Abstract
The biological definition of what counts as sexual selection has gradually changed since Darwin introduced the concept. This paper reviews a sequence of definitions that reflect increasing knowledge of the diverse ways animals participate in reproductive social behavior. Later definitions accommodate more data than Darwin’s primary formulation. The latest approach, suggested in a catalyst meeting held at the National Evolution Synthesis Center in July 2013, distinguishes fertility selection as a density-dependent process from sexual-selection as a frequency-dependent process. The former consists of reproductive social behavior focussed on increasing the size of the reproductive pie, the later on securing a larger share of a given reproductive pie. The approach of social selection advocated here focusses on how to increase the size of the pie rather than on how to monopolize a larger share of a fixed pie. Social selection reverses the logic of sexual selection by starting with offspring production and working back to mating, and by starting with behavioral dynamics and working up to gene pool dynamics. In social selection courtship can potentially be deduced as a negotiation leading to an optimal allocation of tasks during offspring rearing. Mating pairs may form “teams” based on the reciprocal sharing of pleasure. The parent-offspring relation can be managed by the parent considered as the owner of a “family firm” whose product is offspring. The cooperation in reproductive social behavior may often evolve as a mutual direct benefit through individual selection rather than as some form of altruism requiring kin or multi-level selection.
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Notes
- 1.
Parker and Pizarri present an “evolutionary cascade” beginning with the origin of sexual reproduction, continuing through the evolution of anisogamy, and culminating in the emergence of sexual selection, sexual conflict and characteristic sex strategies. They contend this sequence has “remarkable logical beauty” and that sexual selection is a “logical imperative” because “sexual selection emerges deductively as the logical consequence of this evolutionary succession.” I disagree. The Parker and Pizarri master narrative begins with anisogamy as an outcome of a “primordial sexual conflict” between competing gametes. This origin to their narrative is problematic. An alternative possible origin of anisogamy relies on cooperation among gametes to maximize fertilization rates. Union in an anisogamous population among many micro- with a few macro-gametes achieves more surviving zygotes than union in an isogamous population with an intermediate number of same-sized gametes (cf. Roughgarden and Iyer 2011, also termed the “Kalmus” effect). This cooperative advantage, rather than one gamete type parasitizing the investment of the other gamete type, may underlie the origin of male and female gametes. This means that the entire evolutionary cascade can veer off in a sexual-cooperation direction or a sexual-competition direction depending on unknowable initial conditions. Hence, the outcome of such a cascade is an empirical contingency, not a logical necessity. Furthermore, the Parker and Pizarri master narrative is not the only proposed master narrative. In The Genial Gene I sketched an alternative master narrative based on cooperative interactions at each step in the cascade that appears to accord better with the facts (cf. Roughgarden 2009, esp. pp. 235–248). These alternative master narratives should be subjected to test.
- 2.
Parker and Pizarri endorse the Darwin-Bateman Paradigm (DBP) for typical male and female sex roles, contending not only that these sex roles are true but also are logically necessary, and that the Darwin-Bateman rationale for these sex roles provides “a powerful heuristic tool and the most parsimonious explanation for a bewildering diversity of biological patterns”. Again I disagree. The Darwin/Bateman Paradigm is not heuristic. It has not helped to understand female choice or the great many species in which the classic DBP sex roles do not occur. Adherence to the DBP requires an elaborate system of fabricated mimicries and assumptions about deceit to account for animals who do not act, or do not send the right signals, in accordance with DBP expectations. As a dominant and hegemonic paradigm, the DBP has had a chilling effect on innovation. Furthermore, parsimony is not a principle of logic. Whether a proposition is true or not is independent of whether it is simple or complicated. A parsimonious hypothesis may be so simple as to be simplistic, as indeed the DBP may be judged.
- 3.
Gowaty, (Chap. 6 this volume) contends that social selection is not an alternative to sexual selection. She sees sexual selection as a subset of social selection not an alternative. Gowaty is confusing my idea of social infrastructure selection with social selection sensu West-Eberhard (1983). Of course, sexual selection is a subset of West-Eberhard’s social selection because her idea of social selection was explicitly posed as a generalization of sexual selection to begin with. Sexual selection is obviously not a subset of social infrastructure selection as diagrammed in Figs. 1 and 2.
- 4.
As Gowaty (Chap. 6, this volume) notes, I have suggested in particular that “ ‘fancy traits, such as some elaborate secondary sexual characteristics, like … a peacock’s tail, a rooster’s comb, wattle and cockle-doddle-do facilitate male-male interactions’ rather than male-female interactions posited by Darwin”. Specifically, the ornaments may function as admission tickets to power holding cliques. She goes on to state that “I can imagine testing a classical idea about male-male competitive dynamics over number of mates in the absence of cliquey coalitions and male-male competitive dynamics in the presence of cliquey coalitions.” I would welcome such a test.
References
Ah-King M (2011) Female sexual selection in light of the Darwin-Bateman paradigm. Behav Ecol. doi:10.1093/beheco/arr109
Akçay E (2012) Incentives in the family II: Behavioral dynamics and the evolution of non-costly signaling. J theor Biol 294:9–18
Akçay E, Roughgarden J (2007) Extra-pair paternity in birds: review of the genetic benefits. Evol Ecol Res 9:855–868
Alexander RD (1974) The evolution of social behaviour. Ann Rev Ecol Syst 5:325–383.
Amundsen T, Forsgren E, Hansen L (1997) On the function of female ornaments: male bluethroats prefer colourful females. Proc R Soc Lond B 264:1579–1586
Amundsen T (2000) Why are female birds ornamented? Trends. Ecol Evol 4:149–155
Andersson M (1994) Sexual Selection. Princeton University, Princeton
Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2(3):349–368
Birkhead TR (2000) Promiscuity: an evolutionary history of sperm competition. Harvard University, Cambridge
Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339
Coyne J (2004) “Charm schools” (Review of Evolution’s Rainbow by J. Roughgarden). Times Literary Supplement. 30 July 2004.
Clutton-Brock T (2009) Sexual selection in females. Anim Behav 77(1):3–11
Dakin R, Montgomerie R (2011) Peahens prefer peacocks displaying more eyespots, but rarely. Anim Behav 82:21–28
Darwin C (1871) The descent of man and selection in relation to sex. Volumes I. and II. John Murray, London
Darwin C (1874) The descent of man. Cromwell, New York
Dawkins R (1976) The selfish gene. Oxford Univ., Oxford
Dewsbury D (2005) The Darwin-Bateman paradigm in historical context. Integr Comp Biol 45:831–837
Emlen S, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223
Fisher RA (1915) The evolution of sexual preference. Eugenics Rev 7:184–191
Fisher RA (1930) The genetical theory of natural selection. Clarendon, Oxford
Fosgren E, Amundsen T, Borg AA, Bjelvenmark J (2004). Unusually dynamic sex roles in a fish. Nature 429:551–554
Godfray HCJ (1991) Signaling of need by offspring to their parents. Nature 352:328–330.
Godfray H, Johnstone R (2000) Begging and bleating: the evolution of parent-offspring signalling. Phil Trans R Soc Lond B 355:1581–1591
Gould S, Lewontin R (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol Sci 205(1161):581–598
Gowaty P (2011) What is sexual selection and the short herstory of female trait variation. Behav Ecol. doi:10.1093/beheco/arr113
Gowaty P, Kim Y, Anderson W (2012) No evidence of sexual selection in a repetition of Bateman’s classic study of Drosophila melanogaster. Proc Nat Acad Sci U S A 109:11740–11745. www.pnas.org/cgi/doi/10.1073/pnas.1207851109
Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546
Gwynne DT, Simmons LW (1990) Experimental reversal of courtship roles in an insect. Nature 346:172–174
Hadfield JD, Burgess MD, Lord A, Phillimore AB, Clegg SM, Owens IPF (2006) Direct versus indirect sexual selection: genetic basis of colour, size and recruitment in a wild bird. Proc R Soc B 273:1347–1353
Hale M, Verduijn M, Møller A, Wolff K, Petrie M (2009) Is the peacock's train an honest signal of genetic quality at the major histocompatibility complex? J Evol Biol 22:1284–1294
Harcourt AH, Harvey PH, Larson SG, Short RV (1981) Testis weight, body weight and breeding system in primates. Nature 293:55–57
Harris WE, McKane AJ, Wolf JB (2008) The maintenance of heritable variation through social competition. Evolution Int J org Evolution 62:337–347
Johnstone R, Reynolds J, Deutsch J (1996) Mutual mate choice and sex differences in choosiness. Evolution 50:1382–1391
Kirkpatrick M (1982) Sexual selection and the evolution of female choice. Evolution Int J org Evolution 82:1–12
Kotiaho JS, LeBas NR, Puurtinen M, Tomkins JL (2008) On the resolution of the lek paradox. Trends Ecol Evol 23:1–3
Kraaijeveld K, Kraaijeveld-Smit F, Komdeur J (2007) The evolution of mutual ornamentation. Anim Behav 74:657–677
Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci USA 78:3721–3725
Macnair MR, Parker GA (1978) Models of parent-offspring conflict. II. Promiscuity. Anim Behav 26:111–122
Macnair MR, Parker GA (1979) Models of parent-offspring conflict. III. Intra-brood conflict. Anim Behav 27:1202–1209
Maynard Smith J (1982) Evolution and the theory of games. Cambridge University Press, Cambridge
Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge
Millstein R (2011) Sex and sensibility: The role of social selection (book symposium on Joan Roughgarden’s The genial gene). Metascience 20:258–264
Milam E (2010) Looking for a few good males: female choice in evolutionary biology. Johns Hopkins University Press, Baltimore
Miller CW, Moore AJ (2007) A potential resolution to the lek paradox through indirect genetic effects. Proc R Soc B 274:1279–1286
Parker G, Baker R, Smith V (1972) The origin and evolution of gamete dimorphism and the male-female phenomenon. J Theor Biol 36:529–553
Parker G, Macnair M (1978) Models of parent-offspring conflict. I. Monogamy. Anim Behav 26:97–110
Parker G, Macnair M (1979) Models of parent-offspring conflict. IV. Suppression: evolutionary retaliation by the parent. Anim Behav 27:1210–1235
Pizzari T, Foster KR (2008) Sperm sociality: cooperation, altruism, and spite. PLoS Biol 6:e130
Prum RO (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
Qvarnström A, Brommer JE, Gustafsson L (2006) Testing the genetics underlying the co-evolution of mate choice and ornament in the wild. Nature 441:84–86.
Rosvall K (2011) Intrasexual competition in females: evidence for sexual selection? Behavioral Ecology. doi:10.1093/beheco/arr106
Roughgarden J (2004) Evolution’s rainbow: diversity, gender and sexuality in nature and people. University of California Press, Berkeley CA
Roughgarden J (2005) The myth of sexual selection. Calif Wild 53:18–23
Roughgarden J (2007) Challenging Darwin's theory of sexual selection. Daedalus 136:1–14
Roughgarden J (2009) The Genial Gene: Deconstructing Darwinian Selfishness. University of California, Berkeley
Roughgarden J (2012a) The social selection alternative to sexual selection. Phil Trans Roy Soc B doi:10.1098/rstb.2011.0282
Roughgarden J (2012b) Teamwork, pleasure, and bargaining in animal social behavior. J Evol Biol doi:10.1111/j.1420-9101.2012.02505.x
Roughgarden J et al (2013) Sexual Selection Studies: Progress, Challenges, and Future Directions. Final Report from a NESCent Catalyst Meeting. Durham NC, July 15–17, 2013. Revision 1.1, December 11, 2013
Roughgarden J, Oishi M, Akçay E (2006) Reproductive social behavior: cooperative games to replace sexual selection. Science 311:965–969
Roughgarden J, Akçay E (2010) Do we need a sexual selection 2.0? Anim Behav 79:E1–E4
Roughgarden J, Iyer P (2011) Contact, not conflict, causes the evolution of anisogamy. In: Togashi T, Cox P (eds) The evolution of anisogamy: a fundamental phenomenon underlying sexual selection. Cambridge UK, Cambridge University Press, pp 96–110
Roughgarden J, Song Z (2014) Incentives in the family I: The family firm, an evolutionary/economic theory for parent-offspring relations. In: Narvaez D, Valentino K, Fuentes A, McKenna J, Gray P Ancestral landscapes in human evolution: culture, childrearing and social wellbeing. Oxford University Press, New York, pp 221–240
Shuker D (2010) Sexual selection: endless forms or tangled bank? Anim Behav 79:E11–E17
Simmons LW (1992) Quantification of role reversal in relative parental investment in a bush cricket. Nature 358:61–63
Snyder B, Gowaty, PA (2007) A reappraisal of Bateman's classic study of intrasexual selection. Evolution Int J org Evolution 61:2457–2468
Stockley P, Bro-Jørgensen J (2011) Female competition and its evolutionary consequences in mammals. Biol Rev 86:341–366
Takahashi M, Arita H, Hiraiwa-Hasegawa M, Hasegawa T (2008) Peahens do not prefer peacocks with more elaborate trains. Anim Behav 75:1209–1219
Tang-Martinez Z, Ryder TB (2005) The problem with paradigms: Bateman's worldview as a case study. Integr Comp Biol 45:821–830
Tickell WLN (2000) Albatrosses. Yale University Press, New Haven Conn
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine Publishing, Chicago, pp 136–179
Wallace AR (1871) Darwin’s ‘The descent of man and selection in relation to sex’. The Acad 1871:177
West-Eberhard MJ (1983) Sexual selection, social competition and speciation. Quart Rev Biol 58:155–183
Acknowlegements
I thank Thierry Hoquet for organizing the conference and for editing this volume. I also thank him for his translation of The Genial Gene into French. I thank Erol Akçay, Priya Iyer and Jeremy Van Cleve for their insight and counsel over the years.
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Roughgarden, J. (2015). Sexual Selection: Is Anything Left?. In: Hoquet, T. (eds) Current Perspectives on Sexual Selection. History, Philosophy and Theory of the Life Sciences, vol 9. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9585-2_5
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