The original twist added by the Ewalds to this analysis is the importation of the idea of the extended phenotype. The tumour lives and evolves in a micro-environment provided by the surrounding cells of the body. The improved malignant tricks that tumour cells evolve in their within-body natural selection largely consist of manipulations of the micro-environment. For example, tumour cells, no less than other cells – indeed, probably more – need a good blood supply to feed and oxygenate them. Just as a beaver’s genes work on beaver behaviour to construct the extended phenotype which dams a stream to make a lake, so the mutated and evolving genes in a tumour construct an extended phenotype which is an improved blood supply to the tumour. The cells of the enlarged or diverted blood vessels are not cancerous. They are manipulated by the cancer cells and, since this is a true Darwinian adaptation (for the benefit of the cancer, not the body), the changes in the blood supply constitute a true extended phenotype of mutated genes in the tumour. The Ewalds make full use of ‘extended phenotype’ terminology in their paper, and I am delighted that they regard the idea as helpful.
Constraints on perfection
In 1979, John Maynard Smith organized a conference at the Royal Society on ‘The evolution of adaptation by natural selection’. John Krebs and I were each invited to give talks, and we decided to pool our efforts and write a joint one, on the subject of ‘evolutionary arms races’. We already knew we could work well together because of our 1978 paper on ‘Animal signals: information or manipulation?’ (see page 328). I count John as an intellectual brother, although we see too little of each other nowadays. We have always laughed at the same absurdities without the need for explanation. When unpacking his effects as he moved back into the Oxford Zoology Department after a spell abroad, he came upon a useful item that made him think of me: ‘Richard, if you should ever have need of a false beard . . .’ Was he being prophetic? The day may yet come. As with my sister Sarah, I can count on John’s past to include the same funny books and poems as my own: we effortlessly take each other’s allusions. Though a little younger than me, he rightly won his FRS long before I did. Unlike me, he can cope with university politics and civil service administration, and combine them with doing excellent science. He became the knighted head of the British Food Standards Agency and is now a member of the House of Lords and the Head of Jesus, a beautiful old Oxford college.
The opening paragraph of our arms race paper, as delivered at the Royal Society conference in 1979, set the scene:
Foxes and rabbits race against each other in two senses. When an individual fox chases an individual rabbit the race occurs on the time scale of behaviour. It is an individual race, like that between a particular submarine and the ship it is trying to sink. But there is another kind of race, on a different time scale. Submarine designers learn from earlier failures. As technology progresses, later submarines are better equipped to detect and sink ships, and later-designed ships are better equipped to resist. This is an ‘arms race’, and it occurs over a historical time scale. Similarly, over the evolutionary time scale the fox lineage may evolve improved adaptations for catching rabbits, and the rabbit lineage improved adaptations for escaping.
We arranged our examples according to a four-way distinction between inter- versus intra-specific arms races (e.g. predator/prey versus male/male rivalry) and between symmetric versus asymmetric arms races (e.g. male/male rivalry versus parent/offspring conflict). We considered how arms races end, whether in ‘victory’ for one side or in some kind of equilibrium. Inspired by an Aesop fable, we coined the ‘Life/Dinner Principle’ as a way for an arms race to end in ‘victory’: the rabbit runs faster than the fox because the rabbit is running for his life, while the fox is only running for his dinner. There is an asymmetry in the cost of failure on the two sides of the arms race. The asymmetry shows itself in economic terms. Both rabbit and fox would run like a Maserati if they could, but the machinery for running fast is costly. It has to be paid for out of other parts of the body’s economy. The life/dinner asymmetry gives the rabbit an added inducement to divert precious resources into running speed.
A similar asymmetry arises in the ‘Rare Enemy Effect’. Every one of the cuckoo’s ancestors must have succeeded in fooling a foster parent, whereas the foster parent can look back on many ancestors that never encountered a cuckoo in their lives. The cost of failure is higher for the cuckoo than the host, so cuckoos, whose ancestors survived the more stringent side of the arms race, are better equipped to survive future encounters. The arms race idea has proved immensely fruitful and has pervaded many of my books. My friend the Cambridge zoologist N. B. Davies, who could fairly be seen as co-founder with John Krebs of the modern version of behavioural ecology, makes inspired use of the arms race idea in his classic field work on cuckoos.1
Perhaps the most overrated paper in my field, if not in all of biology, originated at the same Royal Society conference: S. J. Gould and R. C. Lewontin’s 1979 ‘Critique of the adaptationist programme’. Lewontin and Gould were alpha males in the field, powerful ringleaders of the 1970s campaign (see page 96) against Edward O. Wilson (who, fortunately, was well able to look after himself). And the bullying tone continued at the 1979 Royal Society conference. Lewontin wasn’t there, so Gould gave the lecture and was at his sneering best, playing for the horse laugh from the back row, and mysteriously ignoring the fact that his central thesis had been comprehensively undermined, earlier in the day, by the thoughtful and thorough presentation of Tim Clutton-Brock and Paul Harvey on ‘Comparison and adaptation’. Perhaps Gould’s failure to deal with Clutton-Brock and Harvey can be excused on the grounds that he had little time to alter his paper. But a brief nod in their direction, and a diminuendo on the sneers, would have been courteous.
The argument was about whether, when we look at some feature of an animal, it is right to assume that it has been shaped by natural selection – is it necessarily an ‘adaptation’? Gould and Lewontin’s attack on such alleged ‘adaptationism’ (an earlier coinage of Lewontin) was largely aimed at straw men, or at second-rate biology, a far cry from what we might call ‘thoughtful adaptationism’. Clutton-Brock and Harvey undermined the Gould–Lewontin attack by demonstrating sophisticated quantitative techniques for testing adaptation hypotheses with true scientific rigour. These techniques, mostly statistical variants of the comparative method, have proceeded apace in subsequent years, in the hands both of Clutton-Brock and Harvey themselves, and of others including my sometime pupil Mark Ridley and later workers at Oxford fostered by Paul Harvey during his very successful years as our Professor of Zoology.
I’m sure I would be criticized as a rampant ‘adaptationist’, but my main contribution in print to the debate was actually called ‘Constraints on perfection’ – the chapter with that title in The Extended Phenotype. A thoughtful rather than straw version of adaptationism (not under that name) had been a major influence in Oxford zoology when I was an undergraduate. It was fostered by my own maestro, Niko Tinbergen, and by the school of E. B. Ford, founder of the subject of ‘ecological genetics’ and a devoted disciple of Sir Ronald Fisher, prodigious innovator in the field of statistics as well as that of population genetics. Ford was such a pernickety aesthete, it is hard to imagine him as a field worker, but he and his many talented colleagues, including Bernard Kettlewell, Arthur Cain and Philip Sheppard, did indeed go out into the woods and fields to measure the pressures of natural selection in nature. Their samplings of butterflies, moths and snails, along with the parallel school of American geneticists under Theodosius Dobzhansky (with whom Lewontin studied), found something quite unexpected. Selection pressures in the wild are hugely stronger than anyone had imagined. Seemingly trivial differences turned out to be massively reflected in differential mortality.
I have already mentioned Marek Kohn’s A Reason for Everything, a spirited group portrait of the ‘British School’ of natural selectionists. Kohn rightly says that Ford left behind him ‘an intensely selectionist atmosphere
that enveloped Oxford zoology and a legend upon which he had worked as meticulously as on his Lepidoptera’. That legend included a cultivated misogyny. Miriam Rothschild (see pages 207–10) was one honoured exception, possibly because she was literally ‘the Honourable’ – the daughter of a Lord – and Ford was a snob. I only met him face to face once, although I attended all his lectures, and I saw him in the department often, using his outstretched hand to thread his way fastidiously through the plebeian throng at coffee time. He called it ‘cocoa’, refusing to admit the existence of Nescafé in much the same way as he preferred not to acknowledge dogs, calling them ‘pussy’. (Kohn relates how Ford once startled a dog-owning lady by inquiring solicitously after her pussy.) The one time I met him socially, his shrewd, even cunning eyes led me to doubt the sincerity of his eccentric pose. On the other hand, the report, which I think originated with Philip Sheppard, that he had been seen in Wytham Wood at night, checking moth traps with a lantern which he swung to and fro while declaiming ‘I am the Light of the World’ suggests the opposite – if indeed he really thought he was unobserved.
Ford’s Ecological Genetics, a beautifully written if rather egocentric treatise, leaves the reader in no doubt of the demonstrated power of natural selection. I imbibed the same spirit as an undergraduate through teachers such as Ford’s junior colleague Robert Creed, John Currey, Niko Tinbergen (who, though not a geneticist, did field experiments on the survival value of animal behaviour which were staunchly adaptationist in style) and above all Arthur Cain, the most philosophically and historically sophisticated of the ‘Oxford School’.
Arthur’s adaptationism was more than staunch. If not quite over the top, it was close to the summit. It was also well thought out. Maynard Smith invited him to introduce the closing discussion of the 1979 Royal Society conference, and his animus towards Gould and Lewontin was palpable. He and I were sitting together in the front row before Gould began his talk, and Arthur was muttering to himself in a frenzy. He was especially incensed by an earlier published jibe by Lewontin against the Ford School as ‘a British upper middle class activity’, presumably an oblique reference to the genteel hobby of butterfly collecting; and he was rehearsing under his breath the reply that eventually appeared in his formal remarks: ‘Presumably when prejudice is strong, facts can be dispensed with as well: my own background and upbringing could only be distinguished by the extreme purist from working class.’ As we waited for Gould to begin, Arthur was bouncing up and down with nervous energy and he quoted to me Stanley Holloway’s ‘Let battle commence’ (from the ‘Sam: pick oop tha moosket’ monologue).
In 1964, Arthur had written a paper called ‘The perfection of animals’, which included a trenchant attack on the idea of ‘trivial’, non-functional characteristics of animals. I drew upon it in introducing my ‘Constraints on perfection’ chapter:
Cain makes a similar point about so-called trivial characters, criticizing Darwin for being too ready, under the at first sight surprising influence of Richard Owen, to concede functionlessness: ‘No one will suppose that the stripes on the whelp of a lion, or the spots on the young blackbird, are of any use to these animals . . .’ Darwin’s remark must sound foolhardy today even to the most extreme critic of adaptationism. Indeed, history seems to be on the side of the adaptationists, in the sense that in particular instances they have confounded the scoffers again and again. Cain’s own celebrated work, with Sheppard and their school, on the selection pressures maintaining the banding polymorphism in the snail Cepaea nemoralis may have been partly provoked by the fact that ‘it had been confidently asserted that it could not matter to a snail whether it had one band on its shell or two’ (Cain, p. 48). ‘But perhaps the most remarkable functional interpretation of a “trivial” character is given by Manton’s work on the diplopod Polyxenus, in which she has shown that a character formerly described as an “ornament” (and what could sound more useless?) is almost literally the pivot of the animal’s life’ (Cain, p. 51).
Astonishingly, however, the most extreme adaptationist quotation I could find was not from Cain but from, of all people, Lewontin himself, writing in 1967 before his contrarian conversion set in: ‘That is the one point which I think all evolutionists are agreed upon, that it is virtually impossible to do a better job than an organism is doing in its own environment.’
Starting with my Oxford bias towards adaptationism, my chapter went some way in what might seem to be the other direction, as I pinpointed some major constraints on perfection. Cain himself recognized that the animal we are looking at might be simply out of date, and he gave a working estimate of two million years as the upper bound for this. A more permanent constraint on perfection was suggested to me when I was an undergraduate by one of my tutors, John Currey (who also did research with Cain on snail population genetics). A branch of one of the cranial nerves, the recurrent laryngeal runs from the brain to the larynx. It doesn’t go straight there, however. Instead, it dives down into the chest, loops around one of the main arteries leaving the heart, and proceeds back up the neck to the larynx. In a giraffe the detour is significant (British understatement) and it is presumably costly. The explanation lies in history, in the nerve’s emergence in our fish ancestors before a discernible neck evolved. In those remote days, the most direct route of that nerve (its fishy equivalent) to what was then its target did indeed lie posterior to what was then the equivalent artery (supplying one of the gills). As I put it in The Extended Phenotype:
A major mutation might have re-routed the nerve completely, but only at a cost of great upheaval in early embryonic processes. Perhaps a prophetic, God-like designer back in the Devonian could have foreseen the giraffe and designed the original embryonic routing of the nerve differently, but natural selection has no foresight.
Years later, in a 2010 Channel Four television documentary called Inside Nature’s Giants, I assisted in a revealing dissection of the recurrent laryngeal nerve of a giraffe which had died in a zoo. The scene had a dream-like quality which made it impossible to forget. The operating theatre was literally a theatre, the stage separated from the seated audience of veterinary students by a great wall of glass. The audience was in semi-darkness, and the fierce lights glaring down on the stage picked out the resemblance between the colour of the giraffe’s patches and the orange overalls of the dissecting team with their uniform white wellington boots. The giraffe had one hind leg hoisted aloft by a derrick, which added to the surreal quality of the scene. From time to time I was invited by the television producer to advance to the glass wall and address the students with a microphone, explaining the evolutionary significance of the laryngeal nerve and its yards and yards of pointless diversion.1
Selection may be powerful, but it is impotent without genetic variation to select from. Pigs might fly, if only the necessary mutations to sprout wings (and change lots of other aerodynamically important things) were forthcoming. It’s controversial how great a constraint this is, and it really belongs in the field of embryology. I returned to the subject, in what I hope was a constructive manner, in Climbing Mount Improbable.
Another apparent constraint is imposed by costs of materials. In The Extended Phenotype I quoted from the ‘Concorde’ paper I had written with Jane Brockmann in 1980:
An engineer, given carte blanche on his drawing board, could design an ‘ideal’ wing for a bird, but he would demand to know the constraints under which he must work. Is he constrained to use feathers and bones, or may he design the skeleton in titanium alloy? How much is he allowed to spend on the wings, and how much of the available economic investment must be diverted into, say, egg production?
It was an economic constraint of this kind that Jane and I invoked to explain the apparent Concordian behaviour of her digger wasps (pages 78–82).
The Darwinian engineer in the classroom
I have explained how my tutorials as an undergraduate at Oxford predisposed me towards the adaptationism which later came in for criticism; and how I, t
ogether with other Oxford colleagues, later became involved in a defence of a more cautious, more thoughtful adaptationism. When I became a tutor myself, I found that my adaptationist bias had pedagogical advantages. It furnishes a narrative flow to help in remembering factual details of biology.
As a lecturer and tutor, I continually sympathized with students facing the task of remembering huge numbers of facts, and I thought about how to make it easier. Medical students suffer the worst, and unfortunately my favourite teaching trick, which I am calling here ‘the Darwinian engineer’, probably would make little dent on the formidable array of sheer, unyielding facts that human anatomy presents. This makes me even more proud of my daughter Dr Juliet Dawkins’s first-class degree, especially given that St Andrews is one of the few remaining medical schools that still teaches anatomy by hands-on dissection. The problem with anatomy, at least at the level of detail the best medical schools teach, is that so many of its facts are discrete snippets of information that resist being threaded together in a necklace of coherent narrative that might prompt memory. Certainly the broad highways of human anatomy make functional sense and can be taught accordingly, but the minute details of exactly which nerve goes over or under which artery – of literally vital importance for a surgeon – just have to be learned. If they make functional sense (and I expect they do) it is deeply buried, probably in internal intricacies of embryology, and hard to discern.
Brief Candle in the Dark Page 33
