The sociobiology of sex: Inclusive fitness consequences of inter-sexual interactions

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1600, 2012, Pages 2314-2323

  Pizzari, Tommaso ^a   Gardner, Andy ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b BALLIOL COLLEGE   (United Kingdom)

Author keywords

Fisherian runaway; Greenbeard; Kin selection; Sexual conflict; Sexual selection

Indexed keywords

FITNESS; INTERSEXUAL INTERACTION; KIN SELECTION; MUTUALISM; SEXUAL CONFLICT; SEXUAL SELECTION; SOCIOBIOLOGY;

EID: 84863822609     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0281     Document Type: Review

References (91)

1. Darwin, C. 1871 The descent of man and selection in relation to sex. London, UK: John Murray.
2. Trivers, R. L. 1972 Parental investment and sexual selection. In Sexual selection and the descent of man 1871-1971 (ed. B. Campbell), pp. 136-179. Chicago, IL: Aldine.
3. Pizzari, T. & Bonduriansky, R. 2010 Sexual behaviour: conflict, cooperation and co-evolution. In Social behaviour: genes, ecology and evolution (eds T. Szekely, A. J. Moore & J. Komdeur), pp. 230-266. Cambridge, UK: Cambridge University Press.
4. Clutton-Brock, T. R. 2007 Sexual selection in males and females. Science 318, 1882-1885. (doi:10.1126/science.1133311)
5. Bonduriansky, R. 2001 The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol. Rev. 76, 305-339. (doi:10.1017/S1464793101005693)
6. Hamilton, W. D. 1964 Genetical evolution of social behaviour. I. J. Theor. Biol. 7, 1-16. (doi:10.1016/0022-5193(64)90038-4J)
7. Hamilton, W. D. 1970 Selfish and spiteful behaviour in an evolutionary model. Nature 228, 1218-1220. (doi:10.1038/2281218a0)
8. Grafen, A. 2006 Optimization of inclusive fitness. J. Theor. Biol. 238, 541-563. (doi:10.1016/j.jtbi.2005.06.009)
9. Hamilton, W. D. 1963 The evolution of altruistic behavior. Am. Nat. 97, 354-356. (doi:10.1086/497114)
10. 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)
11. Grafen, A. 2002 A first formal link between the Price equation and an optimization program. J. Theor. Biol. 217, 75-91. (doi:10.1006/jtbi.2002.3015)
12. Grafen, A. 2009 Formalizing Darwinism and inclusive fitness theory. Phil. Trans. R. Soc. B 364, 3135-3141. (doi:10.1098/rstb.2009.0056)
13. Gardner, A. 2009 Adaptation as organism design. Biol. Lett. 5, 861-864. (doi:10.1098/rsbl.2009.0674)
14. Kokko, H. & Ots, I. 2006 When not to avoid inbreeding. Evolution 60, 467-475. (doi:10.1111/j.0014-3820.2006. tb01128.x)
15. Parker, G. A. 2006 Sexual conflict over mating and fertilization: an overview. Phil. Trans. R. Soc. B 361, 235-259. (doi:10.1098/rstb.2005.1785)
16. Boomsma, J. J. 2007 Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 7, R673-R683. (doi:10.1016/j.cub.2007.06.033)
17. Puurtinen, M. 2011 Mate choice for optimal (k)inbreeding. Evolution 65, 1501-1505. (doi:10.1111/j.1558-5646.2010.01217.x)
18. Rankin, D. J. 2011 Kin selection and the evolution of sexual conflict. J. Evol. Biol. 24, 71-81. (doi:10.1111/j.1420-9101.2010.02143.x)
19. Wild, G., Pizzari, T. & West, S. A. 2011 Sexual conflict in viscous populations: the effect of the timing of dispersal. Theor. Popul. Biol. 80, 298-316. (doi:10.1016/j.tpb. 2011.09.002)
20. West, S. A., Griffin, A. S. & Gardner, A. 2007 Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20, 415-432. (doi:10.1111/j.1420-9101.2006.01258.x)
21. 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)
22. Arnqvist, G. & Rowe, L. 2005 Sexual conflict. Princeton, NJ: Princeton University Press.
23. Andersson, M. & Simmons, L. W. 2006 Sexual selection and mate choice. Trends Ecol. Evol. 21, 296-302. (doi:10.1016/j.tree.2006.03.015)
24. Eberhard, W. G. & Cordero, C. 2003 Female choice of sexually antagonistic male adaptations: a critical review of some current research. J. Evol. Biol. 16, 1-6. (doi:10.1046/j.1420-9101.2003.00506.x)
25. Pizzari, T. & Snook, R. R. 2003 Perspective: sexual conflict and sexual selection: chasing away paradigm shifts. Evolution 57, 1223-1236. (doi:10.1554/02-517)
26. Cameron, E., Day, T. & Rowe, L. 2003 Sexual conflict and indirect benefits. J. Evol. Biol. 16, 1055-1060. (doi:10.1046/j.1420-9101.2003.00584.x)
27. Kokko, H. 2001 Fisherian and 'good genes' benefits of mate choice: how (not) to distinguish between them. Ecol. Lett. 4, 322-326. (doi:10.1046/j.1461-0248.2001.00224.x)
28. Prum, R. O. 2010 The Lande-Kirkpatrick mechanism is the null model of evolution by intersexual selection: implications for meaning, honesty, and design in intersexual signals. Evolution 64, 3085-3100. (doi:10.1111/j.1558-5646.2010.01054.x)
29. Hardin, G. 1968 Tragedy of the commons. Science 162, 1243-1248. (doi:10.1126/science.162.3859.1243)
30. Frank, S. A. 1998 Foundations of social evolution. Princeton, NJ: Princeton University Press.
31. Rankin, D. J., Dieckmann, U. & Kokko, H. 2011 Sexual conflict and the tragedy of the commons. Am. Nat. 177, 780-791. (doi:10.1007/s10886-007-9393-z)
32. Le Galliard, J. F., Fitze, P. S., Ferriere, R. & Clobert, J. 2005 Sex ratio bias, male aggression, and population collapse in lizards. Proc. Natl Acad. Sci. USA 102, 18231-18236. (doi:10.1073/pnas.0505172102)
33. Wigby, S., Sirot, L. K., Linklater, J. R., Buehner, N., Calboli, F. C. F., Bretman, A., Wolfner, M. F. & Chapman, T. 2009 Seminal fluid protein allocation and male reproductive success. Curr. Biol. 19, 751-757. (doi:10.1016/j.cub.2009.03.036)
34. Wigby, S. & Chapman, T. 2004 Female resistance to male harm evolves in response to manipulation of sexual conflict. Evolution 58, 1028-1037. (doi:10.1554/03-568)
35. Wigby, S. & Chapman, T. 2005 Sex peptide causes mating costs in female Drosophila melanogaster. Curr. Biol. 15, 316-321. (doi:10.1016/j.cub.2005.01.051)
36. Crudgington, H. S. & Siva-Jothy, M. T. 2000 Genital damage, kicking and early death-the battle of the sexes takes a sinister turn in the bean weevil. Nature 407, 855-856. (doi:10.1038/35038154)
37. Hotzy, C. & Arnqvist, G. 2009 Sperm competition favors harmful males in seed beetles. Curr. Biol. 19, 404-407. (doi:10.1016/j.cub.2009.01.045)
38. Baeza, J. A. 2008 Social monogamy in the shrimp Pontonia margarita, a symbiont of Pinctada mazatlanica, off the Pacific coast of Panama. Mar. Biol. 153, 387-395. (doi:10.1007/s00227-007-0815-9)
39. Alonzo, S. H. & Pizzari, T. 2010 Male fecundity stimulation: conflict and cooperation within and between the sexes: model analyses and coevolutionary dynamics. Am. Nat. 175, 174-185. (doi:10.1086/649596)
40. Stutt, A. D. & Siva-Jothy, M. T. 2001 Traumatic insemination and sexual conflict in the bed bug Cimex lectularius. Proc. Natl Acad. Sci. USA 98, 5683-5687. (doi:10.1073/pnas.101440698)
41. Parker, G. A. & Pizzari, T. 2010 Sperm competition and ejaculate economics. Biol. Rev. 85, 897-934. (doi: 10.1111/j.1469-185X.2010.00140.x)
42. Snook, R. R., Hosken, D. J. & Karr, T. L. 2011 The biology and evolution of polyspermy: insights from cellular and functional studies of sperm and centrosomal behaviour in the fertilized egg. Reproduction 142, 779-792. (doi:10.1530/REP-11-0255)
43. Maynard Smith, J. & Szathmary, E. 1995 The major transitions in evolution. Oxford, UK: Oxford University Press.
44. 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)
45. Gardner, A. & Grafen, A. 2009 Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. 22, 659-671. (doi:10.1111/j.1420-9101.2008.01681.x)
46. Bourke, A. F. G. 2011 Principles of social evolution. Oxford, UK: Oxford University Press.
47. Hughes, W. O. H., Oldroyd, B. J., 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)
48. 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)
49. Hardling, R., Gosden, T. & Robin, A. 2008 Male mating constraints affect mutual mate choice: prudent male courting and sperm-limited females. Am. Nat. 172, 259-271. (doi:10.1086/589452)
50. Elgar, M. A. & Schneider, J. M. 2004 Evolutionary significance of sexual cannibalism. Adv. Study Behav. 34, 135-163. (doi:10.1016/S0065-3454(04)34004-0)
51. Andrade, M. C. B. 2003 Risky mate search and male self-sacrifice in redback spiders. Behav. Ecol. 14, 531-538. (doi:10.1093/beheco/arg015)
52. Fromhage, L., Elgar, M. A. & Schneider, J. M. 2005 Faithful without care: the evolution of monogyny. Evolution 59, 1400-1405. (doi:10.1554/04-680)
53. Andrade, M. C. B. 1996 Sexual selection for male sacrifice in the Australian redback spider. Science 271, 70-72. (doi:10.1126/science.271.5245.70)
54. Andrade, M. C. B. & Banta, E. M. 2002 Value of male remating and functional sterility in redback spiders. Anim. Behav. 63, 857-870. (doi:10.1006/anbe.2002.2003)
55. Hansen, L. S., Gonzalez, S. F., Toft, S. & Bilde, T. 2008 Thanatosis as an adaptive male mating strategy in the nuptial gift-giving spider Pisaura mirabilis. Behav. Ecol. 19, 546-551. (doi:10.1093/beheco/arm165)
56. Johnson, J. C., Trubl, P., Blackmore, V. & Miles, L. 2011 Male black widows court well-fed females more than starved females: silken cues indicate sexual cannibalism risk. Anim. Behav. 82, 383-390. (doi:10.1016/j.anbehav.2011.05.018)
57. Davies, N. B. 1992 Dunnock behaviour and social evolution. Oxford, UK: Oxford University Press.
58. Hunter, F. M. & Davis, L. S. 1998 Female Adelie penguins acquire nest material from extrapair males after engaging in extrapair copulations. Auk 115, 526-528.
59. Axelrod, R. & Hamilton, W. D. 1981 The evolution of cooperation. Science 211, 1390-1396. (doi:10.1126/science.7466396)
60. Koene, I. M. 2006 Tales of two snails: sexual selection and sexual conflict in Lymnaea stagnalis and Helix aspersa. Int. Comp. Biol. 46, 419-429. (doi:10.1093/icb/icj040)
61. Michiels, N. K. 1998 Mating conflicts and sperm competition in simultaneous hermaphrodites. In Sperm competition and sexual selection (eds T. R. Birkhead & A. P. Møller), pp. 219-254. London, UK: Academic Press.
62. Scharer, L., Littlewood, D. T. J., Waeschenbach, A., Yoshida, W. & Vizoso, D. B. 2011 Mating behavior and the evolution of sperm design. Proc. Natl Acad. Sci. USA 108, 1490-1495. (doi:10.1073/pnas.1013892108)
63. Leonard, J. L. & Pearse, J. S. 2001 Sex in banana slugs: different clades do different things. Am. Zool. 41, 1504.
64. Clutton-Brock, T. H. & Parker, G. A. 1995 Sexual coercion in animal societies. Anim. Behav. 49, 1345-1365. (doi:10.1006/anbe.1995.0166)
65. Clutton-Brock, T. H. & Parker, G. A. 1995 Punishment in animal societies. Nature 373, 209-216. (doi:10.1038/373209a0)
66. Barash, D. P. 1976 Male response to apparent female adultery in mountain bluebird (Sialia currucoides). Evolutionary interpretation. Am. Nat. 110, 1097-1101. (doi:10.1086/283129)
67. Valera, F., Hoi, H. & Kristin, A. 2003 Male shrikes punish unfaithful females. Behav. Ecol. 14, 403-408. (doi:10.1093/beheco/14.3.403)
68. Shellman-Reeve, J. S. 1999 Courting strategies and conflicts in a monogamous, biparental termite. Proc. R. Soc. Lond. B 266, 137-144. (doi:10.1098/rspb.1999.0613)
69. Johnstone, R. A. & Keller, L. 2000 How males can gain by harming their mates: sexual conflict, seminal toxins, and the cost of mating. Am. Nat. 156, 368-377. (doi:10.1086/303392)
70. Lessells, C. M. 2005 Why are males bad for females? Models for the evolution of damaging male mating behaviour. Am. Nat. 165, S46-S63. (doi:10.1086/429356)
71. Grafen, A. 1985 A geometric view of relatedness. Oxf. Surv. Evol. Biol. 2, 28-90.
72. Queller, D. C. 1994 Genetic relatedness in viscous populations. Evol. Ecol. 8, 70-73. (doi:10.1007/BF01237667)
73. Gardner, A. & West, S. A. 2004 Spite and the scale of competition. J. Evol. Biol. 17, 1195-1203. (doi:10. 1111/j.1420-9101.2004.00775.x)
74. Gardner, A., Hardy, I. C. W., Taylor, P. D. & West, S. A. 2007 Spiteful soldiers and sex ratio conflict in polyembryonic parasitoid wasps. Am. Nat. 169, 519-533. (doi:10.1086/512107)
75. West, S. A. & Gardner, A. 2010 Altruism, spite and greenbeards. Science 327, 1341-1344. (doi:10.1126/science.1178332)
76. Ala-Honkola, O., Friman, E. & Lindstrom, K. 2011 Costs and benefits of polyandry in a placental poeciliid fish Heterandria formosa are in accordance with the parentoffspring conflict theory of placentation. J. Evol. Biol. 24, 2600-2610. (doi:10.1111/j.14209101.2011.02383.x)
77. Dagg, J. L. 2006 Could sex be maintained through harmful males? Oikos 112, 232-235. (doi:10.1111/j.0030-1299.2006.14196.x)
78. Rankin, D. J. 2008 Can punishment maintain sex? Oikos 117, 173-176. (doi:10.1111/j.2007.0030-1299.16271.x)
79. Frank, S. A. 1997 Cytoplasmic incompatibility and population structure. J. Theor. Biol. 184, 327-330. (doi:10.1006/jtbi.1996.0276)
80. Haygood, R. & Turelli, M. 2009 Evolution of incompatibility-inducing microbes in subdivided host populations. Evolution 63, 432-447. (doi:10.1111/j.1558-5646.2008. 00550.x)
81. Gardner, A. & West, S. A. 2010 Greenbeards. Evolution 64, 25-38. (doi:10.1111/j.1558-5646.2009.00842.x)
82. Kirkpatrick, M. & Barton, N. H. 1997 The strength of indirect selection on female mating preferences. Proc. Natl Acad. Sci. USA 94, 1282-1286. (doi:10.1073/pnas.94.4.1282)
83. Fromhage, L., Reid, J. M. & Kokko, H. 2009 Evolution of mate choice for genome-wide heterozygosity. Evolution 63, 684-694. (doi:10.1111/j.1558-5646.2008.00575.x)
84. Aparicio, J. M. 2011 The paradox of the resolution of the lek paradox based on mate choice for heterozygosity. Anim. Behav. 81, 1271-1279. (doi:10.1016/j.anbehav. 2011.03.017)
85. Parker, G. A. 1979 Sexual selection and sexual conflict. In Sexual selection and reproductive competition in insects (eds M. S. Blum & N. A. Blum), pp. 123-166. New York, NY: Academic Press.
86. Pizzari, T., Løvlie, H. & Cornwallis, C. K. 2004 Sexspecific, counteracting responses to inbreeding in a bird. Proc. R. Soc. Lond. B 271, 2115-2121. (doi:10. 1098/rspb.2004.2843)
87. Eldakar, O. T., Dlugos, M. J., Pepper, J. W. & Wilson, D. S. 2009 Population structure mediates sexual conflict in water striders. Science 326, 816. (doi:10.1126/science. 1180183)
88. Oh, K. P. & Badyaev, A. V. 2010 Structure of social networks in a passerine bird: consequences for sexual selection and the evolution of mating strategies. Am. Nat. 176, E80-E89. (doi:10.1086/655216)
89. Buckling, A. & Brockhurst, M. A. 2008 Kin selection and the evolution of virulence. Heredity 100, 484-488. (doi:10.1038/sj.hdy.6801093)
90. Roughgarden, J., Oishi, M. & Akcay, E. 2006 Reproductive social behavior: cooperative games to replace sexual selection. Science 311, 965-969. (doi:10.1126/science.1110105)
91. Pizzari, T. & Foster, K. R. 2008 Sperm sociality: cooperation, altruism, and spite. PLoS Biol. 6, e130. (doi:10.1371/journal.pbio.0060130)