Inclusive fitness theory and eusociality

Journal name:
Nature
Volume:
471,
Pages:
E1–E4
Date published:
DOI:
doi:10.1038/nature09831
Received
Accepted
Published online

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson Nature 466, 10571062 (2010); Nowak et al. reply

Nowak et al.1 argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

References

  1. Nowak, M. A., Tarnita, C. E. & Wilson, E. O. The evolution of eusociality. Nature 466, 10571062 (2010)
  2. Hamilton, W. D. The genetical evolution of social behaviour, I & II. J. Theor. Biol. 7, 152 (1964)
  3. Hamilton, W. D. Selfish and spiteful behaviour in an evolutionary model. Nature 228, 12181220 (1970)
  4. Grafen, A. Optimisation of inclusive fitness. J. Theor. Biol. 238, 541563 (2006)
  5. Frank, S. A. Foundations of Social Evolution (Princeton Univ. Press, 1998)
  6. Gardner, A., West, S. A. & Barton, N. H. The relation between multilocus population genetics and social evolution theory. Am. Nat. 169, 207226 (2007)
  7. Rousset, F. Genetic Structure and Selection in Subdivided Populations (Princeton Univ. Press, 2004)
  8. Queller, D. C. A general model for kin selection. Evolution 46, 376380 (1992)
  9. Krebs, J. R. & Davies, N. B. Behavioural Ecology. An Evolutionary Approach 4th edn (Blackwell Scientific, 1997)
  10. Foster, K. R. A defense of sociobiology. Cold Spring Harb. Symp. Quant. Biol. 74, 403418 (2009)
  11. Westneat, D. F. & Fox, C. W. Evolutionary Behavioral Ecology (Oxford Univ. Press, 2010)
  12. Hardy, I. C. W. Sex Ratios: Concepts and Research Methods (Cambridge Univ. Press, 2002)
  13. West, S. A. Sex Allocation (Princeton Univ. Press, 2009)
  14. Queller, D. C. & Strassmann, J. E. Kin selection and social insects. Bioscience 48, 165175 (1998)
  15. Boomsma, J. J. Lifetime monogamy and the evolution of eusociality. Phil. Trans. R. Soc. Lond. B 364, 31913207 (2009)
  16. Ratnieks, F. L. W., Foster, K. R. & Wenseleers, T. Conflict resolution in insect societies. Annu. Rev. Entomol. 51, 581608 (2006)

Download references

Author information

Affiliations

  1. Vanderbilt University, Nashville, Tennessee 37235, USA

    • Patrick Abbot
  2. Laboratory of Applied Entomology, Faculty of Agriculture, Shizuoka University, Sizuoka 422-8529, Japan

    • Jun Abe
  3. School of Life Sciences, PO Box 874501, Arizona State University, Tempe, Arizona 85287-4501, USA

    • John Alcock
  4. UMR CNRS-IRD 2724, Genetics and Evolution of Infectious Diseases, IRD, 911 Avenue Agropolis, B.P. 64501, 34394 Montpellier Cedex 5, France

    • Samuel Alizon &
    • Yannis Michalakis
  5. Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK

    • Joao A. C. Alpedrinha,
    • Jay M. Biernaskie,
    • Sam Brown,
    • Angus Buckling,
    • Max N. Burton-Chellew,
    • Claire El Mouden,
    • Kevin Foster,
    • Andy Gardner,
    • Alan Grafen,
    • Paul H. Harvey,
    • Natalie Jiricny,
    • Alex Kacelnik,
    • Lorenzo Santorelli &
    • Stuart A. West
  6. Department of Zoology, University of Gothenburg, SE 405 30 Gothenburg, Sweden

    • Malte Andersson
  7. CNRS, Université Pierre et Marie Curie, Ecole Normale Supérieure, UMR 7625, Ecologie and Evolution, 75005 Paris, France

    • Jean-Baptiste Andre,
    • Minus van Baalen &
    • Thibaud Monnin
  8. MRC Centre for Outbreak Analysis and Modelling, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College, St Mary’s Campus, Norfolk Place, London W2 1PG, UK

    • Francois Balloux
  9. Department of Psychology, Neuroscience and Behaviour, McMaster University, 1280 Main St West, Hamilton, Ontario L8S 4K1, Canada

    • Sigal Balshine
  10. IST Austria, Am Campus 1, Klosterneuburg 3400, Austria

    • Nick Barton
  11. Evolutionary Genetics, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, NL-9750 AA Haren, The Netherlands

    • Leo W. Beukeboom
  12. Aarhus University, Department of Biological Sciences, Ny Munkegade 1540, 8000 Aarhus C, Denmark

    • Trine Bilde
  13. Department of Biology, University of Maryland, College Park, Maryland 20742-4415, USA

    • Gerald Borgia
  14. Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309-0334, USA

    • Michael Breed
  15. Faculté des sciences, Rue Emile-Argand 11, Case postale 158, 2000 Neuchâtel, Switzerland

    • Redouan Bshary &
    • Laurent Lehmann
  16. Department of Ecology and Evolutionary Biology, University of California, 321 Steinhaus Hall, Irvine, California 92697-2525, USA

    • Nancy T. Burley
  17. Centre for Ecology and Conservation, University of Exeter, Cornwall, Tremough, Penryn TR10 9EZ, UK

    • Michael A. Cant,
    • Sasha R. X. Dall,
    • Allen J. Moore &
    • Andrew J. Young
  18. Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland

    • Michel Chapuisat
  19. Department of Biology, 167 Castetter Hall, MSC03 2020, 1 University of New Mexico, Albuquerque, New Mexico 87131-000, USA

    • Eric L. Charnov
  20. Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK

    • Tim Clutton-Brock,
    • William A. Foster &
    • Rufus A. Johnstone
  21. Evolution, Ecology and Genetics, Research School of Biology, Australian National University, Canberra, ACT 0200, Australia

    • Andrew Cockburn &
    • Hanna Kokko
  22. Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204-5001, USA

    • Blaine J. Cole &
    • Diane C. Wiernasz
  23. Institutes of Evolution, Immunology and Infection Research, School of Biological Sciences, Ashworth Laboratories, University of Edinburgh, Edinburgh EH9 3JT, UK

    • Nick Colegrave &
    • Sarah E. Reece
  24. Department of Psychology, University of California, Santa Barbara, Santa Barbara, California 93106-9660, USA

    • Leda Cosmides
  25. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08540, USA

    • Iain D. Couzin
  26. Department of Ecology and Evolution, The University of Chicago, 1101 E. 57 Street, Chicago, Illinois 60637, USA

    • Jerry A. Coyne
  27. Department of Ecology, Montana State University, Bozeman, Montana 59717, USA

    • Scott Creel
  28. Department of Biosciences, 8888 University Drive, Simon Fraser University, Burnaby, British Columbia V5A1S6, Canada

    • Bernard Crespi
  29. Department of Biology, Villanova University, 800 Lancaster Avenue, Villanova, Pennsylvania 19085, USA

    • Robert L. Curry
  30. Department of Mathematics and Statistics, Queen’s University, Kingston, Ontario K7L 3N6, Canada

    • Troy Day &
    • Peter Taylor
  31. The Cornell Laboratory of Ornithology, Cornell University — The Johnson Center, 159 Sapsucker Woods Road, Ithaca, New York 14850, USA

    • Janis L. Dickinson
  32. Department of Biology, University of Louisville, Louisville, Kentucky 40292, USA

    • Lee Alan Dugatkin
  33. Seeley G. Mudd Hall, Department of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853, USA

    • Stephen T. Emlen,
    • Hudson K. Reeve,
    • Janet Shellmann-Sherman &
    • Paul W. Sherman
  34. USDA-ARS Bee Research Laboratory, BARC-E Bldg 476, Beltsville, Maryland 20705, USA

    • Jay Evans
  35. Laboratoire Ecologie and Evolution, CNRS UMR 7625, Ecole Normale Superieure, 46 rue d’Ulm, 75005 Paris, France; Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, USA

    • Regis Ferriere
  36. School of Life Sciences, John Maynard Smith Building, University of Sussex, Brighton BN1 9QG, UK

    • Jeremy Field
  37. Department Biologie II Behavioral Ecology (Verhaltensökologie), Ludwig-Maximilians-Universität, München Großhaderner Str. 2 D - 82152 Planegg/Martinsried, Germany

    • Susanne Foitzik
  38. Department of Entomology, University of Kentucky, Lexington, Kentucky 40546-0091, USA

    • Charles W. Fox
  39. School of Life Sciences, Arizona State University, PO Box 874501, Tempe, Arizona 85287-4501, USA

    • Juergen Gadau
  40. CEFE - UMR 5175, 1919 route de Mende, F-34293 Montpellier Cedex 5, France

    • Sylvain Gandon
  41. School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, South Australia 5001, Australia

    • Michael G. Gardner &
    • Michael P. Schwarz
  42. Kellogg Biological Station and Department of Zoology, Michigan State University, Hickory Corners, Michigan 49060, USA

    • Thomas Getty
  43. School of Biology and Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, 310 Ferst Drive, Atlanta, Georgia 30332-0230, USA

    • Michael A. D. Goodisman
  44. Department of Evolution and Ecology, College of Biological Sciences, 1 Shields Avenue, UC Davis, Davis, California 95616, USA

    • Rick Grosberg
  45. Center for Pollinator Research, Huck Institutes of the Life Sciences, Pennsylvania State University, Chemical Ecology Lab 4A, University Park, Pennsylvania 16802, USA

    • Christina M. Grozinger
  46. Muséum National d’Histoire Naturelle, CP39, 12 rue Buffon, 75005 Paris, France

    • Pierre-Henri Gouyon
  47. Biology Department, University of Toronto, 3359 Mississauga Road, Mississauga, Ontario L5L 1C6, Canada

    • Darryl Gwynne
  48. Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK

    • Ben J. Hatchwell
  49. Biologie I, Universität Regensburg, D-93040 Regensburg, Germany

    • Jürgen Heinze
  50. Department of Biosciences, PL 65 (Viikinkaari 1), FI-00014 University of Helsinki, Finland

    • Heikki Helantera &
    • Liselotte Sundström
  51. Department of Biology, University of Vermont, Burlington, Vermont 05405, USA

    • Ken R. Helms
  52. School of Human Evolution and Social Change, Arizona State University, Tempe, Arizona 85287-2402, USA

    • Kim Hill
  53. Department of Animal Ecology, Institute of Ecological Science, Faculty of Earth and Life Sciences, Vrije Universiteit, De Boelelaan 1085, NL-1081 HV Amsterdam, The Netherlands

    • E. Toby Kiers
  54. Animal Ecology Group, Centre for Evolutionary and Ecological Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands

    • Jan Komdeur
  55. University of Osnabrueck, Barbarastr.11, D-49076 Osnabrueck, Germany

    • Judith Korb
  56. Harvard University, Museum of Comparative Zoology, 26 Oxford St, Cambridge, Massachusetts 02138, USA

    • Daniel Kronauer
  57. Environmental Microbiology, Swiss Federal Institute of Aquatic Research and Technology, Überlandstrasse 133, CH-8600 Dübendorf, Switzerland

    • Rolf Kümmerli
  58. Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark

    • Timothy A. Linksvayer &
    • Jes S. Pedersen
  59. School of Biological Sciences, Royal Holloway, University of London, Egham TW20 0EX, UK

    • Sébastien Lion
  60. Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, California 95064, USA

    • Bruce Lyon
  61. Department of Computer Science, University of Sheffield, Sheffield S1 4DP, UK

    • James A. R. Marshall
  62. Department of Anthropology and Center for Population Biology, UC Davis, Davis, California 95616, USA

    • Richard McElreath
  63. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, USA

    • Richard E. Michod
  64. Department of Zoology, 730 Van Vleet Oval, University of Oklahoma, Norman, Oklahoma 73019, USA

    • Douglas Mock
  65. Department of Biology, Queen’s University, Kingston, Ontario K7L 3N6, Canada

    • Robert Montgomerie
  66. Integrative Biology, University of Texas at Austin, 1 University Station C0930, Austin, Texas 78712, USA

    • Ulrich G. Mueller
  67. Psychologie — Université de Strasbourg, Ethologie des Primates — DEPE (IPHC CNRS UMR 7178), 23 rue Becquerel — Strasbourg 67087, Cedex, France

    • Ronald Noë
  68. Department of Philosophy, University of Bristol, Bristol BS8 1TB, UK

    • Samir Okasha
  69. Biocenter Oulu and Department of Biosciences, University of Helsinki, Box 65, 00140 University of Helsinki, Finland

    • Pekka Pamilo
  70. Institute of Integrative Biology, Biosciences Building, Crown Street, University of Liverpool, Liverpool L69 7ZB, UK

    • Geoff A. Parker
  71. Theoretical Biology group, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands

    • Ido Pen
  72. Department of Biology, CB#3280, Coker Hall, University of North Carolina, Chapel Hill, NC 27599-3280, USA

    • David Pfennig
  73. Department of Ecology and Evolutionary Biology, Rice University, Houston, Texas 77005-1892, USA

    • David C. Queller &
    • Jeff Smith
  74. Department of Biochemistry, University of Zurich, Building Y27, Office J-46, Winterthurstrasse 190, CH-8057 Zurich, Switzerland; Swiss Institute of Bioinformatics, Quartier Sorge Bâtiment Génopode, CH- 1015 Lausanne, Switzerland

    • Daniel J. Rankin
  75. Research Department of Genetics, Evolution and Environment, Faculty of Life Sciences, University College London, 4 Stephenson Way, London NW1 2HE, UK

    • Max Reuter
  76. Centre for Behaviour and Evolution, Institute of Neuroscience, Faculty of Medical Sciences, Newcastle University, Henry Wellcome Building, Framlington Place, Newcastle upon Tyne NE2 4HH, UK

    • Gilbert Roberts
  77. School of Marine and Tropical Biology, James Cook University, Queensland 4811, Australia

    • Simon K. A. Robson
  78. Station Biologique de Roscoff, CNRS-UPMC UMR 7144, 29680 Roscoff, France

    • Denis Roze
  79. Institut des Sciences de l’Evolution, University of Montpellier 2, Montpellier 34095, France

    • Francois Rousset
  80. Department of Biology, University of North Carolina at Greensboro, 312 Eberhart Building, Greensboro, North Carolina 27403, USA

    • Olav Rueppell
  81. Department of Biology, 3314 Spieth Hall, University of California — Riverside, Riverside, California 92521, USA

    • Joel L. Sachs
  82. ETH Zurich, Institute of Integrative Biology (IBZ), Universitätsstrasse 16, CH.8092 Zürich, Switzerland

    • Paul Schmid-Hempel
  83. School of Philosophy, Psychology and Language Sciences, University of Edinburgh, 3 Charles Street, Edinburgh EH8 9AD, UK

    • Tom Scott-Phillips
  84. School of Biology, University of St Andrews, Harold Mitchell Building, St Andrews, Fife KY16 9TH, UK

    • David M. Shuker
  85. William Paterson University of New Jersey, 300 Pompton Road, Wayne, New Jersey 07470, USA

    • Joseph C. Spagna
  86. Department of Anthropology, 101 West Hall, University of Michigan, Ann Arbor, Michigan 48109, USA

    • Beverly Strassmann
  87. Department of Entomology and Department of Animal Biology, University of Illinois, Urbana, Illinois 61801, USA

    • Andrew V. Suarez
  88. Behavioural Ecology, Institute of Ecology and Evolution, University of Bern, Wohlenstrasse 50a, CH-3032 Hinterkappelen, Switzerland

    • Michael Taborsky
  89. Department of Biology, University of Western Ontario, 1151 Richmond Street North, London, Ontario N6A 5B7, Canada

    • Graham Thompson
  90. Department of Anthropology, University of California, Santa Barbara, California 93106-3210, USA

    • John Tooby
  91. Deptartment of Environmental Science, Policy and Management, 130 Mulford Hall, 3114, University of California Berkeley, Berkeley, California 94720-3114, USA

    • Neil D. Tsutsui
  92. Faculty of Agriculture, University of the Ryukyus, Okinawa 903-0213, Japan

    • Kazuki Tsuji
  93. Dipartimento di Biologia Evoluzionistica, Università degli Studi di Firenze, via Romana 17, 50125 Firenze, Italy

    • Stefano Turillazzi
  94. Department of Ecology and Evolutionary Biology, University of Tennessee Knoxville, Knoxville, Tennessee 37902, USA

    • Francisco Úbeda
  95. Department of Entomology, Box 7613, North Carolina State University, Raleigh, North Carolina 27695-7613, USA

    • Edward L. Vargo
  96. Institute for Theoretical Biology, Humboldt University zu Berlin, Invalidenstr. 43, D-10115 Germany

    • Bernard Voelkl
  97. Departmet of Biology, Zoological Institute, K.U. Leuven, Naamsestraat 59, B-3000 Leuven, Belgium

    • Tom Wenseleers
  98. Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Panamá

    • Mary Jane West-Eberhard
  99. Department of Biology, 101 Morgan Building, University of Kentucky, Lexington, Kentucky 40506-0225, USA

    • David F. Westneat
  100. Department of Applied Mathematics, University of Western Ontario, 1151 Richmond Street North, London, Ontario N6A 5B7, Canada

    • Geoff Wild
  101. Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA

    • Richard Wrangham
  102. Department of Biology and Program in Ecology, Evolution and Conservation Biology, University of Nevada, Reno, Nevada 89557, USA

    • David W. Zeh &
    • Jeanne A. Zeh
  103. Department of Biology, San Francisco State University, San Francisco, California 94132, USA

    • Andrew Zink

Contributions

All authors contributed to the planning, writing and/or revising of this paper. Several others who contributed significantly are not listed because they are named on separate comments.

Competing financial interests

Competing financial interests: declared none.

Corresponding author

Correspondence to:

Author details

Additional data