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The evolution of eusociality

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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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.

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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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