Biology & Philosophy

, Volume 29, Issue 4, pp 445–476 | Cite as

Gene mobility and the concept of relatedness

Article

Abstract

Cooperation is rife in the microbial world, yet our best current theories of the evolution of cooperation were developed with multicellular animals in mind. Hamilton’s theory of inclusive fitness is an important case in point: applying the theory in a microbial setting is far from straightforward, as social evolution in microbes has a number of distinctive features that the theory was never intended to capture. In this article, I focus on the conceptual challenges posed by the project of extending Hamilton’s theory to accommodate the effects of gene mobility. I begin by outlining the basics of the theory of inclusive fitness, emphasizing the role that the concept of relatedness is intended to play. I then provide a brief history of this concept, showing how, over the past fifty years, it has departed from the intuitive notion of genealogical kinship to encompass a range of generalized measures of genetic similarity. I proceed to argue that gene mobility forces a further revision of the concept. The reason in short is that, when the genes implicated in producing social behaviour are mobile, we cannot talk of an organism’s genotype simpliciter; we can talk only of an organism’s genotype at a particular stage in its life cycle. We must therefore ask: with respect to which stage(s) in the life cycle should relatedness be evaluated? For instance: is it genetic similarity at the time of social interaction that matters to the evolution of social behaviour, or is it genetic similarity at the time of reproduction? I argue that, strictly speaking, it is neither of these: what really matters to the evolution of social behaviour is diachronic genetic similarity between the producers of fitness benefits at the time they produce them and the recipients of those benefits at the end of their life-cycle. I close by discussing the implications of this result. The main payoff is that it makes room for a possible new mechanism for the evolution of altruism in microbes that does not require correlated interaction among bearers of the genes for altruism. The importance of this mechanism in nature remains an open empirical question.

Keyword

Gene mobility Kin selection Inclusive fitness Microbiology Relatedness Social evolution 

References

  1. Berleman JE, Chumley T, Cheung P, Kirby JR (2006) Rippling is a predatory behavior in Myxococcus xanthus. J Bacteriol 188:5888–5895CrossRefGoogle Scholar
  2. Biernaskie JM, West SA, Gardner A (2011) Are greenbeards intragenomic outlaws? Evolution 65:2729–2742CrossRefGoogle Scholar
  3. Birch J (2014) Hamilton’s rule and its discontents. Br J Philos Sci. doi:10.1093/bjps/axt016
  4. Bonner JT (1959) The cellular slime molds. Princeton University Press, PrincetonGoogle Scholar
  5. Bourke AFG (2011a) Principles of social evolution. Oxford University Press, OxfordCrossRefGoogle Scholar
  6. Bourke AFG (2011b) The validity and value of inclusive fitness theory. Proc Roy Soc Lond B Biol Sci 278:3313–3320CrossRefGoogle Scholar
  7. Breden F (1990) Partitioning of covariance as a method for studying kin selection. Trends Ecol Evol 5:224–228CrossRefGoogle Scholar
  8. Bushman F (2002) Lateral DNA transfer: mechanisms and consequences. Cold Spring Harbor Laboratory Press, Coldspring Spring HarborGoogle Scholar
  9. Cockerham CC (1954) An extension of the concept of partitioning hereditary variance for analysis of covariances among relatives when epistasis is present. Genetics 39:8659–882Google Scholar
  10. Cornforth DM, Sumpter DJ, Brown SP, Brnnstrm (2012) Synergy and group size in microbial cooperation. Am Nat 180:296–305CrossRefGoogle Scholar
  11. Crespi BJ (2001) The evolution of social behaviour in microorganisms. Trends Ecol Evol 16:178–183CrossRefGoogle Scholar
  12. Davies NB, Krebs JR, West SA (2012) An introduction to behavioural ecology. Wiley, HobokenGoogle Scholar
  13. Dawkins R (1976) The selfish gene. W. W. Norton and Company, New YorkGoogle Scholar
  14. Dunning Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Muoz Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, Ingram J, Nene RV, Shepard J, Tomkins J, Richards S, Spiro DJ, Ghedin E, Slatko BE, Tettelin H, Werren JH (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753–1756CrossRefGoogle Scholar
  15. Dupré J (2012) Processes of life: essays in the philosophy of biology. Oxford University Press, New YorkGoogle Scholar
  16. Falconer DS (1961) Introduction to quantitative genetics (\(1^{{\rm st}}\) edition). Oliver and Boyd, EdinburghGoogle Scholar
  17. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics (\(4^{{\rm th}}\) edition). Longman, LondonGoogle Scholar
  18. Fisher RA (1918) The correlation between relatives on the supposition of Mendelian inheritance. Trans Roy Soc Edinburgh 52:399–433CrossRefGoogle Scholar
  19. Fisher RA (1930) The genetical theory of natural selection, 1st edn. Clarendon Press, OxfordGoogle Scholar
  20. Fisher RA (1941) Average excess and average effect of a gene substitution. Ann Hum Genet 11:53–63Google Scholar
  21. Frank SA (1997) Models of symbiosis. Am Nat 150:S80–S99CrossRefGoogle Scholar
  22. Frank SA (1998) Foundations of social evolution. Princeton University Press, PrincetonGoogle Scholar
  23. Frank SA (2006) Social selection. In: Fox CW, Wolf JB (eds) Evolutionary genetics: concepts and case studies. Oxford University Press, Oxford, pp 350–363Google Scholar
  24. Frost LS, Leplae R, Summers AO, Toussaint A (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3:722–732CrossRefGoogle Scholar
  25. Gardner A, Foster KR (2008) The evolution and ecology of cooperation history and concepts. In: Korb J, Heinze J (eds) Ecology of social evolution. Springer, Heidelberg, pp 1–36CrossRefGoogle Scholar
  26. Gardner A, West SA (2004a) Spite and the scale of competition. J Evol Biol 17:1195–1203CrossRefGoogle Scholar
  27. Gardner A, West SA (2004b) Spite among siblings. Science 305:1413–1414CrossRefGoogle Scholar
  28. Gardner A, West SA (2006) Spite. Curr Biol 16:R662–R664CrossRefGoogle Scholar
  29. Gardner A, West SA (2010) Greenbeards. Evolution 64:25–38CrossRefGoogle Scholar
  30. Gardner A, West SA, Wild G (2011) The genetical theory of kin selection. J Evol Biol 24:1020–1043CrossRefGoogle Scholar
  31. Giraud T, Shykoff JA (2011) Bacterial controlled by mobile elements: kin selection versus infectivity. Heredity 107:277–278CrossRefGoogle Scholar
  32. Grafen A (1985) A geometrical view of relatedness. Oxf Surv Evol Biol 2:28–89Google Scholar
  33. Grafen A (2006) Optimization of inclusive fitness. J Theor Biol 238:541–563CrossRefGoogle Scholar
  34. Haldane JBS (1955) Population genetics. In: Johnson ML, Abercrombie M, Fogg GE (eds) New Biology 18. Penguin, London, pp 34–51Google Scholar
  35. Haldane JBS, Jayakar SD (1962) An enumeration of some human relationships. J Genet 58:81–107CrossRefGoogle Scholar
  36. Hamilton WD (1963) The evolution of altruistic behaviour. Am Nat 97:354–356CrossRefGoogle Scholar
  37. Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1–52CrossRefGoogle Scholar
  38. Hamilton WD (1970) Selfish and spiteful behaviour in an evolutionary model. Nature 228:1218–1220CrossRefGoogle Scholar
  39. Hamilton WD (1971) Selection of selfish and altruistic behaviour in some extreme models. In: Eisenberg JF, Dillon WS (eds) Man and beast: comparative social behavior. Smithsonian Press, Washington, pp 57–91Google Scholar
  40. Hamilton WD (1972) Altruism and related phenomena, mainly in social insects. Ann Rev Ecol Syst 3:193–232CrossRefGoogle Scholar
  41. Hamilton WD (1975) Innate social aptitudes of man: an approach from evolutionary genetics. In: Fox R (ed) Biosocial anthropology. Wiley, New York, pp 133–155Google Scholar
  42. Hardin R (1982) Collective action. John Hopkins University Press, BaltimoreGoogle Scholar
  43. Kagel JH, Roth AE (eds) (1995) The handbook of experimental economics. Princeton University Press, PrincetonGoogle Scholar
  44. Kempthorne O (1954) The correlation between relatives in a random mating population. Proc Roy Soc Lond B Biol Sci 143:103–113CrossRefGoogle Scholar
  45. Kempthorne O (1955) The theoretical values of correlations between relatives in random mating populations. Genetics 40:153–167Google Scholar
  46. Kempthorne O (1957) An introduction to genetic statistics. Wiley, OxfordGoogle Scholar
  47. Lederberg ND, Tatum J (1946) Genetic exchange in Salmonella. J Bacteriol 64:679–699Google Scholar
  48. Lewis D (1970) How to define theoretical terms. J Philos 67:427–446CrossRefGoogle Scholar
  49. Li CC, Sacks L (1954) The derivation of joint distribution and correlation between relatives by the use of stochastic matrices. Biometrics 10:347–360CrossRefGoogle Scholar
  50. McElreath R, Boyd R (2007) Mathematical models of social evolution: a guide for the perplexed. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  51. Mc Ginty SÉ, Rankin DJ, Brown SP (2011) Horizontal gene transfer and the evolution of bacterial cooperation. Evolution 65:21–32CrossRefGoogle Scholar
  52. Mc Ginty SÉ, Rankin DJ (2012) The evolution of conflict resolution between plasmids and their bacterial hosts. Evolution 66:1662–1670CrossRefGoogle Scholar
  53. Mc Ginty SÉ, Lehmann L, Brown SP, Rankin DJ (2013) The interplay between relatedness and horizontal gene transfer drives the evolution of plasmid-carried public goods. Proc Roy Soc Lond B Biol Sci 280:20130400CrossRefGoogle Scholar
  54. Marshall JAR (2011) Group selection and kin selection: formally equivalent approaches. Trends Ecol Evol 26:325–332CrossRefGoogle Scholar
  55. Maynard Smith J (1964) Group selection and kin selection. Nature 200:1145–1147CrossRefGoogle Scholar
  56. Maynard Smith J (1976) Letter to New Scientist. New Sci 71:247Google Scholar
  57. Michod RE, Hamilton WD (1980) Coefficients of relatedness in socio-biology. Nature 288:694–697CrossRefGoogle Scholar
  58. Nogueira T, Rankin DJ, Touchon M, Taddei F, Brown SP, Rocha EPC (2009) Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence. Curr Biol 19(20):1683–1691CrossRefGoogle Scholar
  59. Olson M (1965) The logic of collective action: public goods and the theory of groups. Harvard University Press, CambridgeGoogle Scholar
  60. Okasha, S. 2013. Biological altruism. In E. Zalta (ed), The Stanford encyclopedia of philosophy (Fall 2013 edition). URL=[http://plato.stanford.edu/archives/fall2013/entries/altruism-biological/] (Accessed 18/03/2014)
  61. O’Malley M (ed) (2010) The tree of life [special issue]. Biol Philos 25(4)Google Scholar
  62. O’Malley M (ed) (2013) Philosophy and the microbe [special issue]. Biol Philos 28(2)Google Scholar
  63. O’Malley M, Boucher Y (eds) (2011) Beyond the tree of life. Biol Direct 25(4)Google Scholar
  64. Orlove MJ, Wood CL (1978) Coefficients of relationship and coefficients of relatedness in kin selection: a covariance form for the RHO formula. J Theor Biol 73:679–686CrossRefGoogle Scholar
  65. Pepper JW (2000) Relatedness in trait-group models of social evolution. J Theor Biol 206:355–368CrossRefGoogle Scholar
  66. Price GR (1970) Selection and covariance. Nature 227:520–1CrossRefGoogle Scholar
  67. Price GR (1972) Extension of covariance selection mathematics. Ann Hum Genet 35:485–490CrossRefGoogle Scholar
  68. Provine WB (1971) The origins of theoretical population genetics. Chicago University Press, ChicagoGoogle Scholar
  69. Queller DC (1985) Kinship, reciprocity, and synergism in the evolution of social behaviour. Nature 318:366–7CrossRefGoogle Scholar
  70. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  71. Rankin DJ, Rocha EPC, Brown SP (2011a) What traits are carried on mobile genetic elements, and why? Heredity 106:1–10CrossRefGoogle Scholar
  72. Rankin DJ, Mc Ginty SE, Nogueira T, Touchon M, Taddei F, Rocha EPC, Brown SP (2011b) Bacterial cooperation controlled by mobile genetic elements: kin selection and infectivity are part of the same process. Heredity 107:279–281CrossRefGoogle Scholar
  73. Ridley M, Grafen A (1981) Are green beard genes outlaws? Anim Behav 29:954–955CrossRefGoogle Scholar
  74. Parsek MR, Greenberg EP (2005) Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol 13:27–33CrossRefGoogle Scholar
  75. Seger J (1981) Kinship and covariance. J Theor Biol 91:191–213CrossRefGoogle Scholar
  76. Smead R, Forber P (2013) The evolutionary dynamics of spite in finite populations. Evolution 67:698–707CrossRefGoogle Scholar
  77. Smith J (2001) The social evolution of bacterial pathogenesis. Proc R Soc Lond B Biol Sci 268:61–69Google Scholar
  78. Smith J, van Dyken JD, Zee PC (2010) A generalization of Hamiltons rule for the evolution of microbial cooperation. Science 328:1700–1703CrossRefGoogle Scholar
  79. Strassmann JE, Queller DC (2011) Evolution of cooperation and control of cheating in a social microbe. Proc Natl Acad Sci USA 108:10855–10862CrossRefGoogle Scholar
  80. Strassmann JE, Zhu Y, Queller DC (2000) Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408:965–967CrossRefGoogle Scholar
  81. Thomas CM, Nielsen KM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711–721CrossRefGoogle Scholar
  82. Toro M, Abugov R, Charlesworth B, Michod RE (1982) Exact versus heuristic models of kin selection. J Theor Biol 97:699–713CrossRefGoogle Scholar
  83. Úbeda F, Gardner A (2012) Genomic imprinting in the social brain: elders. Evolution 66:1567–81CrossRefGoogle Scholar
  84. Uyenoyama MK, Feldman MW (1981) On relatedness and adaptive topography in kin selection. Theor Popul Biol 19:87–123CrossRefGoogle Scholar
  85. Velicer GJ, Vos M (2009) Sociobiology of the myxobacteria. Annu Rev Microbiol 63:599–623CrossRefGoogle Scholar
  86. Wenseleers T, Gardner A, Foster KR (2010) Social evolution theory: a review of methods and approaches. In: Szkely T, Moore AJ, Komdeur J (eds) Social behaviour: genes, ecology and evolution. Cambridge University Press, Cambridge, pp 132–58CrossRefGoogle Scholar
  87. West SA, Gardner A (2010) Altruism, spite and greenbeards. Science 327:1341–1344CrossRefGoogle Scholar
  88. West SA, Gardner A (2013) Inclusive fitness and adaptation. Curr Biol 23:R577–R584CrossRefGoogle Scholar
  89. West SA, Griffin AS, Gardner A (2007b) Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol 20:415–432CrossRefGoogle Scholar
  90. West SA, Griffin AS, Gardner A, Diggle SP (2006) Social evolution theory for microbes. Nat Rev Microbiol 4:597–607CrossRefGoogle Scholar
  91. West SA, Diggle SP, Buckling A, Gardner A, Griffin AS (2007a) The social lives of microbes. Annu Rev Ecol Evol Syst 38:53–77CrossRefGoogle Scholar
  92. Wright S (1922) Coefficients of inbreeding and relationship. Am Nat 56:330–338CrossRefGoogle Scholar
  93. Zinder ND, Lederberg J (1952) Genetic exchange in Salmonella. J Bacteriol 64:679–699Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Christ’s CollegeUniversity of CambridgeCambridgeUK

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