Who are you calling selfish?

There’s a bit of a fracas going on about David Dobbs’ article in Aeon on the obsolescence of the ‘selfish gene’: see here and here. In the first of these, Jerry Coyne has criticised the article as woefully misinformed; the second is Richard Dawkins’ response to it. There’s a crucial distinction here (though I’m not sure Coyne really wants to acknowledge it) between the accuracy of Dobbs’ scientific claims and the appropriateness of his objections to the selfish-gene metaphor. Steven Pinker apparently considers the problem here to be the fact that it “seems to be a congenital problem with science journalists [that] they think that it's a profound and revolutionary discovery that genes are regulated”. It might be nice if it were really that simple. But it isn’t. The real issue is whether the fact that genes are regulated (and perhaps more crucially, networked) means that “selfishness” is still an illuminating way to describe how they operate.

Take, for example, Coyne’s point that the polyphenism that Dobbs talks about – the fact that the same genes can create radically different phenotypes in a single organism – is triggered by a regulatory gene. (Coyne doesn’t say whether such a gene has yet been identified for grasshoppers or caterpillar/butterflies, but I’m happy to believe that this is indeed the probable origin of the morphological switch, regardless of whether we know the details.) In this sense, then, the transformation is certainly still under ‘genetic control’ and therefore adaptive in the same sense as any other genetic trait.

But does it mean that the regulatory gene in question – let’s call it gene A – is ‘selfish’? It’s hard to see any meaningful way in which this can be true. Coyne offers his own view of what it means: “during the process of natural selection, genes ‘act’ as if they were selfish.” In other words, it’s a metaphor. You know what, I think we got that already. We didn’t imagine it meant that genes habitually push to the front of queues and steal other genes’ wallets. What we need, though, is some notion of what he thinks “selfish” itself means in this context. That the gene plays a part in its own replication? I guess that’s what Coyne means, because later he says a selfish gene “promotes the reproduction of itself or its carrier.” But hang on – so it’s selfish if it promotes the reproduction of its carrier, meaning all those other genes too? So it’s not behaving in a way that is actually at the expense of other genes, but in fact benefits them? Like, say, the way we might play an active role in society so that it doesn’t collapse and we get shot up by looters? Sorry, so where exactly does the selfishness come in – or do you mean that the gene acts “as if with enlightened self-interest” – which, behaviourists and indeed linguists will tell you, is not the same as selfishness?

Let’s see if we can figure out which of these versions of the pathetic fallacy we’re talking about here. (I fear I might be patronising if I point out that ‘pathetic fallacy’ is not a term of abuse, as though to say that the idea of the selfish gene is pathetically fallacious, but on past experience I’ve found it’s best not to underestimate some folks’ unfamiliarity with figures of speech, particularly if they can otherwise extract offence from them.) This adaptation of gene A relies on the other genes whose expression is modified by the switch doing what they need to do in response to the signal from A. If they don’t ‘comply’, A gets no advantage. Likewise, the adaptation that enables the other genes to realise these alternative phenotypes in response to A’s signal relies on A actually giving that signal at the appropriate time. In other words, there is an intimate cooperativity required here between the way the genes operate, if any of them is to enjoy the mutual benefit.

Now, selfish geneticists might say “But A doesn’t care about those other genes, it is only working for its own benefit!” Well, they might say that, but I hope they won’t, for then they’d be showing that they have fallen for their own metaphor. Gene A doesn’t of course care about its own survival either. A gene doesn’t care about anything; it’s just a bit of a molecule. To use its ‘indifference’ to its fellow genes as an argument for why it is ‘selfish’ is absurd. You could of course say “isn’t it equally spurious to call this behaviour cooperative?” But cooperative behaviour in inanimate particles has a clear meaning in chemical physics: it means that the result depends on the collective interactions between the particles: it can’t result from the behaviour of any one of them acting alone. It doesn’t mean the particles are ‘nice’, or even that they act as if they were ‘nice’.

This sort of argument for why genes can be better regarded as cooperative than selfish is well rehearsed. It is a key aspect of the objections to the selfish-gene metaphor raised by people like Gabriel Dover, Denis Noble and Steven Rose. Noble’s argument in The Music of Life is particularly compelling, and the fact that it is seldom addressed by selfish geneticists, who prefer to imply that it’s just ignorant journalists who get this stuff wrong, is I think something of a backhanded compliment to Denis. (Let me, for the record, point out that Jerry Coyne has certainly laid into Noble in no uncertain terms – but I haven’t seen a good refutation of his specific criticisms of the selfish-gene metaphor.)

To his credit, Richard Dawkins himself does acknowledge some of this. In the 30th anniversary edition of The Selfish Gene he says, for example, “Another good alternative to The Selfish Gene would have been The Cooperative Gene.” That’s because, he says, genes sometimes act in mutually supportive gangs. “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.” The genes are, however, individually still “selfish”, Dawkins says, because they are not cooperating for the benefit of the others. But that assertion only makes sense if you ascribe intentions to the genes – in other words, if you fall for the metaphor (I guess it is for reasons like this that Steven Rose thinks Dawkins doesn’t really understand what a metaphor is). All you can say is that a mutual operation of genes works to their collective benefit. It is simply meaningless to say that in such a circumstance they are acting “as if” they are selfish, just as it is meaningless to say that they are acting “as if” they are altruistic. It is, in effect, implanting a value judgement where none is warranted. Why do that? Well, I’ll come to that shortly.

There’s a deeper level to this debate, however, which I don’t see Coyne taking on board at all. It is about causality. The argument for selfish geneism seems to be that if a gene’s activity results in a change in phenotype, the gene is responsible for it – that it is the ‘cause’. This is equivalent to the old argument that the assassination of Archduke Ferdinand caused World War I. I like to think of it another way. Suppose Howard Webb referees Chelsea vs Manchester United, and Chelsea win 1-0 (I’m going to trust US readers to make the necessary changes mutatis mutandis). Webb has obviously ‘caused’ that result, as well as all the moves that led to it, because he blew the whistle that began the game (and indeed, intervened several times during the match too). The next season Webb referees the same game, but this time Man U triumph 2-0. That’s weird, because the teams have identical players, the pitch is the same, and so on. But Webb did a few things differently this time – he awarded Man U a penalty, say – so he’s obviously the cause of the difference.

The fact is that, of course, the course and outcome of both matches relies on all the players knowing what is required of them, and doing it. There’s already other crucial information in the system. Howard Webb wasn’t the cause of any of it, except in the important sense that without him either chaos would have ensued or the matches would never have started.

If this seems like a fatuous example, or a thin analogy (and sure, best not to push it too far), take a look at Hoel et al., PNAS 110, 19790; 2013 (here). This makes it clear that there are some complex systems in which causality must be seen as a property of higher-level modes of organization, and can’t be meaningfully ascribed to a microscopic event. If that is true in genetics, then neither evo nor devo can necessarily be considered to be under the causal control of specific genes. I don’t mean that the genes don’t underlie the processes, but just that causality does not reside therein. Or to be clear (because there’s a pathological inclination for words to be twisted in some of these disputes), there are of course plenty of cases where specific adaptive phenotypes can be attributed to specific genes (and so can be considered the result of selection at the genetic level), but there’s no reason to think that this is the generic or universal picture, and plenty of reason not to. That doesn’t deny the crucial importance of genes in evo/devo, any more than one would deny the importance of individual actions and decisions in the outbreak of World War I.

One might want to say that if the selfish gene’ metaphor works for Coyne, why not let him have it – it’s only a metaphor, after all. And I’m not unsympathetic to that. But it is of course not just Coyne – this metaphor has powerfully affected the way genetics and evolution have been presented to the public. And I don’t think it is at all unlikely (nor does Gabby Dover) that it has contributed in a major way to the prevailing notion of the “one-gene one-trait” picture that now even geneticists are finding an albatross: how can genes be operating in cooperative networks if each is only looking out for itself? I’m not saying that the selfish geneticists deny that they do, only that one of the many problems with the selfish gene picture is that it implies relentless individualism.

We should probably be honest about this too: it is surely no coincidence that the most vocal adherents of the selfish gene are the same folks who are most vocally anti-religious. It’s hard not to suspect that one of the attractions of this picture is its very harshness: not only does the universe not care in the slightest about your welfare (and I agree with that) but the most fundamental principles of life are positively ‘unkind’ and antagonistic – nasty if you like – and thus as far as it’s possible to get from your fluffy divine benevolence. Can’t you sense a gleeful “take that!” in the way Richard Dawkins serves up this stuff?

I might be unfair here, but I guess I’m searching for a reason why these smart folks are so reluctant to relinquish what is demonstrably a bad metaphor. After all, as Larry Moran (who is no slouch when it comes to beating on religion, although he picks his targets – creationists and ID-ers – rather more selectively) has pointed out, the selfish gene has been largely dead for decades in evolutionary biology.

One final point, since it seems to be a common trope in cases like this for scientists to decry journalists’ ignorance of their subject’s history. Forgive me if I’m wrong, but I have never seen selfish geneticists acknowledge that or explain why their definition of ‘selfish gene’ is different from that typically used in the 1980s by leading thinkers such as Francis Crick, Leslie Orgel, Gabriel Dover, and Ford Doolittle (Nature 284, 601 & 604; 1980). Those guys used selfishness specifically to refer to that subset of genes or genetic elements that have a propensity to proliferate in multiple copies throughout the genome – it was not a property of all genes that enabled them to benefit from natural selection. Indeed, this kind of selfish DNA, said Orgel and Crick, makes no specific contribution to the phenotype. Dawkins mentioned such genetic elements in The Selfish Gene, but selfish geneticists have subsequently been quite happy to see this ‘selfishness’ become a universal attribute of genes. That is evidently not how Crick saw it: he and Orgel make the distinction with ‘business as usual’ genetic selection very explicit.

Theirs seems to be a much more viable idea of selfishness, for the multiple copies of genes don’t benefit the organism. At best this accumulation of ‘junk’ is neutral to the organism, but it is potentially detrimental in the long term, providing a good illustration of the short-termism of natural selection. In this sense, then, selfishness is not a property that enables evolution to happen, but an inevitable by-product caused by its difficulty in dealing with parasitic freeloaders (for a modern view, see J. H. Werren, PNAS 108 (supplement 2), 10863; 2011). I’d much rather see selfishness reserved for this kind of situation. And so would many others. It seems to me that Coyne does a disservice by not acknowledging that the ‘selfish’ metaphor has a long and distinguished history of being applied only in this very restrictive and particular context.

I don’t want to be unnecessarily confrontational. Coyne has done a fine and important job in the past of defending evolution against idiotic attacks, and arguably this is just a debate about the packaging of a process whose basic details are not in doubt. But it’s because I do what I do that I think that packaging is important.