanism of hereditary. Denying that role in natural selection is like claiming that the needle isn't essential to a sewing machine. But the selfish gene concept as I've seen it in practice always (and I mean always) invokes not just this. It's certainly enough to be hugely important. It always invokes notions of genetic determinism and even the notion that natural selection has perfectly adaptive and perfectly pervasive. But these notions are wrong. If gene selection logically requires these consequences, gene selection is wrong too.

      I should think that if gene selection were real the unit of selection, we should find instances where gene replication takes place at the expense of the organism, in a fashion analogous to sexual selection. The discovery of differences in paternal and maternal genes confirms this if I understand it correctly. But the paucity of such examples strongly suggest that gene selection proper is rather closer to group selection in real importance.

      By the way, the membrane of the replicating cell is also a small, persistent unit in reproduction. What exactly does divisibility have to do with it? I propose that the selfish gene be supplemented with the selfish membrane!

      • Tom

        You misunderstand the term "unit of selection". It simply means that genes are what is transmitted, what is replicated, and therefore what is selected—the only thing that can be selected—by natural selection.

        The organism, the phenotype made up of a colony of cells, dies—the functions of its differentiated cells, their membranes, etc are ended—a fraction of its genetic material is propagated in its offspring, depending on the method of reproduction.

        Due to the way DNA replication occurs, a gene or gene complex doesn't need to shape reproductive likelihood to be reproduced. Provided it doesn't find expression that rules out its reproduction, or leads to a chance failure to survive, it can be a passenger from generation to generation.

        Continuing, a gene or gene complex doesn't need to be "deterministic" to shape reproductive likelihood any more than a die needs to be deterministic to come up six about a sixth of the time.

        A gene or gene complex that has a 60% chance of offering a 10% survival advantage through its phenotypic expression will tend—not absolutely, but probabilistically—to reproduce more often than one that does not. Time and a large number of trials will do the rest, that's natural selection.

        There is no doubt there are other mechanisms involved in evolution than natural selection via sexual reproduction. There are no doubt skews of genetic expression—complex organs that develop morphogenetically, complex interactions with environmental stimuli.

        But the point is, differential selection based on any combination and probability distribution of phenotypic characteristics, varying over time in an organism, as a sole consequence of genetic determinism or as a complex consequence of some more sophisticated mechanism, still ultimately has no bearing on the gene's role as the coded unit of selection which can be the only thing that definitively "survives" generationally—not because of what it determines, but simply because it has a digital, coded identity, and it is what is actually replicated in the process of reproduction—it is the mechanism of heredity, as you put it.

        • stevenjohnson2

          First, I managed to leave out "only" in my first sentence, as in "not only genotype differences."

          Second, I did not misunderstand. I said that the selfish gene/gene selection is always associated with genetic determinism. You say that it is not. But you reject the significance of phenotype. Yes, phenotype and genotype is closely related. But the evidence is that they are not perfectly correlated. The evidence that phenotype selection precedes the appearance of mutants favoring the genotype is inexplicable if all you have to say is that the gene is the unit of selection. It's not even wrong.

          I can only repeat that in the common public understanding, selfish gene/gene selection translates into genetic determinism of a kind which, I believe, evidence has long ago refuted. In that context, the insistence that there is no theory of evolution without heredity doesn't tell us much about the natural history of the organism.

          You might argue that I'm factually wrong but I suspect that you already would've if you had good evidence to the contrary. And so far as I know you're only interested in arguing that genes are the unit of selection, rather than arguing against the false impression that genetic determinism is scientifically supported. You even define the purpose of evolutionary theory "is to work out the many noble, ignoble, complex, multimodal simple and improbable ways that (the selfish gene) phenotypically does." This article argues this to be misleading, and I agree. But I disagree there's any question of misunderstanding.

          • MRebolleda

            The Eva Jablonka that is mentioned in the article works at the Cohn Institute for the History and Philosophy of Science and Ideas in Tel Aviv University.

            http://humanities.tau.ac.il/segel/jablonka/

          • Tom

            I don't think you or the article is wrong about the complexity or non-determinism of phenotypic expression. As others have pointed out, though, the issue is that both you and the article still seem to read beyond the intended meaning of Dawkins' "selfish gene" metaphor, so you're sort of battling a straw man here.

            Since only genes get replicated in reproduction, they are the only thing that can be selected generationally. You can't "select" a cell membrane, a rhino horn, or nice blond hair, because when DNA replicates, it replicates genes, not membranes, horns or haircuts.

            At this level, you can't "select" any phenotype because the phenotype will not be replicated, just that fraction of the complex inputs and processes that produced it that happens to be replicated in reproduction—the DNA.

            The selfish gene is not about enforcing a narrow-minded gene determinism vs a more complex interpretation of phenotypic expression. It's a more basic insight—just that it's actually genes that are selected, not the organisms in whose assembly they participate. But this insight is crucial to understanding how the grinding, slow force of natural selection does probabilistically shape phenotypic expression.

            I think you get it by now, but anyway. From this perspective, the details of phenotypic expression are nugatory: the only thing that matters is the reproduction and persistence of genetic material. For example in a hospitable environment where all organisms reproduce, most genes never fail to be replicated, regardless of how this takes place. Likewise if a planet's worth of highly evolved organisms were wiped out by a supernova, no genes would be selected, regardless of the phenotypes that populated this marvellous world.

            You might be right about the "common public understanding" (can't speak for that) but that just goes to show "selfish gene" was, in a way, a poor choice of words by Dawkins. However, in the book itself and his later works on the subject he covers all this ground, which is why I found this article a frustratingly confused 5000 words.

          • Ben Jones

            Thank you Tom, this comment absolutely nailed the slightly uncomfortable feeling I had throughout the article.

          • G. A.

            It seems that you misunderstand what is taking place. Of course, horns are selected or blond hair, because that is the result of gene expression. Without gene expression the gene may as well not exist. Traits are selected, not genes. Genes are mostly replicated, yet even here only 50% will actually be propagated from any particular sexually reproducing organism.

            The attribute of "selfishness" is the worst kind of anthropomorphism. Should we begin describing gravity as behaving selfishly by wishing to hold objects close to it?

            Dawkins was quite clear in rejecting the notion that the "selfish gene" is merely a metaphor, when he described life as being hapless robots beholden to the "selfishness" of their genes. It was rubbish then, and it's rubbish now.

            "We are survival machines – robot vehicles blindly programmed to preserve the selfish molecules known as genes."

            That's not a metaphor. That is a blanket statement arguing that the gene is not only the driver, but the sole reason for existing. It is absurd to argue that the purpose of life is to preserve genes, when the gene itself can't even control whether it is expressed or not.

            Like it or not, there is nothing selfish about the process of life and it is merely a sensationalist use of terminology to sell books while obscuring the science.

          • Seb

            Reread what Tom has written, and you'll find that you're the one who has misunderstood.

          • Dan

            > Traits are selected, not genes.

            Traits are not passed down through generations. Genes are. You have realize how deep and subtle the connection between genes and their corresponding phenotypic effects are. They certainly don't stop at cell walls or even at the organism. If purple hair increases survival, and you color your hair purple, what happens? You survive and have more progeny than your peers.

            But what gets passed down? Certainly not genes for purple hair. Unless an unlikely mutation occurs, they will not have purple hair. But what they will have are genes whose phenotypes, in that particular environment, allow them to color their hair.

            I'm being purposely vague, because evolution works across millions of years. Furthermore my simplistic example is complicated (or maybe complemented) by the fact that we have brains (which are built by genes and were shaped by Natural Selection), which have to ability to rapidly adapt to their environment, and can propagate information via culture and language. So another way to look at it is that the purple hair adaptation would be passed through culture, while the ability to build the types of brains capable of receiving and transmitting culture would be selected for by evolution.

            But it does come down to the gene! None of this is, or anything mentioned in the article is actually contrary to what was written in the "Selfish Gene"

            >That is a blanket statement arguing that the gene is not only the driver, but the sole reason for existing.

            You know you're going beyond the argument that was laid out in the article. Are you trying to make a philosophical or theological argument here? Because from an evolutionary perspective, there is no other reason for the existence of any organism, other than to pass on its genes to the next generation.

            >It is absurd to argue that the purpose of life is to preserve genes, when the gene itself can't even control whether it is expressed or not.

            The gene doesn't care how, or if at all, it has a phenotype expression in the organism. It doesn't even 'know' whether it's expressed at all! A gene, at its basic level, is merely a particular configuration of atoms in a very complicated molecule and obeys the laws of chemistry and physics like any physical matter. That's it.

            The point is that any phenotypic effect it does have on organism will be used by natural selection to select for or against. The phenotypic effect could be A in one environment, or B in another. That doesn't matter. In organisms, if the phenotype improves chances of survival, it improves the chance that the gene will be passed on.

          • stevenjohnson2

            "From this perspective, the details of phenotypic expression are nugatory: the only thing that matters is the reproduction and persistence of genetic material." This is why I don't think linking selfish gene/gene selection to genetic determinism is creating a straw man. The evidence cited shows the change in phenotypes is an indispensable part of an evolutionary story, but this perspective dismisses it.

            I'm not certain but it appears there is a great deal of difficulty in sellfish gener/gene selectionist quarters in dealing with neutral/nearly neutral mutations. That seems to be a consequence of the view that genes are basically it, and everything else is nugatory.

            On a more abstract level, this selfish gene/gene selectionist perspective disappears the phenotype. Certainly you have sharply emphasized its ephemerality. But, I repeat, the evidence shows phenotypes aren't so transitory, pending correction. I think your perspective has misled you into confusing an individual genome with a species genotype. If selfish gene/gene selectionism wasn't genetic determinism, wouldn't the phenotype be regarded as the adaptive landscape of the genes, instead of some ephemeral abstraction? Selfish gene/gene selectionism seems instead to insist that genotype--->phenotype, instead of genotype phenotype. That's not the same thing as sufficient genetic changes=multiplication of species, which we all agree. Or so I think.

            And, although I can't speak to public opinion authoritatively, the prominence of selfish gene/gene selectionists in evolutionary psychology, like Dawkins, Pinker, Coyne (who's coy about his commitment, due to embarrassment) keeps impressing me that selfish gene/gene selectionism is a package deal with genetic determinism and the power of natural selection to reach adaptive peaks. You say that this is not logically necessary but, not to be nasty, aren't these people the authoritaoes about selfish gene/gene selectionism, not you? Many of the pronouncements of these people are grotesquely wrong.

            I've probably already exceeded my store of useful or interesting comments, and will not trouble you further.
            Thank you for you time.

          • Ishi Crew

            i'd say that is totally wrong. the whole point is that the gene is not the only thing selected. the phenotype and environment is also selected---the entire thing ('unit of selection') is selected for. its group, superorganismic, or whatever you want to call it, selection. (even species selection, as s j gould suggested).

            where do you think 'artificial selection' (as in dog breeds, plants, agriculture, etc.---even eugenic ideas) comes from?

            dawkins contradicted himself almost immediately when he wrote 'the extended phenotype' after the selfish gene. almost exactly like chomsky---who decided after 30 years that, what all the people who argued against a 'language instinct' (nativism) in favor of general learning modules (ie the brain, contra fodor) actually were just saying what he was saying. (sortuh like richard nixon saying 'i am against the vietnam war ajnd always have been, even if i didn't make the demonstrations'.

            its really just a 'semantic' (actually, more like syntactic) issue, or ideological. like those who say the only people who discovered the golden rule accept jesus as god's son---and everyone else is going to hell, because the golden rule is written in english in a bible published .liberty college in the usa.

          • Andrew

            Of course more is replicated than genes. Social status, for example—or even something much more subtle, like access to certain minerals or proteins during gestation. I cannot think of a single species capable of replicating *only* genes (maybe some viruses... maybe).

            You are very mistaken to characterize the article as being entirely about genetic determinism—and equally mistaken to insist on a perspective that leads to genetic expression becoming "nugatory". Your "basic insight" is wrong precisely because it is too basic.

          • Tom

            It's not my insight, it's Dawkins'. I'm articulating it as fairly as I can.

            You're quite correct that in some cases, more factors can be reproduced generationally than genetic material—certain definitive survival traits can, as you say, be socially or environmentally selected and reproduced in a manner that's intertwined with the replication of genetic material.

            Take as a thought experiment the idea that birds learn to fly under the supervision of their mothers. From the perspective of the "selfish gene", the phenotypic trait of "having wings" is not selected and reproduced—the genes that happen to express as this trait are simply more likely to survive.

            But it is reasonable to suggest that there may be other vital traits operating here in a different mode.

            Perhaps the tendency of the mother to nurture the young and teach the young to fly is a key factor in the likelihood of the genes shared by both being reproduced. Perhaps, although this tendency is supported by evolved neurochemistry, it also relies on the reproduction of information socially—teaching to fly, teaching to teach—and would not survive a generational disruption if baby birds were abandoned or orphaned.

            It's possible to see other fragile generational structures where a proportion of survival information is not directly reproduced genetically, with human societies being an obvious example.

            But it's important to understand: this does not contradict or negate the selfish gene perspective in the slightest. Once again, the genetic material isn't concerned with how it survives. If in its expression the potential for cooperative multi-organism, multi-generation "social" strategies of survival is unlocked, its replication into the future becomes more likely, and subsequently, that value of fitness is reproduced, and it survives.

            Dawkins' book deals very explicitly with such scenarios, and also discusses other complex phenotypes, symbiosis, etc.

            Once again, though, this article does make a fundamentally wrong argument about the "selfish gene" theory. This is clear from its very first example in which the bimodal existence of locusts and grasshoppers (all with, shock horror, the same genes) is taken to undermine the idea—when in fact it confirms it.

            Can you explain why a grasshopper's potential to "morph" into a locust to promote survival calls the principle of genes as the coded, replicated unit of selection into question?

          • Matt McCandless

            The discussion between you and Tom to this point has been more enlightening that the article for me, a layperson. I would point out, In Dawkins' defense, that he goes to extraordinary lengths in The Selfish Gene to explain the limitations of his theory. Here was his own response to this article:

            http://www.richarddawkins.net/foundation_articles/2013/12/6/adversarial-journalism-and-the-selfish-gene

          • stevenjohnson2

            If I were to read Dawkins on genetics and evolution, I think I would reread The Extended Phenotype. People will insist (including I think Dawkins) that Dawkins doesn't really change his viewpoint. But no one I know of suggests reading it instead.

            Part of this exchange has centered on something that Tom denies, which is that the selfish gene/gene selection theory as popularized is also genetic determinism, and even one in which the phenotype is pretty much the optimum for the organism, what's called a peak in the adaptive landscape. Barring scientific surveys I suppose that there can't be a conclusive resolution to the discussion.

      • saksin

        Re. stevenjohnson2's statement that "Differential reproduction is a key
        part of natural selection, and that is due to phenotype differences, not genotype differences." Not so: to be part of natural selection phenotype differences have to be HERITABLE phenotype differences, and that makes all the difference in the world.

        • stevenjohnson2

          Multiplication of species and the formation of novel adaptations absolutely require changes in the species' genome. Lamarck is dead. Nobody has denied this. Lamarck is a straw man and your rhetorical trickery and logical fallacy will never convince your opponents.

          The selfish gene/gene selection perspective insists on reading the existence of junk DNA as the victory of selfish genes over the organism, not the inevitable consequence that nature can only select phenotypes.

          The selfish gene/gene selection perspective insists in its ordinary everyday presentation on viewing genes as situated on an adaptive peak, ignoring the evidence on the rate of neutral mutations.

          The selfish gene/gene selection perspective doesn't acknowledge genetic drift in populations and the role of natural selection in conserving the species' phenotype. To put it another way, the selfish/gene selection perspective cannot even see that there is a question why sometimes natural selection conserves morphologies, and other times it creates novelties.

          The selfish gene/gene selection perspective doesn't show how sexual reproduction is a failure or success for the selfish gene. Nor does it show how multicellularity is a failure or success for the selfish gene. This perspective only seems to allow its proponents to dismiss these failures as inconsequential, instead of acknowledging the evidence shows it is wrong.

          The selfish gene/gene selection perspective implies that the selfish genes will, as sexual selection does, create traits that are detrimental to the species' phenotype. The fact that there is not much evidence for this but gene selctionists are indifferent to this problem powerfully suggests that the selfish gene/gene selection approach is a logical a prior scheme, redolent of ideological proclivities rather than scientific interest.

          And again the selfish gene/gene selection perspective is invariably associated with notions of genetic determinism and the universality of peak adaptation. Evolutionary psychology, which is rooted in selfish gene/gene selection perspective, has signally failed to "explain" such a pervasive phenomenon as homosexuality. This indifference to repeated failure strongly suggests pseudoscience.

          The selfish gene/gene selection perspective evaluates reproductive success as the replication of specific base pair sequences. This notion of reproductive success has nothing to do with the number of actual organisms, which is downright bizarre.

          The selfish gene/gene selection perspective insists on the primacy of natural selection's operation on genes. The opposing view is not that natural selection doesn't operate on genes, it's that natural selection directly operates on the phenotype and only indirectly operates on the genotype. And, here's the kicker, if you're really interested in what happens in nature, you need to look at the phenotypes, not just the genotypes.

          There is a caveat of course. If there is some wealth of technical literature squirreled away somewhere that I just don't know about, that has been successfully addressing these problems, I would just be wrong.

          But at this point I would still suggest trying to popularize this technical evidence, rather than announcing anyone who doesn't love the selfish gene idea just doesn't understand. I'm sorry but from the evidence I do know about, you people are the ones who don't understand, because of your false perspective.

          • saksin

            Rhetorical trickery and logical fallacy in support of Lamarckism ON MY PART??? I have no idea what you have read or what you are replying to. All I was trying to do in my comment was to firm up your statement about phenotypes in the last sentence of the first paragraph of your comment, to make explicit what you presumably agree with, namely that it is phenotype differences with a component of heritability alone that play a role in evolutionary change. Or, as you say in your PS, "if there is no genetic change in the population there will be no multiplication of species". Indeed, and genetic change in the population is what is behind HERITABLE phenotypic differences, which was the very point, and the only point, I was making. Phenotypic differences are evolutionarily irrelavant unless they have a heritable component. i.e. are traceable to a genetic difference. It would never enter my mind to even think about inheritance of acquired characteristics, since I am a died in the wool Darwinian, and think Lamarck is just as wrong as you regard him to be.

          • Manuel Cruz

            Lamarckism works for species that reproduce by exact replication of the individual (like most unicellular life does). So if an individual gets a mutation later in life, that mutation is also passed to its "descendants".

          • stevenjohnson2

            Neither Lamarck nor Darwin knew about genes. Any talk about either that attributes genetics to Darwin but not to Lamarck is disingenuous, true But by the same token, so is attributing a genetic interpretation to Lamarck. The modern synthesis reformulated Darwin in light of modern genetics.

            It seems Lamarck postulated that adaptations in the sense of adjusting or becoming inured to were promoted by "success" in life, as in the usual example of the giraffe's neck. The proto-giraffe was conceived as using a longer neck to get more leaves, therefore some sort of inner drive in the successful neck led to more neck, etc. culminating in the modern giraffe. I gather Lamarck did not allow for blending inheritance and regression to the mean in breeding, and this is just wrong. That's all but it's enough. I don't understand the need to sneer at Lamarck either.

            As to unicellular organisms (half of all biomass the last I read,) neither Lamarck nor Darwin knew much about them.
            Phenomena such as symbiogenesis do appear to be Lamarckian in the sense that there are hereditary changes acquired without the original organism's genes changing first. But really, that's more of a pseudoLamarckism, a false impression.

            The problem with selfish gene/unit of selection is not the insistence that genes must change but the insistence that changes in genes determine everything. The problem is not the insistence that natural selection operates on genes, but the insistence that the genome is at an adaptive peak. The problem is not the insistence that in the long run there is no heredity without genes, but the insistence that the short run, even the temporal order of real world changes therefore does not matter.

            Jerry Coyne blogged on this article. As part of his supposed rebuttal, he argued that natural selection for the regulatory genes produces plasticity in gene expression and therefore exemplifies. selfish gene/gene selection. He simply assumed that it was in fact possible for genes to be so detailed in their effects that we can assume that any specified outcome is even possible. Since selfish gene/gene selection functions as a pseudonym for genetic determinism, he effectively assumed the conclusion.

            (Coyne also assumed that gene plasticity is necessarily desirable. That is pretty intuitively true for the organism but it's not so obvious from a selfish gene/gene selection perspective. Gene repair mechanisms can preserve a gene, which would be selfish gene/gene selection success, no? But that would mean that gene expression is relevant to defining gene success, which I gather selfish gene/gene selection argues against? There may be a coherent argument to be made by selfish gene/gene selection but I'm not sure these theorists are interested in details like this. Again, if there's some technical literature addressing this I just don't know about, I would be wrong.)

            Also, if the same genes cannot produce certain specified outcomes, therefore variations in the actual organisms are inevitable, one key part of natural selection, heritable variation, is diminished! The evidence so far as known is overwhelming that genes simply cannot act the way he assumes. Anyone who has known identical twins knows that they are not the same, whether trivially (fingerprints) or significantly (personality.) Natural selection cannot choose between a real trait, a necessary genetic plasticity, and a nonexistent trait, genetically determined regulatory gene plasticity.

            Further, on a biochemical level, the effect of regulatory genes must be affected to some slight degree by the mere presence of junk DNA, both in the energy wasted in the its replication and in its mere presence flattening chemical gradients, the effective distance between binding proteins and functional genes. The amount of junk DNA varies dramatically, from (I think) none to speak of in bacteria, but even between closely related species. I don't know of any interest in these questions by selfish gene/gene selection theorists, much less answers.

            You might think that competition between selfish genes might lead to genetic repair mechanisms that dismantled competing genes (if possible) but the selfish gene/gene selectionists don't seem to be interested in that question either.

            This has been a little digressive but I'm trying to support two points. First, none of the problems with selfish gene/gene selection have any reference to Lamarck or denial of the importance of genetics. Second, again, the issue is the inevitable accompany assumptions to selfish gene/gene selection of genetic determinism and a universal adaptive peak for a genome. Prof. Coyne is a very smart man, but misled by a false perspective he committed an elementary fallacy for which a schoolboy would be corrected.

      • k

        "we should find instances where gene replication takes place at the expense of the organism"
        ...transposons?

        • stevenjohnson2

          Since the large majority of transposons appear to be silenced, it seems selfish genes are notable for a common inability to keep good things away from other genes. These are new frontiers and new discoveries may change the picture of course. I'm not sure how much transposons should be considered selfish genes pursuing their selfish interests by migrating. How does migrating help transposons in competition with other genes? Or does their existence come from the inability thus far of natural selection, which selects phenotypes, to perfect a genetic mechanism that can prevent transposons.

          • k

            Transposons aren't inherently bad, they just exist, and we see them in the genome. I think that is all that can be said: transposons exist because they have duplicated themselves within genomes. The jump because that's what they do, and to ascribe them any intention is to just use a convenient metaphor. I think this is very powerful, but also very dangerous.

            A bit ago I walked 200 feet from a grad genetics course to a talk by evelyn fox keller, who was discussing redefining the term "gene" to include the regulatory environment that the protein-coding portion of DNA exists within (and comparing this to defining the notion of personhood to necessarily include inter-personal relations). Many people at the talk who were more humanities-focused saw this as a revolution, but within the context of my genetics class, it was nothing strange. The thing that we call a gene has never been constant, and has always been a convenient metaphor to talk about something unwieldy. I think that talking about genes that are "selfish" or "help" others is an outgrowth of a very popular (but ill-defined) metaphor that even those within the sciences have to really try hard not to rely on.

            Transposons are part of the genome, and in that sense have to be considered on the same footing as everything else. There can be detrimental phenotypic effects due to jumping, but there are many times no effects, and sometimes there have even been advantages. As an example, there is ample evidence that a good amount of gene duplications, which create the raw material for evolution, have been the result of transposons taking with them genes as they "jump". If you were to take away transposons completely, I am not sure if an organism, which is the result of adapting with them present, would be as healthy as it would have been with them. To look at transposons and say "evolution should take care of them" is silly. They are there, and they replicate within a complex network of feedbacks and regulations, a microcosm of the whole organism, but also part of it.

    • edobr

      I agree, the article doesn't do justice to the idea of a gene, or group of genes, surviving at any cost. We are donkey carts. Very smart donkey carts.

    • Asmodeus Belial

      Nicely put. Dobbs, whose credentials seem about completely exhausted by "lives in Vermont," seems to know relatively little about the topic he has taken on.

  • Ken Weiss

    A fine treatment of the problem. The issues are much more complex and subtle even than this article presents, and whether genes cause or respond to things is probably too rigid a dichotomy. One often sees the Dawkinsian 'logic' which is that if you deny a gene-centered view you must be saying that genes don't do anything, which of course is not what any knowledgeable person says.

    Interactions rather than competition are far more prevalent, and hence involve multiple 'genes' at once (we've called this 'cooperation' in our own articles and blog (and in two Aeon articles), as an antidote to the competition-obsession of our culture that is reflected in such views).

    This realization does, however, raise many questions about how to understand things, and this article raises some of the issues and explanations. Exactly how we can build a better theory of biological mechanisms than just to call them networks, or expression differences, etc., or the extent to which we need some fundamentally new conceptualization aren't clear.

    The altruism theory (sacrificing self for your relatives) also has not fared well when closely tested.

    Finally, I would personally don't think we need to patronize the public (to wheedle research funds from them?) by oversimplifying. It is easy enough to say (for example) that we can't understand your house by just looking at each brick, but by how it is organized. Anyone can understand that. So Dawkins' and Sean Carroll's rationale in a sense pander rather than educate.

    And as another commenter pointed out, Sewall Wright was an American.

  • Seb

    I really enjoyed reading this, although I'm not totally sure it's a just argument. I don't think the two ideas are incompatible and ultimately Dawkins' response to your phone call makes sense. At its simplest level evolution and the Selfish Gene remains. You can always go back to the gene as the simplest unit of heredity.

    In my eyes the problem lies in that the extent to (and means by) which epigenetic inheritance occurs, largely remains a mystery to scientists at the moment. Gene expression is hugely complex and modified at every level. Histone proteins, methylation, non-coding RNAs, splicing proteins, transcription factors, RNA binding proteins etc.. These things all combine to create a plastic transcriptome that can respond to change and help us adapt and survive. The role of gene expression in evolution however, does not change the fact that what is inherited is the DNA!
    If epigenetic changes were faithfully passed on resulting in changes to the DNA then maybe the idea of the selfish gene would have to change. However, even though our knowledge of epigenetic inheritance is ever expanding, the primary form of heritable material is DNA and our genes (even non-coding DNA). To write off the selfish gene as a concept now is jumping the gun somewhat.

    Being able to respond to change merely means that those genes or DNA underlying that ability will be perpetuated as long as that ability is favourable. It always goes back to the DNA!

    RNA facilitates our survival as an individual. DNA and selfish genes facilitate their own survival by producing RNA.

    • constantquantum

      Am no expert in any of these fields, but it seems to me your argument regarding evidence that must be recorded in inherited DNA, is a logical loop. DNA represents the information of the gene, while epigenetics are actions that express and change the way the information is processed (i.e. which information is prioritized and when as well as how it will be read), which results in changes in terms of "meaning" (if we are talking about meme/information theory) and in phenotype (when it comes to... body function, traits and/or 'morphology').
      By searching for the 'inheritable transcription' back in the original DNA, you are effectively ignoring the relevance of the change, itself. It's like looking at the alphabet, selecting a word that has become readable by a specific arrangements of its letters, say "disgusted," and then creating a litmus test that denies the legitimacy of "inheritance" to 1) any new words that do not "properly" modify the original word in the traditionally accepted way (by conjugating it correctly in verb form, or by defining it using approved synonyms, let's say), or 2) any new meaning making symbols that might not find a place in the original word or even the original alphabet, but still function as meaning making/morphology changing machines (outside of the prevue of the alphabet and the words it makes up), and 3) any revisionary meanings when it comes to what the original word implied (I'm thinking here about the changing environment, of course).
      What if the changing force of "genetic accommodation" is--to continue the language metaphor--based on sound rather than letters? To say we must look back at the DNA to recognize that some change has been inherited is to deny the possibility of any other way of traits being inherited. Quite the tautology, but not very useful in understanding the subtle shift in the scientific perspective behind the article and the various scientists who are trying to look at these other mechanisms.
      In the end, I wonder if the whole "Selfish Gene" meme is not just a reflection of a cultural marketplace that valorizes the individual... or the original... or the (in)genius/genus over community and the ecosystem. Hasn't complexity theory hit biology? Why are we holding on to the simple answer rather than looking at the complex interaction?
      And, btw: Isn't that new mouse study involving the inheritance of fear aversion instincts interesting?

  • Des Higgins

    "Twenty years ago, phase changes such as those that turn grasshopper to locust were relatively unknown...". It is strange then how I remember getting lectures on this in the 1970s?

    • steve_macdonald

      Hence the qualifier, "relatively". Such things were certainly not known by the average layman with an interest in science.

  • David Rutten

    There were very few concepts here that I did not take away from reading The selfish Gene 10 years ago. It seems the author confuses "unit of evolution" with "centrality". Gene-complexes, gene-expression and things like meiotic drive were as far as I can remember discussed by Dawkins in either The Selfish Gene or The Extended Phenotype.

    No matter how important the environment is (humidity, light, temperature, chemicals) it is not something the a genome has much control over and it therefore cannot be selected for/against. Those parts of the environment that genes DO have control over fall under the 'extended phenotype' category.

    I cannot help but feel that the view being attacked here is a radically stripped down version of the view Dawkins actually put forth.

    • David Rutten

      Incidentally, choosing a title that reads: "Die, selfish gene, die" and a subtitle "The selfish gene is one of the most successful science metaphors ever invented. Unfortunately, it’s wrong" smacks of popularist science journalism. The very fact that the body of the article has to mitigate the boast of the title should have been a sign...

      A sub-title along the lines of "Why a gene-centric approach to evolution cannot explain what we see" would have been more intellectually honest.

      • Allen MacNeill

        And less effective.

  • Jon

    how is the word "protein" nowhere in this article? why doesn't the author bother explaining gene expression beyond vague metaphors of "reading" genes differently? why trot out the very tenuous "meme" model at the end as an explanatory mechanism after spending an article critiquing its root concept, the selfish gene? i learned a lot here but if someone asked me how gene expression works i guess i'll have to start spouting nonsense about scraggly beards and time-machine thought experiments because that's most of what I read. maybe i'll read it differently, ha.

  • klmr

    The problem with this essay is that it fundamentally misunderstands *why* the gene centric view is special. Dawkins’ ultimate argument is that the kind of evolution based on genes that we see in our biology is *universal*. It happens in ecosystems (the “extended phenotype”), it happens in information transmission (the “meme”) and if we ever find some kind of life on other planets, it will have happened there.

    Gene expression and gene regulation is an implementation detail. It is *not* universal. It just so happens that it’s crucial for our biology, and research focus has rightly shifted to it. But it isn’t the same exalted idea as the gene-centric view. It has no (at least direct) equivalent of the extended phenotype, to memes or to extraterrestrial life (unless that shares a common ancestor with us).

    • amphiox

      I am pretty sure that extraterrestrial life will work through gene regulation just as earth life does.

      I am also highly suspicious that when we examine memes in detail, we will find that they too work through environmental regulation of expression. For example, I have little doubt that cat memes arose multiple times in human history, but it took the advent of the regulation on their expression that the internet made possible before they spread.

  • Bob

    "US and British GIs"

    GI is not a synonym for soldier.

  • Daniel Lowe

    ‘We have a more complicated understanding of football than we do genetics and evolution. Nobody thinks just the quarterback wins the game’

    Sadly, Ratings for MONDAY NIGHT GENE EXPRESSION were too low to satisfy advertisers.

    • Thaddeus

      I watched all 3 episodes. Sorry it got canceled.

      • Rick

        Monday Night Gene was a terrible host.

  • Gene

    Surely the most interesting question then would be: what dormant genes does the human genome possess that could be turned on and spread across a generation (dependent on the appropriate environment)? Or what mutant genes have been passed over due to an unfavourable environment or insufficient mating? Any research on this or is the answer simply never-ending..?

    • amphiox

      By "dormant" do you mean a gene that is not expressed, and later turned on by mutation? Such genes are vanishingly rare. Evolution is a "use it or lose it" game. The number of possible mutations that destroy a silent gene are far greater than the number of possible mutations that can turn such a gene on. And since a destroyed gene and a silent gene have exactly the same effect (ie, none) on the specific organism that carries it, selection will not preserve one over the other. Nearly all genes that are silent decay to nonfunctionality.

      The only escape for such a gene is for it not to be silent all the time. If it gets expressed occasionally, so long as the occasions in which it is expressed provide sufficient benefit, then selection will preserve it through the generations. This is the kind of gene whose expression could be greatly increased in response to changing environments, and then be subject to evolutionary change. Such a gene could, for example, mutate in a way that "locks it in" so that it becomes expressed ALL the time, instead of dormant most of the time.

      Mutations that are passed over are the mutations that occur in an environment where they are not favorable. If they are detrimental, they are eliminated. If they are neutral they may spread to a low level in the population through drift. The problem is that because their levels are either low, or they are rapidly eliminated, it is very hard, without enormous luck, to actually identify such genes in a population and even harder to observe or figure out when they arose. So this is a problem that our current scientific methods have great trouble answering.

      In Lenski's bacterial evolution experiment, his team was able to identify some examples of these sorts of mutations retroactively, after the genes became beneficial and spread throughout the population. They managed this because they've been keeping frozen samples of their bacteria at specific generation points back over 20 years, so they could look back at older versions of the bacteria to trace the appearance and disappearances of gene variants. That's not something that can be easily done for organisms other than bacteria.

  • http://quarkyscience.ca/ Wondering

    The "reactive" gene?

    • Carmen

      I was thinking... the emergent genome

  • Dominic Amann

    Aha - so the gene is like hardware, the expression is the software. When the environment changes, we can modify our programming to adapt. When the new programming has settled and proves to be successful, the hardware can then adapt to run the software even better.

    • Hominid

      Nope. The range of adaptation is severely limited in most species - they are exquisitely suited to the selective pressures of their environments. The expression rate changes of genes are NOT preserved in subsequent generations - only the original 'hardware' (genome) is.

      • Dominic Amann

        So you assert.

        I suspect you don't have any proof as to whether a successful expression can "encourage" an adaptive mutation. From the little I know, doesn't adaptation proceed at a faster pace than can be mathematically explained by purely random mutations?

        Most significant advances in science require (at least) unlearning what we "know" to be true.

        • Hominid

          Nope. Not my assertion, it's well-documented, rigorous science that I'm relating. The rest of your post is pedestrian tropes.

          • Dominic Amann

            Well, thank you hominid. It's really nice that real scientists such as yourself can quickly put down laymen who dare to comment on areas of your expertise.

            What "rest of my post"? The idea you think you have debunked was the whole of my post.

            And while we are at it, who are you really? I dislike being attacked by masked men.

          • Hominid

            Where I am ignorant (often the case), I keep my mouth shut and listen. Give it try.

          • Dominic Amann

            My way of listening is that I state what I understood from the discussion to that point, and see if it jives with the understanding of the speaker and other listeners. Which is what I believe I was doing.

            I have taken the time to read some of your vast number of posts on various subjects, and I have come to the conclusion that your chief hobby in life is knocking down people on the internet. I therefore feel little weight from the mighty force of your superior intellect.

          • Hominid

            I don't "knock people down" - I correct people's erroneous thinking & factual inaccuracies. If you take that personally, that's your problem.

        • Rick

          This statement, in particular, is not tenable:

          "From the little I know, doesn't adaptation proceed at a faster pace than can be mathematically explained by purely random mutations?"

          What is this supposed to mean? What are the units of "adaptation" and how are they occurring faster than "can be mathematically explained by purely random mutations?"

          It's the kind of sentence that gets read as "not even wrong". It sounds mathy/sciency but it doesn't really qualify as a scientific claim.

          • Dominic Amann

            Well, as I have mentioned, I am not a geneticist (and I actually believe that most people here are not geneticists either).

            I also don't have a dog in the race. I am just a layman trying to parse the article and make sense of it.

            My comment - and I wouldn't be surprised if it is hard to parse, since I am not a geneticist - is that as far as I know, "the pace of evolution is faster than current models would predict using merely random genetic mutation". Does this phrase land better for you?

            And in the other meta-thread, this way of requiring people to use correct and domain specific scientific language to engage in discussion on this sort of web site strikes me as rather defensive.

      • Dominic Amann

        Many interesting characteristics are preserved from generation to generation, including social ones that probably have little (measurable) to do with our raw genetics - alcoholism, poverty, social class, school attainment etc. These are probably largely environmental, yet we transmit them from generation to generation, and they come with higher disease rates and mortality.

        I get that I am (possibly) conflating ideas that may have no no solid connection, but I can't help but suspect that there is more to what we don't know about reproduction and the transmission of characteristics than we do know.

        We could use more study of people such as fostered and adopted children, as well as twins studies to cover more ground in this area.

        More progress is possible these days as the internet causes specialists to be presented with ideas from out of their fields - ideas that they may find intersect their own specialties.

        • Hominid

          You're a very confused thinker. Intergenerational teaching is very different from genetic inheritance. It is also the case that personality traits - including predilections - are mainly genetically determined. There are many studies of adoption & twins that support these notions - that you are unaware of them is not a valid argument against them.

          • TexasStomp

            Mornin, H. I love "twin" studies, especially identical twins, whether they are separated or live together.

          • Hominid

            As are adoptees who've never had contact with their biological parents. Also the numbers have grown greatly over the past decades increasing the statistical validity of the findings.

          • Dominic Amann

            I think it is possible to argue various points without throwing characterisations at your counterpart. Doing so probably illuminates some reaction on your part.

            I suspect that your evidence for the theory that these traits are genetic is based on the evidence that they are inherited. That does not actually prove that the genes are responsible - just that some part of the reproduction mechanism is responsible. I am aware of the studies, and the fact that most researchers wish there were more, and that more questions and tests were made. I am not aware that the results conclusively prove that only the genetic DNA material is responsible for the shared traits.

            The conclusions that were drawn by most of the research that you infer were based on a world where epigenetics did not exist. Additionally, there are acknowledged areas requiring new mechanisms in existing genetic theory.

          • Hominid

            It's not mine and it's not theory - it's valid and reliable observation that personality traits are mainly determined by genes. Your understanding of genetics and reproduction are woefully lacking.

            Epigenetics has existed for decades - there's nothing new about it. It has recently become the latest fad in junk biology.

            BTW, you need to work on your English usage in order to communicate more lucidly (e.g., "the research that you infer" makes no sense).

          • Dominic Amann

            Are you running some sort of research on internet populations to see how people react to being made wrong? I would be curious to know your results.

            As to the "research you infer" I meant the research that you say exists (and I am not disagreeing with your here) but do not actually cite, or even go so far as to explain the relevance of to the current discussion - beyond the claim that it supports your claims.

            As for the "observation that personality traits are mainly determined by genes" - mainly is a weasel word that allows for a large number of interpretations - possibly including the OPs claims, and thus, as I stated, the evidence may be consistent with your claim, but that same evidence could also be consistent with other theories.

            I don't think you have enough data about me to draw the conclusion that my knowledge of genetics and reproduction are woefully inadequate. In fact, I have 3 children alive who I think are reasonable proof that I do in fact know enough about reproduction.

            Now it so happens that for the purpose of this debate, I know very little about genetics. Possibly less than you. I tend to rely on broad general knowledge and lots of reading. That is why I posted to this thread (rather than, say, a journal on reproductive medicine, or a scientific panel on genetics). I posted in order to see if I understood the claim of the OP, and to possibly get into some discussion which would further my understanding of the subject in general.

            Now here is a theory: I think I have enough data to know that you enjoy the sensation of "being right", and making others wrong more than you enjoy the hard work of rational argument, reasoned rebuttal and in depth research. I say this because your preferred form of rebuttal is one of personal attack, followed by a roundabout dismissal of an idea, with a side serving of vague reference to studies.

            The unfortunate fact is that you may be right about any number of points you have made - I personally don't know if the OP is onto something or just re-hashing junk science myself - but your manner of arguing has not given me any sense of the correctness of either position - or even whether the positions are mutually exclusive (which you seem to think they are).

  • Science Avenger

    ‘We have a more complicated understanding of football than we do genetics and evolution. Nobody thinks just the quarterback wins the game’

    Au contraire, Given the ubiquitous nature of the "He never won the big one" criticism levied at many great quarterbacks, it seems many people believe exactly that.

  • Bjørn Østman

    I'm with Dawkins on this one. Plasticity does not imply that genes do not work the way described in TSG, namely that they are the (I would say, one) unit of selection, and they do act selfishly, even if they often interact (cooperate - I don't think that is a good term for epistasis) with other genes. Changes in gene expression are obviously, and evidently, important for evolution, and no one in their right mind believes in a one-to-one mapping between genotype and phenotype (or even only a many-to-one, aka canalization).

    IMHO West-Eberhard is the one who, while correct that plasticity is important, isn't (publicly, at least) understanding TSG idea. I get that she wants to promote plasticity and genetic accommodation, but that can easily be done without dismantling TSG. People have been working for a long time with plasticity and gene expression without attacking TSG. There is no need for that (other than for West-Eberhard trying to rectify the injustice that she is not as good a writer as Dawkins).

  • thorsonofodin

    I'm still not convinced this is the "battle" between ideologies it is
    made out to be. I see it as more an evolving dialogue of understanding.
    Genome meets environment, inherent traits emerge. We are all in a continuing
    process of development. It is worth pointing out here something David
    neglected in his discussion of Mendel's bee work. Much of Mendel's data
    and notebooks on bees were burned by the Abbot that took control of the monastery after Mendel's death. I can only imagine where we'd
    be today if Mendel's work was widely circulated in its day. Perhaps the
    modern synthesis would have begun 50 years earlier were it not for this
    ignorant act of fear in the face of science.

    • Lexi

      There is truth in the comments that the article doesn't portray the "selfish gene" hypothesis right. It's arguably false to say that the "selfish gene" hypothesis is as nuanced as it's ever going to get, and arguably false to say that we can't think of change as stemming from environment instead of genetics all the time. It is, as you say, emergence.

    • Hominid

      Or if Darwin had opened some of the letters left stacked on his desk after his death that informed him of Mendel's work.

  • Erik P Hoel

    Some people in the comments have defended the selfish gene theory by saying that the author does not understand it.

    First of all, this essay is not the author's synthesis, it comes out of an entire growing branch of evolutionary theory. Those evolutionary biologists do understand selfish gene theory. And this essay is ONLY about genetic accommodation as a strongly supported biological fact that contradicts selfish gene theory. It doesn't even mention other epigenetic effects, which are well-known to exist and are expanding daily, nor the mathematics behind non-kinship based altruism, all of which go against the idea of the selfish gene metaphor of evolution.

    The truth is evolution is substrate neutral. Anything that produces differential survival across variation is evolution. And there's all sorts of different ways to do that - Lamarckian, Darwinian, using discrete units of selection (genes), using fuzzy units of selection (phenotypes), using some fuzzy and some discrete units of selection, using individuals, using populations or subsets of populations, using expression, proteins, RNA, etc. ANY way of transmitting survival-increasing information across generations is evolution in a sense. One can come up with all sorts of genetic algorithms that evolve, but which in their rules and substrates look nothing like discrete selfish genes. It would be a supremely improbable that, of all the multitudes of ways to get evolution done, our entire planet uses ONE way, and that way happens to be so incredibly algorithmically simple it can be taught to middle school children. Much more likely is that evolution uses every single trick in the book.

    As for Dawkins saying that selfish gene theory can expand to incorporate the disparate findings of genetic accommodation, other epigenetic effects, such as those involving prions, multi-level selection, non-kinship altuism, and fuzzy units of selection, I say – good luck.

    • Hominid

      Accommodation theory is NOT "strongly supported."

  • gnollsDOTorg

    First, it's an ominous sign that this entire article was written without the use of the term "epigenetics".

    Second, note the term "gene expression". Whether we're speaking of the potential of a grasshopper to become a locust when food is scarce, the potential of fruit-eating chimpanzees to become carnivorous monkey hunters when fruit is scarce, or the potential of humans to make stone tools when naturally occurring sharp rocks are scarce, the spectrum of available variation in response to environmental pressures is controlled by -- guess what? -- genes.

    Dawkins is well aware of this, as is anyone who has read and understood both The Selfish Gene and The Extended Phenotype. In fact, it is impossible to understand the social insects from the point of view of individual selection: only gene-level selection can make sense of haplodiploidy and sterile castes!

    What I see here is a straw man created by people who either don't understand TSG, or who are trying to make a name for themselves by creating a controversy where none needs to exist.

    JS - gnolls.org

    • Allen MacNeill

      Except that there is now a competing theory (actually, competing theories) for the origin social organization and social organisms that does not rely on kin selection at all. E. O Wilson has recently co-authored several revolutionary papers presenting an alternative model for social evolution, and George R. Price published a seminal article on group selection (with W. D. Hamilton's assistance) that is now revolutionizing such diverse fields as economics, sociology, and evolutionary psychology. In my opinion, both the "modern synthesis" and "selfish gene theory" will ultimately be viewed by historians of evolutionary biology as what my good friend Will Provine calls the "hardening" of the theory: an interlude between Darwin's original theory and the "post-modern" evolutionary theory that is now being synthesized using the pioneering work of Jablonka, Lamb, Margulis, Price, West-Eberhard, and the two Wilsons (David Sloan and Edward Osborne).

      • JR

        The "competing" theory is actually just a re-modelling of the maths, and the basic principle is the same; namely Kin selection.

        • Ishi Crew

          actually, i'd say allen macneill has it right. sure, you can call it 'kin selection' (though actually extended kin selection, since you have to go beyond the classic example of people willing to die for half sibs etc, based on hamilton's rule.

          george price, s frank, etc. have gone thorugh that.

          the math gets extremely difficult, and actually irrelevant---you need a new kind of math (not really new, just 'limit theorems' and things like 'phase transitions' (as in statistical mechanics). sure, its genes, quarks, and such all the way down---mostly turtles-but 'more is different' ( P w anderson Science mag 1972).

    • Hominid

      I would suspect ideologically motivated thinking.

    • LombardoA

      Yup, glad I'm not the only one who missed the glaring omission of the exact word describing the authors ideology. Were the word epigenetics to be used no one would listen; as well they shouldn't,

  • Noah

    The selfish gene metaphor and gene expression aren't really in opposition in the way that the author argues that they are. The problem really comes down to what you define as a "gene." For instance, most gene expression differences are caused by mutations in the regulatory sequences bordering the actual protein coding sequence (or by the downstream consequences of such a mutation). It's not a huge stretch to define a gene as the region containing both protein coding sequence and the flanking regulatory information, in which case regulatory variants could be considered alleles of a gene.

    It's definitely true that evolution is much not just about the presence or absence of genes or protein coding changes in genomes but also is closely related to the timing and location of expression. And it's definitely true that the gene itself is a kind of squishy concept and that evolution isn't limited to changes in protein coding sequences. But framing expression variation as a refutation of the selfish gene concept is kind of misleading.

    • Noah

      Oops that should say "It's definitely true that evolution is not just about the presence or absence of genes or about changes in protein sequences but is also closely related to the timing and location of expression."

      Also, I see a lot of people conflating the selfish gene concept with genetic determinism, when it really doesn't imply such a stance. The genotype-to-phenotype map can be arbitrarily complicated as long as differences in DNA lead to some sort of phenotypic difference with fitness consequences. This includes plasticity and epigenetics, which are really kind of red herrings when it comes to the question of selection causing changes in the frequency of genetic polymorphism.

      • LombardoA

        hear hear. When peoples feel good mentality that all our social problems can be changed in a heart beat because there's no human nature is threatened you get ignorant people playing the expert. And as you said anyway, genes work together or they don't, doesn't threaten the selfish gene theory. I'm not a complete determinist, but when people throw around the idiom "the apple doesn't fall far from the tree," then get all defensive when you suggest it's partly in the genes I can't help but feel we're just deluding ourselves.

        • Hominid

          I agree completely. These weak, socially more palatable "theories" are driven by humanist ideology.

          • LombardoA

            Wait, I thought humanism is about there being a human nature that is partially genetic? In other words it's compatible with both nature and nurture, but leans heavily in favor of nature.

          • Hominid

            You've got it exactly reversed, Lom - humanist ideology strongly favors nurture. Humanists believe people are essentially tabulae rasae that can be molded by their 'wise' elders into 'good' citizens. The humanists also fail to grasp that there is no one or common 'human nature.' Political Liberalism is an extreme form of humanism.

          • LombardoA

            Damn, I've been misusing that term lol. There needs to be humanism that is the opposite, as the term fits the idea of a human nature far more than nurture.

          • Hominid

            There is - it's biology or biological science.

          • LombardoA

            Ha, true enough.

    • Jason

      Noah is right on the money. Regulatory DNA and coding sequences are both heritable at the level of DNA sequence. The vast majority of epigenetic modifications are controlled at the level of regulatory proteins whose instructions for expression and function are precisely controlled at the level of DNA sequence.

      Its been a while since I've read The Selfish Gene, but its not a stretch to define the gene as both cis-regulatory information and coding sequence. Kudos!

      • Hominid

        Mutations of regulatory alleles are heritable, regulatory changes in response to extragenetic factors are NOT heritable.

        • Jason

          I think there may be a problem with terminology here. But putting that aside, either the logic operations that guide 'regulatory changes in response to extra genetic actors' are hard-wired at the level of DNA or they are not.

          But consider that if they were not, then cloning would be impossible!

          • Hominid

            They're "hard-wired' to the degree that DNA sequences are 'hard wired,' but the transcription factors that bind to and control them are reactive to all sorts of signal transduction cascades which in turn are responsive to intra- and extracellular signal molecules. The transcription sequences can be up or down regulated affecting the transcription rates of the protein-encoding genes they control. Does that clear your confusion?

          • Jason

            Absolutely correct! However the responses to extracellular signal molecules are also hard-wired into the structure and function of the genes they control. This would include the expression of the signal transduction machinery, the endogenous factors to which they respond and the intracellular and extracellular systems which cause these factors to be expressed. The "regulatory changes in response to extra genetic factors" of which you speak are all also hard-coded, else it would not be possible for individuals within a species to respond to external cues in exactly the same manner.

            Take the morphing power of the grasshopper as an example. All grasshoppers of the same species possess this capability because it is hard-coded in the nuclei of every grasshopper of that particular species.

            You stated "regulatory changes in response to extragenetic factors are NOT heritable". I am saying that indeed they are heritable. They are heritable because these regulatory changes are a consequence of gene function and expression, both of which are absolutely heritable!

          • Hominid

            Of course, but that's not the question under debate. The epigeneticists are arguing in effect that the regulated STATE of a gene is heritable, i.e., that a gene in an up-regulated state is somehow transferred to the gametes and then transmitted to progeny in that up-regulated state. I see no mechanism whereby that's plausible.

      • Chengora

        It's still not clear to me what a gene is and how it is separated from DNA or any other information-carrier. The debate in these comments has devolved down in the concept stretching and definition. As a social scientist who deals with squishy concepts all the time - suggests that the base idea, the gene, is insufficiently concrete. People are debating what properties a gene possesses, asserting the "true" meaning of someone else's work, expanding some kind of amorphous definition so it can encompass outliers. There's undoubtedly some value to the gene concept, but without a clear, systematically derived definition, we don't have a good sense of its limitations. Concept stretching or "redefinition" is just moving the goalposts or rejecting alternative explanations without fully engaging in them. The "you misunderstand" claim attacks your opponent, but it doesn't advance your argument necessarily.

        As far as I can tell, here's what the wider debate comes down to. We have a unit of heredity called the gene. Within a specific, individual organism, it gets expressed in certain ways under certain conditions, but it can be expressed in other ways under alternative conditions. So we have a constant attempting to explain variation (or more specifically a random variable). You'll note that this is methodologically problematic. Constants by definition cannot lead to change.

        Then, we have some people saying these changes get embedded somehow into the gene (which we still don't have a good definition of), and that gets transmitted across generations - genetic accommodation. So a more concrete Lamarckian evolution mechanism, with little evidence for that jump. We have others saying its about the epigenetic material which really controls gene expression, but that may or may not be heritable. And finally, Dawkins (and a lot of people on this discussion thread) say it all comes back down to that heritable unit anyway, which is "selfish." But we may have to expand what it is that "seeks" to self-replicate.

        Is this all correct? Because if so, it's circular and ridiculous. Without pinning down a clear *and stable* definition of gene, everyone's just talking passed each other. Plus, the concept would fail a basic methodological issue: How do you falsify the selfish gene concept?

        I'm not saying that we need to have some hard, observable "thing" that is a gene. Concepts like "value" in economics or "power" in politics aren't tangible. But so far it seems like we're arguing at the border of a "gene" definition, and it's unfair and methodologically improper to say other people have it wrong when your central concept is amorphous. So give me the bullet point list: What is a gene, what are the indicators, what is not a gene, and how many studies that are being cited actually employ the definition you use? Feel free to reference Dawkins' or whomever's books. Got most of them on my shelf.

      • constantquantum

        Now I am confused. Aren't many regulatory events set off by immune or hormone responses to injury, emotional states, infection, hunger, etc? Those are environmental triggers, and the mechanism for evaluating and delivering change can be neurological (and therefore plastic). How are the thymus, amygdala, T-cells, pain receptors, startle reflex, hormones, etc 'controlled' by the DNA? Does DNA get to be the 'controller' of these events because we couldn't have a brain or bone marrow or a nervous system without DNA? Well, we couldn't have DNA without atoms either (as some other commentator in these threads has already said), and, from what I understand, we have more alien DNA in our bodies than we have human DNA, so why stop your back-to-origin story at the human gene? In how many ways, over the course of human evolution, have bacteria, plague, and parasites managed to shape "inherited" human characteristics.

  • TripleB85

    I’m loyal to Dawkins! The gene is the fundamental unit of selection.

    Am I understanding this article correctly? Maybe?

    Genetic accommodation is a change in gene expression that occurs when an individual is exposed to new environmental pressures. This allows genetic mutations which support or compliment the phenotypic changes produced by genetic accommodation to undergo selection. This selection would not have taken place without an initial change in gene expression.

    In my evolutionary biology course, genetic mutation was discussed as a simple, uncomplicated concept, and was presented as the mechanism by which new genetic variation is introduced into populations. Natural selection will robustly select those very rare gene mutations providing a survival advantage to individuals possessing them.

    As I understand the article, the concept of genetic accommodation describes the significance of gene expression in establishing biological conditions that can enhance and promote the selection of new genetic mutations. The author presents a new understanding of how variation, through genetic mutations can arise within a population and provide new fuel for driving the processes of natural selection.

    The phenomenon of genetic accommodation can refine our understanding of gene mutations. I was taught that mutations are typically deleterious to an organism, and are very rarely advantageous. In the context of genetic accommodation, whether or not a mutation is deleterious or advantageous will depend greatly on an organism's gene expression. Many genetic mutations within an evolutionary lineage may have actually arisen in individuals secondary to changes in their gene expression occurring with exposure to new environmental stressors.

    So it seems to me that Dawkins gene-centric ideas should not be discounted, but rather that we might reconsider its simplistic approach to genetic mutation.

    • Delusion Buster

      Indeed, it's a refinement of Dawkin's work. It doesn't disprove it.
      Newton's theory of gravity was never disproved in total, it was augmented by Einstein.
      Same thing here.

  • Rebecca Gershon, MD

    I'm growing sick of people who write about science who aren't actually scientists.

    • Tyler Brown

      Then get out there and write about science so the nonscientists don't have to!

  • LombardoA

    This reeks of a desire to dismiss an idea because it's popular and works well. The "selfish gene" threatens peoples long held belief that we are created by our environment, and our environment alone, we're not, we're a creation of both get over it. I also can't help but feel the theory is often attacked for the sole reason of its name. Nature or nurture, the selfish gene theory holds up.
    We pass on genes, whether they work together (which they do) or independently doesn't matter. It's like saying natural selection works through group selection, while we know that it works on an individual level at the least, and on a genetic level at the most (which is my opinion). Genes work together means absolutely zilch and doesn't threaten the selfish gene theory.
    .

    • Hominid

      You're on to something. Accommodation theory and epigenetic heritability are simply the latest attempts to promote humanist ideology.

  • DrG

    I find this fascinating and food for much thought. There is one, seemingly key, part that I do not understand. Maybe someone can help me here. In the example of the development of faster running through changes in gene expression, where the author says "By the time your grandchildren show up ... they run much faster than you ever did. And all this has happened without taking on any new genes.", clearly it is implied that these changes in gene expression are passed on from one generation to the next. So WHAT IS THE MECHANISM OF INHERITANCE??? And Is it Lamarckian? (Inheritance of acquired characteristics)?? (And therefore does someone need to re-do Paul Kammerer's experiments with the midwife toad? Sort of joking...) Thank you to anyone who can shed light on this.

    • LombardoA

      What the...Either the author is espousing a Lamarckian view or he doesn't understand how genes are passed on. I completely missed that. This guy just lost what little credibility he had.

      • LombardoA

        Why is this still up when I deleted it? I wrote it thinking my other post didn't go through.

    • LombardoA

      Wait, I missed that. Yes, the author is espousing a Lamarckian view of inheritance. The author has no idea what he's talking about. You're point is exactly that, where is the mechanism of inheritance? Oh right through GENE shuffling. A common Lamarckian example is that the the giraffe got it's long neck by reaching for leaves,..And this author has the nerve to force actual scientists to beat a dead horse disproving such nonsense.

    • Yaser Khan

      "... your kids, hunting with you from EARLY on, soon run faster than you ever did." (emphasis added)

      The fact that your children invested in running fast from birth as opposed to you (the predator) only since the forest fire means that gene expression has a longer time window to effect your children, hence they are faster. Your grand children also start investing at birth but since they started running with your (faster) children they are forced to invest more, hence they mature into even faster predators.

      No Lamarckian inheritance required.

      • LombardoA

        So in other words it's a "combination" of genetic inheritance and Lamarckianism. Sounds like the author is trying to sneak pseudo-science into real science and claim it's a fresh idea by sprinkling some biology in there to hide the bull. It's just like intelligent design ISN'T creationism as it's more scientific and couldn't possibly be an attempt to undermine sound science.
        It's a dead theory resurrected to reassure people that there is no human nature, and that we're all essentially blank slates. Feel good science at it's finest.

        • Yaser Khan

          No. In other words no Lamarckianism.

          • DrG

            Well, first of all, in my comment, I wasn't using Lamarckianism as some smear to imply pseudoscience. It would be very interesting indeed if some non-Darwinian evolutionary mechanisms were discovered, and these things must be determined through observation and evidence, not philosophical preference. Yet, the article seemed to suggest that these kinds of changes were passed on between generations, and the mechanism is unclear to me. In your response you suggest that he is just talking about learned behavior being acquired by successive generations. If that is the case then why all the fuss? We've known about learned behavior for a long time. I don't think that is actually what is being described in the article, but I would love to hear from the author or someone who understands this area of biology.

          • Yaser Khan

            Hello D&G,
            I regret my curt response. I believe the point David is making in this article is that such phenotypic changes precede or lead changes in the genotype. Hence genes and their mutations are still very important. However, they serve only to lock in phenotypes already selected by the environment. It boils down to a question of which change genotypic out phenotypic drives evolution.

          • DrG

            Yes, this is a very interesting concept. I think if this is the way it works it can legitimately be described as a Darwinian/Lamarckian hybrid. The faster running for several generations before any genetic change is obviously an inheritance of a characteristic acquired in response to an environmental change. Then when it gets "locked in" by a genetic change, the mechanism is Darwinian. If this is true, then Lamarck was right!! (and, by the way, Charles Darwin was on record as a believer in Lamarckian inheritance...). So maybe someone really should take another look at Kamerrer's experiments!

        • http://daviddobbs.net/ David Dobbs

          No - as I've noted elsewhere, I did not mean to suggest Lamarckian inheritance here; Yaser Khan just above explains how the children ran faster than the parents: essentially because they had to run fast earlier. A different, faster phenotype is thus created via gene expression changes related to different behavior necessary for survival. The new phenotype is, in that environment, necessary for survival. And while it's made possible by existing genes, the appearance of a new mutation (in the granddaughter, in my example in the story) provides a genetic basis for a phenotype that will be faster even absent the constant training, as it were, generated by the environmental necessity to run faster. This same process — a type of accommodation also known as genetic assimilation — has been recognized as a possibility for decades, as described (among other places) by Massimo Pigluicci here [download] http://chd.ucsd.edu/_files/winter2009/Pigliucci.geneticassimilation.pdf

          This is not meant to be taken as a replacement for more conventional development of such a phenotype, such as the selection of those who already possessed the new "fast" genes, nor is it incompatible with the modern synthesis. In my article, as I stated but clearly failed to emphasize enough (my bad), this is offered as but one example of the sort of evolutionary dynamic that the gene-centric view tends to obscure.

    • Hominid

      It a major hole in accommodation.

  • Yaser Khan

    Hello David,
    I found your article engaging having read "The Selfish Gene" earlier this year. Assuming the validity, and more significantly the primacy, of the generic accommodation point of view how does one explain the emergence of completely novel traits/phenotypes? Specifically, gene expression seems to allow turning on and/or ramping up of phenotypes already coded in the genome that can be locked in by the later arrival of new genes; but how does one explain the building up of a genome with redundant genetic material which allows genetic accommodation. It appears genetic accommodation is equipped to explain reversible phenotypic variation in a population but can it also explain the evolution of life from the first replicators?

    • http://daviddobbs.net/ David Dobbs

      No, it can't, and I didn't mean genetic accommodation be taken as a replacement for more conventional allele- or mutation-driven evolution. I obviously failed to make that dead clear. It was offered (see the passage above its presentation, in the transition from Eisen's quote to the genetic accommodation section) as one example of other dynamics that can shape evolution. It was certainly not meant to be seen as a Lamarckian dynamic.

  • Tyler Brown

    There have been some great rebuttals in the comments here! I agree with many of them, but I also think this was a very well written article. It seems to me that a lot of people are arguing over semantics. If you stick a grasshopper and a locust next to each other and ask a random (non grasshopper enlightened) person why they look and behave differently chances are they would tell you it was because they have different genes/they are a different species. Very few people would say that it is possible that both organisms were almost identical genetically, but different environmental conditions had influenced their genes to form two very different looking creatures. This is the problem. The common perception is that genes just kind of place their bets on the form an organism will need in its life and let it play out for better or worse. It is not the common perception that an organism contains a library of genes that can be manifested differently to shift the organism's form in dynamic response to the environment.
    What all this hooplah is about is explaining the reasons an individual grasshopper you pick up has the form it does. It is not about arguing the fact that genes are ultimately the way advantageous forms are passed down through generations of grasshoppers.

    • klmr

      Forget the grasshoppers. Look at the cells of your body. A heart looks markedly different from the brain, and yet both organs’ constituting cells have the same genome. This isn’t a hard to grasp concept at all, and everybody who has read TSG understands it. To claim that TSG somehow detracts from this is disingenuous.

      • Lexi

        Except that propagation of gene expression levels within an organism is a different thing altogether than propagation of gene expression levels between generations. The latter is a much more tricky problem, and many people rightly say that we don't know enough about how it's done (except in yeast).

        • klmr

          “propagation of gene expression levels between generations” doesn’t happen in the grasshopper/locust transformation. It’s still a change within the organism.

          Whether “propagation of gene expression levels between generations” happens at all is very much an open question. You might be referring to trans-generational epigenetic inheritance which, as I’ve pointed out elsewhere here, is far from a given – the previous research certainly doesn’t show adequately that it even exists (in mammals), much less that it has a tangible influence on evolution. What other mechanisms are there there? Nothing much. That’s not to say that it isn’t happening, just that we have no reason to believe it does.

          • tailwagsdog

            "You might be referring to trans-generational epigenetic inheritance which, as I’ve pointed out elsewhere here, is far from a given – the previous research certainly doesn’t show adequately that it even exists (in mammals), much less that it has a tangible influence on evolution."

            Have you seen this?

            The smell of fear can be inherited, scientists prove
            http://www.independent.co.uk/news/science/the-smell-of-fear-can-be-inherited-scientists-prove-8975995.html

            Mice Inherit Specific Memories, Because Epigenetics?
            http://phenomena.nationalgeographic.com/2013/12/01/mice-inherit-specific-memories-because-epigenetics/

          • klmr

            Yes I’ve seen it, and I’ve explicitly referred to elsewhere on here ([link]). In a nutshell, while this is a fascinating paper, people are generally not convinced of the claim that it demonstrates trans-generational epigenetic inheritance. I can certainly say that none of my coworkers are, and the paper was the subject of a recent journal club at my institute, where this very claim was picked apart.

          • Lexi

            My "propagation of gene expression levels between generations" was actually just referring to your comparison between differentiation of cell types and the actual, understudied phenomenon that was the article's point. It didn't seem analogous since one is easy and the other is not.

          • klmr

            The “actual, understudied phenomenon” – i.e. regulation of gene expression – is the subject of my PhD. And, I can tell you with absolute certainty, it’s anything but understudied. In fact, it’s the focus of most of genomics nowadays.

          • Lexi

            I was actually just pointing to the comparison that you were also pointing to and saying "it doesn't really work, the two are completely different problems and one is harder than the other". Indeed, the conflation made in the article between cell differentiation and modes of genetic accomodation is grating.

            AS FOR epigenetic inheritance, it is definitely an open question -- outside of the lab. I'm pretty sure the problem is not that we can't document how epigenetic inheritance works in controlled environments, it's much more a question of "is it significant in the real world process of evolution or might it as well be a cool molecular biology thing?" (See http://lindquistlab.wi.mit.edu...)

            ...that ^ was the actual intended post. The other I agree was inaccurate, and yet undeletable.

          • Lexi

            I was actually trying to compare epigenetic transfer to cell differentiation (your comparison), and noting that one is much easier to explain/show than the other is as they're not the same problem at all.

            As FOR epigenetic transfer -- it's very much an open question, outside of the lab. As I said before, it's easier to see in yeast than in any organisms we directly observe, so the mechanisms are certainly there. The question is not "can we transfer markers that aren't DNA", because it can happen in a very documented fashion in the lab. The question is "does it have the significance we think it might in the real world, or is it just a cool molecular biology thing". (See http://lindquistlab.wi.mit.edu/wp-content/uploads/2013/06/Grossniklaus2013NatRevGenet.pdf )

          • Lexi

            I was actually just pointing to the comparison that you were making and saying "it doesn't really work, the two are completely different problems and one is harder than the other".

            AS FOR epigenetic inheritance, it is definitely an open question -- outside of the lab. I'm pretty sure the problem is not that we can't document how epigenetic inheritance works in controlled environments, it's much more a question of "is it significant in the real world process of evolution or might it as well be a cool molecular biology thing?" (See http://lindquistlab.wi.mit.edu/wp-content/uploads/2013/06/Grossniklaus2013NatRevGenet.pdf )

  • http://thewayitis.info/ Derek Roche

    This is a really important debate and we need to get it right because it holds out the promise of reconciling the highly successful analytical methodology of the physical sciences with our emerging understanding of complex systems, specifically those that spontaneously form organic wholes.

    Selfish gene theory and its most vocal proponent fall firmly and proudly in the first camp. It is reductionistic, mechanistic, deterministic, even mathematic. And it's not wrong - even if, as the article and many comments here point out, it's not completely right either. In other words, it's not the whole story. An organic whole is more than the sum of its parts; it's what Manfred Eigen and lately Stuart Kauffman call an ensemble i.e. that which acts together, as one.

    The analytical methodology of the physical sciences cannot predict the spontaneous emergence of such an organic whole - i.e. of life from its physical substrate - because of its very methodology. It seems to it like a miracle or at least a stupendously lucky accident. What it suggests to me though is that said methodology is itself incomplete. In other words, it's not the whole story either.

    To tell the whole story we need a different methodology - a methodology of synthesis - predicated on self-causation. Such a methodology, grounded in its own logic, it seems to me, could finally do away with the apparently interventionist miracles of both cosmo- and bio-genesis, something said to be very dear to Richard Dawkins' heart.

  • Delusion Buster

    What a red herring article! "Gene expression" (as opposed to new or mutated genes) also works through natural selection and / or sexual selection. How the heck does this "disprove" Dawkins' view?

    At best this is a refinement of his theory. The title is also misleading. It should read "Augmentation of the selfish gene view"

  • deathisastar

    "We humans, for instance, share more than half our genomes with flatworms; about 60 per cent with fruit flies and chickens; 80 per cent with cows; and 99 per cent with chimps"

    These numbers are nonsense. Only 3% of the human genome can be aligned to the chicken genome, and it's definitely not identical, so the "shared" fraction is less than 3%. 98% of the human genome is aligned to the chimp genome, and it's 98% identical base-per-base, so that's at most 96%, but this is if you ignore large-scale inversions and other differences that are difficult to quantify. Half of the human genome consists of repetitive elements, so it's hard to see how more than half could be shared with flatworms.

    Please stop spreading nonsense.

    • Rick

      People who think percentage comparisons with other species are somehow meaningful simply by citing a number are just diving headfirst into the land of innumeracy. Who cares if 99% of a pair of genomes are identical? A point mutation in a human being can lead to a vastly different individual. That's a single base pair in a single gene among countless genes. The action of a single gene determines whether a fetus is male or female. And we're supposed to be impressed by a mere 99% identity?
      Whoever came up with the percentages above was probably only looking at aligned sequences. Absent such a constraint, genome size alone makes the comparison ridiculous.

  • Leonardo Azevedo

    A thought experiment on "The kids who ran faster than their parents" thought experiment.

    Imagine that those hunter-gatherers were also able to reproduce asexually, to clone themselves in times when it's hard to get sex. In the first generation, there's a fire in the forest, which makes Ana and her friend Alice flee in opposite directions, never to see each other again. Ada then finds new slower prey and starts running to hunt it. In the second generation, her offspring, clone Bobby, is motivated to run faster from childhood, achieving greater speed than her "mother" ever could. The same goes for Charline in the third gen. This won't go on forever, though, and in the 4th Gen, Diana's speed is comparable to Charline. It's important to notice that, since they are clones, if Ana grew up in the same environment as Diana, they would also have comparable speeds.

    Now Diana is running so fast, that she eventually discovers a small oasis with one fertile male. What Diana did not realize, though, is that there's another female around, Daisy, who will compete with her for scarce food and sex. Daisy is the descendant of the missing friend Alice and can also run faster than her great-grandmother ever could. The Natural Selection step will now happen between Diana and Daisy, who are phenotypically different, but genetically identical to Ana and Alice. In the end, the gene which will be passed on will be the one which allowed for greater speed across generations. Indeed, which is faster, Ana or Alice, is not the being selected here, but who has the biggest potential of becoming faster. This may look like a big difference from the classical selfish gene theory, but in fact, it is not.

    • Leonardo Azevedo

      The probability of a gene to be present in the next generation will be proportional to the fitness of the individual who contains it. The fitness of an individual is related with how many offspring she is expected to have and will be both dependent on the phenotypic expression and the environment. How genes determine phenotype (including gene interaction, gene expression and many other factors) and how the phenotype interacts with the environment are both complex questions, which may serve to better model the fitness. Nevertheless, the remaining underlying dynamics remains: genes drive Evolution.

  • Allen MacNeill

    One of the most important reasons that the "gene-centric" model of evolution has remained the core of modern evolutionary biology goes back to Fisher, Haldane, Wright (and Hamilton). It's because the mathematical models that these founders of the "modern synthesis" worked out can't accommodate changes in phenotypes driven by changes in the expression of multiple genes. The models can only use traits that are completely controlled by single genes, with essentially no epigenetic effects. This is crucial because, for evolutionary biology to be considered to be "scientific," it must be grounded in mathematical models, like physics. But if Jablonka, Lamb, and West-Eberhard are correct, this mathematical reduction of evolution cannot be accomplished, at least using the mathematical models we have inherited from the "holy trinity" of Fisher, Haldane, and Wright.

    The real irony of all of this is that Darwin's original theory was, like the emerging "post-modern synthesis," NOT grounded in mathematics at all. Darwin was a notoriously poor mathematician; he could handle basic arithmetic, but anything beyond that was beyond him. For this reason, his theory is grounded in phenotypes, not genotypes. He wouldn't have referred to it that way, because those terms hadn't been invented yet, but his (and his co-creator, Wallace's) theory is focused on natural selection at the level of whole individuals (and, in the case of social animals, on the level of families or groups). Hence, the "extended synthesis" trumpeted by Pigliucci et al is actually a return to a more classically Darwinian version of the theory of evolution, with the added concepts of random change (courtesy of Sewall Wright and Motoo Kimura). Plus ca change, plus c'est la meme chose...

    • Hominid

      Reduction to maths is NOT a criterion for scientific validity.

      • Rick

        "It can be argued, in fact, that maths are the ultimate in delusional thinking."
        Not if you're doing it properly. Mathematics only pertains to relationships between abstract ideas. But there's nothing delusional about that.
        The delusions happen with people think that a mathematically elegant theory must also be true. _That's_ the delusion. Don't blame mathematicians for that.

        • Hominid

          I didn't "blame mathematicians" for anything.

          All ideas are delusional. At best - which is rare among human brains - they are useful approximations of material reality.

    • alqpr

      I suppose this may not be strictly wrong, but it leaves the wrong impression that mathematical models of gene interaction and epigenetic effects do not exist.

  • JonathanMaddox

    Well at least Newton had some humility: "If I have seen further, it is by standing on the shoulders of giants".

    • Hominid

      That remark is widely considered to be disingenuous - Newton was a notorious ego-maniac.

  • Guest

    Looks like Dawkins is hung-up on his own big-"G" word. If you needed any more proof that Dawkins is the type that will try to force facts to fit his theories, look no further.

    Consequently, it's amusing that his crowd so vehemently mocks and ridicules the "God did it" answer because it was lazy and easy, but prefer to stick with their own antiquated and increasingly proven to be inadequate model ("Gene, trait, phenotype" - now with two more steps!) "because when talking to the public, he finds a simple story is a damned good thing to have."

    • LombardoA

      Yes, evolution, biology, neuroscience, and chemistry are ALL very simple to understand. Also physics, which I learned in an afternoon while watching the Lord of the RIngs trilogy. You didn't come up with that idea yourself either, I guarantee it. You don't understand Dawkins, and therefore trust others criticism of him.

  • Jurij

    Sorry to inform you. But you misunderstood the whole theory of the selfish gene. I would recommend you to read "The Selfish Gene" it explains the theory very well. The selfish gene is more cooperative than selfish. So the book title is a bit weird, but read the whole book!

  • David Whitlock

    The problem is with the "centric" view. There is no "center".

    Everything is coupled, and coupled at the level of noise. That is the definition of “noise” in a physiological sense, where “signals” are “interfered with” by physiological and non-physiological things that are not “signals”.

    Genomes don't specify phenotypes. A genome specifies the genomic response of an individual cell to “signals” at the cell surface or inside the cell.

    The phenotype is the emergent property of the zillions of cells working together “in sync” based on local “signaling” between cells.

    All “signaling” is local because there is no 'action at a distance'. There is no “center” that “central signals” can come from.

  • edobr

    The example of a grandchild being spontaneously faster than the other grandchildren (due to a new polymorphism) is a poor argument for this idea. Yes, the grandchild only existed because the grandparent changed their expression levels to be faster but that is chance. The grandparent could have, also by chance, been lucky, or smarter and have had the same results: a group of grandchildren, one of which has a new mutation. My point is that the expression levels of the grandparent are not passed on to the offspring. Only the genes are (as far as we know right now).
    Gene expression is immensely powerful but it comes about from...the genes.

    • constantquantum

      "as far as we know right now" yes. That qualifier, of course, effectively (and properly) de-legitimises the claim of "only" in the previous clause.

      • edobr

        Would this be a more accurate statement?: Epigenetic changes are powerful and might be passed on to offspring but epigenetic mechanisms arise from information coded in the genes.

  • LombardoA

    Everyone must realize one fact. No where in the article does it mention the word epigenetic...but that's what the article is espousing. Why does it do this? Because were it to mention that word, everyone would immediately stop reading and forget it, then wipe their memory clean to clear out space for actual science. Epigenetics is pseudo-science at best, complete hokum at the least. If an author doesn't have the bravery to even mention what it is he's talking about, then it's not worth taking seriously.

    • http://www.totycle.com JulianDavies

      Curious about the intensely negative reaction some posters have to epigenetics. Can you point to a quality critical review we could read that backs your assertions about junk science?

      • LombardoA

        Well, my main problem with epigenetics is that it is seen as a completely revolutionary idea in evolution, when it's not. It's also meant as an alternative to natural selection, which has stood the test of time and is and will always be, in my opinion, the main theory for one of the major ways evolution works. And again, our genes being flexible does NOT change the fact that the gene is the smallest unit of selection.
        Lamarckism is the belief that we evolve by inheriting acquired traits from our ancestors.The problem with that is that the vast, vast majority of traits could not possibly be attained without mutation and the selection of those mutations. Mutations that occur while alive just normally aren't passed on. I don't really need to point to anything new that contradicts this, as the evidence provided for epigenetics as an alternative to natural selection just isn't convincing. This means that our CURRENT view of evolution is the best argument against it.
        To be clear, it's not the discoveries in gene acquisition and flexibility that are the problem, it's the assertion that it's a viable alternative to natural selection which is just ludicrous. Also, and I can't stress this enough, epigenetics as been hijacked to "prove" that you can think your way out of sickness, or that by being fat you'll make your kids fat, or make them gay by being gay, or numerous other ridiculous assertions.
        The titles was meant to be incendiary, and touts new findings in genetics as if it completely destroys a long standing theory...it doesn't, and the author misunderstands this which is kind of embarrassing. Epigenetics as a theory in evolution, hokum, as a description of promising scientific findings, fine.

  • Jonathan Schwartz

    Temporal differences in gene expression are coded by guess what? Other genes.

  • tchad49

    Well done David. Complicated issue, well-translated into every day language. I am not a fan of Dawkins' metaphors, including a vision of humans as "lumbering robots just designed to help our DNA reproduce." (that's not an exact quote) DNA is not destiny. Nor is it a blueprint. Metaphors can often mislead. There is an old article from 20+ years ago that tried to tackle this from a different angle, relevant to the question of whether a person exists from the moment of conception. The author argues there are so many stochastic events that occur during the unique unfolding of embryo, that who you are is not determined by the DNA -- rather by the process of embryogenesis itself. See: “Is an embryo a person?” The
    Nation p.557-9, Nov. 13, 1989 (if you can find it). I think that was a unique argument.

  • jonmep

    Yeah, as other commenters are saying, this is a strange article that reads a little like one of those creationist essays - rubbing its hands in glee because there is some debate about evolution and so therefore "god must have done it". Epigenetics (what this article is about but mysteriously without saying so) is interesting as an ontogenetic mechanism but it doesn't, as this article suggests, disagree with the prevailing view of genetics at all. Sure, there is other stuff at play during the development of an organism but it's still all passed on through genes, including the ability to adapt to a changing environment like the grasshoppers/locusts can.

  • Nick D Waters

    Nothing said in the article affects the basis of the selfish-gene idea. Gene expression is an adaptive trait that is still subject to selection pressure, and ultimately the organism which leaves more copies of its DNA, which includes epigenetic information, most influences the attributes of its successors.

  • janvones

    The author should have quoted Ernst Mayr, who pretty much dismissed Dawkins' beanbag genetics out of hand.

    What are selected are phenotypes (whole live organisms) not genotypes (their individual genes). Anyone who can put the time into understanding the oversimplified selfish gene can understand selection is phenotypic, not genomic.

    This is obvious for things like the sickle-cell anemia gene. It has no definable fitness value outside a specific organism. The gene can kill you, make you resistant to malaria, or make you susceptible to it, all depending on what other genes you have and where you live. On its own, however, knowing this gene is found on one chromosome gives no definable fitness value, from death, to resistance, to irrelevance, at all.

    Note that Dawkins has never published an equation, just anecdotes, and now politics. He's not a scientist. He's just plays one in the media.

  • Rick

    "Then he did something so slick and wonderful I didn’t quite realise what he’d done till after we hung up: he dismissed genetic accommodation… by accommodating it. Specifically, he said that genetic accommodation doesn’t really change anything, because since the gene ends up locking in the change and carrying it forward, it all comes back to the gene anyway."

    You call it "slick". I call it obvious.
    This article is far too concerned with fluffy paradigmatics. Whether the gene is "the central mover" or not isn't really a scientific question.

    • Lexi

      Agreed, and that's another perfectly good way to look at it. It doesn't really investigate the question of whether genes sometimes follow instead of lead, and if so how and by what mechanism, but perhaps such a question is unimportant.

  • Majdar

    Very bad, understand first the biology and then make crazy claims that you are revolutionizing a theory...

  • Grizzly Clark

    David Queller, in one of the greatest rhetorical scientific papers ever composed, would disagree with the authors methods, though he did understand the value of taking on an establishment figure as a means to gain notoriety for oneself. read it; http://academic.evergreen.edu/curricular/adaptation/downloads/Spaniels.pdf

  • Shayne

    Great article, however I have a bit of a bone to pick with the author saying the book is magnificent. If Dawkins wasn't so ignorant of history and philosophy, he would have known not to use a lot of the metaphors he did in the book, especially considering the history of social Darwinism. And in fact Jeffrey Skilling from Enron listed the book amongst his favorites. Did he read it cover to cover? Probably not, but do most Christians read the bible cover to cover, likely not. Also, I see no mention here of morphogenetic fields.

    • Guest

      To quote one of the truly great intellectuals of our time:

      "If you want to change the world, you have to change the metaphor." - Joseph Campell

      Consequently, the "selfish gene" was a crucial and complementary metaphor for Reaganism and Thatcherism.

      • Shayne

        Thanks for the reminder of the Campbell quote. Of course, Dawkins and his clan will never admit to this, because they strictly adhere to the computational theory of mind (Dennett), while Lakoff's work on conceptual metaphor came out of his work with Mark Johnson on the hypothesis of an embodied mind. Iain McGilchrist has since developed this work further with his book, "The Master and his Emissary: The Divided Brain and the Making of the Western World". Others too in neuroscience, have developed this theory of mind further, for myself personally, it's just deeply intuitive, I've used Lakoff's ideas on re-framing with deeply conservative family members and seen it work. Metaphors are indeed self-fulfilling prophecies.

        • Guest

          I've had McGilchrist's book sitting on my desk and have been meaning to read it for awhile now, thanks for that reminder (and especially the endorsement).

          I agree whole-heartedly with what you said, particularly that framing devices and re-framing are exceedingly powerful. I need to look into Lakoff's work, because the name is admittedly new to me (though, I'm sure his work will come across as familiar). For me, author/philosopher Alan Watts employed metaphor with great expertise, and his work helped grant me a new found appreciation for both metaphors in general and the insights of Eastern and Western philosophies and how their accompanying images of the world fundamentally affect us in different ways (thinking, feeling, behaving, etc...) in particular. As did Alfred Korzybski, whose General Semantics and its guiding tenet - "the map is not the territory" - had a world-rearranging impact on me. Along with the work of Robert Anton Wilson (whose work builds off of Korzybski's) and his concept of "reality tunnels" being our own maps of the world:

          "A reality tunnel is the model of reality that you build in your head. It's not reality, it's what you think reality is. Just as Korzybski said, 'the map is not the territory'; as Alan Watts said, 'the menu is not the meal'; in the same way, your reality tunnel is not reality. It's a model you personally built over your entire life, based on your experiences, your memories, your senses, your prejudices, your culture, and to a large and surprising degree, language. And that's fine, that's normal, we need models. We need models to understand what's going on around us, to predict what's going to happen next. But a model is, by definition, a simplified version of something. It may look roughly the same, and it gives you a good idea of things, but there are going to be places where it lacks the detail, or it's just wrong or it's different. And when your reality tunnel doesn't map reality, then you are wrong. And the fact that we use these things means that we will always be wrong."

        • Guest

          Have looked into some of Lakoff's work and found it quite in line with the material I mentioned (his and Mark Johnson's work is even referenced in the General Semantics wiki article). Still, always great to hear the concept stated so clearly and concretely, I look forward to reading some of his books.

          On another note, just came across a pretty powerful metaphor/re-framing of personal identification that illustrates how employing Lakoff's findings on how our "thoughts comes from the nature of the body" can lead to a stark perceptual shift (should be start/be cued up around 1:36.05 and ends shortly thereafter):

          http://youtu.be/jem9zXw0r5g?t=1h36m5s

          And here is a lecture from Alan Watts you might enjoy (for when you have the time) where he discusses some of the world's prevailing myths:

          http://www.youtube.com/watch?v=kLil-GjHiXc

  • Song of the Ape

    Do you know what matters more than the fact that Dawkins is a "he" and he's from Oxford University? The fact that he's right - and that this overly simplistic article, just like other articles that come out every few months or so in things like Aeon or some NPR blog that claim to definitely refute Dawkins or Chomsky or Wilson etc, does absolutely nothing to discredit the selfish gene.

  • stevesailer

    Instead of "The Selfish Gene" a more accurate metaphorical title would have been "The Dynastic Gene."

  • Guy

    I have three comments:
    I won't dismiss gene centralized selection so easily as it has solid evidences, for example in molecular selection for agriculture.

    In addition the idea of genetic accommodation as you explain it here is not different than Lamarckian inheritance. however, If the offspring would inherit fast running from his parents by gene expression changes, one would expect to see a lot of dynasties in Olympic runners.

    Also, it is not clear how a gene emerges to lock the phenotype, is there any evidence for directed emergence of new genes? the current evidence are that new alleles emerge in a random process of mutation.

    • Guest

      Check out this segment from an interview with mycologist Paul Stamets about how a certain plant's survival in a given environment isn't dedicated to and selected solely by its own genome (relevant part should be cued up at 23:41...lasts until about 27:35):

      http://youtu.be/90vhfdj1zic?t=23m41s

  • Matt Baen

    A lot of this ain't new. Do the names Waddington, Schmalhausen, and James Mark Baldwin mean anything to anyone?

    Evolutionary ecology had its day, but it was an oversimplified model. It will be assimilated into a developmental evolutionary synthesis that includes multilevel selection and extragenomic inheritance.

  • Jonathan_Briggs

    So - The gene sequence has no commas, colons, semi-colons and only the one full stop (and even that is doubtful), so like anything written by a lawyer, it is open to infinite interpretation by the reader...

  • John Cory

    I agree that the phenotypes are "selected" - that is, they determine if the organism passes on its genes. But that last bit says it: the genes are passed on. So, the genes remain the inheritable unit.

    And fine that some organisms have this flexibility to be one thing under one set of circumstances and another thing under another set of circumstances, but it is the genes that must provide this flexibility. The human genome may have the flexibility to make us taller under good nutritional circumstances and shorter under poor ones, but it is not crowning my head with a fur cap in winter. why not? Because the genes do not allow for it. If flexibility is demanded in terms of gene expression, this trait will have to be selected - and that is all done via the selfish-gene model of evolution.

  • benny bozetti

    "Mendel to Dawkins have celebrated the supremacy of the gene. Their argument is simple, elegant, and wrong"

    Freelance journalist PAWNS Mendel and Dawkins! Two scientific legacies pulverized in an instant by freelance journalist's laser insights. Ka-BLAM!

  • benny bozetti

    "...Dawkins makes the news so often for buffoonery"

    And "freelance journalist" makes the news for speaking truth to power -- ka-POW! "You Mr Dawkins may be a Fancy-Pants Oxford PhD, but I am a freelance journalist, and I speak for the trees! Ka-BLOM!"

  • Richard Reichart

    Back to Lamarck?!?!?

    • Guest

      Lamarck is dead, long live Lamarck!

  • Guest

    Funny how many defend the "gene-centric" worldview with as much absolute certainty and fundamentalist gusto as the "geo-centric" worldview of yesteryear. Also, in which part of The Selfish Gene did Dawkins discuss the microbiome? Or should we just revise our interpretation yet again and shoehorn that in so Dawkins' legacy can live on?

    Natural Selection And Microbiota
    http://www.science20.com/gerhard_adam/natural_selection_and_microbiota-93828

  • AaronA

    “In order to change an existing paradigm you do not struggle to try and change the problematic model. You create a new model and make the old one obsolete.” - Buckminster Fuller

  • Evolution P.S.A.: Selfish Gene
  • gartfunkel

    So, another way to look at it might be, is that saying genes drive evolution is like saying a stenographer drives the proceedings of a court.

  • sudon’t

    Hmm, it seems Lamarck might have been onto something after all…

  • Trapper

    Really cool discussion, thank you all of you -- almost as edifying as the article! I can only conceive of this discussion in metaphors, not being a genetic scientist. Can it not be seen as: the full orchestra is the genome. This on its own produces the unique sound of warm up before the symphony concert begins. It is the score -- information -- that determines each instrument's sequence and duration, and the conductor expresses them, a protein and gene component similar to the players of the instruments. Gene expression in this analogy is heritable -- or effectively so -- when the information is stored and transmitted through culture (the score written on the paper). A genome creates a body through which it transmits (imperfectly) information to the next generation. I don't see why culture can't be given the same respect just because it isn't tactile.

  • Hwang Kim

    See last part~

    Can I ask? bees are carrying plant's genes??

    that's why Mendel killed Bees...

    you seems like a poet

    but you'd better check real meaning of biological words, not just poet's words

  • Josiah Guttierrez

    Just because Dawkins is a total douchebag (one of the world's biggest douchbags in fact) doesn't mean he's wrong or that we should disagree with his ideas.

    • steve_macdonald

      He's not just a douchebag, like so many of his colleagues he's something of an idiot savant. Brilliant in his chosen field, he reverts to the most puerile, unsophisticated rubbish imaginable when he addresses fields such as theology, about which he apparently knows less than a typical reasonably bright 17 year-old. Someone like Dawkins can no more talk intelligibly about the philosophical profundities embraced by religion than a typical born-again Christian can talk knowledgeably about evolutionary biology. If anything, the typically high but very selective intelligence possessed by scientists and their acolytes seems to actively prevent them from being able to even frame the metaphysical positions against which they rail (Dawkins being the poster child for such unbelievably shallow ranting). I have yet to meet a militant atheist who can even come remotely close to elucidating some of the basic principles tied to various theological schools of thought -- although I do hear a lot about "sky fairies" and such. Nor are they *ever* able to even grasp that there is an epistemological problem with reductive materialism in the first place, much less provide an explanation thereof.

      • lapis

        'Dawkins being the poster child for such unbelievably shallow ranting'
        Please submit some proof.

  • Daniel Munro

    This article is irresponsibly inaccurate.

    "How vital, really, are actual changes in the genetic code?"
    The author needs to look up the definition of 'genetic code'. The genetic code is identical among almost all living organisms.

    "But bear with me a moment, and you’ll understand how you, dear reader, could evolve into a fast and deadly predator."
    Surely the author does not think that an individual can evolve, and if so, he needs to look up the definition of 'evolution' too.

    "Your descendants have a new gene that helps secure the adaptive trait you originally developed through gene expression alone."

    The author apparently doesn't realize that the changes in gene expression that allow individuals to change their bodies had to have previously arisen through long-term evolution. The 'before' and 'after' state of the individual are encoded in genes that regulate the expression of other genes.

  • saksin

    Among the more salient conceptual confusions that plague David Dobbs's article is the one between change in organisms and their evolution. One of the things that evolves on earth by classical mechanisms of natural selection is shapeshifting organisms such as his grasshopper/locust exhibit. Most species lack such a capacity altogether, and the ones that have it have clearly defined options such as from grasshopper to locust (but not to cricket, etc.). Need I ask what defines those options?

    "In social honeybees, the differences between workers, guards, and scouts all arise from gene expression, not gene sequence." And what, pray tell, determines that honeybees have just those three options, and the environment-sensing mechanisms to trigger one or the other of them? The answer, of course, is as before. Most species, meanwhile, are single-issue, albeit with typically two sexes, though some have environmentally triggered sex change as a life history option. Why do we not have that option, except by artificial means? The answer is still the same...

    The "just-so story" illustrating "gene accomodation" is hilarious, but should be clearly recognized for the science fiction that it is, not made any more palatable by its implausibility. Following up on it, Dodds tries to dismiss the crucial role played by the genes (noted by more than one commentator) even in this free fantasy, by claiming that "the new gene didn’t create the new trait. It just made it easier to keep a trait that a change in the environment made valuable." Not so: Dodds is conflating two different traits, namely the speed and muscles acquired phenotypically by exercise, and the speed and muscle vouchsafed on a hereditary basis by the lucky gene that shows up to save the day for the hapless original species... The former trait did not become the latter trait, the latter arose de novo through that felicitous gene. Those two traits have nothing to do with each other except their shared property of rendering a phenotype swift and strong, but through radically different means.

    To get a sense of the plausibility of the purported scenario, do the math on the odds that such a perfectly tailored gene should arise to save the day. I'd hate to entrust the future of my genetic destiny to such odds....

    As for the killer bees, notice that the putative gene expression factor in its genesis is pure conjecture on the part of Robinson. Their aggressiveness might easily have been selected for by standard means, i.e. by selection on a natural range of heritable differences in aggressiveness on the part of ancestral populations.

    And so on... I'll end by paraphrasing a fellow student from my grad school days: "Without genes you have absolutely nothing, but without "gene accomodation" you still have plenty"... That simple and incontrovertible fact is what establishes the primacy of genes in biology. Not to see that is to miss the central explanatory construct of evolutionary theory.

  • dwdp

    Oh, please. I had a microwave dinner last night that was tastier than this warmed-up Lamarckianism. Unless you can demonstrate that changes in gene expression cause heritable changes in germ-line cells (eggs, sperm) then your entire premise is wrong. And there is almost no evidence of heritability of anything other than DNA (whether it's classically-defined "genes", or uncoding regulatory regions). Evidence of heritability of anything that's not based on DNA is sparse, tends to be restricted to specific instances, and does not invalidate the concept of the "heritable unit of selection" in any case.

    There is a tactic of pseudo-science writers. Take a phenomenon that's well-understood in the field but not well-understood or publicised outside the field. Present a distorted version of it as a magical, game-changing idea. Quote a few people out of context and present a few case studies that don't really mean what you think they mean. Darkly suggest a conspiracy to suppress the idea by a vaguely identified group of people, usually including Richard Dawkins. Spice with a few real concepts that are also new to the general public but well-understood in the field. Hey presto! A controversial, link-bait "science" article.

    Thanks for the laugh though.

    • James Bronzeson

      are you serious? See Jablonka and Raz 2009:
      Transgenerational Epigenetic Inheritance: Prevalence, Mechanisms, and Implications for the Study of Heredity and Evolution

      • dwdp

        Thanks. No, I'm not serious: I actually had pizza, not a microwave dinner, and it was pretty good.

        In regards to that paper, it's a good review. However I don't see how it invalidates my conclusion that: "Evidence of heritability of anything that's not based on DNA is sparse, tends to be restricted to specific instances, and does not invalidate the concept of the "heritable unit of selection" in any case."
        This article makes the case that gene expression differences in the somatic cells are a major influence and have a major effect on heritable changes in the germ line cells in many systems (an extraordinary claim that is basically Lamarckianism in drag), misunderstands what Dawkins actually says and instead presents a straw man, makes the case that it's a major controversy and a bit of a cover-up , all the while without providing any evidence. It's just not good science journalism.

        • James Bronzeson

          I was referring to your statement: "And there is almost no evidence of heritability of anything other than DNA (whether it's classically-defined "genes", or uncoding regulatory regions)." You know in every egg there is maternally contributed transcription factors, RNA, organelles....

    • tailwagsdog

      "Unless you can demonstrate that changes in gene expression cause heritable changes in germ-line cells (eggs, sperm) then your entire premise is wrong.

      Hot off the presses:

      The smell of fear can be inherited, scientists prove
      http://www.independent.co.uk/news/science/the-smell-of-fear-can-be-inherited-scientists-prove-8975995.html

      "Scientists have shown for the first time that fear can be transmitted from a father to his offspring through his sperm alone in a ground-breaking study into a new kind of genetic inheritance..."

  • W. Bloom

    Excellent article! Beautifully written, informative, exciting. This is probably the best science article I've read in the last year. I learned cool stuff about grasshoppers and locusts that I suspect I'll remember and regurgitate for years to come. It's a joy to come across writing this good.

    The excellent writing aside, I do have a couple of small problems with the content of the article:

    I didn't like the "buffoonery" comment. That comment, together with the title, seems to betray an axe to grind with Richard Dawkins that has nothing to do with genetics, nothing to do with science, and doesn't really belong in this article. What the author calls "buffoonery" I would characterize in a VERY different way, and the anti-Dawkins stuff makes it harder for me as a reader to get on the author's side.

    Secondly, I don't get it. I'm not a science-person, but the description of gene accommodation doesn't seem to argue against the selfish gene concept to me, but for it. Genes are the hero of that story. The article certainly demonstrates that gene expression plays a fascinating and vital role, and that the relationship of genes to phenotype is more complex than I previously knew. But it still seems like natural selection works upon genes, and that genes that propagate themselves better (via their effects on the organism) spread through a population, which I thought was basically the point of the selfish gene concept.

  • http://www.rknibbe.com/blog RKN

    Gene expression changes perforce a change in the environment that would make muscles perform better is not related to the gene mutation that just-so happened to confer the same phenotype. Those two molecular changes, as given in the hypothetical example anyway, were independent. The author was mistaken to indicate the former drove the latter.

    However, I thought the article was good for pointing out to readers who are saturated & enthralled by the gene-centric theory that there's much more going on in an organism at he molecular level for the process of natural selection to work on. Yes, DNA is the chemical unit that is selected, nothing controversial there, but natural selection describes a *process*, not an outcome. A process whose only as-if interest is supposedly reproductive success, a proposition not without its weaknesses if it's not a tautology.

    Molecular level adaptions to changes in the environment is of course well documented and understood at the level of the cell -- a simple change to the extra-cellular matrix in cell culture can produce dramatic changes in the cells' phenotype, and change an individual cell's fate to divide or die. This, even though the cells are isogenic. Scale this up to whole organisms and you can easily see how natural selection must be operating on more than a mere "parts list" in the nucleus.

    That was my takeaway anyway. Of course, I don't think the author went nearly far enough to show how complexity is manifested at, say, the level of the proteome (post-translational modification anyone!), and how these variations are even stronger determinants of phenotype, phenotypes that can and do vary dramatically across organisms having identical or near identical genotypes.

  • http://www.rknibbe.com/blog RKN

    For commenters wondering if the author has resurrected Lamarck ... consider that if plasticity in the germ line permitted certain "epi-genetic marking" to result from environmental cues (e.g., obesity induced type II diabetes), and say these "marks" are heritable marks, ones which result in changes to the activity of one or more genes, then theoretically one could see that as a possible mechanism for Lamarckian evolution. Not as a replacement for the theory of Mendelian inheritance, but possibly a modulator of it?

    http://www.ncbi.nlm.nih.gov/pubmed/22975443

  • DB

    My question is both to aeon and to the people supporting this article in comments: why on earth should anyone listen to a journalist with no scientific credentials pontificate about Dawkins being "wrong"? I am aware of Mr. Dobbs' previous work as a science journalist, as well as his previous dodges when asked for credentials. All he has done here is cherry pick some opinions from actual scientists (some of them also unqualified to proclaim a theory "wrong"). At least in this piece, your tone is inappropriate and your confidence hollow, Mr. Dobbs.

  • tailwagsdog

    A recent finding (released just this past week) worth consideration:

    The smell of fear can be inherited, scientists prove
    http://www.independent.co.uk/news/science/the-smell-of-fear-can-be-inherited-scientists-prove-8975995.html

    Mice Inherit Specific Memories, Because Epigenetics?
    http://phenomena.nationalgeographic.com/2013/12/01/mice-inherit-specific-memories-because-epigenetics/

  • AndrewM

    There is so much that is right (and interesting) about this article that it is a shame that it gets some basic ideas confused. But that is because there are such complex and poorly understood ideas involved, so of course we get confused. Here is the easiest way I can think of to explain.
    Take a locust and a grasshopper. This is a stunning example - two organisms that look like different species, but have the same genes, and in fact can transform from one to to the other. The missing ingredient? Gene expression.
    But here is the (critical) thing. Do grasshoppers just happen to have the ability to transform into locusts? No. They have INHERITED the ability to transform the expression of their genes. Now, what form does that inheritance take? Is it a particular string of base pairs on a chromosome somewhere? Or is some other mechanism involved? I have no idea. It is a great question. But whatever it is, it can be called a gene (or genes) in the broad sense. As the article itself points out, the identification of DNA sequence as what is inherited comes late in the story and is not theoretically essential.
    Same with the predator thought experiment. The ability to express your genes in the form quick-and-sneaky and also in the form strong-and-fast is an inherited ability. It is probably there because of natural selection for exactly that flexibility. If it is there by accident, then it is a familiar case of a trait that happens to be useful in novel circumstances that then gets shored up by natural selection.
    Nothing new here, move along.

    • Roy Niles

      "If it is there by accident, then it is a familiar case of a trait that happens to be useful in novel circumstances that then gets shored up by natural selection."
      What you don’t seem to understand is that a behavioral trait cannot be acquired by accident. All such traits are intelligently contrived. Accidents don’t contrive experience, they require organisms to react to adapt to what that experience teaches them. And if you don’t understand that learning from experience has required all life forms to have and use some form of trial and error intelligence, then you haven’t learned what you could and should have from this “even if it’s less than perfect” article.

  • mysterics

    This doesn't seem to contradict the selfish gene at all, the fact the same gene is expressed differently doesn't challenge the idea that organisms are vehicles for genetics.

  • http://neuroautomaton.com/ Zachary Stansfield

    The author of this essay appears to build a straw man argument against the "gene-centric" model, most notably by implicitly equating phenotype with heredity.

    It is undeniable at this point that gene expression can vary widely as a result of environmental influences and interactions with the products of other genes. Such plasticity in gene expression can have a major effect on the current generation, and if we buy into the epigenetic hype, it may sometimes also produce effects on the offspring, although current evidence has only conclusively shown that this lasts for about one generation.

    Nonetheless, the genes themselves represent a limiting factor on the kinds of expression changes which can occur. In order for traits to change across evolution, we need a vector that will last. And, it is the gene, not its variable pattern of expression, which provides the vector for this evolutionary shift.

    Gene accommodation is a nice name, but it adds nothing truly unique: it is an implicit component of the current paradigm. Of course, a species needs to adapt to a new environmental niche in the short-term in order to survive--in cases where this is not possible, the species dies out. But, over the long term, it is genetic changes which allow this new species to adapt itself efficiently for its environment.

    Who cares "which comes first"? Where is the paradigm shift? Genes are critical to heredity and their expression is critical to the phenotype of an organism. Nothing new there. Dawkins sees this for all of his "simplicity". He wasn't being slick, he was just being consistent.

  • Enrique Povo

    I was relieved when I read most of the comments. I thought it was just me who could not see how gene expression was altering the fundamental key role of genes. I was a bit apprehensive when I started reading the article, expecting a fatal blow to the Selfish Gene - which never came.

  • John Ashton

    Every few years someone comes up with some variation on Baldwin's effect and thinks that they have overturned the Modern Synthesis. Yawn....

    There is a bit of brouhaha, some gullible journalism, sneering at the creators and popularizers of The Modern Synthesis (like Dawkins) as being terrible stick-in-the-muds. Then it all fades away ind it is business as usual until the next variation on Baldwin's effect is "discovered".

    Even such a luminous thinker as Karl Popper (in "Unended Quest" put forward his own theory of Baldwin's effect and thought he'd corrected Darwin (he later recanted). Dawkin's pal Daniel Dennett gives a very nice description of Baldwin's effect in "Darwin's Dangerous Idea" but presents it as just part of standard Darwinism (which it is).

    Just wait, this too will pass...jAnd then someone new will arise to "overthrow" The Modern Synthesis with yet another manifestation of old old old ideas.

  • https://www.twitter.com/nirax No Mist

    Dobbs tried to read "The Selfish Gene" and couldn't understand the Game theoretic reasoning. He guessed that others too are as ignorant. Hence "why not lay it to rest" ...

    This article is just so much ROFL-worthy ...

  • Agga

    Today was the day I realised once and for all, that science is a religion, Dawkins is God, and the people of the internet are his minions.

    I read this piece, and the ones "debunking" it. What it comes down to is that there is a holy man whose holy writ should not be challenged. The so called "factual errors" turn out not to be the reason this article is wrong, they are just proof that this must be so. The reason the article is wrong is because it is wrong, dammit! It boils down to how one makes sense of a certain metaphor, and what this metaphor is taken to mean.

    Pinker actually claimed Dobbs "hates genetic evolution". Only a blind fundamentalist could have taken that from this article. Sheeple.

  • Dr Don Stewart

    Dear Seawall, A long article but I didn't see any mention of the term "epigenetic" let alone any discussion what it might be.

  • Erick H

    I was pleased near the end when the author had called Dawkins to see what he thought about "gene accommodation," and Dawkins's response was the same as mine. To paraphrase, this writer seems to have misunderstood; genes are not active agents, they don't act alone, and they can prepare an organism to be flexible when flexibility itself is necessary. They are filtered by the environment, and their expression is informed by the environment; there is no contradiction. Genes are just the mechanism for passing on useful traits.

    Derision can't bring down such a brilliant observation.

    Look at his example of the normal person who mates with a fast runner -- no change in genes, the author says, but there is! He/she selected a particularly fast person to mix up with. Then there is a mutation that makes someone even faster, and they are mixed with too if speed has panache. This is all correct. And the expression of grasshopper to locust is just an expression of flexibility which has been selected for. Genes didn't "decide" to do that; the mixes that couldn't express that way are periodically weeded out.

    I think it's not so confusing or contradictory as Dobbs makes it out to be. At best its just misunderstanding but maybe he's trying to make a name for himself like, er, David to Dawkins' Goliath. I do like that he seems to accept Dawkins' memes anyway, although he calls it "gruesome" that Dawkins scored that one too. But although he admits the Selfish Gene is a powerful meme, but by "the selfish gene has become a selfish meme" he shows a misunderstanding of the concept of selfishness. All genes and memes are selfish in that they only exist if they replicate. Yes they do work in teams, rarely alone, because they tend to replicate better that way. It's a brilliant, simple idea that is so popular, for good reasons I'd add, that headlines like this catch your attention.

  • J Davis

    Guess I am too simple but I believe GOD created Adam and everything else. Then came the genes and adaptions to the environment.

  • Paul Trembath

    You seem to be trying to rebut a caricature of genetics that nobody would want to defend. Gene expression is not a mystical alternative to genes - gene expression is determined by genes. And I share 80% of my genome with a cow because we have more than 3 billion years of evolutionary history in common, and are made of almost the same parts.

  • http://wildernessvagabonds.com/ Mike Lewinski

    Epigenetics, as it describes the regulation of gene expression, seems incredibly complex. We have not only our own genome in conversation with itself, but also with the genomes of the 2000+ species of bacteria, fungi and others living in and on our bodies as part of the microbiome.

    We can and probably do have epigenetic effects on them too, turning their genes on and off in response to what we do (and especially what we eat). In turn I'm almost certain that they can and do have epigenetic effects on us.

    What a marvelous black box!

  • Jerry Adams

    What a strange article, I take the author is either looking for controversy where none exists, or has not understood or read the selfish gene the extended phenotype or unweaving the rainbow, Dawkins is quite explicit in these popular books that genes are not to be considered in isolation; 'genetic accomodation'? ....there's nothing new under the sun.

  • TheMatrixDNA

    Social genome?! Good, you are arriving next to the world view of Matrix/DNA Theory. But, still far away. It is not a genomic society that drives evolution. It is the system that contains all genomes. Like human societies, its destiny is driven by the ideology that was created by the social system, an ideology executed by the government. This ideology is the system itself, it arises from the sum of informations of all parts plus the new informations generated by internal fuzzy logics that emerges from parts interactions, which generates new informations. So, there is no individual with same ideology as the system.

    Then, all genomes obeys a more deep and invisible commander, from who comes the instructions, rules, etc. This commander is a system, beyond the social genome. The universal formula for natural systems and life's cycles, which is shown at my website, is suggesting which system, and which "ideology" is driven biological evolution at Earth. It is the source of all forces and elements interacting at Earth's surface, included cosmic radiation with their informations: it is the Milk Way. But, biological evolution is not the whole History.

    Biological evolution is merely a micro-cycle of a bigger evolution, the cosmological evolution of a unique system has is coming evolving since the Big Bang. Above this galaxy and its "ideology", there is a powerfull agent, at the level of the Universe, with its different ideology. Then, biological evolution is at the middle of a conflict between two powers, with two different goals. This powerful agent has inserted here its novelty, which we call "consciousness". Evolutionary biologists need to know the Matrix/DNA formula and knows that there seven variables acting over evolution here, not only the three variables discovered by Darwin.

  • Rick Rodstrom

    Let us do some experimenting in how the way we read something can completely change its meaning.

    Take the sentence above. But instead of starting from the 1st letter, we start with the 2nd, but still keep the same division of letters to spaces.

    etu sd os omee xperimentingi nh owt hew ayw er eads omethingc anc ompletelyc hangei tsm eaning.

    The point at which you start reading the sequence makes all the difference. So if you have a long chain of DNA, where you start to read the sequence can make enormous changes in its meaning, and subsequently in its expression.

  • Hale

    The ignorance of Dawkins full statements on the subject was baffling until I ran across the ad hominem: "these days, Dawkins makes the news so often for buffoonery, one might wonder how he became so celebrated."

    Well, there you go.

    • Agga

      Yes, there we go indeed. That does seem to be the important point to be made here. How dare the author not, as another commenter put it, "cower before" Dawkins.

  • Skeptic

    It seems like you didn't even read the selfish gene.

  • Eduardo I

    The way this article is presented is extremely stupid.
    Not one of the arguments presented counter in any way the theses promoted by Dawkings.
    Nevertheless, while the author appears as priding himself of independence with respect to the theses of one of the most respected geneticists alive, he bends down at the ones of a lesser known biologist (West-Eberard), without really understanding what she says. Or what he (Dawkings) says, for the matter.
    Funny, if it was meant to be ironic.
    Stupid if it was meant -as I suspect- to be serious.

  • BobW

    OK, I stopped after Dawkins explained it to the author and the author and West-Eberhard preferred to ignore the explanation in favor of a manufactured 'controversy'. The fact is that very little gets passed between parents and offspring except DNA. If an organism can express genes differently due to the environment, that's because the genome is constructed to allow that. Never had some many words been wasted on a non issue.

  • S

    This article is not only disrespectful of intellects that Dobbs should cower before, it is factually wrong in numerous places.
    If you want to slay giants you should do your homework better.

    A key problem is that the regulation of gene expression is conducted by, wait for it..., other genes. The selfish gene concept is alive and well, and applies to regulatory genes, genes for transcription factors etc.

    Move along folks, nothing to see here.

  • vanalex

    I think Richard Dawkins has the last word, his scholar clarity is still awe inspiring. His reply is already a classic: One can quickly and clearly appreciate the methodological thought process of a trained scientist.
    Adversarial Journalism and The Selfish Gene
    by Richard Dawkins posted on December 06, 2013 04:21PM GMT http://www.richarddawkins.net/foundation_articles/2013/12/6/adversarial-journalism-and-the-selfish-gene

  • Michael Edwards

    Great article, Mr. Dobbs! I'm a bioinformatician that does a lot of work analyzing global gene expression, and I see the connected nature of genes in all the array data I analyze. Complex processes require many changes to occur at once, and a change to one gene can't accomplish evolution on its own.

    You see the same thing in cancer: it's never just one mutation that causes cancer, but many genes that need to be disrupted. I wonder if it's possible that mutations in cancer lock in changes in gene expression that are already occurring in precancerous cells? It would make sense because we see a lot of chromosome remodeling genes mutated frequently in many types of tumors.

    I wouldn't worry too much about the negative comments. I can only image the response to this article if you would have included the searchable term "Sarah Palin".

    Again, superb article and please keep up the good work!

    • lapis

      Your lack of understanding is alarming.

      • Michael Edwards

        "A
        scientist with an open mind, who can question the present knowledge of
        science, will have more of a chance of discovering a higher truth." -Zen Master Thich Nhat Hanh

        • lapis

          What is ‘Higher truth’? Does that imply faith without
          evidence?

          The first part is the very essence of science, but that
          simple fact seem to elude you.

          • Agga

            It doesn't take a genius (though perhaps a debater who realises the importance of the principle of charity in argument) to understand that what is implied by "higher truth" here is a theory or piece of knowledge that is closer to the truth than the previous theory or piece of knowledge. The context was science, after all, not theology. Scientific inquiry is continually edging closer to "knowing" the nature of things, it is not a one step process. Indeed, the scientist who is able to cast off an outdated paradigm is at an advantage.

  • smora

    My memory goes back to a fellowship 30 years ago but there are examples of genomes that contain multiple complete copies, each optimized for a different environmental situaltion. I believe frogs contain copies of their genomes optimized for different temperatures to allow them to function over a range of environments. This was thought to be the explanation of why the frog genome is three to four times larger than the human. It seems that the evolution of euthermia might have been driven by a need for a more parsimonious genome.
    Also, many organisms have genes that expressed only under environment conditions of injury or duress, producing so called "heat shock" proteins that help in cellular recovery.
    The histone story is also one of gene regulation by environmental factors, eg, calcium influx into the nucleus that can turn on/off or modulate gene activity.
    It seems to me that these types of mechanisms might mimic the appearance of genetic accomodation. There also seems to be a "slight of hand" when everybody is running as fast as they can and "miracle of miracles" the right gene mutation pops up in the right chromosome to fix the gain in phenotype capabilties. Unless one posits that accomodating genes are, first, very preferentially predisposed to mutate in contrast to their neighbors and, second, that the mutation would be more more frequently beneficial than not (the opposite generally being the case), it would take very many generations (?hundreds? thousands) of running as fast as possible for such a propitious (and very low probability) event to occur

  • Dobbs, are you an idiot?

    Dobbs is a journalist who wants scientists to explain their work to the public, yet when a certain R. Dawkins writes 10+ books doing just that, he misunderstands and then obfuscates for his own commercial benefit. Pratt!

    http://www.richarddawkins.net/foundation_articles/2013/12/6/adversarial-journalism-and-the-selfish-gene#comment-box-1

  • Patrick MacKinnon

    Aha. I had wondered for years how an activity as complicated and universal as the bee dance could have been an evolutionary development alone. It would be necessary for the whole species to not only develop the dance as an evolutionary
    change but to at the same time understand its meaning. Gene expression explains it better.

  • klmr

    “and those changes can be passed down to offspring”

    Rarely, if ever. Epigenetics is firmly established. Trans-generational inheritance of epigenetic marks isn’t – except *maybe* in very special cases, and even there I’m highly sceptical. Even the recent paper about olfactory experience being passed down hasn’t caused universal acceptance of this.

  • Hominid

    The flimsiest of 'evidence.'