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.

  • Article
  • Published:

Evolution of an obligate social cheater to a superior cooperator

Nature volume 441, pages 310–314 (2006)Cite this article

Abstract

Obligate relationships have evolved many times and can be parasitic or mutualistic. Obligate organisms rely on others to survive and thus coevolve with their host or partner. An important but little explored question is whether obligate status is an evolutionarily terminal condition or whether obligate lineages can evolve back to an autonomous lifestyle. The bacterium Myxococcus xanthus survives starvation by the social development of spore-bearing fruiting bodies. Some M. xanthus genotypes defective at fruiting body development in isolation can nonetheless exploit proficient genotypes in chimaeric groups. Here we report an evolutionary transition from obligate dependence on an altruistic host to an autonomous mode of social cooperation. This restoration of social independence was caused by a single mutation of large effect that confers fitness superiority over both ancestral genotypes, including immunity from exploitation by the ancestral cheater. Thus, a temporary state of obligate cheating served as an evolutionary stepping-stone to a novel state of autonomous social dominance.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Total spore production, OC-derived sub-population frequencies and developmental population phenotypes during the original six-cycle competition between OC and GJV2.
Figure 2: Pure-culture spore production of strains GJV2, OC and PX.
Figure 3: Log-transformed ratios of PX sporulation efficiency relative to that of GJV2 and OC in direct pairwise competitions at multiple mixing frequencies.
Figure 4: Frequency of PX in direct competition with GJV2 over six cycles of development.
Figure 5: Fruiting morphology effects of the PX-specific mutation.
Figure 6: Developmental expression of the putative acetyltransferase immediately downstream of the PX mutation.

Similar content being viewed by others

References

  1. Pierce, N. E. et al. The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu. Rev. Entomol. 47, 733–771 (2002)

    Article  CAS  Google Scholar 

  2. Keeling, P. J. & Fast, N. M. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu. Rev. Microbiol. 56, 93–116 (2002)

    Article  CAS  Google Scholar 

  3. Alexander, J., Satoskar, A. R. & Russell, D. G. Leishmania species: models of intracellular parasitism. J. Cell Sci. 112, 2993–3002 (1999)

    CAS  PubMed  Google Scholar 

  4. Williamson, V. M. & Gleason, C. A. Plant-nematode interactions. Curr. Opin. Plant Biol. 6, 327–333 (2003)

    Article  CAS  Google Scholar 

  5. Pellmyr, O. & Krenn, H. W. Origin of a complex key innovation in an obligate insect-plant mutualism. Proc. Natl Acad. Sci. USA 99, 5498–5502 (2002)

    Article  ADS  CAS  Google Scholar 

  6. Lopez-Vaamonde, C., Rasplus, J. Y., Weiblen, G. D. & Cook, J. M. Molecular phylogenies of fig wasps: partial cocladogenesis of pollinators and parasites. Mol. Phylogenet. Evol. 21, 55–71 (2001)

    Article  CAS  Google Scholar 

  7. Moran, N. A. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108, 583–586 (2002)

    Article  CAS  Google Scholar 

  8. Moran, N. A. Tracing the evolution of gene loss in obligate bacterial symbionts. Curr. Opin. Microbiol. 6, 512–518 (2003)

    Article  CAS  Google Scholar 

  9. Rothstein, S. I. & Robinson, S. K. Parasitic Birds and their Hosts: Studies in Coevolution (Oxford Univ. Press, New York, 1998)

    Google Scholar 

  10. Lorenzi, M. C., Cervo, R., Zacchi, F., Turillazzi, S. & Bagneres, A. G. Dynamics of chemical mimicry in the social parasite wasp Polistes semenowi (Hymenoptera: Vespidae). Parasitology 129, 643–651 (2004)

    Article  CAS  Google Scholar 

  11. Sumner, S., Aanen, D. K., Delabie, J. & Boomsma, J. J. The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery's rule. Insectes Soc. 51, 37–42 (2004)

    Article  Google Scholar 

  12. Cervo, R., Macinai, V., Dechigi, F. & Turillazzi, S. Fast growth of immature brood in a social parasite wasp: A convergent evolution between avian and insect cuckoos. Am. Nat. 164, 814–820 (2004)

    Article  Google Scholar 

  13. Foitzik, S., Fischer, B. & Heinze, J. Arms races between social parasites and their hosts: geographic patterns of manipulation and resistance. Behav. Ecol. 14, 80–88 (2003)

    Article  Google Scholar 

  14. Pellmyr, O. & Thompson, J. N. Multiple occurrences of mutualism in the yucca moth lineage. Proc. Natl Acad. Sci. USA 89, 2927–2929 (1992)

    Article  ADS  CAS  Google Scholar 

  15. Sorenson, M. D. & Payne, R. B. A single ancient origin of brood parasitism in African finches: implications for host-parasite coevolution. Evol. Int. J. Org. Evol. 55, 2550–2567 (2001)

    Article  CAS  Google Scholar 

  16. Dale, C., Wang, B., Moran, N. & Ochman, H. Loss of DNA recombinational repair enzymes in the initial stages of genome degeneration. Mol. Biol. Evol. 20, 1188–1194 (2003)

    Article  CAS  Google Scholar 

  17. Maynard Smith, J. & Szathmáry, E. The Major Transitions in Evolution (Freeman Spektrum, Oxford, 1995)

    Google Scholar 

  18. Seidler, R. J. & Starr, M. P. Isolation and characterization of host-independent Bdellovibrios. J. Bacteriol. 100, 769–785 (1969)

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Lutzoni, F., Pagel, M. & Reeb, V. Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411, 937–940 (2001)

    Article  ADS  CAS  Google Scholar 

  20. Dawid, W. Biology and global distribution of myxobacteria in soils. FEMS Microbiol. Rev. 24, 403–427 (2000)

    Article  CAS  Google Scholar 

  21. Rosenberg, E. & Varon, M. in Myxobacteria: Development and Cell Interactions (ed. Rosenberg, E.) 109–125 (Springer, New York, 1984)

    Google Scholar 

  22. Wu, S. S. & Kaiser, D. Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus. Mol. Microbiol. 18, 547–558 (1995)

    Article  CAS  Google Scholar 

  23. Shimkets, L. J. Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu. Rev. Microbiol. 53, 525–549 (1999)

    Article  CAS  Google Scholar 

  24. Wireman, J. W. & Dworkin, M. Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. J. Bacteriol. 129, 796–802 (1977)

    CAS  Google Scholar 

  25. Fiegna, F. & Velicer, G. J. Exploitative and hierarchical antagonism in a cooperative bacterium. PLoS Biol. 3, 1980–1987 (2005)

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  27. Rainey, P. B. & Rainey, K. Evolution of cooperation and conflict in experimental bacterial populations. Nature 425, 72–74 (2003)

    Article  ADS  CAS  Google Scholar 

  28. Sachs, J. L. & Bull, J. J. Experimental evolution of conflict mediation between genomes. Proc. Natl Acad. Sci. USA 102, 390–395 (2005)

    Article  ADS  CAS  Google Scholar 

  29. Velicer, G. J. & Yu, Y. T. Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus. Nature 425, 75–78 (2003)

    Article  ADS  CAS  Google Scholar 

  30. Velicer, G. J., Kroos, L. & Lenski, R. E. Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc. Natl Acad. Sci. USA 95, 12376–12380 (1998)

    Article  ADS  CAS  Google Scholar 

  31. Dugatkin, L. A., Perlin, M., Lucas, J. S. & Atlas, R. Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm. Proc. R. Soc. Lond. B 272, 79–83 (2005)

    Article  Google Scholar 

  32. Greig, D. & Travisano, M. The Prisoner's Dilemma and polymorphism in yeast SUC genes. Proc. R. Soc. Lond. B 271 (Suppl 3), S25–S26 (2004)

    CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  34. Velicer, G. J. Social strife in the microbial world. Trends Microbiol. 11, 330–337 (2003)

    Article  CAS  Google Scholar 

  35. Velicer, G. J., Lenski, R. E. & Kroos, L. Rescue of social motility lost during evolution of Myxococcus xanthus in an asocial environment. J. Bacteriol. 184, 2719–2727 (2002)

    Article  CAS  Google Scholar 

  36. Fiegna, F. & Velicer, G. J. Competitive fates of bacterial social parasites: persistence and self-induced extinction of Myxococcus xanthus cheaters. Proc. R. Soc. Lond. B 270, 1527–1534 (2003)

    Article  Google Scholar 

  37. Frank, S. A. Perspective: repression of competition and the evolution of cooperation. Evol. Int. J. Org. Evol. 57, 693–705 (2003)

    Google Scholar 

  38. Keller, L. Levels of Selection in Evolution (Princeton Univ. Press, Princeton, New Jersey, 1999)

    Google Scholar 

  39. Travisano, M. & Velicer, G. J. Strategies of microbial cheater control. Trends Microbiol. 12, 72–78 (2004)

    Article  CAS  Google Scholar 

  40. Foster, K. R., Shaulsky, G., Strassmann, J. E., Queller, D. C. & Thompson, C. R. L. Pleiotropy as a mechanism to stabilize cooperation. Nature 431, 693–696 (2004)

    Article  ADS  CAS  Google Scholar 

  41. Lenski, R. E., Ofria, C., Pennock, R. T. & Adami, C. The evolutionary origin of complex features. Nature 423, 139–144 (2003)

    Article  ADS  CAS  Google Scholar 

  42. Velicer, G. J., et al. Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proc. Natl Acad. Sci. USA (in the press)

  43. Vetting, M. W. et al. Structure and functions of the GNAT superfamily of acetyltransferases. Arch. Biochem. Biophys. 433, 212–226 (2005)

    Article  CAS  Google Scholar 

  44. Rodriguez, A. M. & Spormann, A. M. Genetic and molecular analysis of cglB, a gene essential for single-cell gliding in Myxococcus xanthus. J. Bacteriol. 181, 4381–4390 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Orr, H. A. The genetic theory of adaptation: A brief history. Nature Rev. Genet. 6, 119–127 (2005)

    Article  CAS  Google Scholar 

  46. Kaiser, D. Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc. Natl Acad. Sci. USA 76, 5952–5956 (1979)

    Article  ADS  CAS  Google Scholar 

  47. Wall, D., Kolenbrander, P. E. & Kaiser, D. The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for Type IV pilus biogenesis, social motility and development. J. Bacteriol. 181, 24–33 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Bretscher, A. P. & Kaiser, D. Nutrition of Myxococcus xanthus, a fruiting myxobacterium. J. Bacteriol. 133, 763–768 (1978)

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank S. Elena, K. Foster, M. Grbic and our laboratory members for discussions and/or comments on the manuscript. We also thank S. Deiss and H. Keller for technical assistance. This work was partially funded by a grant from the Deutsche Forschungsgemeinschaft. Author Contributions F.F. (primarily) and G.J.V. (secondarily) performed population-level experiments, Y.-T.N.Y performed the analysis of mutation function, S.V.K. performed the real-time PCR analysis and all four authors contributed to writing the paper.

Author information

Authors and Affiliations

  1. Max Planck Institute for Developmental Biology, Spemannstrasse 35, D-72076, Tübingen, Germany

    Francesca Fiegna, Yuen-Tsu N. Yu, Supriya V. Kadam & Gregory J. Velicer

Authors
  1. Francesca Fiegna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuen-Tsu N. Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Supriya V. Kadam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gregory J. Velicer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gregory J. Velicer.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fiegna, F., Yu, YT., Kadam, S. et al. Evolution of an obligate social cheater to a superior cooperator. Nature 441, 310–314 (2006). https://doi.org/10.1038/nature04677

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04677

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced 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