“How complex and even perverse the real world can be”: W.D. Hamilton's early work on social wasps (1964–1968)

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Highlights

  • The article provides a new perspective on the development of Hamilton's early work on social evolution.

  • The article complements and enriches existing narratives about the field of social evolution.

  • Differently from existing narratives, the article shows the importance of Hamilton's empirical work.

  • The article details for the first time Hamilton's empirical work on social wasps in the 1960s.

  • The article presents new and unreleased material from Hamilton's archive at the British Library.

Abstract

William D. Hamilton's name is often connected to important theoretical accomplishments, from the theory of inclusive fitness and kin selection to the so-called Hamilton's rule and the haplodiploidy hypothesis. This article asks: How did Hamilton attempt to test his theory and hypothesis against the complexity of the biological world? The article reconstructs Hamilton's empirical work with social wasps between 1963 and 1968, the years before and after the publication of the groundbreaking “The Genetical Evolution of Social Behavior” in 1964. It points out the centrality of Hamilton's work on wasps and shows how the British scientist attempted to test theories and hypotheses with naturalistic, developmental, and physiological observations as well as, at times, with experimental manipulations. The article offers a new perspective on the history of the scientific understanding of the evolution of social behavior. In contrast to existing narratives, this perspective emphasizes the importance of empirical work—e.g. natural history, physiology, comparative anatomy—which is often obscured by a nearly exclusive focus on theoretical developments in this field.

Introduction

William D. Hamilton's name is often connected to important theoretical accomplishments, from the theory of inclusive fitness and kin selection to the so-called Hamilton's rule and the haplodiploidy hypothesis (Charnov, 1977, Hamilton, 1963, Hamilton, 1964a, Hamilton, 1964b). Inclusive fitness theory shows how the genetic relatedness of individuals affects their behavior towards one another. Hamilton's rule points out that social behavior evolves under specific combinations of costs, benefits, and relatedness (Hamilton, 1963). The haplodiploidy hypothesis explains how self-sacrificing behaviors evolved in social insects of the order Hymenoptera, including wasps, bees and ants (Hamilton, 1964b). Rules, theory and hypothesis have dominated the attention of most scholars since the publication of “The Genetical Evolution of Social Behavior” in 1964 (Wilson, 1971, Grafen, 2004). This paper asks: How did Hamilton seek to test his theory and hypothesis against the complexity of the biological world? How did he attempt to see if the theory, the rule and the hypothesis could help explain the evolution of social behavior in specific biological systems?

In some notes for the preparation of a lecture in the late 1970s, Hamilton wrote: “I feel very strongly that a theorist ought not to become too detached from the things he theorizes about—at least I find it salutary to keep reminding myself by observation and experimentation of how complex and even perverse the real world can be” (Hamilton; Undated; Z1X90/1/18). Though mostly a theorist, Hamilton maintained that scientists should always pay close attention to the complexity and even perversity of real biological phenomena. Complex and perverse features of wasp societies posed challenges to Hamilton's theory of inclusive fitness and to the haplodiploidy hypothesis (Hamilton, 1964b). In his work during the 1960s and early 1970s, though not always systematically, Hamilton addressed these challenges by investigating societies of tropical and non-tropical wasps.

Social wasps occupy a central place in Hamilton's publications and notebooks as well as in his correspondence with colleagues, family and friends. Borrowing an expression from the evolutionary biologist M.J. West-Eberhard, wasps were for Hamilton a microcosm for the investigation of social life (West-Eberhard, 1996). There are two main reasons for Hamilton's interest for wasps. First, the human-like features of wasp societies fascinated him. For instance, Hamilton talked about the: “indescribable quality of the wasps' life itself—wayward, mysterious, almost human” (Hamilton to West-Eberhard; 5 October 1967; Z1X83/1/10). This feature distinguishes most wasp societies from the perfect organization of many ant and bee societies (e.g. Hölldobler & Wilson, 2009). The second reason was that wasps provided ‘touchstone puzzles’ to the theory of inclusive fitness and to the haplodiploidy hypothesis (Caniglia, 2017). According to this theory, altruistic acts, such as the self-sacrificing behavior of most workers and auxiliaries in wasp colonies, evolve because beneficiaries and self-sacrificing actors, under certain ecological conditions, share copies of the same genes (Hamilton, 1964b, Hamilton, 1964a). Therefore, the self-sacrificing individuals can pass on their genes to their offspring by helping their relatives, who carry copies of the same genes (Hamilton, 1963). However, most social wasps show behaviors that tend to lower the relatedness of the individuals in a colony and therefore challenge explanations in terms of inclusive fitness (e.g. Gadagkar, 2009).

This article reconstructs Hamilton's investigations on social wasps between 1963 and 1968. This reconstruction complements existing narratives about Hamilton's work and about our scientific understanding of the evolution of social life. Such narratives have privileged the theoretical development of Hamilton's ideas and of the whole field (e.g. Grafen, 2004, Queller, 2001) as well as Hamilton's correspondence with important evolutionary theorists of his time from J. Maynard Smith to G. Price (Borrello, 2010, Harman, 2010, Segerstrale, 2013). They have often described Hamilton's empirical work as a compulsive tendency to follow his own “boyhood training” (Hamilton, 1996a, p. 117), a need to escape formal academic environments (Dugatkin, 2011), a necessity to feed his imaginative mind (Grafen, 2004) or even as derived from a political interest in “human society and his concern for man's future” (Swenson, 2015a, p. 47). With some exceptions (Hughes, 2002), such narratives have deprived Hamilton's empirical work of scientific interest and importance (Grafen, 2004, p. 119). By detailing Hamilton's early work on wasps, this article provides an alternative and complementary narrative to existing ones and brings Hamilton's empirical work to the foreground.

Hamilton's empirical work on wasps often did not reach the stage of publication (Wilson, 1971, Grafen, 2004). Yet, Hamilton's notebooks, loose papers, and correspondence stored in Hamilton's Archive at The British Library document the importance the British scientist attributed to empirical work. Archival material also shows that Hamilton's empirical work was nourished by a network of relationships with scientists, such as the Brazilian W.E. Kerr and the young evolutionary biologist M.J. West (later M.J. West-Eberhard), who made important contributions not only to the theory of social evolution but also to its empirical foundations. Though not in the form of published papers, Hamilton's empirical investigations influenced the way many scientists started looking for empirical evidence in order to understand whether abstract theories and models of social evolution could help explain why social life evolved (e.g. Strassmann, 1979, Strassmann, 1981, West, 1967, West-Eberhard, 1973, West-Eberhard, 1975). Thus, the reconstruction of Hamilton's empirical work invites us to consider these empirically-oriented investigations as an important component in the historical development of scientific ideas on social evolution.

This article follows Hamilton's investigations in the years between 1963, when Hamilton's first publication in The American Naturalist came out, and 1968, when Hamilton left for his second trip to Latin America. First, it sketches the main features of Hamilton's theory of inclusive fitness (Hamilton, 1963, Hamilton, 1964a) and the haplodiploidy hypothesis (Hamilton, 1964b) as they emerged from Hamilton's publications of the time. Second, it details Hamilton's attempts to conduct empirical work on wasp societies during his first trip to Latin America from August 1964 to late summer 1965. Third, it reconstructs Hamilton's reflections about the value and meaning of his empirical investigations between 1964 and 1968. Finally, it provides an outlook on how Hamilton sought to evaluate inclusive fitness theory with empirical evidence after 1968.

Section snippets

The genetical theory of social behavior (1964)

Since his college years at Cambridge, Hamilton had worked strenuously on the problem of biological altruism (Hamilton, 1996a, Segerstrale, 2013). In order to approach this problem, he had engaged with earlier foundational works in evolutionary biology and population genetics, chiefly Fisher's The Genetical Theory of Natural Selection (1930) and Haldane's The Causes of Evolution (1932), in the development of his theories and ideas (e.g. Grafen, 2004, Segerstrale, 2013, Harman, 2010). Since 1962,

Theory evaluation and empirical explorations during the first trip to South America

As Hamilton admitted in the Introduction to Part II of “The Genetical Evolution of Social Behavior”, after he had provided a mathematical formulation of the theory, he felt the need to see whether he could support the theory with evidence from biological facts (Hamilton, 1964b, p. 17). In Narrow Roads of Gene Land, remembering the times when he was writing his 1964 paper, he admitted that he: “desperately needed examples … where both self-sacrifice and the limits to it were indisputable” (

Addressing wasps' puzzling behaviors

Hamilton's observations and experiments during the trip to South America focused on features of wasp social life that could provide information about the level of relatedness within the colonies. To Hamilton, wasp societies had two most interesting and puzzling features. The first was polygyny, say the presence on the nest of multiple egg-laying and potentially unrelated females, both at nest foundation (pleometrosis) and during the whole colony life cycle (true polygyny) (Pardi, 1948). The

Planning more empirical work and doing more theory

In the late 1960s, Hamilton's work had radically impacted the field of evolutionary biology (e.g. Wilson, 1971, West-Eberhard, 1969). During these years Hamilton worked on several publications in which he refined his ideas about social evolution (Hamilton, 1970a, Hamilton, 1970b, Hamilton, 1971a, Hamilton, 1971b, Hamilton, 1972). One of the major events of this time was Hamilton's second trip to South America from April 1968 to January 1969. During five of the nine months he spent in South

Conclusions

In the 1960s and 1970s, Hamilton's theory of inclusive fitness was new and contentious (Alexander, 1974, Lin and Michener, 1972, West-Eberhard, 1975). It was unclear whether or not it would identify the appropriate parameters (i.e. relatedness, costs and benefits) for the explanation of the evolution of social behaviors in specific biological cases (Hamilton, 1964b). In the years after the publication of “The Genetical Theory of Social Behavior”, some scientists enthusiastically embraced the

Acknowledgements

I thank the American Philosophical Association as well as the Center for Biology and Society at Arizona State University for supporting two visits to W.D. Hamilton's archive at the British Library. I am very thankful to Jane Maienschein, Manfred Laubichler, Sandra Mitchell, and Jürgen Gadau for reading previous drafts of this manuscript and giving me helpful comments. I also wish to thank Bert Hölldobler, Gro Amdam, Christopher Starr, Jean-Baptiste Grodwhol, Stefano Turillazzi, David Hughes,

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    Present address: Institute of Ethics and Transdisciplinary Sustainability Research, Leuphana University of Lüneburg, Scharnhorststraße 1, C11.210b, 21335 Lüneburg, Germany.

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