Abstract
Social selection influences the evolution of weapons, ornaments and behaviour in both males and females. Thus, social interactions in both sexual and non-sexual contexts can have a powerful influence on the evolution of traits that would otherwise appear to be detrimental to survival. Although clearly outlined by West-Eberhard in the early 1980s, the idea that social selection is a comprehensive framework for the study of ornaments and weapons has largely been ignored. In West-Eberhard's view, sexual selection is a form of social selection—a concept supported by several lines of evidence. Darwin's distinction between natural and sexual selection has been useful, but recent confusion about the limits of sexual selection suggests that some traits are not easily categorized as naturally or sexually selected. Because social selection theory has much to offer the current debates about both sexual selection and reproductive competition in females, it is sometimes viewed, narrowly, to be most useful when considering female roles. However, social selection theory encompasses much more than female reproductive competition. Our goal here was to provide that broader perspective.
Footnotes
References
- 1
West-Eberhard M. J. . 1979Sexual selection, social competition, and evolution. Proc. Am. Phil. Soc. 123, 222–234. ISI, Google Scholar - 2
West-Eberhard M. J. . 1983Sexual selection, social competition, and speciation. Q. Rev. Biol. 58, 155–183.doi:10.1086/413215 (doi:10.1086/413215). Crossref, ISI, Google Scholar - 3
West-Eberhard M. J. . 1984Sexual selection, competitive communication and species-specific signals in insects. Insect communication (ed.& Lewis T. ), pp. 283–324. New York, NY: Academic Press. Google Scholar - 4
West-Eberhard M. J. . 1991Sexual selection and social behavior. Man and beast revisited (eds, Robinson M. H.& Tiger L. ), pp. 159–172. Washington, DC: Smithsonian Press. Google Scholar - 5
Crook J. H. . 1972Sexual selection, dimorphism, and social organization in the primates. Sexual selection and the descent of man (1871–1971) (ed.& Campbell B. G. ), pp. 231–281. Chicago, IL: Aldine. Google Scholar - 6
Moore A. J., Brodie E. D.& Wolf J. B. . 1997Interacting phenotypes and the evolutionary process. I. Direct and indirect genetic effects of social interactions. Evolution 51, 1352–1362.doi:10.2307/2411187 (doi:10.2307/2411187). Crossref, PubMed, ISI, Google Scholar - 7
Rice W. R.& Holland B. . 1997The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav. Ecol. Sociobiol. 41, 1–10.doi:10.1007/s002650050357 (doi:10.1007/s002650050357). Crossref, ISI, Google Scholar - 8
Darwin C. . 1871The descent of man, and selection in relation to sex, v ol. 2. London, UK: John Murray. Google Scholar - 9
Parker G. A. . 1970Sperm competition and its evolutionary consequences in insects. Biol. Rev. Camb. Phil. Soc. 45, 525–567.doi:10.1111/j.1469-185X.1970.tb01176.x (doi:10.1111/j.1469-185X.1970.tb01176.x). Crossref, ISI, Google Scholar - 10
Arnqvist G.& Rowe L. . 2005Sexual conflict. Princeton, NJ: Princeton University Press. Crossref, Google Scholar - 11
Kokko H., Jennions M. D.& Brooks R. . 2006Unifying and testing models of sexual selection. Annu. Rev. Ecol. Evol. Syst. 37, 43–66.doi:10.1146/annurev.ecolsys.37.091305.110259 (doi:10.1146/annurev.ecolsys.37.091305.110259). Crossref, ISI, Google Scholar - 12
Ryan M. J. . 2011Replication in field biology: the case of the frog-eating bat. Science 334, 1229–1230.doi:10.1126/science.1214532 (doi:10.1126/science.1214532). Crossref, PubMed, ISI, Google Scholar - 13
Tobias J. A., Montgomerie R.& Lyon B. E. . 2012The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Phil. Trans. R. Soc. B 367, 2274–2292.doi:10.1098/rstb.2011.0280 (doi:10.1098/rstb.2011.0280). Link, ISI, Google Scholar - 14
Andersson M. . 1994Sexual Selection. Princeton, NJ: Princeton University Press. Crossref, Google Scholar - 15
Lyon B. E., Eadie J. M.& Hamilton L. D. . 1994Parental choice selects for ornamental plumage in American coot chicks. Nature 371, 240–243.doi:10.1038/371240a0 (doi:10.1038/371240a0). Crossref, ISI, Google Scholar - 16
Amundsen T. . 2000Why are female birds ornamented. Trends Ecol. Evol. 15, 149–155.doi:10.1016/S0169-5347(99)01800-5 (doi:10.1016/S0169-5347(99)01800-5). Crossref, PubMed, ISI, Google Scholar - 17
Kraaijeveld K., Kraaijeveld-Smit F. J. L.& Komdeur J. . 2007The evolution of mutual ornamentation. Anim. Behav. 74, 657–677.doi:10.1016/j.anbehav.2006.12.027 (doi:10.1016/j.anbehav.2006.12.027). Crossref, ISI, Google Scholar - 18
Tobias J. A., Gamarra-Toledo V., Garcia-Olaechea D., Pulgarin P. C.& Seddon N. . 2011Year-round resource defence and the evolution of male and female song in suboscine birds: social armaments are mutual ornaments. J. Evol. Biol. 24, 2118–2138.doi:10.1111/j.1420-9101.2011.02345.x (doi:10.1111/j.1420-9101.2011.02345.x). Crossref, PubMed, ISI, Google Scholar - 19
- 20
Queller D. C. . 1994Male–female conflict and parent–offspring conflict. Am. Nat. 144, S84–S99.doi:10.1086/285654 (doi:10.1086/285654). Crossref, ISI, Google Scholar - 21
Nesse R. M. . 2007Runaway social selection for displays of partner value and altruism. Biol. Theory 2, 143–155.doi:10.1162/biot.2007.2.2.143 (doi:10.1162/biot.2007.2.2.143). Crossref, Google Scholar - 22
Hosken D. J.& House C. M. . 2011Sexual selection. Curr. Biol. 21, R62–R65.doi:10.1016/j.cub.2010.11.053 (doi:10.1016/j.cub.2010.11.053). Crossref, PubMed, ISI, Google Scholar - 23
Wynne-Edwards V. C. . 1962Animal dispersion in relation to social behaviour. Edinburgh, UK: Oliver and Boyd. Google Scholar - 24
Ghiselin M. T. . 1974The economy of nature and the evolution of sex. Berkeley, CA: University of California Press. Google Scholar - 25
Tanaka Y. . 1996Social selection and the evolution of animal signals. Evolution 50, 512–523.doi:10.2307/2410827 (doi:10.2307/2410827). Crossref, PubMed, ISI, Google Scholar - 26
Wolf J. B., Brodie E. D.& Moore A. J. . 1999Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. Am. Nat. 153, 254–266.doi:10.1086/303168 (doi:10.1086/303168). Crossref, PubMed, ISI, Google Scholar - 27
McGlothlin J. W., Moore A. J., Wolf J. B.& Brodie E. D. . 2010Interacting phenotypes and the evolutionary process. III. Social evolution. Evolution 64, 2558–2574.doi:10.1111/j.1558-5646.2010.01012.x (doi:10.1111/j.1558-5646.2010.01012.x). Crossref, PubMed, ISI, Google Scholar - 28
Maynard Smith J. . 1982Evolution and the theory of games. Cambridge, UK: Cambridge University Press. Crossref, Google Scholar - 29
Bradbury J. W.& Vehrencamp S. L. . 1998Principles of animal communication. Sunderland, MA: Sinauer. Google Scholar - 30
Searcy W. A.& Nowicki S. . 2005The evolution of animal communication: reliability and deception in signaling systems. Princeton, NJ: Princeton University Press. Google Scholar - 31
Emlen D. J. . 2008The evolution of animal weapons. Annu. Rev. Ecol. Evol. Syst. 39, 387–413.doi:10.1146/annurev.ecolsys.39.110707.173502 (doi:10.1146/annurev.ecolsys.39.110707.173502). Crossref, ISI, Google Scholar - 32
Røskaft E.& Rohwer S. . 1987An experimental study of the function of the red epaulettes and the black-body color of male red-winged blackbirds. Anim. Behav. 35, 1070–1077.doi:10.1016/S0003-3472(87)80164-1 (doi:10.1016/S0003-3472(87)80164-1). Crossref, ISI, Google Scholar - 33
Chaine A. S., Tjernell K. A., Shizuka D.& Lyon B. E. . 2011Sparrows use multiple status signals in winter social flocks. Anim. Behav. 81, 447–453.doi:10.1016/j.anbehav.2010.11.016 (doi:10.1016/j.anbehav.2010.11.016). Crossref, ISI, Google Scholar - 34
Chaine A. S.& Lyon B. E. . 2008Intrasexual selection on multiple plumage ornaments in the lark bunting. Anim. Behav. 76, 657–667.doi:10.1016/j.anbehav.2008.03.014 (doi:10.1016/j.anbehav.2008.03.014). Crossref, ISI, Google Scholar - 35
Legge S. . 2000Siblicide in the cooperatively breeding laughing kookaburra (Dacelo novaeguineae). Behav. Ecol. Sociobiol. 48, 293–302.doi:10.1007/s002650000229 (doi:10.1007/s002650000229). Crossref, ISI, Google Scholar - 36
Lincoln G. A. . 1992Biology of antlers. J. Zool. 226, 517–528.doi:10.1111/j.1469-7998.1992.tb07495.x (doi:10.1111/j.1469-7998.1992.tb07495.x). Crossref, ISI, Google Scholar - 37
Watson N. L.& Simmons L. W. . 2010Reproductive competition promotes the evolution of female weaponry. Proc. R. Soc. B 277, 2035–2040.doi:10.1098/rspb.2009.2335 (doi:10.1098/rspb.2009.2335). Link, ISI, Google Scholar - 38
Rohwer S. . 1977Status signaling in Harris sparrows—some experiments in deception. Behaviour 61, 107–129.doi:10.1163/156853977X00504 (doi:10.1163/156853977X00504). Crossref, ISI, Google Scholar - 39
Murphy T. G., Hernandez-Mucino D., Osorio-Beristain M., Montgomerie R.& Omland K. E. . 2009Carotenoid-based status signaling by females in the tropical streak-backed oriole. Behav. Ecol. 20, 1000–1006.doi:10.1093/beheco/arp089 (doi:10.1093/beheco/arp089). Crossref, ISI, Google Scholar - 40
Mock D. W.& Parker G. A. . 1998The evolution of sibling rivalry. New York, NY: Oxford University Press. Google Scholar - 41
Roulin A., Kolliker M.& Richner H. . 2000Barn owl (Tyto alba) siblings vocally negotiate resources. Proc. R. Soc. Lond. B 267, 459–463.doi:10.1098/rspb.2000.1022 (doi:10.1098/rspb.2000.1022). Link, ISI, Google Scholar - 42
Clutton-Brock T. . 2009Sexual selection in females. Anim. Behav. 77, 3–11.doi:10.1016/j.anbehav.2008.08.026 (doi:10.1016/j.anbehav.2008.08.026). Crossref, ISI, Google Scholar - 43
Stankowich T.& Caro T. . 2009Evolution of weaponry in female bovids. Proc. R. Soc. B 276, 4329–4334.doi:10.1098/rspb.2009.1256 (doi:10.1098/rspb.2009.1256). Link, ISI, Google Scholar - 44
Clutton-Brock T. . 2007Sexual selection in males and females. Science 318, 1882–1885.doi:10.1126/science.1133311 (doi:10.1126/science.1133311). Crossref, PubMed, ISI, Google Scholar - 45
Rubenstein D. R.& Lovette I. J. . 2009Reproductive skew and selection on female ornamentation in social species. Nature 462, 786–789.doi:10.1038/nature08614 (doi:10.1038/nature08614). Crossref, PubMed, ISI, Google Scholar - 46
Tibbetts E. A.& Dale J. . 2004A socially enforced signal of quality in a paper wasp. Nature 432, 218–222.doi:10.1038/nature02949 (doi:10.1038/nature02949). Crossref, PubMed, ISI, Google Scholar - 47
Cervo R., Dapporto L., Beani L., Strassmann J. E.& Turillazzi S. . 2008On status badges and quality signals in the paper wasp Polistes dominulus: body size, facial colour patterns and hierarchical rank. Proc. R. Soc. B 275, 1189–1196.doi:10.1098/rspb.2007.1779 (doi:10.1098/rspb.2007.1779). Link, ISI, Google Scholar - 48
- 49
Noe R.& Hammerstein P. . 1994Biological markets—supply-and-demand determine the effect of partner choice in cooperation, mutualism and mating. Behav. Ecol. Sociobiol. 35, 1–11.doi:10.1007/BF00167053 (doi:10.1007/BF00167053). Crossref, ISI, Google Scholar - 50
Sinervo B.& Clobert J. . 2003Morphs, dispersal behavior, genetic similarity, and the evolution of cooperation. Science 300, 1949–1951.doi:10.1126/science.1083109 (doi:10.1126/science.1083109). Crossref, PubMed, ISI, Google Scholar - 51
Keller L.& Ross K. G. . 1998Selfish genes: a green beard in the red fire ant. Nature 394, 573–575.doi:10.1038/29064 (doi:10.1038/29064). Crossref, ISI, Google Scholar - 52
Schwabl H. . 1993Yolk is a source of maternal testosterone for developing birds. Proc. Natl Acad. Sci. USA 90, 11 446–11 450.doi:10.1073/pnas.90.24.11446 (doi:10.1073/pnas.90.24.11446). Crossref, ISI, Google Scholar - 53
Schwabl H., Mock D. W.& Gieg J. A. . 1997A hormonal mechanism for parental favouritism. Nature 386, 231.doi:10.1038/386231a0 (doi:10.1038/386231a0). Crossref, PubMed, ISI, Google Scholar - 54
Kilner R. M. . 2006Function and evolution of color in young birds. Bird coloration, v ol. 2 (eds, Hill G.& McGraw K. ), pp. 201–232. London, UK: Harvard University Press. Google Scholar - 55
Lande R. . 1981Models of speciation by sexual selection on polygenic traits. Proc. Natl Acad. Sci. USA 78, 3721–3725.doi:10.1073/pnas.78.6.3721 (doi:10.1073/pnas.78.6.3721). Crossref, PubMed, ISI, Google Scholar - 56
Forstmeier W., Martin K., Bolund E., Schielzeth H.& Kempenaers B. . 2011Female extrapair mating behavior can evolve via indirect selection on males. Proc. Natl Acad. Sci. USA 108, 10 608–10 613.doi:10.1073/pnas.1103195108 (doi:10.1073/pnas.1103195108). Crossref, ISI, Google Scholar - 57
Kolliker M., Brinkhof M. W. G., Heeb P., Fitze P. S.& Richner H. . 2000The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care. Proc. R. Soc. Lond. B 267, 2127–2132.doi:10.1098/rspb.2000.1259 (doi:10.1098/rspb.2000.1259). Link, ISI, Google Scholar - 58
Nonacs P. . 2011Kinship, greenbeards, and runaway social selection in the evolution of social insect cooperation. Proc. Natl Acad. Sci. USA 108, 10 808–10 815.doi:10.1073/pnas.1100297108 (doi:10.1073/pnas.1100297108). Crossref, ISI, Google Scholar - 59
Oliveira R., Taborsky M.& Brockmann H. J. . 2008Alternative reproductive tactics—an integrative approach. Cambridge, UK: Cambridge University Press. Crossref, Google Scholar - 60
Sinervo B.& Lively C. M. . 1996The rock-paper-scissors game and the evolution of alternative male strategies. Nature 380, 240–243.doi:10.1038/380240a0 (doi:10.1038/380240a0). Crossref, ISI, Google Scholar - 61
Lyon B. E.& Eadie J. M. . 2008Conspecific brood parasitism in birds: a life-history perspective. Annu. Rev. Ecol. Evol. Syst. 39, 343–363.doi:10.1146/annurev.ecolsys.39.110707.173354 (doi:10.1146/annurev.ecolsys.39.110707.173354). Crossref, ISI, Google Scholar - 62
Henson S. A.& Warner R. R. . 1997Male and female alternative reproductive behaviors in fishes: a new approach using intersexual dynamics. Annu. Rev. Ecol. Syst. 28, 571–592.doi:10.1146/annurev.ecolsys.28.1.571 (doi:10.1146/annurev.ecolsys.28.1.571). Crossref, Google Scholar - 63
Zahavi A. . 1991On the definition of sexual selection, Fisher model, and the evolution of waste and of signals in general. Anim. Behav. 42, 501–503.doi:10.1016/S0003-3472(05)80052-1 (doi:10.1016/S0003-3472(05)80052-1). Crossref, ISI, Google Scholar - 64
Enquist M.& Arak A. . 1993Selection of exaggerated male traits by female aesthetic senses. Nature 361, 446–448.doi:10.1038/361446a0 (doi:10.1038/361446a0). Crossref, PubMed, ISI, Google Scholar - 65
Shubin N., Tabin C.& Carroll S. . 2009Deep homology and the origins of evolutionary novelty. Nature 457, 818–823.doi:10.1038/nature07891 (doi:10.1038/nature07891). Crossref, PubMed, ISI, Google Scholar - 66
Moore T.& Haig D. . 1991Genomic imprinting in mammalian development: a parental tug-of-war. Trend. Genet. 7, 45–49.doi:10.1016/0168-9525(91)90230-N (doi:10.1016/0168-9525(91)90230-N). Crossref, PubMed, ISI, Google Scholar - 67
Trivers R. L. . 1974Parent–offspring conflict. Am. Zool. 14, 249–264.doi:10.1093/icb/14.1.249 (doi:10.1093/icb/14.1.249). Crossref, Google Scholar - 68
Platt J. R. . 1964Strong inference—certain systematic methods of scientific thinking may produce much more rapid progress than others. Science 146, 347–353.doi:10.1126/science.146.3642.347 (doi:10.1126/science.146.3642.347). Crossref, PubMed, ISI, Google Scholar - 69
Travis J. . 2006Is it what we know or who we know? Choice of organism and robustness of inference in ecology and evolutionary biology. Am. Nat. 167, 303–314.doi:10.1086/501507 (doi:10.1086/501507). Crossref, PubMed, ISI, Google Scholar


