Brief Candle in the Dark

by Richard Dawkins

  Keats may not have intended it literally, but the idea of nightingale song working as a drug is not totally far fetched. Consider what it is doing in nature, and what natural selection has shaped it to do. Male nightingales need to influence the behaviour of female nightingales, and of other males. Some ornithologists have thought of song as conveying information: ‘I am a male of the species Luscinia megarhynchos, in breeding condition, with a territory, hormonally primed to mate and build a nest.’ Yes, the song does contain that information, in the sense that a female who acted on the assumption that it was true could benefit thereby. But another way to look at it has always seemed to me more vivid. The song is not informing the female but manipulating her. It is not so much changing what the female knows as directly changing the internal physiological state of her brain. It is acting like a drug.

  There is experimental evidence from measuring the hormone levels of female doves and canaries, as well as their behaviour, that the sexual state of females is directly influenced by the vocalisations of males, the effects being integrated over a period of days. The sounds from a male canary flood through the female’s ears into her brain where they have an effect that is indistinguishable from one that an experimenter can procure with a hypodermic syringe. The male’s ‘drug’ enters the female through the portals of her ears rather than through a hypodermic, but this difference does not seem particularly telling.

  In my more grandiose moments I dreamed of encompassing the whole field of animal communication in extended phenotypic action at a distance. In theory,

  genetic action at a distance could include almost all interactions between individuals of the same or different species. The living world can be seen as a network of interlocking fields of replicator power.

  Unfortunately, it is still

  hard for me to imagine the kind of mathematics that the understanding of the details will eventually demand. I have a dim vision of phenotypic characters in an evolutionary space being tugged in different directions by replicators under selection.

  And it is still true that

  I have not the wings to fly in mathematical spaces. There must be a verbal message . . . Most serious field biologists now subscribe to the theorem, largely due to Hamilton, that animals are expected to behave as if maximising the survival chances of all the genes inside them. I have amended this to a new central theorem of the extended phenotype: An animal’s behaviour tends to maximise the survival of the genes ‘for’ that behaviour, whether or not those genes happen to be in the body of the particular animal performing the behaviour. The two theorems would amount to the same thing if animal phenotypes were always under the unadulterated control of their own genotypes and uninfluenced by the genes of other organisms.

  Rediscovering the organism: passengers and stowaways

  What, then, of the organism as vehicle? There may be planets out there with life forms whose replicators (I conjecture that there must be replicators at the root, wherever life might be found) have no bounded vehicles; planets where the whole biosphere is a crisscrossing web of extended phenotypic influences radiating out from unbounded replicators. But on our planet it isn’t like that. Organisms, discrete units shared by lots of cooperating replicators, dominate. Almost all replicators, instead of being free, ride together inside massive vehicles – ‘swarm inside great lumbering robots, sealed off from the outside world’, as I put it in a controversially much quoted passage of The Selfish Gene. Why do our genes swarm together and work together to one end? Whence the organism?

  In The Extended Phenotype I conjured a thought experiment with two hypothetical seaweeds, renamed in the second edition of The Selfish Gene as ‘Splurgeweed’ (which simply grows at its margins and then fragments vegetatively) and ‘Bottlewrack’ (whose genes, unlike those of Splurgeweed, are funnelled down to a single-celled propagule, a genetic bottleneck in every generation). Rather than repeating the argument here I’ll go straight to the more practical conclusion which, in a sense, flows naturally from the very idea of the extended phenotype. The genes in a discretely ‘vehicular’ organism work together to a common end because they all share the same (‘bottleneck’) exit route to the future – the sperms or eggs of the organism that they share. If some genes have a different exit route, for instance getting sneezed out of the present organism instead of ejaculated, they don’t cooperate and we use a name like ‘virus’. The coherent unity of the organism depends on the fact that its genes share an exit route and hence share their expectations, even ‘hopes’, of the future.

  Fluke genes and snail genes favour different optima for snail-shell thickness. Snail genes are more ‘interested’ in snail reproduction and fluke genes more ‘interested’ in snail survival. Fluke genes would ‘agree with’ snail genes only if their reproductive propagules made the journey to the next generation in the sperms or eggs of their shared snail. If a bacterium had no other way to reach the future than to enter its host’s eggs and hence the bodies of only its host’s offspring, its genes and the host’s genes would be subject to near-identical selection pressures. Both would ‘want’ not only that the host should survive but also that she should build a nest, attract a mate, ward off egg-stealers, feed the young, even care for grandchildren. Such a parasite would cease to deserve the name. Its genes would evolve to become so intimately wedded to those of the host that its identity would merge into that of the host, with only a Cheshire Cat grin left behind to betray its parasitic origin. Mitochondria (those vital little energy-releasing bodies that swarm inside all our cells) started out as bacterial stowaways, but they became proper passengers because they came to share an exit route – the vehicle’s eggs – with all the other genes of the cooperative. So subtle was the Cheshire grin of the mitochondria (the image is borrowed from my sometime Oxford colleague Professor David C. Smith) that we’ve only just noticed that they originated as bacteria. The reason they cooperate with us rather than fight us is that they share not only the big vehicles that we call bodies (many virulent parasites do that) but also – crucially – the mini-vehicles, eggs, which, in this hypothetical case, transport them from body to body. The surreal-sounding conclusion, which follows from the logic of the extended phenotype, is that all our genes, all our ‘own’ genes, all our own genes, can be thought of as a gigantic colony of viruses: amicable viruses, distinguished from the malevolent ones only by the fact that their expected route to the future is to be not sneezed out, not coughed or breathed or excreted out, but pumped out through the ‘legitimate’ conduit of sperms or eggs directly into the offspring of the present host.

  Our ‘own’ genes, ‘amicable viruses’, can be thought of as paid-up passengers in the vehicle, as opposed to ‘stowaways’ like the chickenpox virus or the various flu viruses. At its deepest level, the difference between the two lies in their exit route from the vehicle. This is perhaps the main message of The Extended Phenotype, and it would be my Exhibit A at the pearly court of St Peter. It’s nearly obvious when you think it through, but I don’t think anybody else ever put it in this way.

  Aftermaths to The Extended Phenotype

  Three aftermaths to The Extended Phenotype have given me particular pleasure. The first, in 1999, was the marvellously insightful afterword to a new paperback printing, written by the distinguished philosopher of science (and first Simonyi Lecturer, also in 1999) Daniel Dennett. The second was a special issue of the journal Biology and Philosophy devoted to a critically retrospective look at the first twenty years of The Extended Phenotype. And the third was a conference near Copenhagen organized by David Hughes, convened to review the successes and failures of the idea of the extended phenotype.

  Dan Dennett’s afterword to the 1999 reprinting gave me especial joy because here was a philosopher arguing the case for The Extended Phenotype as a work of philosophy. I confess to a certain exasperation when I read people bending over backwards to be complimentary about my science, as a prelude to saying that I should stick to science and not stray into the terr
itory of philosophy. But what is the territory of philosophy other than clear and logical thinking? Don’t scientists have to think clearly and logically too? It is of course true that a professional biologist is typically not as well read in the philosophers of the past as he would be if his degree were in philosophy. This might make him neglect an apposite citation of Hume, Locke or Wittgenstein. But that doesn’t, of itself, mean he can’t present a clear and logical argument of a philosophical character. I hope I won’t sound too defensive, therefore, if I quote Dennett on the subject:

  Why is a philosopher writing an Afterword for this book? Is The Extended Phenotype science or philosophy? It is both; it is science, certainly, but it is also what philosophy should be, and only intermittently is: A scrupulously reasoned argument that opens our eyes to a new perspective, clarifying what had been murky and ill-understood, and giving us a new way of thinking about topics we thought we already understood. As Richard Dawkins says at the outset, ‘The extended phenotype may not constitute a testable hypothesis in itself, but it so far changes the way we see animals and plants that it may cause us to think of testable hypotheses that we would otherwise never have dreamed of.’ And what is this new way of thinking? It is not just the ‘gene’s-eye point of view’ made famous in Dawkins’s 1976 book, The Selfish Gene. Building here on that foundation, he shows how our traditional way of thinking about organisms should be replaced by a richer version in which the boundary between organism and environment first dissolves and then gets partially rebuilt on a deeper foundation . . .

  For the professional philosopher, I cannot resist adding, there is a feast: some of the most masterful, sustained chains of reasoning I have ever encountered . . .

  Forgive the self-indulgence in my quoting that last sentence. I am, perhaps oversensitively, trying to redress the balance after being described as philosophically naive. Dennett develops his theme, illustrating it with page citations from the book. His examples include some of my thought experiments, and this is especially interesting as he himself is a pre-eminent master of the thought experiment as an ‘intuition pump’.

  Continuing the theme of The Extended Phenotype as a work of philosophy, in 2002 the Australian philosopher Kim Sterelny, editor of Biology and Philosophy, decided to mark the twentieth anniversary of the book with a special issue of that interdisciplinary journal. In the event, owing to various delays, the commemorative issue didn’t finally come out until 2004, but that didn’t matter. Sterelny commissioned three scholars, Kevin Laland, J. Scott Turner and Eva Jablonka, each to write a retrospective evaluation and critique of the book, to be followed by a detailed response from me. We all four accepted the invitation, and I must say I enjoyed reading the papers and writing my response more than I expected to.

  The title of my reply was ‘Extended phenotype – but not too extended’. ‘Not too extended’ is a phrase I had used before, in response to audience questions about human artefacts. ‘If a weaver bird’s nest is an extended phenotype, would you say the same of the Sydney Opera House or the Chrysler Building?’ No I wouldn’t, and the answer is more interesting than the question. A bird’s nest or a caddis house or a mud-dauber’s set of pipes is a product of natural selection. Natural selection chose genes that fostered good building behaviour. Ancestral weaver birds varied in their building styles and skills; some of that variation was genetic, and was favoured or disfavoured by virtue of the success or failure of the resulting nests in protecting eggs and nestlings containing the genes concerned. In order for man-made buildings to qualify as extended phenotypes, it would be necessary for variation among buildings to be caused by variation in architects’ genes. We can’t absolutely rule that out but, to put it mildly, it doesn’t strike me as a promising line of research. It wouldn’t surprise me to find genetic variance in architectural talent. If one identical twin were good at three-dimensional visualization, I would expect that his twin would be too. But I’d be very surprised to find genes for gothic arches, postmodern finials or neo-classical architraves, whereas I would expect to find their equivalents in caddis larvae, mud-daubing wasps or dam-building beavers.

  The extension to human architects was not the only ‘too extended’ that I had in mind in the title of my Biology and Philosophy paper. My main problem there was with a voguish (and rather tiresome) notion called ‘niche construction’. A big example shows how this loose and vague idea confuses people. The free oxygen in our atmosphere is entirely put there by plants (including photosynthetic bacteria). Early in life’s history there was no free oxygen. The green bacteria (and later plants) who put it there massively changed the niches of all subsequent life forms, including themselves. Most creatures today would die instantly without oxygen. That was niche changing, an incidental, not ‘constructed’, by-product of photosynthetic activity. Photosynthesis was naturally selected because of its immediate nutritional benefits for the green bacteria themselves. It was not naturally selected because of its effects on the atmosphere. Those green bacteria made oxygen not because they or their descendants or anyone else would benefit from breathing oxygen in the future. They made oxygen as a by-product, because they couldn’t help it when photosynthesizing. After the oxygen was made, subsequent natural selection favoured those bacteria and other creatures capable of flourishing in oxygen. The niche was inadvertently changed, and everybody subsequently evolved to cope with what was at first a pollutant.

  Natural selection implies a discriminating genetic advantage to the organism concerned, as opposed to general advantage to the world at large. When positive advantage accrues, meaning genetic advantage specifically for the individual doing it as opposed to the world at large, we have an extended phenotype. Otherwise we have no extended phenotype and no niche construction, merely niche changing.

  A true extended phenotype, such as a bird’s nest or a beaver dam or the subverted parental behaviour of a cuckoo’s foster parent, has to be a Darwinian adaptation for the benefit of the genes that mediate it. ‘Niche construction’ is a phrase that can be meaningful if used with care. Since it is so often used without care and without full Darwinian understanding, it is a phrase that I would prefer to see not used. When it is used properly and with care, it becomes a special case of an extended phenotype, the special case where an animal changes its niche for the benefit of its own genes. A beaver dam is an example. There may not be many others.

  The same confusion, between the extended phenotype and niche construction improperly used as a synonym for niche changing, was somewhat in evidence at the third of my ‘aftermaths’: a conference on extended phenotypes convened in 2008 in a large country house near Copenhagen. The organizer was David Hughes, a talented young Irish biologist now working in America, and he attracted a splendid cast list of distinguished scientists, including both critics and supporters of the extended phenotype. There’s a good report on the conference in the journal Science Daily, with the title ‘European evolutionary biologists rally behind Richard Dawkins’ extended phenotype’.1 The description ‘European’, by the way, was belied by the presence of American scientists including the distinguished geneticist Marc Feldman (one of the critics).

  David Hughes is now the world’s leading exponent in practice of the theoretical idea of the extended phenotype. He would be the ideal first director of the hypothetical ‘Extended Phenotypics Institute’ of the future, the fantasy pipe-dream I described as the climax to my Biology and Philosophy paper:

  After the formal unveiling by a Nobel Prizewinning scientist (Royalty wasn’t considered good enough) the guests are shown wonderingly around the new building. There are three wings: the Zoological Artefact Museum (ZAM), the laboratory of Parasite Extended Genetics (PEG) and the Centre for Action at a Distance (CAD) . . . In all three wings, familiar phenomena are studied from an unfamiliar perspective: different angles on a Necker cube. [The scientists in all three wings pride themselves] on the disciplined rigour of their theory.2 The motto carved over the main door of their Institute is a one-locus
mutation of St Paul: ‘But the greatest of these is clarity.’

  It would now be necessary to add a Medical Wing to my fantasy Institute. The American biologist Paul Ewald is one of today’s leaders, along with Randolph Nesse3 and David Haig, of the burgeoning field of Darwinian medicine. I’m grateful to that inspired pioneer Robert Trivers for calling my attention to a fascinating paper by Paul and Holly Ewald on a Darwinian approach to cancer which makes use of the idea of the extended phenotype. It is well understood that the cells within a tumour are subject to natural selection within the tumour. But it’s time-limited rather than open-ended natural selection: mutant cells that become ‘better’ (better at being cancerous, emphatically not better for the patient) outcompete less malignant cells within the tumour, becoming more numerous in the tumour. But that evolutionary process terminates with the death of the patient. And there exists a parallel, but more long-term (because transgenerational) selection of genes in the rest of the body, to resist cancers, erect barriers against them, develop immunological tricks against them and so on. It’s an asymmetric arms race, because the anti-cancer tricks have been honed against cancers of many past generations. The tricks of the tumours themselves have to be evolved afresh in each generation, for they begin their malign evolution anew in each body, starting as normal, healthy cells which then are naturally selected to evolve, step by step, the qualities needed to outcompete other cancer cells in the race to multiply.

  The idea of an arms race between bodies and their cancers prompts interesting thoughts. Cancers are parasites, and particularly insidious ones because their cells are almost (but importantly not quite) identical to their hosts’. This makes them harder for the body (and for medical therapies) to discriminate against than ‘foreign’ parasites like tapeworms or bacteria. Over many generations, and many tussles against successive cancers, ‘skills’ for recognizing suspected cancer cells are honed. As in any such arms race, a balance must be struck between being too risk-averse (seeing danger where none exists) and too ‘laid back’ (failing to see danger where it really exists). This is analogous to the dilemma of a grazing antelope who sees a rustle in the long grass and has to decide whether it is a predator or just the wind. The jumpy antelope who reacts fearfully to every rustle ends each day undernourished because it kept interrupting its grazing to flee. The laid-back antelope who carries on grazing where others would flee is at risk of ending up in a leopard’s stomach. Natural selection of antelope genes settles on a judicious balance between the risk-averse Scylla and the laid-back Charybdis. The immune system walks the same tightrope in detecting malignant cells. Too laid-back and the patient dies of cancer. Too ‘jumpy’, too risk-averse, and the immune system attacks harmless normal cells, wrongly ‘suspecting’ them of being cancerous. Well, can you think of a better explanation for auto-immune diseases like alopecia, psoriasis or eczema? Allergies too, of course, can be understood as risk-averse, ‘trigger-happy’ over-reaction of the immune system.