Richard Dawkins - 2004 - Extended Phenotype

Biology and Philosophy 19: 377–396, 2004. © 2004 Kluwer Academic Publishers. Printed in the Netherlands. Extended Phenotype – But Not Too Extended. A Reply to Laland, Turner and Jablonka RICHARD DAWKINS University Museum of Natural History, University of Oxford, UK I am grateful to the three commentators for their thoughtful and penetrating remarks, and to the Editor for commissioning them. All three have forced me to think, re-opening neural pathways that had suffered neglect as I turned to other things in the years since The Extended Phenotype (henceforth EP) was published. Their essays raise so many interesting points, it would take another book to reply to them properly. Instead, on the basis that it is better to say a few things thoroughly than lots sketchily, I shall concentrate on what I take to be each author’s central argument. J. Scott Turner and Kevin Laland both, in their different ways, want to go further than me in extending the phenotype. Or so they see it. I am not so sure that further is the right word. Progress implies movement in a useful direction, whereas their extensions – of the organism, and into niche creation – occasionally reminded me of Stephen Leacock’s knight who jumped on his horse and galloped off in all directions. I don’t intend that flippantly or disrespectfully. The relevant point about the extended phenotype is that it is a disciplined extension. There are lots of other tempting ‘extensions’, which sound similar but take us off in misleading directions. I have always fought shy of misapplying the phrase to a profligate range of apparently plausible extensions. To take a more extreme example than these commentators consider, when I am asked by lay people (as I frequently am) whether buildings count as extended phenotypes, I answer no, on the grounds that the success or failure of buildings does not affect the frequency of architects’ genes in the gene pool. Extended phenotypes are worthy of the name only if they are candidate adaptations for the benefit of alleles responsible for variations in them. I might admit the theoretical possibility of generalising to other kinds of replicators such as memes (or something ‘epigenetic’ that Eva Jablonka might be able to explain but I wouldn’t), in which case my ‘no’ answer might be softened. But it is enough of a problem already, getting my more hard-headed scientific colleagues to accept the extended phenotype, without arousing their active hostility by mentioning memes (which many see as simplistic) or ‘epigenetic 378 inheritance systems’ (which some might write off as obscurantist). I shall return to the important point, which I enthusiastically accept, that replicators do not have to be made of DNA in order for the logic of Darwinism to work. Laland speaks, I suspect, for all three authors when he espouses cyclical causation. He quotes me as saying There are causal arrows leading from genes to body. But there is no causal arrow leading from body to genes. Laland, who disagrees, generously wants to absolve me from responsibility for this, saying that he is quoting out of context. But I am happy to stand by it. ‘Cyclical causation’ leaves me cold. I must, however, make very clear that I mean causation statistically. Experimentally induced changes in bodies are never correlated with changes in genes, but changes in genes (muta- tions) are sometimes correlated with changes in bodies (and all evolution is the consequence). Of course most mutations occur naturally rather than experimentally, but (because corrrelation can’t establish causation) I need to focus on ‘experimentally induced’ in order to pin down the direction of the causal arrow. It is in this statistical sense that development’s arrow goes only one way. Attempts to argue for a reverse arrow recur through the history of biology, and always fail except in unimportant special-pleading senses. Sterelny, Smith and Dickerson (1996), follow Griffiths and Gray in saying “Most acorns rot, so acorn genomes correlate better with rotting than with growth”. But this is dead wrong. It misunderstands the very meaning of correlation which is, after all, a statistical technical term. Admitting that most genomes rot, the relevant question is whether such variation as there may be in acorn genomes correlates with such variation as there may be in tendency to rot. It probably does, but that isn’t the point. The point is that the question of covariance is the right question to ask. Sterelny and Kitcher (1988) in their excellent paper on ‘The Return of the Gene’ are very clear on the matter. Think variation. Variation, variation, variation. Heritable variation; covariation between phenotype as dependent variable, and putative replicator as independent variable. This has been my leitmotif as I read all three commentators, and it will be my refrain throughout my reply. Laland’s main contribution to our debate is ‘niche construction’. The problem I have with niche construction is that it confuses two very different impacts that organisms might have on their environments. As Sterelny (2000) put it, Some of these impacts are mere effects; they are byproducts of the organisms’s way of life. But sometimes we should see the impact of organism on environment as the organism engineering its own environ- ment: the environment is altered in ways that are adaptive for the engineering organism. 379 Niche construction is a suitable name only for the second of these two (and it is a special case of the extended phenotype). There is a temptation, which I regard as little short of pernicious, to invoke it for the first (byproducts) as well. Let’s call the first type by the more neutral term, ‘niche changing’, with none of the adaptive implications of niche construction or – for that matter – of the extended phenotype. A beaver dam, and the lake it creates, are true extended phenotypes insofar as they are adaptations for the benefit of replicators (presumably alleles but conceivably something else) that statistically have a causal influence on their construction. What crucially matters (here’s the leitmotif again) is that variations in replicators have a causal link to variations in dams such that, over generations, replicators associated with good dams survive in the replicator pool at the expense of rival replicators associated with bad dams. Note what a stringent requirement this is. Although it is not necessary that we should already have evidence for the replicator-phenotype covariance, extended phenotype language commits us to a can only have come about through replicator-phenotype covariance. The beaver’s dam is as much an adaptation as the beaver’s tail. In neither case have we done the necessary research to show that it results from gene selection. In both, we have strong plausibility grounds to think it is. The same is not true – would not even be claimed by Laland and his colleagues – of most of their proposed examples of niche construction. See how different is the ‘pernicious’ sense of niche construction, the byproduct that I’d prefer to sideline as ‘niche changing’. Here, the dam alters the environment of the future, in some way that impinges on the life and wellbeing of beavers in general, and probably others too. Not particularly the welfare of the beavers that built the dam, not even of their children or grandchildren. The dam is good for beaverdom, and more. Beavers, frogs, fishes and marsh marigolds all benefit from a beaver-induced flooding of their niche. This is too loose and vague to count as a true extended phenotype, or as true niche construction. The deciding question is ‘Who benefits?’ And the reason it matters is that we have a Darwinian explanation of the dam only if dam-friendly alleles of the dam builders themselves benefit at the expense of alternative alleles. I have no wish to downplay the importance of niche changing. It is a fair description of many important biological events, ranging from the irreversible oxygenation of Earth’s early atmosphere by green bacteria and now by plants, to the greening of deserts by ecological successions of plants climaxing in dense forest communities, and including Scott Turner’s heuweltjies (a fascinating example, of which I had been ignorant). 380 Most biologists would accept that the beaver dam is an evolved adaptation for the benefit of the genes of the responsible beaver. It would be a bold scientist (James Lovelock, perhaps) who would suggest that the oxygenation of the atmosphere by plants is an adaptation for the benefit of something. The oxygenation of the atmosphere is a hugely important niche change, and woe betide any creature, including any plant, that fails to adapt to it. But the presence of oxygen is nobody’s adaptation (or at least, you’ll have your work cut out if you want to argue that it is). It is a byproduct of plant biochemistry to which all living creatures, plants included, must adapt. Beaver dams may or may not benefit other beavers, or fishes or water beetles or pondweeds, but such diffuse and unfocused benefits cannot explain why they are there. The only benefits that can be adduced in Darwinian explanation of dams are benefits to the alleles (or other responsible replicators) of the particular beavers that build them. Otherwise, natural selection could not have shaped their evolution. Long-term consequences of niche changing are interesting and important, but they do not provide a Darwinian explanation for why animals change their niches. Laland pays some lip service to this point when he speaks of ecological inheritance, and says that it resembles the inheritance of territory or property. Local exclusiveness is indeed a vital ingredient of true niche construction. As long as beavers have a high chance passing their lake on to their own grandchildren rather than to somebody else’s grandchildren, there is at least a chance of making a workable Darwinian model of niche construction. But the rhetoric of niche construction neglects to follow the lip service, and we are left believing it to be a larger and a grander theory than it really is. Those aspects of niche construction theory that work are already included within extended phenotype theory. Those aspects that don’t fit within existing extended phenotype theory don’t work. Don’t work as Darwinian adaptations, that is. They can still be interesting in other ways. Earthworms are mentioned by both Laland and Turner, and Laland’s splendid ‘accessory kidneys’ are a gift to Turner and his ‘extended organism’. Earthworms radically change the environment in which they, and all other soil organisms including – significantly – rival earthworms live. Again, we certainly have niche alteration but, please, not niche construction until a lot more work has been done to establish this onerous claim. Ecological succession is a form of niche changing – not niche construc- tion – which follows a repeatable, regular pattern. A desert is colonised by weeds, which then change conditions sufficiently to allow the subsequent invasion by an orderly succession of plants and animals, each wave altering niches in ways that favour the next wave, culminating in a climax forest. But, important and repeatable as ecological succession is, it is not a Darwinian 381 adaptation on the part of prior member of the succession on behalf of later members. Rather, natural selection within the gene pools of later members of the succession favours those individuals that take advantage of the conditions inadvertently set up by earlier members. The climax forest is a consequence of colonisation by weeds decades or even centuries earlier. The forest is not an extended phenotype of the weeds’ genes, nor is it helpful or illuminating to call it a niche constructed by the weeds. The same can be said of the repeatably regular pattern of development of coral reefs, in which generations of polyps build literally on the environment provided by centuries of dead predecessors, and form the foundation – literally and metaphorically – for the marine equivalent of a climax forest community. Moving on from ecological succession to longer-term processes that look a bit like niche construction, coevolutionary arms races are the outstanding example (Dawkins and Krebs 1979). Predators impose new selection pres- sures on prey, which respond in evolutionary time such that future generations of prey impose changed selection pressures on future generations of pred- ators. The coevolutionary positive feedback spirals that result are responsible for the most advanced and stunning illusions of design that the natural world has to offer. Again this is a case of animals changing future niches, and changing them in fascinating ways, but again it isn’t niche construction, and no helpful purpose is served by lumping it with beaver dams or ecological succession. Understanding requires us to respect clear distinctions. I don’t denigrate niche changing as an important biological phenomenon. But it is not the same thing as true niche construction. Nothing but confusion will result from treating one as a continuation of the other. Since this seems to be a misunderstanding that is eagerly waiting to happen, niche construction is a phrase that should be abandoned forthwith. That’s all I want to say about niche construction. Now, the extended organism, which is J Scott Turner’s main contribution to our debate. Turner, like Laland, is aware of the distinction between benefit to the agents respon- sible for a phenotype, and benefit to the world at large. But, as with Laland, his enthusiasm is in danger of misleading others into forgetting the distinction. Turner, like Jablonka as we shall see, thinks I am too much of a genetic triumphalist. For the moment I shall leave that on one side while I focus on the wonderful examples of would-be extended organisms that Turner offers us from his own work on termites. Yes, the Macrotermes nest, with its underground living and brooding chambers and its overground ventila- tion apparatus, has many of the attributes of an organism. And yes, it is an intriguing conceit that the fungi are cultivating the termites, rather 382 than the other way around. Indeed, I said something pretty similar about cellulose-digesting gut microbes in EP (p. 208): Could the evolution of eusociality in the Isoptera be explained as an adaptation of the microscopic symbionts rather than of the termites themselves? Once again, note that the extended phenotype is a disciplined hypothesis. Speculative as my suggestion was, it was a very specific and tightly limited speculation. Implicitly it postulated alleles in microorganisms (or fungi to take in Turner’s hypothesis) which vary in their effects upon termite social behaviour (or mounds). The fact that there is no actual evidence for either speculation need not worry us at this stage. The point is to be precise about the genetic nature of the speculation. Adaptive hypotheses, however wild and speculative, must not be vaguely Panglossian but precisely limited to specified alleles (or other replicators) which vary and which exert a causal influence on variation in the phenotype of interest. Let’s apply these rigorous standards to the hypothesis that a termite mound is an extended organism. We shall conclude in favour, but it is important to make the case properly, in what I have called a disciplined manner. We shall take for granted the physiological, homeostatic and thermodynamic arguments put by Turner – not because they are unimportant but because he has made them so well. Instead, we concentrate on the genetics (using genes to stand for other conceivable replicators). Mound morphology is sure to be influenced by a number of genes, acting via mound embryology which, in the terms of our discussion, is another name for termite behaviour. These genes are to be found in the cells of many different organisms (using ‘organism’ in the conventional, non-extended sense). They include genes in the cell nuclei of numerous individual worker termites. They also might include genes in fungi, genes in gut symbionts, and genes in mitochondria or other cytoplasmic elements in the cells of termites, fungi or gut symbionts. So, we potentially have a rich pandemonium of genetic inputs to our mound phenotype, coming at it from as many as three kingdoms. For my money, the analogy of mound with organism stands up well. The fact that we have a heterogeneously sourced genetic input to the embry- ology of the phenotype doesn’t matter. Lots of genes affect each aspect of my bodily phenotype, including, for all I know, mitochondrial genes. My ‘own’ nuclear genes tug me in more or less different directions, and my phenotype is some sort of quantitative polygenic compromise. So that is not a difference that might stop the mound being an organism. What, then, is the prime characteristic of an organism? It is that, at least to a quantitatively appreciable extent, all its genes are passed on to the next generation together, in a small ‘bottlenecked’ propagule. The rationale for this is given in EP, 383 especially Chapter 12, ‘Host phenotypes of parasite genes’ and Chapter 14, ‘Rediscovering the Organism’, and I shall not repeat it here. Instead, let’s go straight to the termite mound to see how well it holds up. Pretty well. Each new nest is founded by a single queen (or king and queen) who then, with a lot of luck, produces a colony of workers who build the mound. The founding genetic injection is, by the standards of a million-strong termite colony, an impressively small bottleneck. The same is, at least quantitatively, true of the gut symbionts with which all termites in the new nest are infected by anal licking, ultimately from the queen – the bottleneck. And the same is quantitatively true of the fungus, which is carefully transported, as a small inoculum, by the founding queen from her natal nest. All the genes that pass from a parent mound to a daughter mound do so in a small, shared package. By the bottleneck criterion, the termite mound passes muster as an extended organism, even though it is the phenotype of a teeming mass of genes sitting in many thousands of workers. I won’t miss an opportunity to emphasise (though again I shall not repeat the full argument from EP) that every organism (conventionally defined) is already a symbiotically cooperating union of its ‘own’ genes. What draws them, in a Darwinian sense, to cooperate is again ‘bottlenecking’: a shared statistical expectation of the future. This shared expectation follows directly from the method of reproduction, according to which all of an organism’s ‘own’ nuclear genes, and its cytoplasmic genes for good measure, pass to the next generation in a shared propagule. To the extent that this is true of parasite genes (for example bacteria that travel inside the host’s egg), to that very same extent aggressive parasitism will give way in evolutionary time to amicable and cooperative symbiosis. The parasite genes and the host genes see eye to eye on what is an optimum host phenotype. Both ‘want’ a host phenotype that survives and reproduces. But to the extent that parasite genes pass to their own next generation via some sideways route which is not shared with those of the host genes, to that same extent the parasite will tend to be vicious and dangerous. In such cases, the optimum phenotype from the parasite genes’ point of view may well be dead – perhaps having burst in a cloud parasite spores. All our ‘own’ genes are mutually parasitic, but they are amicably cooperative parasites because their shared route to the future in every generation leads them to ‘see eye to eye’ on the optimal phenotype. A termite mound, then, is a good extended organism. A heuweltjie, by my reading of Turner’s description, is not. It is more like a forest or a coral reef. The genes that contribute to the putative heuweltjie phenotype