Experimental social evolution with Myxococcus xanthus

Abstract

Genetically-based social behaviors are subject to evolutionary change in response to natural selection. Numerous microbial systems provide not only the opportunity to understand the genetic mechanisms underlying specific social interactions, but also to observe evolutionary changes in sociality over short time periods. Here we summarize experiments in which behaviors of the social bacterium Myxococcus xanthus changed extensively during evolutionary adaptation to two relatively asocial laboratory environments. M. xanthus moves cooperatively, exhibits cooperative multicellular development upon starvation and also appears to prey cooperatively on other bacteria. Replicate populations of M. xanthus were evolved in both structured (agar plate) and unstructured (liquid) environments that contained abundant resources. The importance of social cooperation for evolutionary fitness in these habitats was limited by the absence of positive selection for starvation-induced spore production or predatory efficiency. Evolved populations showed major losses in all measured categories of social proficiency- motility, predation, fruiting ability, and sporulation. Moreover, several evolved genotypes were observed to exploit the social behavior of their ancestral parent when mixed together during the developmental process. These experiments that resulted in both socially defective and socially exploitative genotypes demonstrate the power of laboratory selection experiments for studying social evolution at the microbial level. Results from additional selection experiments that place positive selection pressure on social phenotypes can be integrated with direct study of natural populations to increase our understanding of principles that underlie the evolution of microbial social behavior.

This is a preview of subscription content, log in to check access.

References

  1. Adami C, Ofria C & Collier TC (2000) Evolution of biological complexity. Proc. Natl. Acad. Sci. USA 97: 4463–4468.

    PubMed  CAS  Article  Google Scholar 

  2. Adams DG (2000) Heterocyst formation in cyanobacteria. Curr. Opin. Microbiol. 3: 618–624.

    PubMed  CAS  Article  Google Scholar 

  3. Bever JD & Simms EL (2000) Evolution of nitrogen fixation in spatially structured populations of Rhizobium. Heredity 85 Pt 4: 366–372.

    PubMed  CAS  Article  Google Scholar 

  4. Bjorkman J, Hughes D & Andersson DI (1998) Virulence of antibiotic-resistant Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 95: 3949–3953.

    PubMed  CAS  Article  Google Scholar 

  5. Bouma JE & Lenski RE (1988) Evolution of a bacteria/plasmid association. Nature 335: 351–352.

    PubMed  CAS  Article  Google Scholar 

  6. Bretscher AP & Kaiser D (1978) Nutrition of Myxococcus xanthus, a fruiting myxobacterium. J. Bacteriol. 133: 763–768.

    PubMed  CAS  Google Scholar 

  7. Bull HJ, McKenzie GJ, Hastings PJ & Rosenberg SM (2000) Evidence that stationary-phase hypermutation in the Escherichia coli chromosome is promoted by recombination. Genetics 154: 1427–1437.

    PubMed  CAS  Google Scholar 

  8. Burkholder JM (1999) The lurking perils of Pfiesteria. Sci. Am. 281: 42–49.

    PubMed  CAS  Article  Google Scholar 

  9. Chao L & Levin BR (1981) Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc. Natl. Acad. Sci. USA 78: 6324–6328.

    PubMed  CAS  Article  Google Scholar 

  10. Chao L & Tran TT (1997) The advantage of sex in the RNA virus φ6. Genetics 147: 953–959.

    PubMed  CAS  Google Scholar 

  11. Cooper VS & Lenski RE (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736–739.

    PubMed  CAS  Article  Google Scholar 

  12. Crespi BJ (2001) The evolution of social behavior in microorganisms. Trends Ecol. Evol. 16: 178–183.

    PubMed  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  14. de Visser JAGM, Zeyl CW, Gerrish PJ, Blanchard JL & Lenski RE (1999) Diminishing returns from mutation supply rate in asexual populations. Science 283: 404–406.

    CAS  Article  Google Scholar 

  15. Denison RF (2000) Legume sanctions and the evolution of symbiotic cooperation by Rhizobia. Am. Nat. 156: 567–576.

    Article  Google Scholar 

  16. Engelberg-Kulka H & Glaser G (1999) Addiction modules and programmed cell death and antideath in bacterial cultures. Annu. Rev. Microbiol. 53: 43–70.

    PubMed  CAS  Article  Google Scholar 

  17. Giraldeau L-A & Caraco T (2000). Social Foraging Theory. Princeton University Press, Princeton, NJ.

    Google Scholar 

  18. Imhof M & Schlotterer C (2001) Fitness effects of advantageous mutations in evolving Escherichia coli populations. Proc. Natl. Acad. Sci. USA 98: 1113–1117.

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  20. Kaiser D, Kroos L & Kuspa A (1985). Cell interactions govern the temporal pattern of Myxococcus development. Cold Spring Harbor Symp. Quant. Biol. (pp 823–830). Cold Spring Harbor Laboratory, L: Cold Spring Harbor.

    Google Scholar 

  21. Kelemen GH, Viollier PH, Tenor J, Marri L, Buttner MJ & Thompson CJ (2001) A connection between stress and development in the multicellular prokaryote Streptomyces coelicolor A3(2). Mol. Microbiol. 40: 804–814.

    PubMed  CAS  Article  Google Scholar 

  22. Kroos L, Kuspa A & Kaiser D (1986) A global analysis of developmentally regulated genes in Myxococcus xanthus. Dev. Biol. 117: 252–266.

    PubMed  CAS  Article  Google Scholar 

  23. Lenski RE (1988a) Experimental studies of pleiotropy and epistasis in Escherichia coli. I. Variation in competitive fitness among mutants resistant to virus T4. Evolution 42: 425–432.

    Article  Google Scholar 

  24. Lenski RE (1988b) Experimental studies of pleiotropy and epistatsis in Escherichia coli. II. Compensation for maladaptic pleiotropic effects associated with resistance to virus T4. Evolution 42: 433–440.

    Article  Google Scholar 

  25. Lenski RE, Ofria C, Collier TC & Adami C (1999) Genome complexity, robustness and genetic interactions in digital organisms. Nature 400: 661–664.

    PubMed  CAS  Article  Google Scholar 

  26. Lenski RE, Simpson SC & Nguyen TT (1994) Genetic analysis of a plasmid-encoded, host genotype-specific enhancement of bacterial fitness. J. Bacteriol. 176: 3140–3147.

    PubMed  CAS  Google Scholar 

  27. Lewis K (2000) Programmed death in bacteria. Microbiol. Mol. Biol. Rev. 64: 503–514.

    PubMed  CAS  Article  Google Scholar 

  28. Mann J (1997) Myxobacterial bounty. Nature 385: 117.

    PubMed  CAS  Article  Google Scholar 

  29. McBride MJ (2001) Bacterial gliding motility: multiple mechanisms for cell movement over surfaces. Annu. Rev. Microbiol. 55: 49–75.

    PubMed  CAS  Article  Google Scholar 

  30. Miguelez EM, Hardisson C & Manzanal MB (2000) Streptomycetes: a new model to study cell death. Int. Microbiol. 3: 153–158.

    PubMed  CAS  Google Scholar 

  31. Miller MB & Bassler BL (2001) Quorum sensing in bacteria. Annu. Rev. Microbiol. 55: 165–199.

    PubMed  CAS  Article  Google Scholar 

  32. Modi RI, Wilke CM, Rosenzweig RF & Adams J (1991) Plasmid macro-evolution: selection of deletions during adaptation in a nutrient-limited environment. Genetica 84: 195–202.

    PubMed  CAS  Article  Google Scholar 

  33. Moore FB-G, Rozen DE & Lenski RE (2000) Pervasive compensatory adaptation in Escherichia coli. Proc. R. Soc. Lond. B. Biol. Sci. 267: 515–522.

    CAS  Article  Google Scholar 

  34. O'Conner K & Zusman D (1988) Reexamination of the role of autolysis in the development of Myxococcus xanthus. J. Bacteriol. 170: 4103–4112.

    Google Scholar 

  35. O'Toole G, Kaplan HB & Kolter R (2000) Biofilm formation as microbial development. Annu. Rev. Microbiol. 54: 49–79.

    PubMed  Article  Google Scholar 

  36. Redfield RJ, Schrag MR & Dean AM (1997) The evolution of bacterial transformation: sex with poor relations. Genetics 146: 27–38.

    PubMed  CAS  Google Scholar 

  37. Reichenbach H (1999) The ecology of the myxobacteria. Environ. Microbiol. 1: 15–21.

    PubMed  CAS  Article  Google Scholar 

  38. Ricklefs RE & Miller GL (1999). Evolution and social behavior. Ecology. W. H. Freeman and Company, New York. (pp 699–719).

    Google Scholar 

  39. Rosenberg E, Keller K & Dworkin M (1977) Cell density-dependent growth of Myxococcus xanthus on casein. J. Bacteriol. 129: 770–777.

    PubMed  CAS  Google Scholar 

  40. Rosenberg E & Varon M (1984). Antibiotics and lytic enzymes. In: Rosenberg E (Ed) Myxobacteria: Development and Cell Interactions (pp 109–125). Springer-Verlag, New York.

    Google Scholar 

  41. Schrag SJ, Perrot V & Levin BR (1997) Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc. R. Soc. Lond. B Biol. Sci. 264: 1287–1291.

    CAS  Article  Google Scholar 

  42. Shi W & Zusman DR (1993) The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. Proc. Natl. Acad. Sci. USA 90: 3378–3382.

    PubMed  CAS  Article  Google Scholar 

  43. Shimkets L & Woese CR (1992) A phylogenetic analysis of the myxobacteria: basis for their classification. Proc. Natl. Acad. Sci. USA 89: 9459–9463.

    PubMed  CAS  Article  Google Scholar 

  44. Shimkets LJ (1999) Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu. Rev. Microbiol. 53: 525–549.

    PubMed  CAS  Article  Google Scholar 

  45. Shub DA (1994) Bacterial viruses. Bacterial altruism? Curr. Biol. 4: 555–556.

    PubMed  CAS  Article  Google Scholar 

  46. Sniegowski PD, Gerrish PJ & Lenski RE (1997) Evolution of high mutation rates in experimental populations of Escherichia coli. Nature 387: 703–705.

    PubMed  CAS  Article  Google Scholar 

  47. Souza V, Turner PE & Lenski RE (1997) Long-term experimental evolution in Escherichia coli. 5. Effects of recombination with immigrant genotypes on the rate of bacterial evolution. J. Evol. Biol. 10: 743–769.

    Article  Google Scholar 

  48. Spormann AM (1999) Gliding motility in bacteria: Insights from studies of Myxococcus xanthus. Microbiol. Mol. Biol. Rev. 63: 621–641.

    PubMed  CAS  Google Scholar 

  49. Stephens DW & Krebs JR (1986). Foraging Theory. Princeton University Press, Princeton, NJ.

    Google Scholar 

  50. Strassmann JE, Zhu Y & Queller DC (2000) Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408: 965–967.

    PubMed  CAS  Article  Google Scholar 

  51. Turner PE & Chao L (1999) Prisoner's dilemma in an RNA virus. Nature 398: 441–443.

    PubMed  CAS  Article  Google Scholar 

  52. Velicer GJ, Kroos L & Lenski RE (1998) Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc. Natl. Acad. Sci. USA 95: 12376–12380.

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  55. Vulic M, Lenski RE & Radman M (1999) Mutation, recombination, and incipient speciation of bacteria in the laboratory. Proc. Natl. Acad. Sci. USA 96: 7348–7351.

    PubMed  CAS  Article  Google Scholar 

  56. Vulic M, Kolter R (2001) Evolutionary cheating in Escherichia coli stationary phase cultures. Genetics 158: 519–526.

    PubMed  CAS  Google Scholar 

  57. Watve MG, Shete AM, Jadhav N, Wagh SA, Shelar SP, Chakraborti SS, Botre AP & Kulkarni AA (1999) Myxobacterial diversity in Indian soils-How many species do we have? Curr. Sci. 77: 1089–1095.

    Google Scholar 

  58. Weijer CJ (1999) Morphogenetic cell movement in Dictyostelium. Semin. Cell Dev. Biol. 10: 609–619.

    PubMed  CAS  Article  Google Scholar 

  59. Wilke CO, Wang JL, Ofria C, Lenski RE & Adami C (2001) Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412: 331–333.

    PubMed  CAS  Article  Google Scholar 

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

    CAS  Google Scholar 

  61. Withers H, Swift S & Williams P (2001) Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr. Opin. Microbiol. 4: 186–193.

    PubMed  CAS  Article  Google Scholar 

  62. Yu YT & Snyder L (1994) Translation elongation factor Tu cleaved by a phage-exclusion system. Proc. Natl. Acad. Sci. USA 91: 802–806.

    PubMed  CAS  Article  Google Scholar 

  63. Zahavi A & Ralt D (1984). Social adaptations in myxobacteria. In: Rosenberg E (Ed) Myxobacteria: Development and Cell Interactions (pp 215–220). Springer-Verlag, New York.

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Gregory J. Velicer.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Velicer, G.J., Stredwick, K.L. Experimental social evolution with Myxococcus xanthus . Antonie Van Leeuwenhoek 81, 155 (2002). https://doi.org/10.1023/A:1020546130033

Download citation

  • behavior
  • cooperation
  • evolution
  • predation
  • Myxococcus
  • social