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Animal Behavior, Population Biology and the Modern Synthesis (1955–1985)

  • Jean-Baptiste GrodwohlEmail author
Original Research

Abstract

This paper examines the history of animal behavior studies after the synthesis period. Three episodes are considered: the adoption of the theory of natural selection, the mathematization of ideas, and the spread of molecular methods in behavior studies. In these three episodes, students of behavior adopted practices and standards developed in population ecology and population genetics. While they borrowed tools and methods from these fields, they made distinct uses (inclusive fitness method, evolutionary theory of games, emphasis on individual selection) that set them relatively apart and led them to contribute, in their own way, to evolutionary theory. These episodes also highlight some limitations of “conjunction narratives” centered on the relation between a discipline and the modern synthesis. A trend in conjunction narratives is to interpret any development related to evolution in a discipline as an “extension,” an “integration,” or as a “delayed” synthesis. I here suggest that this can lead to underestimate discontinuities in the history of evolutionary biology.

Keywords

Evolutionary biology Modern synthesis Animal behavior Population biology Behavioral ecology Sociobiology 

Notes

Acknowledgements

This work was supported by funding from the Coordenação de Aperfeicoamento de Pessoal de Nível Superior (Brasil) and by the John Templeton Foundation Grant #60501. Unpublished materials quoted in this text were accessed thanks to the kind help of the staffs of the American Philosophy of Science Library, the British Library, the University of Bristol Library, the Library of Congress, the Stony Brook University Libraries and the Yale University Library. Geoffrey Parker has kindly allowed me to quote from his correspondence. This paper has benefitted from numerous conversations with scientists and historians, and from substantial critical comments by Andrew Buskell, David Depew, Philippe Huneman, Tim Lewens, G.A. Parker, Anya Plutynski, Alexandre Tanase and two anonymous reviewers. Rebecca Kilner and John Welch made very encouraging suggestions. All are gratefully thanked.

References

  1. Alexander, R.D. 1974. The Evolution of Social Behavior. Annual Review of Ecology and Systematics 5: 325–383.CrossRefGoogle Scholar
  2. Alexander, R.D. 1975. The Search for a General Theory of Behavior. Systems Research and Behavioral Science 20 (2): 77–100.CrossRefGoogle Scholar
  3. Antonovics, J. 1987. The Evolutionary Dys-synthesis: Which Bottles for Which Wine? The American Naturalist 129 (3): 321–331.CrossRefGoogle Scholar
  4. Aronson, J.D. 2002. “Molecules and Monkeys”: George Gaylord Simpson and the Challenge of Molecular Evolution. History and Philosophy of the Life Sciences 24 (3–4): 441–465.CrossRefGoogle Scholar
  5. Baron, C. 2013. The Handicap Principle and the Argument of Subversion from Within. Studies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences 44 (3): 347–355.CrossRefGoogle Scholar
  6. Bates, M. 1958. Food-Getting Behavior. AE Roe, GG Simpson (eds.), Behavior and Evolution. New Haven:Yale University Press, pp. 206–223.Google Scholar
  7. Bateson, P. 2005. The Return of the Whole Organism. Journal of Biosciences 30 (1): 31–39.CrossRefGoogle Scholar
  8. Bateson, P., and K.N. Laland, 2013. Tinbergens Four Questions: An Appreciation and an Update. Trends in Ecology & Evolution 28 (12): 712–718.CrossRefGoogle Scholar
  9. Beatty, J. 1994. The Proximate/Ultimate Distinction in the Multiple Careers of Ernst Mayr. Biology and Philosophy 9 (3): 333–356.CrossRefGoogle Scholar
  10. Borrello, M.E. 2009. Shifting Balance and Balancing Selection: A Group Selectionist’s Interpretation of Wright and Dobzhansky. Transactions of the American Philosophical Society 99 (1): 323–344.Google Scholar
  11. Brown, J. 1975. The Evolution of Behavior. New York:Norton.Google Scholar
  12. Burkhardt, R.W. 2005. Patterns of Behavior: Konrad Lorenz, Niko Tinbergen, and the Founding of Ethology. Chicago:University of Chicago Press.Google Scholar
  13. Cain, J. 2009. Rethinking the Synthesis Period in Evolutionary Studies. Journal of the History of Biology 42 (4): 621–648.CrossRefGoogle Scholar
  14. Caniglia, G. 2017. “How Complex and Even Perverse the Real World Can Be”: W. D. Hamilton’s Early Work on Social Wasps (1964–1968). Studies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences 64: 41–52.CrossRefGoogle Scholar
  15. Charnov E.L., and G.H. Orians. 1973. Optimal Foraging: Some Theoretical Explorations, unpublished manuscript, Scholars Archive@OSU. https://ir.library.oregonstate.edu/downloads/w9505093w
  16. Collins, J.P. 1986. Evolutionary Ecology and the Use of Natural Selection in Ecological Theory. Journal of the History of Biology 19 (2): 257–288.CrossRefGoogle Scholar
  17. Craig, R., and R.H. Crozier. 1979. Relatedness in the Polygnous Ant Myrmecia pilosula. Evolution 33 (1): 335–341.CrossRefGoogle Scholar
  18. Crick, F. 1979. Split Genes and RNA Splicing. Science 204 (4390): 264–271.CrossRefGoogle Scholar
  19. Crook, J.H. 1964. The Evolution of Social Organisation and Visual Communication in the Weaver Birds (Ploceinae). Behaviour. Supplement 10: 1–201.Google Scholar
  20. Crook, J.H. 1970. The Socio-Ecology of Primates. JH Crook (ed.), Social Behaviour in Birds and Mammals: Essays on the Social Ethology of Animals and Man. London:Academic Press, pp. 103–166.Google Scholar
  21. Crook, J.H., and J.S. Gartlan. 1966. Evolution of Primate Societies. Nature 210 (5042): 1200–1203.CrossRefGoogle Scholar
  22. Davies, N.B. 2010. Birds, Butterflies and Behavioural Ecology. L Drickamer, D Dewsbury (eds.), Leaders in Animal Behavior: The Second Generation. Cambridge:Cambridge University Press, pp. 143–164.Google Scholar
  23. Davis, G.K, M.R. Dietrich, and D.K. Jacobs. 2009. Homeotic Mutants and the Assimilation of Developmental Genetics into the Evolutionary Synthesis, 1915-1952. Transactions of the American Philosophical Society 99 (1): 133–154.Google Scholar
  24. Davies, N.B, and J.R. Krebs. 1978. Introduction: Ecology, Natural Selection and Social Behaviour. JR Krebs, NB Davies (eds.), Behavioural Ecology: An Evolutionary Approach. Oxford:Blackwell Scientific Publications, pp. 1–22.Google Scholar
  25. Dewsbury, D.A. 1992. Essay on Contemporary Issues in Ethology: On the Problems Studied in Ethology, Comparative Psychology, and Animal Behavior. Ethology 92 (2): 89–107.CrossRefGoogle Scholar
  26. Dewsbury, D.A. 1995. Americans in Europe: The Role of Travel in the Spread of European Ethology after World War II. Animal Behaviour 49 (6): 1649–1663.CrossRefGoogle Scholar
  27. Dietrich, M.R. 1998. Paradox and Persuasion: Negotiating the Place of Molecular Evolution within Evolutionary Biology. Journal of the History of Biology 31 (1): 85–111.CrossRefGoogle Scholar
  28. Dobzhansky, T. 1951. Genetics and the Origin of Species, 2nd ed. New York:University of Columbia Press.Google Scholar
  29. Emerson, A.R. 1958. The Evolution of Behavior Among Social Insects. AE Roe, GG Simpson (eds.), Behavior and Evolution. New Haven:Yale University Press, pp. 311–335.Google Scholar
  30. Erickson, P. 2015. The World the Game Theorists Made. Chicago:University of Chicago Press.CrossRefGoogle Scholar
  31. Gadagkar, R. 2011. Science as a Hobby: How and Why I Came to Study the Social Life of an Indian Primitively Eusocial Wasp. Current Science 100 (6): 845–858.Google Scholar
  32. Gayon, J. 1995. Neo-Darwinism. G Wolters, JG Lennox (eds.), Concepts, Theories, and Rationality in the Biological Sciences. Konstanz and Pittsburgh:University of Pittsburgh Press, pp. 1–25.Google Scholar
  33. Gould, S.J. 1980. Is a New and General Theory of Evolution Emerging? Paleobiology 6 (1): 119–130.CrossRefGoogle Scholar
  34. Gould, N.E.S.J, and N. Eldredge. 1972. Punctuated Equilibria: An Alternative to Phyletic Gradualism. TJM Schopf (ed.), Models in Paleobiology. San Francisco:Freeman Cooper, pp. 82–115.Google Scholar
  35. Gould, S.J, and R.C. Lewontin. 1979. The Spandrels of San Marco and the Panglossian Paradigm: A Critique of the Adaptationist Programme. Proceedings of the Royal Society of London B: Biological Sciences 205 (1161): 581–598.CrossRefGoogle Scholar
  36. Grafen, A. 1984. Natural Selection, Kin Selection and Group Selection. JR Krebs, NB Davies (eds.), Behavioural Ecology: An Evolutionary Approach. Cambridge:Blackwell, pp. 62–84.Google Scholar
  37. Griffiths, P.E. 2008. Ethology, Sociobiology, and Evolutionary Psychology. S Sarkar, A Plutynski (eds.), A Companion to the Philosophy of Biology. Oxford:Blackwell Publishing Ltd., pp. 393–414.Google Scholar
  38. Haffer, J. 2007. Ornithology, Evolution and Philosophy: The Life and Science of Ernst Mayr. Berlin:Springer.Google Scholar
  39. Hagen, J.B. 1999. Naturalists, Molecular Biologists, and the Challenges of Molecular Evolution. Journal of the History of Biology 32 (2): 321–341.CrossRefGoogle Scholar
  40. Hagen, J.B. 2015. Camels, Cormorants, and Kangaroo Rats: Integration and Synthesis in Organismal Biology After World War II. Journal of the History of Biology 48 (2): 169–199.CrossRefGoogle Scholar
  41. Hamilton, W.D. 1964a. The Genetical Theory of Social Behavior. I. Journal of Theoretical Biology 7 (1): 1–16.CrossRefGoogle Scholar
  42. Hamilton, W.D. 1964b. The Genetical Theory of Social Behavior. II. Journal of Theoretical Biology 7 (1): 17–52.CrossRefGoogle Scholar
  43. Hamilton, W.D. 1967. Extraordinary Sex Ratios. Science 156 (3774): 477–488.CrossRefGoogle Scholar
  44. Hamilton, W.D. 1996. Narrow Roads of the Gene Land. Evolution of Social Behavior. New York:W. H. Freeman at MacMillan Press Limited.Google Scholar
  45. Haraway, D. 1990. Remodelling the Human Way of Life: Sherwood Washburn and the New Physical Anthropology, 1950-1980. GW Stocking (ed.), Bones, Bodies and Behavior: Essays in Behavioral Anthropology. Madison:University of Wisconsin Press, pp. 206–260.Google Scholar
  46. Harman, O. 2011. Birth of the First ESS: George Price, John Maynard Smith, and the Discovery of the Lost Antlers’ Paper. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 316 (1): 1–9.CrossRefGoogle Scholar
  47. Hinde, R.A. 1956. Ethological Models and the Concept of ‘Drive’. The British Journal for the Philosophy of Science 6 (24): 321–331.CrossRefGoogle Scholar
  48. Hinde, R.A, Tinbergen, N. 1958. The Comparative Study of Species-Specific Behavior. AE Roe, GG Simpson (eds.), Behavior and Evolution. New Haven:Yale University Press, pp. 251–268.Google Scholar
  49. Hubby, J.L., and R.C. Lewontin. 1966. A Molecular Approach to the Study of Genic Heterozygosity in Natural Populations. I. The Number of Alleles at Different Loci in Drosophila Pseudoobscura. Genetics 54 (2): 577–594.Google Scholar
  50. Hull, D.L. 1988. Science as a Process: An Evolutionary Account of the Social and Conceptual Development of Science. Chicago:University of Chicago Press.CrossRefGoogle Scholar
  51. Huxley, J.S. 1958. Cultural Process and Evolution. AE Roe, GG Simpson (eds.), Behavior and Evolution. New Haven:Yale University Press, pp. 437–454.Google Scholar
  52. Johnson, K. 2009. The Return of the Phoenix: the 1963 International Congress of Zoology and American Zoologists in the Twentieth Century. Journal of the History of Biology 42 (3): 417–456.CrossRefGoogle Scholar
  53. Kimura, M. 1983. The Neutral Theory of Molecular Evolution. Cambridge:Cambridge University Press.CrossRefGoogle Scholar
  54. King, C.E, and P.S Dawson (eds.). 1983. Population Biology. Retrospect and Prospect. New York:Columbia University Press.Google Scholar
  55. Kingsland, S.E. 1995. Modeling Nature. Chicago:University of Chicago Press.Google Scholar
  56. Kitcher, P. 1985. Vaulting Ambition: Sociobiology and the Quest for Human Nature. Cambridge:MIT Press.Google Scholar
  57. Kohler, R.E. 2002. Landscapes and Labscapes: Exploring the Lab-Field Border in Biology. Chicago:University of Chicago Press.CrossRefGoogle Scholar
  58. Krebs, J.R, and N.B. Davies (eds.). 1978. Behavioural Ecology: An Evolutionary Approach. Oxford:Blackwell Scientific Publications.Google Scholar
  59. Krebs, J.R., and N.B. Davies (eds.). 1997. The Evolution of Behavioural Ecology. In Behavioural Ecology: An Evolutionary Approach, [4th edition], ed. Krebs and Davies, 3–12. Oxford: Blackwell Scientific Publications.Google Scholar
  60. Kruuk, H. 2003. Niko’s Nature: The Life of Niko Tinbergen and His Science of Animal Behaviour. Oxford:Oxford University Press.Google Scholar
  61. Lack, D. 1965. Evolutionary Ecology. The Journal of Animal Ecology 34 (2): 223–231.CrossRefGoogle Scholar
  62. Levallois, C. 2017. The Development of Sociobiology in Relation to Animal Behavior Studies, 1946–1975. Journal of the History of Biology, 1–26.Google Scholar
  63. Lewontin, R.C. 1968. Introduction. RC Lewontin (ed.), Population Biology and Evolution. Syracuse:Syracuse University Press, pp. 1–4.Google Scholar
  64. Love, A.C. 2009. Marine Invertebrates, Model Organisms, and the Modern Synthesis: Epistemic values, Evo-Devo, and Exclusion. Theory in Biosciences 128 (1): 19–42.CrossRefGoogle Scholar
  65. MacArthur, R.H. 1965. Ecological Consequences of Natural Selection. TH Waterman, H Morowitz (eds.), Theoretical and Mathematical Biology. New York:Blaisdell, pp. 388–397.Google Scholar
  66. Maynard Smith, J. 1958. The Theory of Evolution. London:Penguin Books.Google Scholar
  67. Maynard Smith, J. 1984. Palaeontology at the High Table. Nature 309 (5967): 401–402.CrossRefGoogle Scholar
  68. Maynard Smith, J. 1985. In Haldane’s Footsteps. DA Dewsbury (ed.), Studying Animal Behavior: Autobiographies of the Founders. Chicago:University of Chicago Press, pp. 347–354.Google Scholar
  69. Maynard Smith, J, and G.A. Parker. 1976. The Logic of Asymmetric Contests. Animal Behaviour 24 (1): 159–175.CrossRefGoogle Scholar
  70. Maynard Smith, J., and G.R. Price. 1973. The Logic of Animal Conflict. Nature 246: 15–18.CrossRefGoogle Scholar
  71. Mayr, E. 1958. Behavior and Systematics. AE Roe, GG Simpson (eds.), Behavior and Evolution. New Haven:Yale University Press, pp. 341–362.Google Scholar
  72. Mayr, E. 1959. Where Are We? Genetics and Twentieth Century Darwinism. In Cold Spring Harbor Symposia on Quantitative Biology 24: 1–14. Cold Spring Harbor, N.Y.: The Biological Laboratory.Google Scholar
  73. Mayr, E. 1961. Cause and Effect in Biology. Science 134 (3489): 1501–1506.CrossRefGoogle Scholar
  74. Mayr, E. 1983. How to Carry out the Adaptationist Program? The American Naturalist 121 (3): 324–334.CrossRefGoogle Scholar
  75. Mayr, E., and W.B. Provine (eds.). 1981. The Evolutionary Synthesis: Perspectives on the Unification of Biology. Cambridge:Harvard University Press.Google Scholar
  76. Milam, E.L. 2009. “The Experimental Animal from the Naturalist’s Point of View”: Behavior and Evolution at the American Museum of Natural History, 1928-1954. Transactions of the American Philosophical Society 99 (1): 157–178.Google Scholar
  77. Milam, E.L. 2010a. Looking for a Few Good Males: Female Choice in Evolutionary Biology. Baltimore:The John Hopkins University Press.Google Scholar
  78. Milam, E.L. 2010b. The Equally Wonderful Field: Ernst Mayr and Organismic Biology. Historical Studies of the Natural Sciences 40 (3): 279–317.CrossRefGoogle Scholar
  79. Mitman, G. 1992. The State of Nature: Ecology, Community, and American Social Thought, 1900-1950. Chicago:University of Chicago Press.Google Scholar
  80. Nesse, R.M. 2013. Tinbergen’s Four Questions, Organized: A Response to Bateson and Laland. Trends in Ecology & Evolution 28 (12): 681–682.CrossRefGoogle Scholar
  81. Okasha, S. 2005. Maynard Smith on the Levels of Selection Question. Biology and Philosophy 20 (5): 989–1010.CrossRefGoogle Scholar
  82. Orgel, L.E, and F.H. Crick 1980. Selfish DNA: The Ultimate Parasite. Nature 284 (5757): 604–607.CrossRefGoogle Scholar
  83. Parker, G.A. 1974. Assessment Strategy and Evolution of Fighting Behavior. Journal of Theoretical Biology 47: 223–243.CrossRefGoogle Scholar
  84. Parker, G.A. 2010. Reflections Before Dusk. L Drickamer, D Dewsbury (eds.), Leaders in Animal Behavior: the Second Generation. Cambridge:Cambridge University Press, pp. 429–463.Google Scholar
  85. Parker, G.A. 2013. Foreword: A Personal History of the Development of Animal Contest Theory and its Role in the 1970’s. ICW Hardy, M Briffa (eds.), Animal Contests. Cambridge:Cambridge University Press, pp. xi–xx.CrossRefGoogle Scholar
  86. Pigliucci, M., and G.B. Müller. 2008. eds. Evolution, the Extended Synthesis, Cambridge (Ms.): MIT Press.Google Scholar
  87. Price, G.R. 1970. Selection and Covariance. Nature 227: 520–521.CrossRefGoogle Scholar
  88. Queller, D.C, and K.F. Goodnight. 1989. Estimating Relatedness Using Genetic Markers. Evolution 43 (2): 258–275.CrossRefGoogle Scholar
  89. Queller, D.C, and J. Strassmann. 1988. Reproductive Success and Group Nesting in the Paper Wasp Polistes annularis. TH Clutton-Brock (ed.), Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems. Chicago:University of Chicago Press, pp. 76–96.Google Scholar
  90. Radick, G. 2017. Animal Agency in the Age of the Modern Synthesis: W. H. Thorpe’s Example. British Journal of the History of Science: Themes 2: 35–56.Google Scholar
  91. Roe, A.E., and G.G. Simpson (eds.). 1958. Behavior and Evolution. New Haven:Yale University Press.Google Scholar
  92. Romer, A.S. 1958. Phylogeny and Behavior with Special Reference to Vertebrate Evolution. AE Roe, GG Simpson (eds.), Behavior and Evolution. New Haven:Yale University Press, pp. 48–75.Google Scholar
  93. Schwartz, J. 2002. Population Genetics and Sociobiology: Conflicting Views of Evolution. Perspectives in Biology and Medicine 45 (2): 224–240.CrossRefGoogle Scholar
  94. Segerstrale, U. 2000. Defenders of the Truth: The Sociobiology Debate. Oxford:Oxford University Press.Google Scholar
  95. Simpson, G.G. 1958a. The Study of Evolution: Methods and Present Status of Theory. AE Roe, GG Simpson (eds.), Behavior and Evolution. New Haven:Yale University Press, pp. 7–26.Google Scholar
  96. Simpson, G.G. 1958b. Behavior and Evolution. AE Roe, GG Simpson (eds.), Behavior and Evolution. New Haven:Yale University Press, pp. 507–536.Google Scholar
  97. Simpson, G.G. 1978. Concession to the Improbable. An Unconventional Autobiography. New Haven and London:Yale University Press.Google Scholar
  98. Slobodkin, L.B. 1966. The Light and the Way in Evolution. The Quarterly Review of Biology 41 (2): 191–194.CrossRefGoogle Scholar
  99. Stebbins, G.L. 1950. Variation and Evolution in Plants. New York:Columbia Biological Series.Google Scholar
  100. Sterner, B, Lidgard, S. 2018. Moving Past the Systematics Wars. Journal of the History of Biology 51 (1): 31–67.CrossRefGoogle Scholar
  101. Strassmann, J.E. 2014. Tribute to Tinbergen: The Place of Animal Behavior in Biology. Ethology 120 (2): 123–126.CrossRefGoogle Scholar
  102. Taylor, P.D, Jonker, L.B. 1978. Evolutionary Stable Strategies and Game Dynamics. Mathematical Biosciences 40 (1–2): 145–156.CrossRefGoogle Scholar
  103. Tinbergen, N. 1963. On Aims and Methods of Ethology. Ethology 20 (4): 410–433.Google Scholar
  104. Trivers, R.L. 1971. The Evolution of Reciprocal Altruism. The Quarterly Review of Biology 46 (1): 35–57.CrossRefGoogle Scholar
  105. Trivers, R.L. 2002. Natural Selection and Social Theory: Selected Papers of Robert Trivers. Oxford:Oxford University Press.Google Scholar
  106. Von Frisch, K. 1976. Foreword. Behavioral Ecology and Sociobiology 1.Google Scholar
  107. West, S.A, A.S. Griffin, A. Gardner, and S.P. Diggle. 2006. Social Evolution Theory for Microorganisms. Nature Reviews Microbiology 4(8): 597–607.CrossRefGoogle Scholar
  108. Williams, G.C. 1966a. Adaptation and Natural Selection. A Critique of Some Current Evolutionary Thought. Princeton:Princeton University Press.Google Scholar
  109. Williams, G.C. 1966b. Natural Selection, the Costs of Reproduction, and a Refinement of Lack’s Principle. The American Naturalist 100 (916): 687–690.CrossRefGoogle Scholar
  110. Williams, G.C. (ed.). 1971. Group Selection. Chicago:Aldine Atherton.Google Scholar
  111. Wilson, E.O. 1971a. The Insect Societies. Cambridge:Belknap Press of Harvard University Press.Google Scholar
  112. Wilson, E.O. 1971b. The Prospects for a Unified Sociobiology. American Scientist 59 (4): 400–403.Google Scholar
  113. Wilson, E.O. 1975. Sociobiology: The New Synthesis. Cambridge:Belknap Press of Harvard University Press.Google Scholar
  114. Wynne-Edwards, V.C. 1962. Animal Dispersion: in Relation to Social Behavior. Edinburgh:Oliver and Boyd.Google Scholar

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Authors and Affiliations

  1. 1.Department of History and Philosophy of ScienceUniversity of CambridgeCambridgeUK

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