W. D. Hamilton’s Darwinian Precursors

Sir, – Matt Ridley’s review (June 14) of Narrow Roads of Gene Land by W. D. Hamilton (which I have only just seen) gives a foreshortened view of history. He writes that in evolutionary theory ‘the collection of insights [Hamilton] has ... amassed in a lifetime of research is unmatched in this century, even by giants such as J. B. S. Haldane’, and goes on to suggest that Hamilton, together with George Williams, has been largely responsible for ‘the revolutionary change in our understanding of evolution’ which made biologists abandon species-competition theories in favour of individual-competition theories.

Before this version of events becomes accepted, a few facts should be recalled. The Genetical Theory of Natural Selection by R. A. Fisher (Oxford), first published in 1930, is the book which established a firm theoretical basis for evolution by selection acting within species. Not for nothing did Richard Dawkins refer to Fisher in The Blind Watchmaker as ‘the greatest of [Darwin’s] successors’. The importance of parental investment, which Ridley cites as one of the ‘eight main chapters in this revolution’, is discussed by Fisher in Chapter VI Sexual reproduction and sexual selection. The evolution of female choice, another of Ridley’s ‘eight’, is also treated in this chapter, but the idea is found much earlier in Fisher’s 1915 paper The evolution of sexual preference (Eugenics Review 7, 184-192). In Chapter VIII Man and society Fisher attributes the idea of the evolutionary importance of parental expenditure to Leonard Darwin, Charles Darwin’s fourth son, to whom The Genetical Theory is dedicated. Hamilton himself told me, some years ago, that as an undergraduate he found The Genetical Theory in his Cambridge college library and devoured it avidly.

Hamilton read Genetics in Cambridge in 1960 when I was a research student in the department (from which Fisher had only recently retired). One of my projects was to test Fisher’s theory of natural selection and the sex ratio (from his Chapter VI) on mice, and Hamilton was assigned to me as a student to help with the project. The theory involves the concept of parental expenditure, so Hamilton encountered both that idea and the idea that sex ratios have a selective significance, which he treated in his 1967 paper. My experiment (which failed) is mentioned in Natural selection and the sex ratio (Annals of Human Genetics, 24, 239-244, 1960; reprinted in George Williams’s Group Selection, Chicago, 1971), in which W. F. Bodmer and I gave a mathematical account of Fisher’s theory, parental expenditure and all.

Next, take kin selection, another of Ridley’s ‘eight’. The idea of inclusive fitness goes back at least as far as Fisher’s lecture to the Cambridge University Eugenics Society in 1912 (Eugenics Review, 5, 309-315, 1914), in which he used as his example the nephews that could replace ‘genetically’ a childless man killed in war. J. B. S. Haldane first wrote about inclusive fitness in Darwinism Today, one of his famous essays published in 1927 (Possible Worlds and other essays; London), and then, in The Causes of Evolution (1932; London), he included an appendix Outline of the Mathematical Theory on Natural Selection which contained a section Socially Valuable but Individually Disadvantageous Characters. Hamilton mentioned Haldane in his 1964 papers eulogised by Ridley, and even pointed out with a quotation that in The Genetical Theory (Chapter VIII Mimicry) Fisher had invoked inclusive fitness to explain the evolution of distastefulness in insects, yet still Ridley thinks Hamilton had no precursors. ‘It seems such a banal idea in retrospect. It started the whole business of what Richard Dawkins came to call selfish genes’. Perhaps; but in 1912, not 1964.

Or take evolutionary game theory, which Ridley surmises Hamilton feels ‘he could have beaten John Maynard Smith to’. In fact, as P. G. Martin reminded readers of Nature in 1982 (300, 572), the application of game theory to evolution goes back at least as far as 1957, when Fisher promoted it ‘at Dr Cavalli’s invitation’ (see Polymorphism and natural selection, Journal of Ecology, 46, 289-293, 1958). Professor Cavalli-Sforza, who had been an Assistant in Research in Fisher’s Cambridge department, tells me that he recalls making the suggestion.

Matt Ridley quotes Hamilton as saying that Haldane, Fisher and Sewall Wright ‘had not tried very hard to apply their Mendelised Darwinism to social behaviour’. This is true of Wright, less so of Haldane (one of the essays in Possible Worlds is Eugenics and social reform), but for Fisher it is preposterous. The last five chapters of The Genetical Theory of Natural Selection are devoted to man; indeed, the first of them is entitled Man and society. Take any number of the Eugenics Review between 1914 and 1934 and you will find endless annotations by Fisher of relevant material from the wider genetics literature.

Hamilton is heir to the Darwinian tradition transmitted through Charles’s son Leonard and R. A. Fisher. Fisher knew Darwin’s writings backwards (he had chosen the complete works, in 13 volumes, as a school prize), and The Genetical Theory of Natural Selection is a kind of Mendelian appendix to On the Origin of Species by means of Natural Selection. Hamilton in his turn read The Genetical Theory and studied genetics in the Cambridge department which Fisher created.

Of The Genetical Theory Sewall Wright wrote ‘It is a book which is certain to take rank as one of the major contributions to the theory of evolution’, whilst Haldane called it ‘brilliant’. Although there were differences of detail between Fisher, Wright and Haldane, they jointly founded the subject of population genetics, but in recent years a new, and prolific, group of biologists has invented evolutionary biology without, it now appears, sufficient reading in population genetics. The concepts over which they enthuse have percolated into this ‘new’ subject, but its practitioners are wont to be so carried away by their enthusiasm - and their metaphors and their catch-phrases - that some of them have fallen into the trap of exaggerating the originality of their ideas.

A. W. F. Edwards