Biology & Philosophy

, Volume 29, Issue 4, pp 477–515 | Cite as

Inclusive fitness and the sociobiology of the genome

Article

Abstract

Inclusive fitness theory provides conditions for the evolutionary success of a gene. These conditions ensure that the gene is selfish in the sense of Dawkins (The selfish gene, Oxford University Press, Oxford, 1976): genes do not and cannot sacrifice their own fitness on behalf of the reproductive population. Therefore, while natural selection explains the appearance of design in the living world (Dawkins in The blind watchmaker: why the evidence of evolution reveals a universe without design, W. W. Norton, New York, 1996), inclusive fitness theory does not explain how. Indeed, Hamilton’s rule is equally compatible with the evolutionary success of prosocial altruistic genes and antisocial predatory genes, whereas only the former, which account for the appearance of design, predominate in successful organisms. Inclusive fitness theory, however, permits a formulation of the central problem of sociobiology in a particularly poignant form: how do interactions among loci induce utterly selfish genes to collaborate, or to predispose their carriers to collaborate, in promoting the fitness of their carriers? Inclusive fitness theory, because it abstracts from synergistic interactions among loci, does not answer this question. Fitness-enhancing collaboration among loci in the genome of a reproductive population requires suppressing alleles that decrease, and promoting alleles that increase the fitness of its carriers. Suppression and promotion are effected by regulatory networks of genes, each of which is itself utterly selfish. This implies that genes, and a fortiori individuals in a social species, do not maximize inclusive fitness but rather interact strategically in complex ways. It is the task of sociobiology to model these complex interactions.

Keywords

Inclusive fitness Hamilton’s rule Sociobiology 

References

  1. Abbot P et al (2011) Inclusive fitness and eusociality. Nature 471:E1–E4CrossRefGoogle Scholar
  2. Akçay E, van Cleve J (2012) Behavioral responses in structured populations pave the way to group optimality. Am Nat 179(2):257–269CrossRefGoogle Scholar
  3. Akçay E, Roughgarden J (2011) The evolution of payoff matrices: providing incentives to cooperate. Proc R Soc B 278:2198–2206CrossRefGoogle Scholar
  4. Akin E (1982) Cycling in simple genetic systems. J Math Biol 13(3):305–324CrossRefGoogle Scholar
  5. Bourke AFG (2011) Principles of social evolution. Oxford University Press, OxfordCrossRefGoogle Scholar
  6. Bowles S, Gintis H (2011) A cooperative species: human reciprocity and its evolution. Princeton University Press, PrincetonGoogle Scholar
  7. Brown JL (1974) Alternate routes to sociality in jays—with a theory for the evolution of altruism and communal breeding. Am Zool 14(1):63–80Google Scholar
  8. Burt A, Trivers R (2006) Genes in conflict: the biology of selfish genetic elements. Harvard University Press, CambridgeGoogle Scholar
  9. Buss LW (1987) The evolution of individuality. Princeton University Press, PrincetonGoogle Scholar
  10. Charnov EL (1978) Sex-ratio selection in eusocial Hymenoptera. Am Nat 112(984):317–326CrossRefGoogle Scholar
  11. Crow JF (1954) Breeding structure of populations. II. Effective population number. In: Kempthorne O, Bancroft TA, Gowen JW, Lush JL (eds) Statistics and mathematics in biology, Iowa State University Press, Ames, IA, pp 543–556Google Scholar
  12. Darwin C (1871) The descent of man, and selection in relation to sex. Murray, LondonCrossRefGoogle Scholar
  13. Dawkins R (1976) The selfish gene. Oxford University Press, OxfordGoogle Scholar
  14. Dawkins R (1982) Replicators and vehicles. In: King’s College Sociobiology Group (eds) Current problems in sociobiology. Cambridge University Press, Cambridge, pp 45–64Google Scholar
  15. Dawkins R (1996) The blind watchmaker: why the evidence of evolution reveals a universe without design. W. W. Norton, New YorkGoogle Scholar
  16. Dobzhansky T (1953) A review of some fundamental concepts and problems of population genetics. In: Cold Springs Harbor Symposium, pp 1–15Google Scholar
  17. Edwards AWF (1994) The fundamental theorem of natural selection. Biol Rev 69:443–474CrossRefGoogle Scholar
  18. Elaydi SN (1999) An introduction to difference equations. Springer, New YorkCrossRefGoogle Scholar
  19. Ewens WJ (1969) A generalized fundamental theorem of natural selection. Genetics 63:531–537Google Scholar
  20. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Benjamin Cummings, New YorkGoogle Scholar
  21. Feldman MW, Liberman U (1986) An evolutionary reduction principle for genetic modifiers. Proc Natl Acad Sci 83(13):4824–4827CrossRefGoogle Scholar
  22. Fisher RA (1915) The evolution of sexual preference. Eugen Rev 7:184–192Google Scholar
  23. Fletcher JA, Doebili M (1915) A simple and general explanation for the evolution of altruism. Proc R Soc B 276:13–19CrossRefGoogle Scholar
  24. Foster KR, Wenseleers T, Ratnieks FLW (2001) Spite: Hamilton’s unproven theory. Ann Zool Fennici 38:229–238Google Scholar
  25. Frank SA (1996) Models of parasite virulence. Q Rev Biol 71:37–78CrossRefGoogle Scholar
  26. Frank SA (1997) The Price equation, Fisher’s fundamental theorem, kin selection, and causal analysis. Evolution 51(6):1712–1729CrossRefGoogle Scholar
  27. Frank SA (1998) Foundations of social evolution. Princeton University Press, PrincetonGoogle Scholar
  28. Frank SA (2003) Repression of competition and the evolution of cooperation. Evolution 57:693–705Google Scholar
  29. Frank SA, Slatkin M (1992) Fisher’s fundamental theorem of natural selection. Trends Ecol Evol 7(3):92–95CrossRefGoogle Scholar
  30. Galef BG, Laland KN (2005) Social learning in animals: empirical studies and theoretical models. Bioscience 55(6):489–499CrossRefGoogle Scholar
  31. Gardner A, Welsh JJ (2011) A formal theory of the selfish gene. J Evol Biol 24:1801–1813CrossRefGoogle Scholar
  32. Gardner A, West SA, Buckling A (2004) Bacteriocins, spite and virulence. Proc R Soc Lond B 271:1529–1535CrossRefGoogle Scholar
  33. Gardner A, West SA, Wild G (2011) The genetical theory of kin selection. J Evol Biol 24:1020–1043CrossRefGoogle Scholar
  34. Gardner A, West SA, Barton NH (2007) The relation between multilocus population genetics and social evolution theory. Am Nat 169(2):207–226CrossRefGoogle Scholar
  35. Gardner H (2009) The bounds of reason: game theory and the unification of the behavioral sciences. Princeton University Press, PrincetonGoogle Scholar
  36. Gardner H (2009) Game theory evolving. 2nd edn. Princeton University Press, PrincetonGoogle Scholar
  37. Goodnight C, Rauch E, Sayama H, De Aguiar MA, Baranger M, Bar-yam Y (2005) Evolution in spatial predator–prey models and the ‘prudent predator’: the inadequacy of steady-state organism fitness and the concept of individual and group selection. Complexity 13(5):23–44CrossRefGoogle Scholar
  38. Grafen A (1984) Natural selection, kin selection, and group selection. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, Sinauer, Sunderland, MAGoogle Scholar
  39. Grafen A (1985) A geometric view of relatedness. In: Dawkins R, Ridley M (eds) Oxford surveys in evolutionary biology, vol 2, Oxford University Press, Oxford, pp 28–89Google Scholar
  40. Grafen A (1999) Formal darwinism, the individual-as-maximizing-agent: analogy, and bet-hedging. Proc R Soc Lond B 266:799–803Google Scholar
  41. Grafen A (2002) A first formal link Between the Price equation and an optimization program. J Theor Biol 217:75–91CrossRefGoogle Scholar
  42. Grafen A (2006) Optimization of inclusive fitness. J Theor Biol 238:541–563CrossRefGoogle Scholar
  43. Haig D, Grafen A (1991) Genetic scrambling as a defence against meiotic drive. J Theor Biol 153(4):531–558CrossRefGoogle Scholar
  44. Hamilton WD (1963) The evolution of altruistic behavior. Am Nat 96:354–356CrossRefGoogle Scholar
  45. Hamilton WD (1964a) The genetical evolution of social behavior, I. J Theor Biol 7:1–16CrossRefGoogle Scholar
  46. Hamilton WD (1964b) The genetical evolution of social behavior, II. J Theor Biol 7:17–52Google Scholar
  47. Hamilton WD (1970b) Selfish and spiteful behaviour in an evolutionary model. Nature 228:1218–1220Google Scholar
  48. Hamilton WD (1975) Innate social aptitudes of man: an approach from evolutionary genetics. In: Robin F (eds) Biosocial anthropology, Wiley, New York, pp 115–132Google Scholar
  49. Hamilton WD, Peter H, Leimar O (2006) Cooperating for direct fitness benefits. J Evol Biol 19:1400–1402CrossRefGoogle Scholar
  50. Hamilton WD, Reichert S (1988) Payoffs and strategies in spider territorial contests: ESS analysis of two ecotypes. Evol Ecol 2:115–138CrossRefGoogle Scholar
  51. Hardin G (1968) The tragedy of the commons. Science 162:1243–1248CrossRefGoogle Scholar
  52. Holland JH (1986) Escaping brittleness: the possibilities of general purpose learning algorithms applied to parallel Rule-based systems. In: Michalski RS, Carbonell JG, Mitchell TM (eds) Machine learning: an artificial intelligence approach, Morgan Kaufmann, Los Altos, CAGoogle Scholar
  53. Hölldobler B, Wilson EO (1990) The ants. BelKnap Press, CambridgeCrossRefGoogle Scholar
  54. Keller L, Ross KG (1998) Selfish genes: a green beard in the red fire ant. Science 394:573–575Google Scholar
  55. Koella JC (2000) The spatial spread of altruism versus the evolutionary response of egoists. Proc R Soc B 267(1456):1979–1985Google Scholar
  56. Krackauer AH (2005) Kin selection and cooperative courtship in wild turkeys. Nat Biotechnol 434:69–72Google Scholar
  57. Leffler EM (2013) Multiple instances of ancient balancing selection shared between humans and chimpanzees. Science 339:1578–1582CrossRefGoogle Scholar
  58. Leigh EG (1971) Adaptation and diversity. Freeman, Cooper, San Francisco, CAGoogle Scholar
  59. Leigh EG (1977) How does selection reconcile individual advantage with the good of the group? Proc Natl Acad Sci USA 74(10):4542–4546Google Scholar
  60. Levin SA (2009) Games, groups, and the global good. Springer, New YorkCrossRefGoogle Scholar
  61. Lewontin RC (1970) The units of selection. In: Johnston R (eds) Annual review of ecology and systematics, Annual Review Inc., Palo AltoGoogle Scholar
  62. Malécot G (1948) Les Mathématiques de l’Hérédité. Masson, ParisGoogle Scholar
  63. Mandeville B (1924) The fable of the bees: private vices, publick benefits. Clarendon, Oxford, 1924[1705]Google Scholar
  64. Mas-Colell A, Whinston MD, Green JR (1995) Microeconomic theory. Oxford University Press, New YorkGoogle Scholar
  65. Maynard Smith J (1964) Group selection and kin selection. Nature 201:1145–1147CrossRefGoogle Scholar
  66. Maynard Smith J (1982) Evolution and the theory of games. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  67. Maynard Smith J (1988) Evolutionary progress and levels of selection. In: Nitecki MH (eds) Evolutionary progress, University of Chicago Press, Chicago, pp 219–230Google Scholar
  68. Maynard Smith J, Szathmáry E (1995) The major evolutionary transitions. Nature 374:227–232CrossRefGoogle Scholar
  69. Maynard Smith J, Szathmáry E (1997) The major transitions in evolution. Oxford University Press, OxfordGoogle Scholar
  70. Maynard Smith J, Ridpath MG (1972) Wife sharing in the Tasmanian native hen, Tribonyx mortierii: a case of kin selection? Am Nat 96:447CrossRefGoogle Scholar
  71. Mayr E (1997) The objects of selection. Proc Natl Acad Sci 94:2091–2094Google Scholar
  72. Metz JAJ, Mylius SD, Diekmann O (2008) When does evolution optimize. Evol Ecol Res 10:629–654Google Scholar
  73. Michod RE (1997) Cooperation and conflict in the evolution of individuality. 1. The multilevel selection of the organism. Am Nat 149:607–645CrossRefGoogle Scholar
  74. Michod RE, Hamilton W (1980) Coefficients of relatedness in sociobiology. Nature 288:694–697CrossRefGoogle Scholar
  75. Mitchell M (2009) Complexity: a guided tour. Oxford University Press, OxfordGoogle Scholar
  76. Moran PAP (1964) On the nonexistence of adaptive topographies. Ann Hum Genet 27:383–393CrossRefGoogle Scholar
  77. Morowitz H (2002) The emergence of everything: how the world became complex. Oxford University Press, OxfordGoogle Scholar
  78. Noble D (2011) Neo-Darwinism, the modern synthesis and selfish genes: are they of use in physiology? J Physiol 589(5):1007–1015CrossRefGoogle Scholar
  79. Nowak MA (2006) Evolutionary dynamics: exploring the equations of life. Belknap Press, CambridgeGoogle Scholar
  80. Nowak MA (2006) Five rules for the evolution of cooperation. Science 314:1560–1563CrossRefGoogle Scholar
  81. Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466(26):1057–1062CrossRefGoogle Scholar
  82. Olson M (1965) The logic of collective action: public goods and the theory of groups. Harvard University Press, CambridgeGoogle Scholar
  83. Pepper JW (2007) Simple models of assortment through environmental feedback. Artif Life 13(1):1–9CrossRefGoogle Scholar
  84. Price GR (1970) Selection and covariance. Nature 227:520–521CrossRefGoogle Scholar
  85. Price GR (1972) Fisher’s ‘fundamental theorem’ made clear. Ann Hum Genet 36:129–140CrossRefGoogle Scholar
  86. Queller DC (1992) A general model for kin selection. Evolution 42(2):376–380CrossRefGoogle Scholar
  87. Ratnieks F (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132(2):217–236CrossRefGoogle Scholar
  88. Ratnieks FLW, Reeves HK (1992) Conflict in single-queen hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species. J Theor Biol 158:33–65CrossRefGoogle Scholar
  89. Ridley M, Grafen A (1981) Are green beard genes outlaws? Anim Behav 29(3):954–955CrossRefGoogle Scholar
  90. Riley MA, Lizotte-Waniewski M (2009) Population genomics and the bacterial species concept. Methods Mol Biol 532:367–377CrossRefGoogle Scholar
  91. Rousset F, Billard S (2007) A theoretical basis for measures of kin selection in subdivided populations. Proc Natl Acad Sci 61:2320–2330Google Scholar
  92. Skutch AF (1961) Helpers among birds. Condor 63:198–226CrossRefGoogle Scholar
  93. Smaldino PE, Schank JC, McElreath R (2013) Increased costs of cooperation help cooperators in the long run. Am Nat 181(4):451–463CrossRefGoogle Scholar
  94. Sober E, Lewontin RC (1982) Artifact, cause, and genic selection. Philos Sci 48:157–180CrossRefGoogle Scholar
  95. Takeuchi Y (1996) Global dynamical properties of Lotka–Volterra systems. World Scientific, SingaporeCrossRefGoogle Scholar
  96. Taylor P (1989) Evolutionary stability in one-parameter models under weak selection. Theor Popul Biol 36(2):125–143CrossRefGoogle Scholar
  97. Taylor P (1992) Altruism in viscous populations: an inclusive fitness model. Evol Ecol 6:352–356CrossRefGoogle Scholar
  98. Taylor P (1996) Inclusive fitness arguments in genetic models of behavior. J Math Biol 34:654–674CrossRefGoogle Scholar
  99. Traulsen A, Nowak MA (2006) Evolution of cooperation by multilevel selection. Proc Natl Acad Sci 103(29):10952–10955Google Scholar
  100. Trivers RL, Hare H (1976) Haplodiploidy and the evolution of social insects. Science 191:249–263CrossRefGoogle Scholar
  101. Uyenoyama MK, Feldman MW (1980) Theories of kin and group selection: a population genetics approach. Theor Popul Biol 17:380–414CrossRefGoogle Scholar
  102. van Veelen Ma (2009) Group selection, kin selection, altruism, and cooperation: when inclusive fitness is right and when it can be wrong. J Theor Biol 259:589–600CrossRefGoogle Scholar
  103. Weibull JW (1995) Evolutionary game theory. MIT Press, Cambridge, MAGoogle Scholar
  104. Wenseleers T, Ratnieks FLW (2004) Tragedy of the commons in Melipona bees. Proc R Soc Lond B 271:S310–S312Google Scholar
  105. West-Eberhard MJ (1975) The evolution of social behavior by kin selection. Q Rev Biol 50:1–33CrossRefGoogle Scholar
  106. West SA (2009) Sex allocation. Princeton University Press, Princeton, NJGoogle Scholar
  107. West SA, Diggle SP, Buckling A, Gardner A, Griffin AS (2007) The social lives of microbes. Annu Rev Ecol Evol Syst 38:53–77CrossRefGoogle Scholar
  108. West S, Mouden CE, Gardner A (2011) Sixteen common misconceptions about the evolution of cooperation in humans. Evol Hum Behav 32(4):231–262CrossRefGoogle Scholar
  109. Wheeler WM (1928) The social insects. Harcourt, Brace, New YorkGoogle Scholar
  110. Wilson DSl (1977) Structured demes and the evolution of group-advantageous traits. Am Nat 111:157–185CrossRefGoogle Scholar
  111. Wilson DS, Pollock GB, Dugatkin LA (1992) Can altruism evolve in purely viscous populations? Evol Ecol 6:331–341CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Santa Fe InstituteSanta FeUSA

Personalised recommendations