Foxes In The Snow

Foreword to a new edition of George Williams’ Adaptation and Natural Selection (2018)

The neo-Darwinian synthesis of the 1930s and 1940s was a collective Anglo-American achievement, de)ned by a recognizable ‘canon’ of seminal books, those of Fisher, Haldane, Mayr, Dobzhan sky, Simpson and others. Julian Huxley’s Evolution: the modern synthesis bequeathed its title to the whole movement although for its theoretical content it doesn’t stand out. If I were asked to nominate one book from the second half of the twentieth century that deserves to take an honoured place alongside the ‘canon’ of the 1930s and 1940s, I would choose Adaptation and Natural Selection by George C. Williams.

On opening it I have the feeling of being ushered into the presence of a penetrating and outstanding mind, the same feeling I get, indeed, from reading The Genetical Theory of Natural Selection, although Williams, unlike Fisher, was no mathematician. In George Williams we have an author of immense learning and incisive critical intelligence, who thought deeply about every aspect of evolution and ecology. Williams not only enlarged the synthesis, he exposed with great clarity where many of its followers had gone astray, even in some cases the original authors themselves. 'is is a book that every serious student of biology must read, a book that irrevocably changes the way we look at life. Throughout my career as an Oxford tutor, I obviously recommended many books to my students. But I think this was the only one I insisted that all should read. Here’s a list of major mistakes a student is likely to make before reading this book, but will not make afterwards.

‘Mutations are an adaptation to speed up evolution.’ ‘Dominance hierarchies are an adaptation to make sure the strongest individuals reproduce.’ ‘Territoriality is an adaptation to space the species out and beneficially limit the population.’ ‘Sex ratios are optimized to make the best use of species resources.’ ‘Death from old age is an adaptation to clear superannuated individuals out of the way and make room for the young.’ ‘Natural selection favours species that resist extinction.’ ‘Species parcel out niches for the benefit of a balanced ecosystem.’ ‘Predators hunt “prudently,” taking care not to deplete prey that they are going to need in the future.’ ‘Individuals limit their reproduction to avoid overpopulation.’

‘Adaptation’ is the first word in the title and the book is largely a plea for a proper, scientific study of adaptation – a scientific teleonomy, to adopt Pittendrigh’s term as advocated by Williams. But Williams is the last person who could justly be tarred as a naive ‘adaptationist’. 'is pejorative was given wide currency by Gould and Lewontin in their overrated ‘spandrels paper’ of 1979. It denotes those who assume without evidence that everything an animal is or does must be an adaptation. Unfortunately, their critique of adaptationism has been misunderstood, not least by some philosophers such as the late Jerry Fodor,* as a critique of the very idea of adaptation itself.

A ‘spandrel’ is a non-adaptive by-product. 'e name comes from the gaps between gothic arches which are a necessary but non-functional by-product of the functionally important arches themselves. Long before the word was introduced into biology, Williams, a leading advocate of adaptation as a proper subject for scientific study, gave an incisive critique of what would later be called spandrels. His vivid example, which regularly grabbed the attention of my Oxford students, was a fox repeatedly running along its own tracks in the snow. Its paws increasingly flattened the snow, which made each successive journey easier and faster. But it would be wrong to say the fox’s paws were adapted to flattened snow. They can’t help flattening snow. This particular beneficial effect is a by-product. Williams summed up the message pithily: adaptation is an ‘onerous concept’.

If I might paraphrase the Anglican marriage service in a way that Williams might not, any attribution of adaptation should not be entered into unadvisedly or lightly; but reverently, discreetly, advisedly, soberly and in the fear of Occam’s Razor. You must first assure yourself that you could, if called upon to do so, translate your adaptation theory back into the rigorous terms of neo-Darwinism. The ‘adaptation’ you postulate must not just be ‘beneficial’ in some vague, panglossian sense. You must clearly set out, and be prepared to defend, a strictly Darwinian pathway to the evolution of the alleged adaptation. The 'benefit’ must accrue at the proper level in the hierarchy of life, which is the unit of Darwinian natural selection. And the proper level, for Williams as for me, is that of the individual genes responsible for the putative adaptation.

The term ‘panglossian’ was introduced into biology by J. B. S.Haldane, one of the architects of the synthesis. His star pupil John Maynard Smith reported that Haldane proposed three ‘theorems’ to satirize errors in scientific thinking.

Aunt Jobiska’s Theorem (from Edward Lear): ‘It’s a fact the whole world knows.’

The Bellman’s Theorem (from Lewis Carroll): ‘What I tell you three times is true.’

Pangloss’s Theorem (from Voltaire and applying especially to biology): ‘All is for the best in the best of all possible worlds.’

My second paragraph above was a list of panglossian errors frequently perpetrated by professors and students alike (including my own undergraduate self). Adaptations cannot be just ‘good’. It is not enough that they convey ‘benefit’. They have to be good for some entity that has been naturally selected precisely because of benefit to itself. And that entity, as Williams powerfully argues, will normally be the gene. I’m fond of a Williams bon mot from his later book, Natural Selection: ‘A gene pool is an imperfect record of a running average of selection pressures over a long period of time in an area often much larger than individual dispersal distances.’ But why the gene? And ‘gene’ in what sense? Williams’ rationale was so clear and irrefutable, I’m inclined to quote it in full, but you only have to turn to page 23, the ‘Socrates paragraph’, which also grabbed my Oxford students by the collar when they read it. Here’s the central point.