The validity and value of inclusive fitness theory

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1723, 2011, Pages 3313-3320

  Bourke, Andrew F G ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Altruism; Eusociality; Inclusive fitness; Kin selection; Relatedness; Social evolution

Indexed keywords

ALTRUISM; EUSOCIALITY; EVOLUTIONARY BIOLOGY; INCLUSIVE FITNESS; KIN SELECTION; LITERATURE REVIEW; QUEEN; RELATEDNESS; WORKER CASTE;

EID: 80053934775     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.1465     Document Type: Review

References (106)

1. Hamilton, W. D. 1964 The genetical evolution of social behaviour I, II. J. Theor. Biol. 7, 1-52. (doi:10.1016/0022-5193(64)90038-4)
2. Grafen, A. 1985 A geometric view of relatedness. In Oxford surveys in evolutionary biology, vol. 2 (eds R. Dawkins & M. Ridley), pp. 28-89. Oxford, UK: Oxford University Press.
3. Lehmann, L. & Keller, L. 2006 The evolution of cooperation and altruism-a general framework and a classification of models. J. Evol. Biol. 19, 1365-1376. (doi:10.1111/j.1420-9101.2006.01119.x)
4. West, S. A., Griffin, A. S. & Gardner, A. 2007 Evolutionary explanations for cooperation. Curr. Biol. 17, R661-R672. (doi:10.1016/j.cub.2007.06.004)
5. Bourke, A. F. G. 2011 Principles of social evolution. Oxford, UK: Oxford University Press.
6. West, S. A., Diggle, S. P., Buckling, A., Gardner, A. & Griffin, A. S. 2007 The social lives of microbes. Annu. Rev. Ecol. Evol. Syst. 38, 53-77. (doi:10.1146/annurev. ecolsys.38.091206.095740)
7. Cant, M. A. & Johnstone, R. A. 2008 Reproductive conflict and the separation of reproductive generations in humans. Proc. Natl Acad. Sci. USA 105, 5332-5336. (doi:10.1073/pnas.0711911105)
8. Dawkins, R. 1976 The selfish gene. Oxford, UK: Oxford University Press.
9. Hamilton, W. D. 1972 Altruism and related phenomena, mainly in social insects. Annu. Rev. Ecol. Syst. 3, 193-232. (doi:10.1146/annurev.es.03.110172.001205)
10. Dawkins, R. 1979 Twelve misunderstandings of kin selection. Z. Tierpsychol. 51, 184-200.
11. Killingback, T., Bieri, J. & Flatt, T. 2006 Evolution in group-structured populations can resolve the tragedy of the commons. Proc. R. Soc. B 273, 1477-1481. (doi:10.1098/rspb.2006.3476)
12. Nowak, M. A. 2006 Five rules for the evolution of cooperation. Science 314, 1560-1563. (doi:10.1126/science.1133755)
13. Ohtsuki, H., Hauert, C., Lieberman, E. & Nowak, M. A. 2006 A simple rule for the evolution of cooperation on graphs and social networks. Nature 441, 502-505. (doi:10.1038/nature04605)
14. Traulsen, A. & Nowak, M.A. 2006 Evolution of cooperation by multilevel selection. Proc. Natl Acad. Sci. USA 103, 10952-10955. (doi:10.1073/pnas.0602530103)
15. Fletcher, J. A. & Doebeli, M. 2009 A simple and general explanation for the evolution of altruism. Proc. R. Soc. B 276, 13-19. (doi:10.1098/rspb.2008.0829)
16. Grafen, A. 2007 Detecting kin selection at work using inclusive fitness. Proc. R. Soc. B 274, 713-719. (doi:10.1098/rspb.2006.0140)
17. Grafen, A. 2007 An inclusive fitness analysis of altruism on a cyclical network. J. Evol. Biol. 20, 2278-2283. (doi:10.1111/j.1420-9101.2007.01413.x)
18. Lehmann, L., Keller, L. & Sumpter, D. J. T. 2007 The evolution of helping and harming on graphs: the return of the inclusive fitness effect. J. Evol. Biol. 20, 2284-2295. (doi:10.1111/j.1420-9101.2007.01414.x)
19. Lehmann, L., Keller, L., West, S. & Roze, D. 2007 Group selection and kin selection: two concepts but one process. Proc. Natl Acad. Sci. USA 104, 6736-6739. (doi:10.1073/pnas.0700662104)
20. Bijma, P. & Aanen, D. K. 2010 Assortment, Hamilton's rule and multilevel selection. Proc. R. Soc. B 277, 673-675. (doi:10.1098/rspb.2009.1093)
21. Alonso, W. J. 1998 The role of kin selection theory on the explanation of biological altruism: a critical review. J. Comp. Biol. 3, 1-14.
22. Alonso, W. J. & Schuck-Paim, C. 2002 Sex-ratio conflicts, kin selection, and the evolution of altruism. Proc. Natl Acad. Sci. USA 99, 6843-6847. (doi:10.073/pnas.092584299)
23. Hunt, J. H. 1999 Trait mapping and salience in the evolution of eusocial vespid wasps. Evolution 53, 225-237. (doi:10.2307/2640935)
24. Hunt, J. H. 2007 The evolution of social wasps. New York, NY: Oxford University Press.
25. Wilson, E. O. 2005 Kin selection as the key to altruism: its rise and fall. Soc. Res. 72, 159-166.
26. Wilson, E. O. & Hölldobler, B. 2005 Eusociality: origin and consequences. Proc. Natl Acad. Sci. USA 102, 13 367-13 371. (doi:10.1073/pnas.0505858102)
27. Wilson, D. S. & Wilson, E. O. 2007 Rethinking the theoretical foundation of sociobiology. Q. Rev. Biol. 82, 327-348. (doi:10.1086/522809)
28. Wilson, E. O. 2008 One giant leap: how insects achieved altruism and colonial life. BioScience 58, 17-25. (doi:10. 1641/B580106)
29. Wilson, D. S. & Wilson, E. O. 2008 Evolution 'for the good of the group'. Am. Sci. 96, 380-389. (doi:10. 1511/2008.74.1)
30. Hölldobler, B. & Wilson, E. O. 2009 The superorganism. New York, NY: W.W. Norton and Company.
31. Foster, K. R., Wenseleers, T. & Ratnieks, F. L. W. 2006 Kin selection is the key to altruism. Trends Ecol. Evol. 21, 57-60. (doi:10.1016/j.tree.2005.11.020)
32. Thompson, G. J. 2006 Kin selection in disguise? Insect. Soc. 53, 496-497. (doi:10.1007/s00040-005-0893-6)
33. Helanterä, H. & Bargum, K. 2007 Pedigree relatedness, not greenbeard genes, explains eusociality. Oikos 116, 217-220. (doi:10.1111/j.0030-1299.2007.15411.x)
34. Crozier, R. H. 2008 Advanced eusociality, kin selection and male haploidy. Austr. J. Entomol. 47, 2-8. (doi:10.1111/j.1440-6055.2007.00621.x)
35. Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W. 2008 Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213-1216. (doi:10.1126/science.1156108)
36. Monnin, T. & Liebig, J. 2008 Understanding eusociality requires both proximate and ultimate thinking and due consideration of individual and colony-level interests. Oikos 117, 1441-1443. (doi:10.1111/j.0030-1299.2008.16946.x)
37. Foster, K. R. 2009 A defense of sociobiology. Cold Spring Harb. Symp. Quant. Biol. 74, 403-418. (doi:10. 1101/sqb.2009.74.041)
38. Nowak, M. A., Tarnita, C. E. & Wilson, E. O. 2010 The evolution of eusociality. Nature 466, 1057-1062. (doi:10.1038/nature09205)
39. Doebeli, M. 2010 Inclusive fitness is just bookkeeping. Nature 467, 661. (doi:10.1038/467661b)
40. Van Veelen, M., García, J., Sabelis, M. W. & Egas, M. 2010 Call for a return to rigour in models. Nature 467, 661. (doi:10.1038/467661d)
41. Gadagkar, R. 2010 Sociobiology in turmoil again. Curr. Sci. 99, 1036-1041.
42. Abbot, P. et al. 2011 Inclusive fitness theory and eusociality. Nature 471, E1-E4. (doi:10.1038/nature09831)
43. Boomsma, J. J., Beekman, M., Cornwallis, C. K., Griffin, A. S., Holman, L., Hughes, W. O. H., Keller, L., Oldroyd, B. P. & Ratnieks, F. L. W. 2011 Only full-sibling families evolved eusociality. Nature 471, E4-E5. (doi:10.1038/nature09832)
44. Strassmann, J. E., Page, R. E., Robinson, G. E. & Seeley, T. D. 2011 Kin selection and eusociality. Nature 471, E5-E6. (doi:10.1038/nature09833)
45. Ferriere, R. & Michod, R. E. 2011 Inclusive fitness in evolution. Nature 471, E6-E8. (doi:10.1038/nature09834)
46. Herre, E. A. & Wcislo, W. T. 2011 In defence of inclusive fitness theory. Nature 471, E8-E9. (doi:10.1038/nature09835)
47. Ratnieks, F. L. W., Foster, K. R. & Wenseleers, T. 2011 Darwin's special difficulty: the evolution of 'neuter insects' and current theory. Behav. Ecol. Sociobiol. 65, 481-492. (doi:10.1007/s00265-010-1124-8)
48. Gardner, A., West, S. A. & Wild, G. 2011 The genetical theory of kin selection. J. Evol. Biol. 24, 1020-1043. (doi:10.1111/j.1420-9101.2011.02236.x)
49. Rousset, F. & Lion, S. 2011 Much ado about nothing: Nowak et al.'s charge against inclusive fitness theory. J. Evol. Biol. 24, 1386-1392. (doi:10.1111/j.1420-9101.2011.02251.x)
50. Marshall, J. A. R. 2011 Group selection and kin selection: formally equivalent approaches. Trends Ecol. Evol. 26, 325-332. (doi:10.1016/j.tree.2011.04.008)
51. Nowak, M. A., Tarnita, C. E. & Wilson, E. O. 2011 Nowak et al. reply. Nature 471, E9-E10. (doi:10.1038/nature09836)
52. Grafen, A. 1982 How not to measure inclusive fitness. Nature 298, 425-426. (doi:10.1038/298425a0)
53. Grafen, A. 1984 Natural selection, kin selection and group selection. In Behavioural ecology (eds J. R. Krebs & N. B. Davies), pp. 62-84, 2nd edn. Oxford, UK: Blackwell.
54. Taylor, P. D. & Frank, S. A. 1996 How to make a kin selection model. J. Theor. Biol. 180, 27-37. (doi:10.1006/jtbi.1996.0075)
55. Frank, S. A. 1998 Foundations of social evolution. Princeton, NJ: Princeton University Press.
56. Wenseleers, T., Gardner, A. & Foster, K. R. 2010 Social evolution theory: a review of methods and approaches. In Social behaviour: genes, ecology and evolution (eds T. Székely, J. Komdeur & A. J. Moore), pp. 132-158. Cambridge, UK: Cambridge University Press.
57. Frank, S. A. 1995 Mutual policing and repression of competition in the evolution of cooperative groups. Nature 377, 520-522. (doi:10.1038/377520a0)
58. Ratnieks, F. L. W. & Reeve, H. K. 1992 Conflict in single-queen Hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species. J. Theor. Biol. 158, 33-65. (doi:10.1016/S0022-5193(05)80647-2)
59. Trivers, R. L. 1974 Parent-offspring conflict. Am. Zool. 14, 249-264.
60. Trivers, R. L. & Hare, H. 1976 Haplodiploidy and the evolution of the social insects. Science 191, 249-263. (doi:10.1126/science.1108197)
61. Ratnieks, F. L. W., Foster, K. R. & Wenseleers, T. 2006 Conflict resolution in insect societies. Annu. Rev. Entomol. 51, 581-608. (doi:10.1146/annurev.ento.51.110104.151003)
62. th edn. Oxford, UK: Blackwell.
63. Maynard Smith, J. & Szathmáry, E. 1995 The major transitions in evolution. Oxford, UK: W.H. Freeman.
64. Dawkins, R. 1982 The extended phenotype. Oxford, UK: W. H. Freeman.
65. Alexander, R. D. 1974 The evolution of social behavior. Annu. Rev. Ecol. Syst. 5, 325-383. (doi:10.1146/annurev.es.05.110174.001545)
66. Charnov, E. L. 1978 Evolution of eusocial behavior: offspring choice or parental parasitism? J. Theor. Biol. 75, 451-465. (doi:10.1016/0022-5193(78)90356-9)
67. Bourke, A. F. G. & Franks, N. R. 1995 Social evolution in ants. Princeton, NJ: Princeton University Press.
68. Stark, R. E., Hefetz, A., Gerling, D. & Velthuis, H. H. W. 1990 Reproductive competition involving oophagy in the socially nesting bee Xylocopa sulcatipes. Naturwissenschaften 77, 38-40. (doi:10.1007/BF01131797)
69. Liebig, J., Monnin, T. & Turillazzi, S. 2005 Direct assessment of queen quality and lack of worker suppression in a paper wasp. Proc. R. Soc. B 272, 1339-1344. (doi:10.1098/rspb.2005.3073)
70. Sundström, L., Chapuisat, M. & Keller, L. 1996 Conditional manipulation of sex ratios by ant workers: a test of kin selection theory. Science 274, 993-995. (doi:10.1126/science.274.5289.993)
71. Bourke, A. F. G. 1994 Worker matricide in social bees and wasps. J. Theor. Biol. 167, 283-292. (doi:10.1006/jtbi.1994.1070)
72. nd edn. Oxford, UK: Blackwell.
73. Alexander, R. D., Noonan, K. M. & Crespi, B. J. 1991 The evolution of eusociality. In The biology of the naked mole-rat (eds P. W. Sherman, J. U. M. Jarvis & R. D. Alexander), pp. 3-44. Princeton, NJ: Princeton University Press.
74. Seger, J. 1991 Cooperation and conflict in social insects. In Behavioural ecology (eds J. R. Krebs & N. B. Davies), pp. 338-373, 3rd edn. Oxford, UK: Blackwell.
75. Bourke, A. F. G. 1999 Colony size, social complexity and reproductive conflict in social insects. J. Evol. Biol. 12, 245-257. (doi:10.1046/j.1420-9101.1999.00028.x)
76. Crespi, B. J. 1994 Three conditions for the evolution of eusociality: are they sufficient? Insectes Soc. 41, 395-400. (doi:10.1007/BF01240642)
77. Queller, D. C. & Strassmann, J. E. 1998 Kin selection and social insects. BioScience 48, 165-175. (doi:10. 2307/1313262)
78. Cowan, D. P. 1991 The solitary and presocial Vespidae. In The social biology of wasps (eds K. G. Ross & R. W. Matthews), pp. 33-73. Ithaca,NY:Comstock Publishing Associates.
79. Bourke, A. F. G. 1997 Sociality and kin selection in insects. In Behavioural ecology (eds J. R. Krebs & N. B. Davies), pp. 203-227, 4th edn. Oxford, UK: Blackwell.
80. Boomsma, J. J. 2007 Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17, R673-R683. (doi:10.1016/j.cub.2007.06.033)
81. Stark, R. E. 1992 Cooperative nesting in the multivoltine large carpenter bee Xylocopa sulcatipes Maa (Apoidea: Anthophoridae): do helpers gain or lose to solitary females? Ethology 91, 301-310. (doi:10.1111/j.1439-0310.1992.tb00871.x)
82. Boomsma, J. J. 2009 Lifetime monogamy and the evolution of eusociality. Phil. Trans. R. Soc. B 364, 3191-3207. (doi:10.1098/rstb.2009.0101)
83. Grimaldi, D. & Engel, M. S. 2005 Evolution of the insects. Cambridge, UK: Cambridge University Press.
84. Dawkins, R. 2004 The ancestor's tale. London, UK: Weidenfeld & Nicolson.
85. West-Eberhard, M. J. 1975 The evolution of social behavior by kin selection. Q. Rev. Biol. 50, 1-33. (doi:10.1086/408298)
86. Hechinger, R. F., Wood, A. C. & Kuris, A. M. 2011 Social organization in a flatworm: trematode parasites form soldier and reproductive castes. Proc. R. Soc. B 278, 656-665. (doi:10.1098/rspb.2010.1753)
87. Cornwallis, C. K., West, S. A., Davis, K. E. & Griffin, A. S. 2010 Promiscuity and the evolutionary transition to complex societies. Nature 466, 969-972. (doi:10. 1038/nature09335)
88. Fletcher, D. J. C. & Michener, C. D. (eds) 1987 Kin recognition in animals. New York, NY: John Wiley and Sons.
89. Keller, L. 1997 Indiscriminate altruism: unduly nice parents and siblings. Trends Ecol. Evol. 12, 99-103. (doi:10.1016/S0169-5347(96)10065-3)
90. Komdeur, J., Richardson, D. S. & Hatchwell, B. 2008 Kin-recognition mechanisms in cooperative breeding systems: ecological causes and behavioral consequences of variation. In The ecology of social evolution (eds J. Korb & J. Heinze), pp. 175-193. Berlin, Germany: Springer.
91. Bourke, A. F. G. 2005 Genetics, relatedness and social behaviour in insect societies. In Insect evolutionary ecology (eds M. D. E. Fellowes, G. J. Holloway &J. Rolff), pp. 1-30. Wallingford, UK: CABI Publishing.
92. Wenseleers, T. & Ratnieks, F. L. W. 2006 Comparative analysis of worker reproduction and policing in eusocial Hymenoptera supports relatedness theory. Am. Nat. 168, E163-E179. (doi:10.1086/508619)
93. Emlen, S. T. 1995 An evolutionary theory of the family. Proc. Natl Acad. Sci. USA 92, 8092-8099.
94. Mock, D. W. & Parker, G. A. 1997 The evolution of sibling rivalry. Oxford, UK: Oxford University Press.
95. Burt, A. & Trivers, R. 2006 Genes in conflict. Cambridge, MA: Belknap Press.
96. Meunier, J., West, S. A. & Chapuisat, M. 2008 Split sex ratios in the social Hymenoptera: a meta-analysis. Behav. Ecol. 19, 382-390. (doi:10.1093/beheco/arm143)
97. Crozier, R. H. & Pamilo, P. 1996 Evolution of social insect colonies. Oxford, UK: Oxford University Press.
98. West, S. A. 2009 Sex allocation. Princeton, NJ: Princeton University Press.
99. Queller, D. C. 2000 Relatedness and the fraternal major transitions. Phil. Trans. R. Soc. Lond. B 355, 1647-1655. (doi:10.1098/rstb.2000.0727)
100. Queller, D. C. & Strassmann, J. E. 2009 Beyond society: the evolution of organismality. Phil. Trans. R. Soc. B 364, 3143-3155. (doi:10.1098/rstb.2009.0095)
101. Chapman, T.W., Crespi, B. J., Kranz, B. D. & Schwarz, M. P. 2000 High relatedness and inbreeding at the origin of eusociality in gall-inducing thrips. Proc. Natl Acad. Sci. USA 97, 1648-1650. (doi:10.1073/pnas.020510097)
102. Russell, A. F. & Hatchwell, B. J. 2001 Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate. Proc. R. Soc. Lond. B 268, 2169-2174. (doi:10.1098/rspb.2001.1790)
103. Richardson, D. S., Burke, T. & Komdeur, J. 2003 Sexspecific associative learning cues and inclusive fitness benefits in the Seychelles warbler. J. Evol. Biol. 16, 854-861. (doi:10.1046/j.1420-9101.2003.00592.x)
104. Nam, K.-B., Simeoni, M., Sharp, S. P. & Hatchwell, B. J. 2010 Kinship affects investment by helpers in a cooperatively breeding bird. Proc. R. Soc. B 277, 3299-3306. (doi:10.1098/rspb.2010.0737)
105. Helanterä, H., Strassmann, J. E., Carrillo, J. & Queller, D. C. 2009 Unicolonial ants: where do they come from, what are they and where are they going? Trends Ecol. Evol. 24, 341-349. (doi:10.1016/j.tree.2009.01.013)
106. Korb, J. & Heinze, J. (eds) 2008 Ecology of social evolution. Berlin, Germany: Springer.