Modelling the Evolution of Mutualistic Symbioses

Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 804)

Abstract

Mutualistic microbial symbioses are one of the key innovations in the evolution of biological diversity, enabling the expansion of species’ niches and the production of sophisticated structures such as the eukaryotic cell. For some of the best-studied cases, we are beginning to have network models of symbiotic metabolism, but this work is in its infancy and has not been developed with an evolutionary perspective. However, theoreticians have long been interested in how these symbioses arise and persist and have applied modelling approaches from economics, evolution, ecology, and sociobology to a number of fundamental questions. We provide an overview of these questions, followed by specific modelling examples. We cover economic game theory, including the Prisoner’s Dilemma, the Snowdrift game, and biological markets. We also describe the eco-evolutionary framework of adaptive dynamics, inclusive fitness, and population genetic models. We aim to provide insight into the strengths and weaknesses of each approach and into how current evolutionary methods can benefit an understanding of the mechanistic basis of host–symbiont interactions elucidated by molecular network models.

Key words

Symbiosis Mutualism Game theory Adaptive dynamics Inclusive fitness Biological markets Population genetics Cooperative bargaining 

Notes

Acknowledgments

We thank D. Drown, B. Foley, the volume editors, and an anonymous reviewer for helpful comments on the manuscript. This work was supported by NSF PGRP 0820846 to S. Nuzhdin and NSF DMS 0540524 to R. Gomulkiewicz.

References

  1. 1.
    Cavalier-Smith T. (2006) Origin of mitochondria by intracellular enslavement of a photosynthetic purple bacterium. Proc R Soc B-Biol Sci, 273:1943–1952.CrossRefGoogle Scholar
  2. 2.
    Gould SB, Waller RF, McFadden GI. (2008) Plastid evolution. Annu Rev Plant Biol, 59:491–517.PubMedCrossRefGoogle Scholar
  3. 3.
    Archibald JM. (2009) The puzzle of plastid evolution. Curr Biol, 19:R81–R88.PubMedCrossRefGoogle Scholar
  4. 4.
    Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB. (2001) Molecular evidence for the early colonization of land by fungi and plants. Science, 293:1129–1133.PubMedCrossRefGoogle Scholar
  5. 5.
    Kneip C, Lockhart P, Voß C, Maier U. (2007) Nitrogen fixation in eukaryotes: new models for symbiosis. BMC Evol Biol, 7:55.Google Scholar
  6. 6.
    Moya A, Peretó J, Gil R, Latorre A. (2008) Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet, 9:218–229.Google Scholar
  7. 7.
    Moran NA. (2006) Symbiosis. Curr Biol, 16:R866–R871.PubMedCrossRefGoogle Scholar
  8. 8.
    Sachs JL, Mueller UG, Wilcox TP, Bull JJ. (2004) The evolution of cooperation. Q Rev Biol, 79:135–160.PubMedCrossRefGoogle Scholar
  9. 9.
    West SA, Griffin AS, Gardner A. (2007) Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol, 20:415–432.PubMedCrossRefGoogle Scholar
  10. 10.
    van Baalen M, Jansen VAA. (2001) Dangerous liaisons: the ecology of private interest and common good. Oikos, 95:211–224.CrossRefGoogle Scholar
  11. 11.
    Frean MR, Abraham ER. (2004) Adaptation and enslavement in endosymbiont-host associations. Phys Rev E, 69:051913.CrossRefGoogle Scholar
  12. 12.
    Hardin G. (1968) The tragedy of the commons. Science, 162:1243–1248.CrossRefGoogle Scholar
  13. 13.
    Grube M, Cardinale M, de Castro JV, Mueller H, Berg G. (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J, 3:1105–1115.PubMedCrossRefGoogle Scholar
  14. 14.
    Douglas AE. (2009) The microbial dimension in insect nutritional ecology. Funct Ecol, 23:38–47.Google Scholar
  15. 15.
    Honegger R. (1991) Functional aspects of the lichen symbiosis. Annu Rev Plant Phys, 42:553–578.CrossRefGoogle Scholar
  16. 16.
    Nyholm SV, McFall-Ngai M. (2004) The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol, 2:632–642.PubMedCrossRefGoogle Scholar
  17. 17.
    Oliver KM, Degnan PH, Burke GR, Moran NA. (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol, 55:247–266.PubMedCrossRefGoogle Scholar
  18. 18.
    McCutcheon JP, Moran NA. (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci U S A, 104:19392–19397.PubMedCrossRefGoogle Scholar
  19. 19.
    Thomas GH, Zucker J, Macdonald SJ, Sorokin A, Goryanin I, Douglas AE. (2009) A fragile metabolic network adapted for cooperation in the symbiotic bacterium Buchnera aphidicola. BMC Syst Biol, 3:24.Google Scholar
  20. 20.
    Resendis-Antonio O, Reed JL, Encarnación S, Collado-Vides J, Palsson BØ. (2007) Metabolic reconstruction and modeling of nitrogen fixation in Rhizobium etli. PLoS Comput Biol, 3:1887–1895.Google Scholar
  21. 21.
    Rodriguez-Llorente I, Caviedes MA, Dary M, Palomares AJ, Cánovas FM, Peregrín-Alvarez JM. (2009) The symbiosis interactome: a computational approach reveals novel components, functional interactions and modules in Sinorhizobium meliloti. BMC Syst Biol, 3:63.Google Scholar
  22. 22.
    Noë R, Hammerstein P. (1994) Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behav Ecol Sociobiol, 35:1–11.CrossRefGoogle Scholar
  23. 23.
    West SA, Kiers ET, Simms EL, Denison RF. (2002) Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc R Soc B-Biol Sci, 269:685–694.CrossRefGoogle Scholar
  24. 24.
    Frank SA. (1994) Genetics of mutualism: the evolution of altruism between species. J Theor Biol, 170:393–400.PubMedCrossRefGoogle Scholar
  25. 25.
    von Neumann J, Morgenstern O. (1944) Theory of Games and Economic Behavior. Princeton University Press, Princeton, NJ.Google Scholar
  26. 26.
    Trivers RL. (1971) Evolution of reciprocal altruism. Q Rev Biol, 46:35–57.CrossRefGoogle Scholar
  27. 27.
    Axelrod R, Hamilton WD. (1981) The evolution of cooperation. Science, 211:1390–1396.PubMedCrossRefGoogle Scholar
  28. 28.
    Doebeli M, Knowlton N. (1998) The evolution of interspecific mutualisms. Proc Natl Acad Sci U S A, 95:8676–8680.PubMedCrossRefGoogle Scholar
  29. 29.
    Doebeli M, Hauert C. (2005) Models of cooperation based on the Prisoner’s Dilemma and the Snowdrift game. Ecol Lett, 8:748–766.CrossRefGoogle Scholar
  30. 30.
    Doebeli M, Hauert C, Killingback T. (2004) The evolutionary origin of cooperators and defectors. Science, 306:859–862.PubMedCrossRefGoogle Scholar
  31. 31.
    Schwartz MW, Hoeksema JD. (1998) Specialization and resource trade: biological markets as a model of mutualisms. Ecology, 79:1029–1038.CrossRefGoogle Scholar
  32. 32.
    Nash JF. (1950) The bargaining problem. Econometrica, 18:155–162.CrossRefGoogle Scholar
  33. 33.
    Nash JF. (1953) Two-person cooperative games. Econometrica, 21:128–140.CrossRefGoogle Scholar
  34. 34.
    Akçay E, Roughgarden J. (2007) Extra-pair parentage: a new theory based on transactions in a cooperative game. Evol Ecol Res, 9:1223–1243.Google Scholar
  35. 35.
    Lodwig EM, Hosie AHF, Bordes A, Findlay K, Allaway D, Karunakaran R, Downie JA, Poole PS. (2003) Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature, 422:722–726.PubMedCrossRefGoogle Scholar
  36. 36.
    Heath KD, Tiffin P. (2009) Stabilizing mechanisms in a legume-rhizobium mutualism. Evolution, 63:652–662.PubMedCrossRefGoogle Scholar
  37. 37.
    Noë R, Hammerstein P. (1995) Biological markets. Trends Ecol Evol, 10:336–339.Google Scholar
  38. 38.
    Johnstone RA, Bshary R. (2008) Mutualism, market effects and partner control. J Evol Biol, 21:879–888.PubMedCrossRefGoogle Scholar
  39. 39.
    Johnstone RA, Bshary R. (2002) From parasitism to mutualism: partner control in asymmetric interactions. Ecol Lett, 5:634–639.CrossRefGoogle Scholar
  40. 40.
    Metz JAJ, Nisbet RM, Geritz SAH. (1992) How should we define “fitness” for general ecological scenarios? Trends Ecol Evol 7:198–202.Google Scholar
  41. 41.
    Dieckmann U, Law R. (1996) The dynamical theory of coevolution: a derivation from stochastic ecological processes. J Math Biol, 34:579–612.PubMedCrossRefGoogle Scholar
  42. 42.
    Ferrière R, Bronstein JL, Rinaldi S, Law R, Gauduchon M. (2002) Cheating and the evolutionary stability of mutualisms. Proc R Soc B-Biol Sci, 269:773–780.CrossRefGoogle Scholar
  43. 43.
    Geritz SAH, Metz JAJ, Kisdi E, Meszéna G. (1997) Dynamics of adaptation and evolutionary branching. Phys Rev Lett, 78:2024–2027.CrossRefGoogle Scholar
  44. 44.
    Law R, Dieckmann U. (1998) Symbiosis through exploitation and the merger of lineages in evolution. Proc R Soc B-Biol Sci, 265:1245–1253.CrossRefGoogle Scholar
  45. 45.
    Hamilton WD (1964) Genetical evolution of social behaviour I. J Theor Biol, 7:1–16.Google Scholar
  46. 46.
    Frank SA (1998) Foundations of Social Evolution. Princeton University Press, Princeton, NJGoogle Scholar
  47. 47.
    West SA, Diggle SP, Buckling A, Gardner A, Griffins AS. (2007) The social lives of microbes. Annu Rev Ecol Evol System, 38:53–77.CrossRefGoogle Scholar
  48. 48.
    Mideo N, Alizon S, Day T. (2008) Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol Evol, 23:511–517.Google Scholar
  49. 49.
    Nuismer SL, Gomulkiewicz R, Morgan MT. (2003) Coevolution in temporally variable environments. Am Nat, 162:195–204.PubMedCrossRefGoogle Scholar
  50. 50.
    Gandon S. (2002) Local adaptation and the geometry of host–parasite coevolution. Ecol Lett, 5:246–256.CrossRefGoogle Scholar
  51. 51.
    Gandon S, Michalakis Y. (2002) Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time. J Evol Biol, 15:451–462.CrossRefGoogle Scholar
  52. 52.
    Nuismer SL, Thompson JN, Gomulkiewicz R. (1999) Gene flow and geographically structured coevolution. Proc R Soc B-Biol Sci, 266:605–609.CrossRefGoogle Scholar
  53. 53.
    Day T, Nagel L, Van Oppen MJH, Caley MJ. (2008) Factors affecting the evolution of bleaching resistance in corals. Am Nat, 171:E72–E88.PubMedCrossRefGoogle Scholar
  54. 54.
    Ridenhour BJ, Nuismer SL (2007) Polygenic traits and parasite local adaptation. Evolution, 61:368–376.PubMedCrossRefGoogle Scholar
  55. 55.
    Kopp M, Gavrilets S. (2006) Multilocus genetics and the coevolution of quantitative traits. Evolution, 60:1321–1336.PubMedGoogle Scholar
  56. 56.
    Rispe C, Moran NA. (2000) Accumulation of deleterious mutations in endosymbionts: Muller’s ratchet with two levels of selection. Am Nat, 156:425–441.CrossRefGoogle Scholar
  57. 57.
    Wolfram Research Inc. (2008) Mathematica Version 7.0. Wolfram Research Inc., Champaign, IL.Google Scholar
  58. 58.
    MathWorks. (2009) MATLAB Version 7.9. MathWorks, Natick, MA.Google Scholar
  59. 59.
    R Development Core Team. (2009) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  60. 60.
    Ritchie D. (1972) C Programming Language. Bell Telephone Laboratories, Murray Hill, NJ.Google Scholar
  61. 61.
    Stroustrup B. (1979) C++ Programming Language. Bell Telephone Laboratories, Murray Hill, NJ.Google Scholar
  62. 62.
    Railsback SF, Lytinen SL, Jackson SK. (2006) Agent-based simulation platforms: review and development recommendations. Simul Trans Soc Model Simul Int, 82:609–623.CrossRefGoogle Scholar
  63. 63.
    Foster KR, Wenseleers T. (2006) A general model for the evolution of mutualisms. J Evol Biol, 19:1283–1293.PubMedCrossRefGoogle Scholar
  64. 64.
    Griffin A, West S, Buckling A. (2004) Cooperation and competition in pathogenic bacteria. Nature, 430:1024.PubMedCrossRefGoogle Scholar
  65. 65.
    Morgan AD, Gandon S, Buckling A. (2005) The effect of migration on local adaptation in a coevolving host–parasite system. Nature, 437:253–256.PubMedCrossRefGoogle Scholar
  66. 66.
    Buckling A, Brockhurst MA (2008) Kin selection and the evolution of virulence. Heredity, 100:484–488.PubMedCrossRefGoogle Scholar
  67. 67.
    Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol, 21:585–592.Google Scholar
  68. 68.
    Otto SP, Day T. (2007) A Biologist’s Guide to Mathematical Modeling in Ecology and Evolution. Princeton University Press, Princeton, NJ.Google Scholar
  69. 69.
    Edelstein-Keshet L. (1988) Mathematical Models in Biology. Random House, New York, NY.Google Scholar
  70. 70.
    Hastings A. (1997) Population Biology: Concepts and Models. Springer, New York, NY.Google Scholar
  71. 71.
    Connor RC. (1995) The benefits of mutualism: a conceptual framework. Biol Rev Camb Philos Soc, 70:427–457.CrossRefGoogle Scholar
  72. 72.
    Hofbauer J, Sigmund K. (1998) Evolutionary Games and Population Dynamics. Cambridge University Press, Cambridge.Google Scholar
  73. 73.
    McElreath R, Boyd R. (2007) Mathematical Models of Social Evolution: A Guide for the Perplexed. University of Chicago Press, Chicago, IL.Google Scholar
  74. 74.
    Dercole F, Rinaldi S. (2008) Analysis of Evolutionary Processes: The Adaptive Dynamics Approach and Its Applications. Princeton University Press, Princeton, NJ.Google Scholar
  75. 75.
    Taylor PD, Frank SA. (1996) How to make a kin selection model. J Theor Biol, 180:27–37.PubMedCrossRefGoogle Scholar
  76. 76.
    Roughgarden J. (1979) Theory of Population Genetics and Evolutionary Ecology: An Introduction. Macmillan Publishing Company, New York, NY.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of Molecular and Computational BiologyUniversity of Southern CaliforniaLos AngelesUSA
  2. 2.School of Biological SciencesWashington State UniversityPullmanUSA

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