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R. A. Fisher and Social Insects: The Fisher-Darwin Model of the Evolution of Eusociality

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Abstract

Fisher recognized that the evolution of social insect colonies needed explaining, a point which Charles Darwin had avoided discussing in detail. Fisher, in his 1930 book The Genetical Theory of Natural Selection, outlined in detail how eusociality could evolve, and developed a verbal model by connecting selection on fecundity with the sterility of workers. Fisher saw social insect colonies as harmonious units, in contrast to human societies that exhibit intra-communal conflict. Fisher’s development of the model was strongly influenced by his correspondence with Leonard Darwin, and so I call it the Fisher-Darwin model. However, Fisher was not influenced by Lamarckian views on the evolution of social insects that were common at that time. The Fisher-Darwin model presages almost exactly the mathematical model recently proposed by Nowak and colleagues.

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Notes

  1. Major Leonard Darwin was the second youngest of Charles Darwin’s five sons and was an important mentor and supporter of Fisher and his work (Bennett 1983). Fisher dedicated GT to him.

  2. Henceforth I will mostly quote page numbers from this second edition as this is likely to be more accessible for readers than the 1930 edition.

  3. Fisher’s comparison of human and insect societies is completely different from the view of the German Lamarckian Theodore Eimer (1890, p. 434), who thought that human society should take the social life of the bees as its model, and humans should give up their independence for the common good.

  4. This is similar to the idea of a social insect colony as a “superorganism.” This concept originated with William Morton Wheeler in a lecture given in 1910 (Wheeler 1911), and as Wilson (1971, p. 317) points out, “During some 40 years, from 1911 to about 1950, this concept was a dominant theme in the literature on social insects.” However, Fisher does not use the word superorganism, and does not pursue this line of reasoning.

  5. This echoes Darwin’s statement in the Origin that “selection may be applied to the family, as well as to the individual.” Darwin continued,

    I do not doubt that a breed of cattle, always yielding oxen with extraordinary long horns, could be slowly formed by carefully watching which individual bulls and cows, when matched, produced oxen with the longest horns; and yet no one ox could ever have propagated its kind. Thus I believe it has been with social insects: a slight modification of structure or instinct, correlated with the sterile condition of certain members of the community, has been advantageous to the community; consequently the fertile males and females of the same community flourished, and transmitted to their fertile offspring a tendency to produce sterile members having the same modification. (Darwin 1859, p. 238)

    This is now commonly defined as colony-level selection, and formally can be stated as: if inherited variation of characters expressed by workers, or reproductive offspring, exists and leads to differential productivity or survival of colonies, then the reproductive success of the founding queen and male is determined by selection at the level of the colony (Owen 1986). This, I believe, is very close to what Darwin intended. Therefore, colony-level selection as defined here is selection on mating types or fertilities of founding queens and males for properties of colonies, which are the traits expressed by the workers. Mating-type (or fertility) selection simply means that the reproductive success of an individual depends not only on its own genotype but also on the genotype of its mate. Darwin saw the evolution of different forms of neuter workers in a social insect colony as a greater difficulty for his theory of natural selection than the evolution of eusociality itself.

  6. Fisher (1930, p. 43) does not approve of Darwin’s phrase “struggle for existence” (Darwin 1859, Chap. 3), which implies excessive production of offspring always and excludes fecundity from being subject to selection itself. He writes (p. 44): “The historical fact that both Darwin and Wallace were led through reading Malthus’s essay on population to appreciate the efficacy of selection, though extremely instructive as to the philosophy of their age, should no longer constrain us to confuse the consequences of that principle with its foundations.”

  7. Fisher did have other verbal models in GT; e.g., in the section on “equilibrium involving two factors” (1958, pp. 116–118) he discusses simultaneous selection at two gene loci.

  8. Francis Darwin (1848–1925), the third son of Charles Darwin, was a botanist, and many of his ideas stemmed from his work with his father on the power of movement in plants and the controlling influence of the root (Bowler 1983; Baluška et al. 2009).

  9. Wheeler’s delightful book Social Life among the Insects is a printed version of a series of lectures given at the Lowell Institute in Boston in March 1922.

  10. Émile Roubaud (1882–1962) was an entomologist and a professor in the Institut Pasteur in Paris.

  11. In this discussion Wheeler invokes two different types of castration, trophic (partial starvation of larvae) and nutricial (partial starvation of adults), leading to the sterility of social insect workers. These mechanisms were differentiated by Marchal (1897).

  12. Wheeler’s paper had been read before the Royce Club on May 20, 1917.

  13. J. T. Cunningham was a Sometime Fellow of University College, Oxford and Lecturer in Zoology at East London College, University of London. He was a well known, although not strictly orthodox, Lamarckian and had translated Eimer’s (1898) book on evolution as a result of the inheritance of acquired characters, and was the author of a biology textbook with a Lamarckian emphasis (Hentschel 1929; Bowler 1983).

  14. In fact Wheeler (1910, pp. 116–117) and most other myrmecologists did reject this (Sleigh 2004).

  15. When Fisher was appointed at Rothamsted in 1922 he became friends with D. M. Moreland of the Ministry of Agriculture Bee Section, which stimulated his interest in honeybees; and he took up beekeeping for a while (Box 1978, pp. 167-168).

  16. Fisher does discuss Lamarckism twice elsewhere, in Chap. I of GT and in Fisher (1932, p. 579).

  17. However, in fairness to Fisher, it should be emphasized that his views were those of a positive eugenist rather than those prevailing in the Eugenics Society in Britain, which were negative with a “frightened loathing of the lower classes” (Mazumdar 1992, p. 102). Also Fisher, from 1923 on, was extremely critical of the Eugenics Society’s research methods, and tried to persuade them to follow the correct statistical procedures that he had developed and was developing through his work at Rothamsted (Mazumdar 2002).

  18. The quotation “If I have seen farther, it is by standing on the shoulders of giants” is attributed to Isaac Newton. He did indeed write this in a letter to Robert Hooke, but in fact it goes back to Richard Burton who wrote in 1642, “Pigmies placed on the shoulders of giants see more than the giants themselves,” which itself may have even earlier antecedents (Boller and George 1989).

  19. Although for a different perspective on the Modern Synthesis see Cain (2009).

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Acknowledgments

I thank the following for their helpful comments on an earlier version of the manuscript: Anthony Edwards, Kevin Foster, Jean-Baptist Grodwohl, Chris Plowright, and Chris Starr.

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  1. Department of Biology, Mount Royal University, Calgary, AB, Canada

    Robin E. Owen

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Owen, R.E. R. A. Fisher and Social Insects: The Fisher-Darwin Model of the Evolution of Eusociality. Biol Theory 9, 347–356 (2014). https://doi.org/10.1007/s13752-014-0168-9

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