I have been asked to respond to an article by David Dobbs called ‘Die, selfish gene, die’. It’s a fluent piece of writing featuring some interesting biological observations, but it’s fatally marred: infected by an all-too-common journalistic tendency, the adversarial urge to (presumably) boost circulation and harvest clicks by pretending to be controversial. You have a topic X, which you laudably want to pass on to your readers. But it’s not enough that X is interesting in its own right; you have to adversarialise it: yell that X is revolutionary, new, paradigm-shifting, dramatically overthrowing some Y.
I had almost finished writing this reply when Jerry Coyne – my goto guru on population genetics since the death of John Maynard Smith – posted his own much more thorough retort to Dobbs. I thought about abandoning my own effort, but was reluctant to throw away my more personal response to Dobbs’ traducing of my earlier work. Even if you don’t have time to read my article, however, do please read Jerry’s: http://whyevolutionistrue.wordpress.com/2013/12/05/david-dobbs-mucks-up-evolution-part-i/ This is Part 1. Part 2 has yet to appear, and I look forward to it.
The Y in Dobbs’ article is my book, The Selfish Gene, and his main X is the important but far from new point that genes are not always expressed in the same way. He calls it phenotypic plasticity. Locusts are transformed grasshoppers: same genes, differently expressed. A caterpillar and the butterfly it morphs into have exactly the same genome, expressed in different ways. An animal is the way it is, not just because of the genes it possesses but because the context in which a gene sits affects how – and indeed whether – it is expressed. Dobbs makes some sensible points about all this, but there’s not a single one of them that I wouldn’t be happy to make myself – and in most cases did make, either in The Selfish Gene itself or in my other books. But his headline conclusion, namely that recent findings negate the thesis of The Selfish Gene, is not just untrue but deeply and perversely untrue.
The Selfish Gene has a lot to say about the social insects, laying particular stress on the fact that the difference between a queen and a sterile worker is non-genetic. Indeed, it has got to be non-genetic. If a gene were unconditionally “for” sterility it couldn’t be favoured by natural selection. It has to be conditionally expressed, conditional upon the environment. The difference between a massive-jawed soldier ant and the tiny minor worker riding shotgun on its head, is nongenetic too. As far as its genes are concerned, any female ant could have become any caste of worker or a queen. Genes express themselves differently when switched, by environmental triggers, into different embryological pathways. It’s a special case of another idea that received prominence in The Selfish Gene, the “conditional strategy” concept of John Maynard Smith.
This is just an extension of a deep principle of embryonic differentiation. Muscle cell, liver cell, nerve cell . . . all contain the same genes, the diploid genotype of the organism. The differences between them arise ultimately because different genes are expressed – turned on or off by the characteristic chemical environments in the three types of cell. The Selfish Gene is a book about evolution not embryology, but these facts about embryology, known to everybody who has ever taken an elementary biology course, obviously lurk behind that book, and I discussed them explicitly in other books such as The Ancestor’s Tale (2004) and The Greatest Show on Earth (2009).
As I explained in those two books, and elsewhere, the difference between species has more to do with which genes are expressed and when, than with the repertoire of protein-encoding genes that they possess. I likened that repertoire to the “toolbox” of built-in subroutines which a computer (in those days I happened to be familiar with the Mac: my details may now be out of date) makes permanently available to programmers. Here’s how I put it in 2004:
The Mac has a toolbox of routines stored in ROM (Read Only Memory) or in System files permanently loaded at start-up time. There are thousands of these toolbox routines, each one doing a particular operation, which is likely to be needed, over and over again, in slightly different ways, in different programs. For example the toolbox routine called ObscureCursor hides the cursor from the screen until the next time the mouse is moved. Unseen to you, the Obscure- Cursor ‘gene’ is called every time you start typing and the mouse cursor vanishes. Toolbox routines lie behind the familiar features shared by all programs on the Mac (and their imitated equivalents on Windows machines): pulldown menus, scrollbars, shrinkable windows that you can drag around the screen with the mouse, and many others.
The reason all Mac programs have the same ‘look and feel’ (that very similarity famously became the subject of litigation) is precisely that all Mac programs, whether written by Apple, or by Microsoft, or by anybody else, call the same toolbox routines. If you are a programmer who wishes to move a whole region of the screen in some direction, say following a mouse drag, you would be wasting your time if you didn’t invoke the ScrollRect toolbox routine. Or if you want to place a check mark by a pulldown menu item, you would be mad to write your own code to do it. Just write a call of CheckItem into your program, and the job is done for you. If you look at the text of a Mac program, whoever wrote it, in whatever programming language and for whatever purpose, the main thing you’ll notice is that it consists largely of invocations of familiar, built-in toolbox routines. The same repertoire of routines is available to all programmers. Different programs string calls of these routines together in different combinations and sequences.
The genome, sitting in the nucleus of every cell, is the toolbox of DNA routines available for performing standard biochemical functions. The nucleus of a cell is like the ROM of a Mac. Different cells, for example liver cells, bone cells and muscle cells, string ‘calls’ of these routines together in different orders and combinations when performing particular cell functions including growing, dividing, or secreting hormones. Mouse bone cells are more similar to human bone cells than they are to mouse liver cells — they perform very similar operations and need to call the same repertoire of toolbox routines in order to do so. This is the kind of reason why all mammal genomes are approximately the same size as each other — they all need the same toolbox.
Nevertheless, mouse bone cells do behave differently from human bone cells; and this too will be reflected in different calls to the toolbox in the nucleus. The toolbox itself is not identical in mouse and man, but it might as well be identical without in principle jeopardizing the main differences between the two species. For the purpose of building mice differently from humans, what matters is differences in the calling of toolbox routines, more than differences in the tool- box routines themselves.
Does Dobbs, then, really expect me to be surprised to learn from him that:
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.
Does Dobbs really think the existence of genes controlling the expression of other genes is either a surprise to me or remotely discomfiting to the theory of the selfish gene? Genes controlling other genes are exactly the kind of genes I have in mind when I speak of “selfish genes” as the “immortal replicators”, the “units of natural selection”.
In 1982 in The Extended Phenotype I used the evolution of homosexuality as an example to stress the universal importance of differential gene expression and why we must never forget it. Here’s the relevant paragraph, but I have said the same thing in different ways in many other places.
Time and again, I have gone out of my way to emphasise the cautious hesitation with which we should adopt linguistic conventions such as “gene for . . .” some phenotypic characteristic. Time and again I have explained that there is no deterministic, one-to-one, atomistic causal relationship between a gene and an object of phenotype. These were not grudging admissions but enthusiastic emphases.
I have actually gone further than Dobbs in stressing the importance of environmental context as a modifier of gene expression. The chapter called ‘The Selfish Cooperator’ in my 1998 book Unweaving the Rainbow is devoted to the idea that a gene must not be seen in isolation, but as surrounded by an environment consisting of the other genes in the gene pool. The other genes matter because they are the genes with which it repeatedly shares bodies; they are the companions through evolutionary time, with whom it participates in the repeated shuffling deals of sexual reproduction. Thus the gene pool of a species becomes a cartel of mutually cooperative, mutually supportive genes. A gene transported into a different “climate” or “context” of other genes can have a completely different expression, and would be subject to completely different selection pressures. The Selfish Cooperator could indeed have been a good title for my original 1976 book. In the 2006 Thirtieth Anniversary Edition I mused on the way the original title had been misunderstood and continued . . .
Another good alternative to The Selfish Gene would have been The Cooperative Gene. It sounds paradoxically opposite, but a central part of the book argues for a form of cooperation among self-interested genes. This emphatically does not mean that groups of genes prosper at the expense of their members, or at the expense of other groups. Rather, each gene is seen as pursuing its own self-interested agenda against the background of the other genes in the gene pool—the set of candidates for sexual shuffling within a species. Those other genes are part of the environment in which each gene survives, in the same way as the weather, predators and prey, supporting vegetation and soil bacteria are parts of the environment. From each gene’s point of view, the ‘background’ genes are those with which it shares bodies in its journey down the generations. In the short term, that means the other members of the genome. In the long term, it means the other genes in the gene pool of the species. Natural selection therefore sees to it that gangs of mutually compatible—which is almost to say cooperating— genes are favoured in the presence of each other. At no time does this evolution of the ‘cooperative gene’ violate the fundamental principle of the selfish gene. Chapter 5 develops the idea, using the analogy of a rowing crew, and Chapter 13 takes it further.
The other main idea that Dobbs thinks is inimical to The Selfish Gene is “genetic accommodation.” It’s an interesting notion, one that I’ve often promoted under its earlier name of the Baldwin Effect. I don’t need to spell it out here because there really is no disagreement: it is wholly compatible with The Selfish Gene. That book might have been improved if I had given it prominence, as Mary Jane West-Eberhard did in her remarkably thorough and scholarly Developmental Plasticity and Evolution (2003). But the fact that I didn’t go out of my way to stress it doesn’t even begin to mean that it is incompatible with the central thesis of The Selfish Gene. I can think of no reason why Dobbs should suggest such a thing, other than a journalistic desire to fabricate controversy where none exists. Which pretty much sums up his whole article.
Afterthought. After this was written, Steven Pinker sent an email commenting on Jerry Coyne’s article on the same theme. Steve said
"Brilliant! This seems to be a congenital problem with science journalists — they think that it's a profound and revolutionary discovery that genes are regulated, not stopping to think that the alternative would consist of every cell in the body synthesizing all 21,000 proteins around the clock. Part of the blame goes to molecular biologists, who hijacked the term "gene" for protein-coding sequences, confusing everyone.”
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