Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Division of labour in microorganisms: an evolutionary perspective

Abstract

The division of labour, whereby individuals within a group specialize in certain tasks, has long been appreciated as central to the evolution of complex biological societies. In recent years, several examples of division of labour in microorganisms have arisen, which suggests that this strategy may also be important in microbial species. In this Opinion article, we explore the set of conditions that define division of labour and propose that cooperation between different phenotypes is a defining feature of division of labour. Furthermore, we discuss how clarifying what constitutes division of labour highlights key evolutionary questions, including what form division of labour takes and why it is favoured by natural selection.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Division of labour.
Figure 2: Why divide labour?
Figure 3: How to divide?

References

  1. 1

    Lewis, K. Persister cells, dormancy and infectious disease. Nat. Rev. Microbiol. 5, 48–56 (2006).

    PubMed  Google Scholar 

  2. 2

    Veening, J.-W., Smits, W. K. & Kuipers, O. P. Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol. 62, 193–210 (2008).

    CAS  PubMed  Google Scholar 

  3. 3

    Ackermann, M. A functional perspective on phenotypic heterogeneity in microorganisms. Nat. Rev. Microbiol. 13, 497–508 (2015).

    CAS  PubMed  Google Scholar 

  4. 4

    Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L. & Leibler, S. Bacterial persistence as a phenotypic switch. Science 305, 1622–1625 (2004).

    CAS  PubMed  Google Scholar 

  5. 5

    Veening, J.-W. et al. Transient heterogeneity in extracellular protease production by Bacillus subtilis. Mol. Syst. Biol. 4, 1–15 (2008).

    Google Scholar 

  6. 6

    Claessen, D., Rozen, D. E., Kuipers, O. P., Søgaard-Andersen, L. & van Wezel, G. P. Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat. Rev. Microbiol. 12, 115–124 (2014).

    CAS  PubMed  Google Scholar 

  7. 7

    van Gestel, J., Vlamakis, H. & Kolter, R. in Microbial Biofilms 2nd edn (eds Ghannoum, M., Parsek, M., Whiteley, M. & Mukherjee, P.) 67–97 (ASM press, 2015).

    Google Scholar 

  8. 8

    Ghoul, M., Griffin, A. S. & West, S. A. Toward an evolutionary definition of cheating. Evolution 68, 318–331 (2014).

    PubMed  Google Scholar 

  9. 9

    Voelz, K. et al. 'Division of labour' in response to host oxidative burst drives a fatal Cryptococcus gattii outbreak. Nat. Commun. 5, 5194 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Maynard Smith, J. & Szathmáry, E. The Major Transitions in Evolution (Oxford Univ. Press, 1998).

    Google Scholar 

  11. 11

    Bourke, A. F. G. Principles of Social Evolution (Oxford Univ. Press, 2011).

    Google Scholar 

  12. 12

    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).

    CAS  PubMed  Google Scholar 

  13. 13

    Crespi, B. J. & Yanega, D. The definition of eusociality. Behav. Ecol. 6, 109–115 (1995).

    Google Scholar 

  14. 14

    West, S. A., Griffin, A. S. & Gardner, A. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20, 415–432 (2007).

    CAS  PubMed  Google Scholar 

  15. 15

    Tinbergen, N. On aims and methods of Ethology. Zeitschrift Tierpsychol. 20, 410–433 (1963).

    Google Scholar 

  16. 16

    Flores, E. & Herrero, A. Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat. Rev. Microbiol. 8, 39–50 (2009).

    Google Scholar 

  17. 17

    Davidson, C. J. & Surette, M. G. Individuality in bacteria. Annu. Rev. Genet. 42, 253–268 (2008).

    CAS  PubMed  Google Scholar 

  18. 18

    West, S. A., Griffin, A. S., Gardner, A. & Diggle, S. P. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4, 597–607 (2006).

    CAS  PubMed  Google Scholar 

  19. 19

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

    CAS  PubMed  Google Scholar 

  20. 20

    Grafen, A. Optimization of inclusive fitness. J. Theor. Biol. 238, 541–563 (2006).

    PubMed  Google Scholar 

  21. 21

    West, S. A. & Gardner, A. Adaptation and inclusive fitness review. Curr. Biol. 23, R577–R584 (2013).

    CAS  PubMed  Google Scholar 

  22. 22

    Ackermann, M. et al. Self-destructive cooperation mediated by phenotypic noise. Nature 454, 987–990 (2008).

    CAS  PubMed  Google Scholar 

  23. 23

    Diard, M. et al. Stabilization of cooperative virulence by the expression of an avirulent phenotype. Nature 494, 353–356 (2013).

    CAS  PubMed  Google Scholar 

  24. 24

    Strassmann, J. E., Zhu, Y. & Queller, D. C. Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408, 965–967 (2000).

    CAS  PubMed  Google Scholar 

  25. 25

    Velicer, G. J., Kroos, L. & Lenski, R. E. Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404, 598–601 (2000).

    CAS  PubMed  Google Scholar 

  26. 26

    Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998).

    CAS  PubMed  Google Scholar 

  27. 27

    Kim, W., Levy, S. B. & Foster, K. R. Rapid radiation in bacteria leads to a division of labor. Nat. Commun. 7, 10508 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 28

    Griffin, A. S., West, S. A. & Buckling, A. Cooperation and competition in pathogenic bacteria. Nature 430, 1024–1027 (2004).

    CAS  PubMed  Google Scholar 

  29. 29

    Jiricny, N. et al. Fitness correlates with the extent of cheating in a bacterium. J. Evol. Biol. 23, 738–747 (2010).

    CAS  PubMed  Google Scholar 

  30. 30

    Andersen, S. B., Marvig, R. L., Molin, S., Krogh Johansen, H. & Griffin, A. S. Long-term social dynamics drive loss of function in pathogenic bacteria. Proc. Natl Acad. Sci. USA 112, 10756–10761 (2015).

    CAS  PubMed  Google Scholar 

  31. 31

    Diggle, S. P., West, S. A., Griffin, A. S. & Campbell, G. S. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450, 411–414 (2007).

    CAS  PubMed  Google Scholar 

  32. 32

    West, S. A., Winzer, K., Gardner, A. & Diggle, S. P. Quorum sensing and the confusion about diffusion. Trends Microbiol. 20, 586–594 (2012).

    CAS  PubMed  Google Scholar 

  33. 33

    Ghoul, M., West, S. A., Diggle, S. P. & Griffin, A. S. An experimental test of whether cheating is context dependent. J. Evol. Biol. 27, 551–556 (2014).

    CAS  PubMed  Google Scholar 

  34. 34

    van Gestel, J., Vlamakis, H. & Kolter, R. From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate. PLoS Biol. 13, e1002141 (2015).

    PubMed  PubMed Central  Google Scholar 

  35. 35

    Michod, R. E. Evolution of individuality during the transition from unicellular to multicellular life. Proc. Natl Acad. Sci. USA 104, 8613–8618 (2007).

    CAS  PubMed  Google Scholar 

  36. 36

    Michod, R. E., Viossat, Y., Solari, C. A. & Hurand, M. Life-history evolution and the origin of multicellularity. J. Theor. Biol. 239, 257–272 (2006).

    PubMed  Google Scholar 

  37. 37

    Ispolatov, I., Ackermann, M. & Doebeli, M. Division of labour and the evolution of multicellularity. Proc. Biol. Sci. 279, 1768–1776 (2012).

    PubMed  Google Scholar 

  38. 38

    Gavrilets, S. Rapid transition towards the division of labor via evolution of developmental plasticity. PLoS Comput. Biol. 6, e1000805 (2010).

    PubMed  PubMed Central  Google Scholar 

  39. 39

    Oster, G. F. & Wilson, E. O. Caste and Ecology in the Social Insects (Princeton Univ. Press, 1978).

    Google Scholar 

  40. 40

    Charnov, E. L. The Theory of Sex Allocation (Princeton Univ. Press, 1982).

    Google Scholar 

  41. 41

    Koufopanou, V. & Bell, G. Soma and germ: an experimental approach using Volvox. Proc. R. Soc. B: Biol. Sci. 254, 107–113 (1993).

    Google Scholar 

  42. 42

    Rossetti, V. et al. The evolutionary path to terminal differentiation and division of labor in cyanobacteria. J. Theor. Biol. 262, 23–34 (2010).

    PubMed  Google Scholar 

  43. 43

    Wilson, E. O. Ergonomics of caste in social insects. Am. Nat. 102, 41–66 (1968).

    Google Scholar 

  44. 44

    Koufopanou, V. The evolution of soma in the Volvocales. Am. Nat. 143, 907–931 (1994).

    Google Scholar 

  45. 45

    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).

    CAS  PubMed  Google Scholar 

  46. 46

    Solari, C. A., Kessler, J. O. & Michod, R. E. A. Hydrodynamics approach to the evolution of multicellularity: flagellar motility and germ–soma differentiation in volvocalean green algae. Am. Nat. 167, 537–554 (2006).

    PubMed  Google Scholar 

  47. 47

    Solari, C. A., Ganguly, S., Kessler, J. O., Michod, R. E. & Goldstein, R. E. Multicellularity and the functional interdependence of motility and molecular transport. Proc. Natl Acad. Sci. USA 103, 1353–1358 (2006).

    CAS  PubMed  Google Scholar 

  48. 48

    Wolf, J. B. et al. Fitness trade-offs result in the illusion of social success. Curr. Biol. 25, 1086–1090 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 49

    Gilbert, O. M., Foster, K. R., Mehdiabadi, N. J., Strassmann, J. E. & Queller, D. C. High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc. Natl Acad. Sci. USA 104, 8913–8917 (2007).

    CAS  PubMed  Google Scholar 

  50. 50

    Mehdiabadi, N. J. et al. Kin preference in a social microbe. Nature 442, 881–882 (2006).

    CAS  PubMed  Google Scholar 

  51. 51

    Kuzdzal-Fick, J. J., Queller, D. C., Fox, S. A. & Strassmann, J. E. High relatedness is necessary and sufficient to maintain multicellularity in Dictyostelium. Science 334, 1548–1551 (2011).

    CAS  PubMed  Google Scholar 

  52. 52

    Bastiaans, E., Debets, A. J. M. & Aanen, D. K. Experimental evolution reveals that high relatedness protects multicellular cooperation from cheaters. Nat. Commun. 7, 1–10 (2016).

    Google Scholar 

  53. 53

    Fisher, R. M., Cornwallis, C. K. & West, S. A. Group formation, relatedness, and the evolution of multicellularity. Curr. Biol. 23, 1120–1125 (2013).

    CAS  PubMed  Google Scholar 

  54. 54

    Maynard Smith, J. & Price, G. R. The logic of animal conflict. Nature 246, 15–18 (1973).

    Google Scholar 

  55. 55

    Dawkins, R. The Selfish Gene (Oxford Univ. Press, 1976).

    Google Scholar 

  56. 56

    Bonner, J. T. Cellular Slime Molds (Princeton Univ. Press, 1967).

    Google Scholar 

  57. 57

    Shelton, D. E., Desnitskiy, A. G. & Michod, R. E. Distributions of reproductive and somatic cell numbers in diverse Volvox (Chlorophyta) species. Evol. Ecol. Res. 14, 707–727 (2012).

    PubMed  PubMed Central  Google Scholar 

  58. 58

    Bell, G. & Mooers, A. O. Size and complexity among multicellular organisms. Biol. J. Linnean Soc. 60, 345–363 (1997).

    Google Scholar 

  59. 59

    Frank, S. A. Host–symbiont conflict over the mixing of symbiotic lineages. Proc. Biol. Sci. 263, 339–344 (1996).

    CAS  PubMed  Google Scholar 

  60. 60

    Gore, J., Youk, H. & van Oudenaarden, A. Snowdrift game dynamics and facultative cheating in yeast. Nature 459, 253–256 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61

    Ross-Gillespie, A., Gardner, A., West, S. A. & Griffin, A. S. Frequency dependence and cooperation: theory and a test with bacteria. Am. Nat. 170, 331–342 (2007).

    PubMed  Google Scholar 

  62. 62

    Haig, D. Weismann rules! OK? Epigenetics and the Lamarckian temptation. Biol. Philos. 22, 415–428 (2006).

    Google Scholar 

  63. 63

    Maynard Smith, J. Group selection. Q. Rev. Biol. 51, 277–283 (1976).

    Google Scholar 

  64. 64

    Gordon, D. M. From division of labor to the collective behavior of social insects. Behav. Ecol. Sociobiol. 70, 1101–1108 (2015).

    PubMed  PubMed Central  Google Scholar 

  65. 65

    Rainey, P. B. & Kerr, B. Cheats as first propagules: a new hypothesis for the evolution of individuality during the transition from single cells to multicellularity. Bioessays 32, 872–880 (2010).

    PubMed  Google Scholar 

  66. 66

    Hammerschmidt, K., Rose, C. J., Kerr, B. & Rainey, P. B. Life cycles, fitness decoupling and the evolution of multicellularity. Nature 515, 75–79 (2015).

    Google Scholar 

  67. 67

    Veening, J.-W. et al. Bet-hedging and epigenetic inheritance in bacterial cell development. Proc. Natl Acad. Sci. USA 105, 4393–4398 (2008).

    CAS  PubMed  Google Scholar 

  68. 68

    Kirk, D. L. Asymmetric division, cell size and germ–soma specification in Volvox. Semin. Dev. Biol. 6, 369–379 (1995).

    Google Scholar 

  69. 69

    Schmitt, R. Differentiation of germinal and somatic cells in Volvox carteri. Curr. Opin. Microbiol. 6, 608–613 (2003).

    CAS  PubMed  Google Scholar 

  70. 70

    Nedelcu, A. M. & Michod, R. E. The evolutionary origin of an altruistic gene. Mol. Biol. Evol. 23, 1460–1464 (2006).

    CAS  PubMed  Google Scholar 

  71. 71

    Hanschen, E. R., Ferris, P. J. & Michod, R. E. Early evolution of the genetic basis for soma in the Volvocaceae. Evolution 68, 2014–2025 (2014).

    CAS  PubMed  Google Scholar 

  72. 72

    Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon, 1930).

    Google Scholar 

  73. 73

    Grafen, A. The formal Darwinism project: a mid-term report. J. Evol. Biol. 20, 1243–1254 (2007).

    CAS  PubMed  Google Scholar 

  74. 74

    Leigh, E. G. When does the good of the group override the advantage of the individual? Proc. Natl Acad. Sci. USA 80, 2985–2989 (1983).

    CAS  PubMed  Google Scholar 

  75. 75

    Gardner, A. & Grafen, A. Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. 22, 659–671 (2009).

    CAS  PubMed  Google Scholar 

  76. 76

    Shelton, D. E. & Michod, R. E. Philosophical foundations for the hierarchy of life. J. Evol. Biol. 25, 391 (2010).

    Google Scholar 

  77. 77

    Sturm, A. et al. The cost of virulence: retarded growth of Salmonella Typhimurium cells expressing type III secretion system 1. PLoS Pathog. 7, e1002143 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank K. Boomsma, A. P. Escudero, K. Foster, A. Gardner, M. Ghoul, J. Gore, A. Griffin, R. May, J. Strassmann, D. Unterweger and J. van Gestel for very useful discussions. The authors also thank M. Ackermann, R. May, R. Michod and J.-W. Veening for kindly providing images. G.A.C was funded by the Engineering and Physical Sciences Research Council (EPSRC).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Stuart A. West.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information S1 (box)

Intentional Language and Adaptation (DOC 40 kb)

Supplementary information S2 (box)

The Mutation Test (DOC 25 kb)

Supplementary information S3 (box)

Different Types of Division (DOC 30 kb)

Supplementary information S4 (box)

Graphing Efficiency Benefits (DOC 27 kb)

Supplementary information S5 (box)

Can You Get Division of Labour Between Species? (DOC 44 kb)

Supplementary information S6 (box)

Variation in Mechanism Within Species (DOC 29 kb)

Supplementary information S7 (box)

Selection Versus Adaptation (DOC 28 kb)

Supplementary information S8 (box)

Can Bet-Hedging be Cooperative? (DOC 28 kb)

Supplementary information S9 (box)

Can You Get Division of Labour With Spiteful Traits? (DOC 30 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

West, S., Cooper, G. Division of labour in microorganisms: an evolutionary perspective. Nat Rev Microbiol 14, 716–723 (2016). https://doi.org/10.1038/nrmicro.2016.111

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing