Division of labour is a common feature of social groups, from biofilms to complex animal societies. However, we lack a theoretical framework that can explain why division of labour has evolved on certain branches of the tree of life but not others. Here, we model the division of labour over a cooperative behaviour, considering both when it should evolve and the extent to which the different types should become specialized. We found that: (1) division of labour is usually—but not always—favoured by high efficiency benefits to specialization and low within-group conflict; and (2) natural selection favours extreme specialization, where some individuals are completely dependent on the helping behaviour of others. We make a number of predictions, several of which are supported by the existing empirical data, from microbes and animals, while others suggest novel directions for empirical work. More generally, we show how division of labour can lead to mutual dependence between different individuals and hence drive major evolutionary transitions, such as those to multicellularity and eusociality.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Nature Communications Open Access 24 November 2022
Nature Communications Open Access 27 April 2022
Nature Communications Open Access 25 January 2022
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Rent or buy this article
Prices vary by article type
Prices may be subject to local taxes which are calculated during checkout
Maynard Smith, J. & Szathmary, E. The Major Transitions in Evolution (Oxford Univ. Press, Oxford, 1997).
Bourke, A. F. Principles of Social Evolution (Oxford Univ. Press, Oxford, 2011).
Boomsma, J. J. Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17, R673–R683 (2007).
West, S. A., Fisher, R. M., Gardner, A. & Kiers, E. T. Major evolutionary transitions in individuality. Proc. Natl Acad. Sci. USA 112, 10112–10119 (2015).
Queller, D. C. Relatedness and the fraternal major transitions. Phil. Trans. R. Soc. Lond. B 355, 1647–1655 (2000).
Michod, R. E., Viossat, Y., Solari, C. A., Hurand, M. & Nedelcu, A. M. Life-history evolution and the origin of multicellularity. J. Theor. Biol. 239, 257–272 (2006).
Oster, G. F. & Wilson, E. O. Caste and Ecology in the Social Insects. (Princeton Univ. Press: Princeton, 1978).
Wilson, E. O. The ergonomics of caste in the social insects. Am. Nat. 102, 41–66 (1968).
Willensdorfer, M. On the evolution of differentiated multicellularity. Evolution 63, 306–323 (2009).
Rossetti, V., Schirrmeister, B. E., Bernasconi, M. V. & Bagheri, H. C. The evolutionary path to terminal differentiation and division of labor in cyanobacteria. J. Theor. Biol. 262, 23–34 (2010).
Ispolatov, I., Ackermann, M. & Doebeli, M. Division of labour and the evolution of multicellularity. Proc. R.Soc. B 279, 1768–1776 (2012).
Solari, C. A., Kessler, J. O. & Goldstein, R. E. A general allometric and life-history model for cellular differentiation in the transition to multicellularity. Am. Nat. 181, 369–380 (2013).
Rueffler, C., Hermisson, J. & Wagner, G. P. Evolution of functional specialization and division of labor. Proc. Natl Acad. Sci. USA 109, E326–E335 (2012).
Tannenbaum, E. When does division of labor lead to increased system output? J. Theor. Biol. 247, 413–425 (2007).
Michod, R. E. Evolution of individuality during the transition from unicellular to multicellular life. Proc. Natl Acad. Sci. USA 104, 8613–8618 (2007).
West, S. A. & Cooper, G. A. Division of labour in microorganisms: an evolutionary perspective. Nat. Rev. Microbiol. 14, 716–723 (2016).
Arnold, K. E., Owens, I. P. & Goldizen, A. W. Division of labour within cooperatively breeding groups. Behaviour 142, 1577–1590 (2005).
Hamilton, W. D. The genetical evolution of social behaviour. I and II. J. Theor. Biol. 7, 1–52 (1964).
Ackermann, M. et al. Self-destructive cooperation mediated by phenotypic noise. Nature 454, 987–990 (2008).
Gardner, A. & Grafen, A. Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. 22, 659–671 (2009).
Michod, R. E. Evolution of the individual. Am. Nat. 150, S5–S21 (1997).
Frank, S. A. Foundations of Social Evolution. (Princeton Univ. Press: Princeton, 1998).
Parker, G. A. & Smith, J. M. Optimality theory in evolutionary biology. Nature 348, 27–33 (1990).
Fisher, R. M., Cornwallis, C. K. & West, S. A. Group formation, relatedness, and the evolution of multicellularity. Curr. Biol. 23, 1120–1125 (2013).
Flores, E. & Herrero, A. Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat. Rev. Microbiol. 8, 39–50 (2010).
Herron, M. D., Hackett, J. D., Aylward, F. O. & Michod, R. E. Triassic origin and early radiation of multicellular volvocine algae. Proc. Natl Acad. Sci. USA 106, 3254–3258 (2009).
Strassmann, J. E., Zhu, Y. & Queller, D. C. Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408, 965–967 (2000).
Velicer, G. J., Kroos, L. & Lenski, R. E. Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404, 598–601 (2000).
Veening, J.-W. et al. Transient heterogeneity in extracellular protease production by Bacillus subtilis. Mol. Syst. Biol. 4, 184 (2008).
Herron, M. D. & Michod, R. E. Evolution of complexity in the volvocine algae: transitions in individuality through Darwin’s eye. Evolution 62, 436–451 (2008).
Koenig, W. D. & Dickinson, J. L. Ecology and Evolution of Cooperative Breeding in Birds (Cambridge Univ. Press, Cambridge, 2004).
Hughes, W. O., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216 (2008).
Cornwallis, C. K., West, S. A., Davis, K. E. & Griffin, A. S. Promiscuity and the evolutionary transition to complex societies. Nature 466, 969–972 (2010).
Lukas, D. & Clutton-Brock, T. Cooperative breeding and monogamy in mammalian societies. Proc. R. Soc. B 279, 2151–2156 (2012).
Bastiaans, E., Debets, A. J. & Aanen, D. K. Experimental evolution reveals that high relatedness protects multicellular cooperation from cheaters. Nat. Commun. 7, 11435 (2016).
Kuzdzal-Fick, J. J., Fox, S. A., Strassmann, J. E. & Queller, D. C. High relatedness is necessary and sufficient to maintain multicellularity in Dictyostelium. Science 334, 1548–1551 (2011).
Giron, D., Dunn, D. W., Hardy, I. C. & Strand, M. R. Aggression by polyembryonic wasp soldiers correlates with kinship but not resource competition. Nature 430, 676–679 (2004).
Nonacs, P. Monogamy and high relatedness do not preferentially favor the evolution of cooperation. BMC Evol. Biol. 11, 58 (2011).
Olejarz, J. W., Allen, B., Veller, C. & Nowak, M. A. The evolution of non-reproductive workers in insect colonies with haplodiploid genetics. eLife 4, e08918 (2015).
Leggett, H. C., El Mouden, C., Wild, G. & West, S. Promiscuity and the evolution of cooperative breeding. Proc. R. Soc. B 279, 1405–1411 (2012).
Davies, N. G. & Gardner, A. Monogamy promotes altruistic sterility in insect societies. R. Soc. Open Sci. 5, 172190 (2018).
Gavrilets, S. Rapid transition towards the division of labor via evolution of developmental plasticity. PLoS Comput. Biol. 6, e1000805 (2010).
Lehmann, L. & Rousset, F. How life history and demography promote or inhibit the evolution of helping behaviours. Phil. Trans. R. Soc. B 365, 2599–2617 (2010).
Seger, J. Partial bivoltinism may cause alternating sex-ratio biases that favour eusociality. Nature 301, 59–62 (1983).
Quiñones, A. E. & Pen, I. A unified model of hymenopteran preadaptations that trigger the evolutionary transition to eusociality. Nat. Commun. 8, 15920 (2017).
Bonner, J. T. Perspective: the size-complexity rule. Evolution 58, 1883–1890 (2004).
Taylor, P. D. & Frank, S. A. How to make a kin selection model. J. Theor. Biol. 180, 27–37 (1996).
Brown, S. P. & Taylor, P. D. Joint evolution of multiple social traits: a kin selection analysis. Proc. R. Soc. B 277, 415–422 (2010).
Diard, M. et al. Stabilization of cooperative virulence by the expression of an avirulent phenotype. Nature 494, 353–356 (2013).
The authors thank the following people for helpful discussion and comments on the manuscript: S. Levin, M. dos Santos, J. Biernaskie, A. Griffin, C. Cornwallis, P. Taylor, K. Boomsma, D. Unterwegger, K. Foster, G. Wild, A. Grafen, G. Taylor, T. Kiers and R. Fisher. We acknowledge the use of the University of Oxford Advanced Research Computing (ARC) facility in carrying out this work. G.A.C. is funded by the Engineering and Physical Sciences Research Council (EP/F500394/1).
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Cooper, G.A., West, S.A. Division of labour and the evolution of extreme specialization. Nat Ecol Evol 2, 1161–1167 (2018). https://doi.org/10.1038/s41559-018-0564-9
This article is cited by
Nature Communications (2022)
Nature Communications (2022)
Nature Communications (2022)
Nature Ecology & Evolution (2020)
Nest defence and offspring provisioning in a cooperative bird: individual subordinates vary in total contribution, but no division of tasks among breeders and subordinates
Behavioral Ecology and Sociobiology (2020)