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The evolution of eusociality

Nature volume 466, pages 1057–1062 (2010)Cite this article

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Abstract

Eusociality, in which some individuals reduce their own lifetime reproductive potential to raise the offspring of others, underlies the most advanced forms of social organization and the ecologically dominant role of social insects and humans. For the past four decades kin selection theory, based on the concept of inclusive fitness, has been the major theoretical attempt to explain the evolution of eusociality. Here we show the limitations of this approach. We argue that standard natural selection theory in the context of precise models of population structure represents a simpler and superior approach, allows the evaluation of multiple competing hypotheses, and provides an exact framework for interpreting empirical observations.

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Figure 1: The ultimate superorganisms.
Figure 2: Species on either side of the eusociality threshold.
Figure 3: The limitation of inclusive fitness.
Figure 4: Solitary and primitively eusocial wasps.

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References

  1. Hölldobler, B. & Wilson, E. O. The Ants (Harvard Univ. Press, 1990)

    Book  Google Scholar 

  2. Foster, K. R. & Ratnieks, F. L. W. A new eusocial vertebrate? Trends Ecol. Evol. 20, 363–364 (2005)

    Article  Google Scholar 

  3. Hamilton, W. D. The genetical evolution of social behaviour, I, II. J. Theor. Biol. 7, 1–16 (1964)

    Article  CAS  Google Scholar 

  4. Wilson, E. O. The Insect Societies (Harvard Univ. Press, 1971)

    Google Scholar 

  5. Wilson, E. O. Sociobiology: The New Synthesis (Harvard Univ. Press, 1975)

    Google Scholar 

  6. Wilson, E. O. One giant leap: how insects achieved altruism and colonial life. Bioscience 58, 17–25 (2008)

    Article  Google Scholar 

  7. Linksvayer, T. A. & Wade, M. J. The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: maternal effects, sib-social effects, and heterochrony. Q. Rev. Biol. 80, 317–336 (2005)

    Article  Google Scholar 

  8. Queller, D. C. & Strassmann, J. E. Kin selection and social insects. Bioscience 48, 165–175 (1998)

    Article  Google Scholar 

  9. Costa, J. T. The Other Insect Societies (Harvard Univ. Press, 2006)

    Google Scholar 

  10. Cole, B. J. & Wiernacz, D. C. The selective advantage of low relatedness. Science 285, 891–893 (1999)

    Article  CAS  Google Scholar 

  11. Hughes, W. O. H. & Boomsma, J. J. Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58, 1251–1260 (2004)

    Article  Google Scholar 

  12. Rheindt, F. E., Strehl, C. P. & Gadau, J. A genetic component in the determination of worker polymorphism in the Florida harvester ant Pogonomyrmex badius. Insectes Soc. 52, 163–168 (2005)

    Article  Google Scholar 

  13. Jones, J. C., Myerscough, M. R., Graham, S. & Oldroyd, B. P. Honey bee nest thermoregulation: diversity supports stability. Science 305, 402–404 (2004)

    Article  CAS  ADS  Google Scholar 

  14. Schwander, T., Rosset, H. & Chapuisat, M. Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors. Behav. Ecol. Sociobiol. 59, 215–221 (2005)

    Article  Google Scholar 

  15. Wilson, E. O. & Hölldobler, B. Eusociality: origin and consequence. Proc. Natl Acad. Sci. USA 102, 13367–13371 (2005)

    Article  CAS  ADS  Google Scholar 

  16. Fletcher, J. A., Zwick, M., Doebeli, M. & Wilson, D. S. What’s wrong with inclusive fitness? Trends Ecol. Evol. 21, 597–598 (2006)

    Article  Google Scholar 

  17. Traulsen, A. Mathematics of kin- and group-selection: formally equivalent? Evolution 64, 316–323 (2010)

    Article  Google Scholar 

  18. Doebeli, M. & Hauert, C. Limits to Hamilton’s rule. J. Evol. Biol. 19, 1386–1388 (2006)

    Article  CAS  Google Scholar 

  19. Wolf, J. B. & Wade, M. J. On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter? J. Evol. Biol. 14, 347–356 (2001)

    Article  Google Scholar 

  20. Grafen, A. in Behavioural Ecology Ch. 3 (eds Krebs, J. R. & Davies, N. B.) (Blackwell, 1984) 62–84.

  21. Frank, S. A. Foundations of Social Evolution (Princeton Univ. Press, 1998)

    Google Scholar 

  22. Rousset, F. Genetic Structure and Selection in Subdivided Populations (Princeton Univ. Press, 2004)

    Google Scholar 

  23. van Veelen, M. Group selection, kin selection, altruism and cooperation: when inclusive fitness is right and when it can be wrong. J. Theor. Biol. 259, 589–600 (2009)

    Article  MathSciNet  Google Scholar 

  24. Fletcher, J. A. & Doebeli, M. A simple and general explanation for the evolution of altruism. Proc. R. Soc. Lond. B 276, 13–19 (2009)

    Article  Google Scholar 

  25. West, S. A., Griffin, A. S. & Gardner, A. Evolutionary explanations for cooperation. Curr. Biol. 17, R661–R672 (2007)

    Article  CAS  Google Scholar 

  26. Nowak, M. A. Five rules for the evolution of cooperation. Science 314, 1560–1563 (2006)

    Article  CAS  ADS  Google Scholar 

  27. Ohtsuki, H., Hauert, C., Lieberman, E. & Nowak, M. A. A simple rule for the evolution of cooperation on graphs and social networks. Nature 441, 502–505 (2006)

    Article  CAS  ADS  Google Scholar 

  28. Traulsen, A. & Nowak, M. A. Evolution of cooperation by multilevel selection. Proc. Natl Acad. Sci. USA 103, 10952–10955 (2006)

    Article  CAS  ADS  Google Scholar 

  29. Taylor, P. D., Day, T. & Wild, G. Evolution of cooperation in a finite homogeneous graph. Nature 447, 469–472 (2007)

    Article  CAS  ADS  Google Scholar 

  30. Antal, T., Ohtsuki, H., Wakeley, J., Taylor, P. D. & Nowak, M. A. Evolution of cooperation by phenotypic similarity. Proc. Natl Acad. Sci. USA 106, 8597–8600 (2009)

    Article  CAS  ADS  Google Scholar 

  31. Tarnita, C. E., Antal, T., Ohtsuki, H. & Nowak, M. A. Evolutionary dynamics in set structured populations. Proc. Natl Acad. Sci. USA 106, 8601–8604 (2009)

    Article  CAS  ADS  Google Scholar 

  32. Tarnita, C. E., Ohtsuki, H., Antal, T., Fu, F. & Nowak, M. A. Strategy selection in structured populations. J. Theor. Biol. 259, 570–581 (2009)

    Article  MathSciNet  Google Scholar 

  33. Ohtsuki, H. & Nowak, M. A. Evolutionary games on cycles. Proc. R. Soc. Lond. B 273, 2249–2256 (2006)

    Article  Google Scholar 

  34. Grafen, A. An inclusive fitness analysis of altruism on a cyclical network. J. Evol. Biol. 20, 2278–2283 (2007)

    Article  CAS  Google Scholar 

  35. Hunt, J. H. The Evolution of Social Wasps (Oxford Univ. Press, 2007)

    Book  Google Scholar 

  36. Gadagkar, R. The Social Biology of Ropalidia marginata: Toward Understanding the Evolution of Eusociality (Harvard Univ. Press, 2001)

    Google Scholar 

  37. Thorne, B. L., Breisch, N. L. & Muscedere, M. L. Evolution of eusociality and the soldier caste in termites: influence of accelerated inheritance. Proc. Natl Acad. Sci. USA 100, 12808–12813 (2003)

    Article  CAS  ADS  Google Scholar 

  38. Khila, A. & Abouheif, E. Evaluating the role of reproductive constraints in ant social evolution. Phil. Trans. R. Soc. B 365, 617–630 (2010)

    Article  Google Scholar 

  39. Pepper, J. W. & Smuts, B. A mechanism for the evolution of altruism among nonkin: positive assortment through environmental feedback. Am. Nat. 160, 205–213 (2002)

    Article  Google Scholar 

  40. Fletcher, J. A. & Zwick, M. Strong altruism can evolve in randomly formed groups. J. Theor. Biol. 228, 303–313 (2004)

    Article  MathSciNet  Google Scholar 

  41. Wade, M. J. Group selections among laboratory populations of Tribolium. Proc. Natl Acad. Sci. USA 73, 4604–4607 (1976)

    Article  CAS  ADS  Google Scholar 

  42. Swenson, W., Wilson, D. S. & Elias, R. Artificial ecosystem selection. Proc. Natl Acad. Sci. USA 97, 9110–9114 (2000)

    Article  CAS  ADS  Google Scholar 

  43. Wade, M. J. et al. Multilevel and kin selection in a connected world. Nature 463, E8–E9 (2010)

    Article  CAS  ADS  Google Scholar 

  44. Clutton-Brock, T. Cooperation between non-kin in animal societies. Nature 462, 51–57 (2009)

    Article  CAS  ADS  Google Scholar 

  45. Johns, P. M., Howard, K. J., Breisch, N. L., Rivera, A. & Thorne, B. L. Nonrelatives inherit colony resources in a primitive termite. Proc. Natl Acad. Sci. USA 106, 17452–17456 (2009)

    Article  CAS  ADS  Google Scholar 

  46. Wilson, D. S. & Wilson, E. O. Rethinking the theoretical foundation of sociobiology. Q. Rev. Biol. 82, 327–348 (2007)

    Article  Google Scholar 

  47. Wilson, D. S. & Wilson, E. O. Evolution “for the good of the group.”. Am. Sci. 96, 380–389 (2008)

    Article  Google Scholar 

  48. Sakagami, S. F. & Maeta, Y. in Animals and Societies: Theories and Facts (eds Itô, Y., Brown, J. L. & Kikkawa, J.) (Japan Scientific Societies Press, 1987), 1–16.

  49. Wcislo, W. T. Social interactions and behavioral context in a largely solitary bee, Lasioglossum (Dialictus) figueresi (Hymenoptera, Halictidae). Insectes Soc. 44, 199–208 (1997)

    Article  Google Scholar 

  50. Jeanson, R., Kukuk, P. F. & Fewell, J. H. Emergence of division of labour in halictine bees: Contributions of social interactions and behavioural variance. Anim. Behav. 70, 1183–1193 (2005)

    Article  Google Scholar 

  51. Toth, A. L. et al. Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318, 441–444 (2007)

    Article  CAS  ADS  Google Scholar 

  52. Hunt, J. H. et al. A diapause pathway underlies the gyne phenotype in Polistes wasps, revealing an evolutionary route to caste-containing insect societies. Proc. Natl Acad. Sci. USA 104, 14020–14025 (2007)

    Article  CAS  ADS  Google Scholar 

  53. Hunt, J. H. & Amdam, G. V. Bivoltinism as an antecedent to eusociality in the paper wasp genus Polistes. Science 308, 264–267 (2005)

    Article  CAS  ADS  Google Scholar 

  54. Robinson, G. E. & Page, R. E. in The Genetics of Social Evolution (eds Breed, M. D. & Page, R. E. Jr) (Westview Press, 1989), 61–80.

  55. Bonabeau, E., Theraulaz, G. & Deneubourg, J. L. Quantitative study of the fixed threshold model for the regulation of division of labour in insect societies. Proc. R. Soc. Lond. B 263, 1565–1569 (1996)

    Article  ADS  Google Scholar 

  56. Abouheif, E. & Wray, G. A. Evolution of the gene network underlying wing polyphenism in ants. Science 297, 249–252 (2002)

    Article  CAS  ADS  Google Scholar 

  57. Ross, K. G. & Keller, L. Genetic control of social organization in an ant. Proc. Natl Acad. Sci. USA 95, 14232–14237 (1998)

    Article  CAS  ADS  Google Scholar 

  58. West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, 2003)

    Google Scholar 

  59. Duffy, J. E. in Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms (eds Duffy, J. E. & Thiel, M.) (Oxford Univ. Press, 2007), 387–409.

  60. Sakagami, S. F. & Hayashida, K. Biology of the primitively social bee, Halictus duplex Dalla Torre II. Nest structure and immature stages. Insectes Soc. 7, 57–98 (1960)

    Article  Google Scholar 

  61. Cowan, D. P. in The Social Biology of Wasps (eds Ross, K. G. & Mathews, R. W.) (Comstock Pub. Associates, 1991), 33–73.

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Acknowledgements

We thank K. M. Horton for advice and help in preparing the manuscript. M.A.N. and C.E.T. gratefully acknowledge support from the John Templeton Foundation, the NSF/NIH joint program in mathematical biology (NIH grant R01GM078986), the Bill and Melinda Gates Foundation (Grand Challenges grant 37874), and J. Epstein.

Author information

Authors and Affiliations

  1. Department of Mathematics, Department of Organismic and Evolutionary Biology, Program for Evolutionary Dynamics, Harvard University, Cambridge, 02138, Massachusetts, USA

    Martin A. Nowak & Corina E. Tarnita

  2. Museum of Comparative Zoology, Harvard University, Cambridge, 02138, Massachusetts, USA

    Edward O. Wilson

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  1. Martin A. Nowak
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  3. Edward O. Wilson
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Contributions

M.A.N., C.E.T. and E.O.W. collaborated on all aspects of this research project. C.E.T. led the development of the mathematical framework, presented in Part A of the Supplementary Information, which proves the foundational weakness of inclusive fitness theory.

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Correspondence to Martin A. Nowak.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Information in 3 parts comprising: Natural selection versus kin selection; Empirical tests re-examined and a Mathematical model for the origin of eusociality (see contents list for full details). Also included are Supplementary Figures 1-6 with legends and additional References. (PDF 649 kb)

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Nowak, M., Tarnita, C. & Wilson, E. The evolution of eusociality. Nature 466, 1057–1062 (2010). https://doi.org/10.1038/nature09205

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