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.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Scientific Reports Open Access 07 January 2022
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Hölldobler, B. & Wilson, E. O. The Ants (Harvard Univ. Press, 1990)
Foster, K. R. & Ratnieks, F. L. W. A new eusocial vertebrate? Trends Ecol. Evol. 20, 363–364 (2005)
Hamilton, W. D. The genetical evolution of social behaviour, I, II. J. Theor. Biol. 7, 1–16 (1964)
Wilson, E. O. The Insect Societies (Harvard Univ. Press, 1971)
Wilson, E. O. Sociobiology: The New Synthesis (Harvard Univ. Press, 1975)
Wilson, E. O. One giant leap: how insects achieved altruism and colonial life. Bioscience 58, 17–25 (2008)
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)
Queller, D. C. & Strassmann, J. E. Kin selection and social insects. Bioscience 48, 165–175 (1998)
Costa, J. T. The Other Insect Societies (Harvard Univ. Press, 2006)
Cole, B. J. & Wiernacz, D. C. The selective advantage of low relatedness. Science 285, 891–893 (1999)
Hughes, W. O. H. & Boomsma, J. J. Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58, 1251–1260 (2004)
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)
Jones, J. C., Myerscough, M. R., Graham, S. & Oldroyd, B. P. Honey bee nest thermoregulation: diversity supports stability. Science 305, 402–404 (2004)
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)
Wilson, E. O. & Hölldobler, B. Eusociality: origin and consequence. Proc. Natl Acad. Sci. USA 102, 13367–13371 (2005)
Fletcher, J. A., Zwick, M., Doebeli, M. & Wilson, D. S. What’s wrong with inclusive fitness? Trends Ecol. Evol. 21, 597–598 (2006)
Traulsen, A. Mathematics of kin- and group-selection: formally equivalent? Evolution 64, 316–323 (2010)
Doebeli, M. & Hauert, C. Limits to Hamilton’s rule. J. Evol. Biol. 19, 1386–1388 (2006)
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)
Grafen, A. in Behavioural Ecology Ch. 3 (eds Krebs, J. R. & Davies, N. B.) (Blackwell, 1984) 62–84.
Frank, S. A. Foundations of Social Evolution (Princeton Univ. Press, 1998)
Rousset, F. Genetic Structure and Selection in Subdivided Populations (Princeton Univ. Press, 2004)
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)
Fletcher, J. A. & Doebeli, M. A simple and general explanation for the evolution of altruism. Proc. R. Soc. Lond. B 276, 13–19 (2009)
West, S. A., Griffin, A. S. & Gardner, A. Evolutionary explanations for cooperation. Curr. Biol. 17, R661–R672 (2007)
Nowak, M. A. Five rules for the evolution of cooperation. Science 314, 1560–1563 (2006)
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)
Traulsen, A. & Nowak, M. A. Evolution of cooperation by multilevel selection. Proc. Natl Acad. Sci. USA 103, 10952–10955 (2006)
Taylor, P. D., Day, T. & Wild, G. Evolution of cooperation in a finite homogeneous graph. Nature 447, 469–472 (2007)
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)
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)
Tarnita, C. E., Ohtsuki, H., Antal, T., Fu, F. & Nowak, M. A. Strategy selection in structured populations. J. Theor. Biol. 259, 570–581 (2009)
Ohtsuki, H. & Nowak, M. A. Evolutionary games on cycles. Proc. R. Soc. Lond. B 273, 2249–2256 (2006)
Grafen, A. An inclusive fitness analysis of altruism on a cyclical network. J. Evol. Biol. 20, 2278–2283 (2007)
Hunt, J. H. The Evolution of Social Wasps (Oxford Univ. Press, 2007)
Gadagkar, R. The Social Biology of Ropalidia marginata: Toward Understanding the Evolution of Eusociality (Harvard Univ. Press, 2001)
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)
Khila, A. & Abouheif, E. Evaluating the role of reproductive constraints in ant social evolution. Phil. Trans. R. Soc. B 365, 617–630 (2010)
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)
Fletcher, J. A. & Zwick, M. Strong altruism can evolve in randomly formed groups. J. Theor. Biol. 228, 303–313 (2004)
Wade, M. J. Group selections among laboratory populations of Tribolium. Proc. Natl Acad. Sci. USA 73, 4604–4607 (1976)
Swenson, W., Wilson, D. S. & Elias, R. Artificial ecosystem selection. Proc. Natl Acad. Sci. USA 97, 9110–9114 (2000)
Wade, M. J. et al. Multilevel and kin selection in a connected world. Nature 463, E8–E9 (2010)
Clutton-Brock, T. Cooperation between non-kin in animal societies. Nature 462, 51–57 (2009)
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)
Wilson, D. S. & Wilson, E. O. Rethinking the theoretical foundation of sociobiology. Q. Rev. Biol. 82, 327–348 (2007)
Wilson, D. S. & Wilson, E. O. Evolution “for the good of the group.”. Am. Sci. 96, 380–389 (2008)
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.
Wcislo, W. T. Social interactions and behavioral context in a largely solitary bee, Lasioglossum (Dialictus) figueresi (Hymenoptera, Halictidae). Insectes Soc. 44, 199–208 (1997)
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)
Toth, A. L. et al. Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318, 441–444 (2007)
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)
Hunt, J. H. & Amdam, G. V. Bivoltinism as an antecedent to eusociality in the paper wasp genus Polistes. Science 308, 264–267 (2005)
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.
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)
Abouheif, E. & Wray, G. A. Evolution of the gene network underlying wing polyphenism in ants. Science 297, 249–252 (2002)
Ross, K. G. & Keller, L. Genetic control of social organization in an ant. Proc. Natl Acad. Sci. USA 95, 14232–14237 (1998)
West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, 2003)
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.
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)
Cowan, D. P. in The Social Biology of Wasps (eds Ross, K. G. & Mathews, R. W.) (Comstock Pub. Associates, 1991), 33–73.
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.
The authors declare no competing financial interests.
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)
About this article
Cite this article
Nowak, M., Tarnita, C. & Wilson, E. The evolution of eusociality. Nature 466, 1057–1062 (2010). https://doi.org/10.1038/nature09205
This article is cited by
Scientific Reports (2022)
Journal of Biosciences (2022)
Long-time behavior of a PDE replicator equation for multilevel selection in group-structured populations
Journal of Mathematical Biology (2022)