This is a guest post by Angarika Deb.
Sexual Selection theory, though much celebrated, has faced criticism since its inception. A new model now proposes sexual reproduction and reproductive social behaviour to be cooperative instead of competitive, as was initially advocated earlier by Darwin.
After the sensational theory of natural selection, Darwin outlined the theory of sexual selection in his book, The Origin of Species (Darwin, 1869) and developed it in The Descent of Man and Selection in Relation to Sex (Darwin, 1871). This was in an effort to explain the structural and behavioural peculiarities in animals that did not make complete sense under the light of natural selection, for example ornamented plumage, mate signalling under predation risk etc. Natural selection is dependent on a struggle for enhancing individual survival; whereas sexual selection advocates a struggle between the sexes (intersexual competition) and amongst them (intrasexual competition) for rearing maximum progeny. ‘The result is not death to the unsuccessful competitor, but few or no offspring’, as explained by Darwin (1871). Heritable traits that are deemed detrimental to survival, were explained by sexual selection as conferring an advantage in intrasexual competition for finding mates and intersexual competition between mates to increase their own future reproductive fitness.
Since its advent sexual selection has become a largely popular theory, but it has not fared without scrutiny. An upsurge in the number of studies has brought forward many exceptions leading researchers to question the plausibility of the theory (Wallace, 1889). Conspicuous characteristics like bright colours, songs, special structures and modes of display behaviour, to which Darwin assigned display functions for attracting mates, have now been shown to serve other purposes like species recognition and speciation (West-Eberhard, 1983). Based on such evidence, a remodelling of sexual selection has been proposed under the general theory of ‘social competition’ – in which an individual competes with conspecifics for access to some resource (mates, in the case of sexual selection) (Moore et al., 2002; West-Eberhard, 1979). The debate continues, as Maynard Smith remarked that “no topic in evolutionary biology has presented greater difficulties for theorists” (Smith, 1991)
A recent paper by Roughgarden et al (2006) attempts to replace sexual selection altogether by the theory of social selection. It has introduced and celebrated the idea of cooperative game theory (Nash, 1950) as the mathematical basis for social selection. Cooperative games lead to bargaining solutions, where individuals cooperate to play as a team to maximise ‘team fitness’. The optimal equilibrium solution suggested here, is called a Nash Bargaining solution (NBS). In cooperative play, secondary sex characters – that had been assigned mate attraction and signalling functions by sexual selection – are social-inclusionary traits or ‘admission tickets’ permitting group participation for optimal offspring production. Players make threats, promises, and side payments to each other, exchange benefits to increase the number of offspring and form and dissolve coalitions. Proximal motivation for such teamwork, has been suggested to be reciprocal sharing of pleasure, where physical and vocal intimacy lead to hormonal surges and activation of neural pleasure centres. Cooperative play has thus been recommended as a better alternative to non-cooperative play (Smith, 1972). In non-cooperative games, every individual play to maximise their own (reproductive) fitness given the other players’ fixed strategy, reaching an equilibrium result known as Nash Competitive Equilibrium (NCE). The interplay of the strategies used for reaching NCE and NBS is shown in Figure 1.
It is however, to be noted that the bargaining procedure was originally modelled as a non-cooperative game (Rubinstein, 1982). Nash (1953) proposed Nash Bargaining Solution as the equilibrium state in a (non-cooperative) game, where players are uncertain about payoffs, and NBS is reached when the uncertainty vanishes. Cooperative games can reach NBS, only in the presence of an external enforcing agent or arbitrator, which is also the principal condition for a game to be cooperative. These strategies come under the purview of game theory (Nash, 1951) which has been used as a powerful approach to study behavioural traits in evolutionary biology, first introduced by Smith (1982). Game theory mathematically models behaviour into possible strategies that can be used by players under given conditions. An analysis of all possible combinations of strategies, gives us the optimal equilibrium solution called Evolutionarily Stable Strategy (ESS), which can be either NCE, NBS or both. Both NCE and NBS can be modelled under non-cooperative game theory, and it provides a low-level approach in modelling taking into account all procedural details of the game. Cooperative game, on the other hand, provides a simplified approach in describing the structure, strategies and payoffs of coalitions and models only NBS. Cooperative game theory can thus, be analysed under non-cooperative game theory by making certain assumptions (Brandenburger, 2007).
The non-cooperative game theory approach in sexual selection has successfully explained behavioural as well as genetic dimorphism (Smith, 1972). However, Roughgarden (2012) suggests behavioural and genetic evolution to be split up into a two-tier system, as selection acts upon them in different ways. The upper tier represents evolution of the gene pool, in which selection acts to optimise population traits, leading to an ESS (NCE) from competitive dynamics. The lower tier represents behavioural interactions between individuals, in which individuals incrementally accumulate fitness over its lifetime by playing various strategies. The accumulated fitness represents genetic fitness and can be gained both by cooperative and non-cooperative play. However, the authors take a clear bias towards cooperative game theory here (Roughgarden et al., 2006), whereas instances of competition for successful copulation, are much more prevalent in nature.
The factoring in of individual time budgets, and their allocation to playing each strategy is based on the economic approach to cooperation via repeated games, and might be a spurious factor in this model for two reasons: a) we are interested in understanding a general mechanism of behaviour that is most profitably shown over generations; b) it requires repeated play, to logically decide the best strategy, both of which might not be possible in a lot of cases.
The paper gives examples of peacock wrasses and Eurasian oystercatchers who cooperate and form coalitions for reproduction. In such coalitions, other ecological benefits can also be exchanged like access to food, safeguarding from predators, etc (Roughgarden et al., 2006). This allows genetically inferior individuals to mate and pass on their genes, reducing exclusive success of the genetically superior individuals (like alpha males and females) as seen in baboons (Ryne et al., 1997). This is in keeping with the fact that a hierarchy of variation is seen in nature where both superior and inferior individuals exist. Roughgarden et al (2006) also suggest the idea of optimal courtship and parental care as the equilibrium states for creating a social infrastructure where the offspring is reared successfully. This can be measured in the field by a ‘production function’, Maximising which is the shared motive, and leads to joint allocation of effort by the parents. However, there is plenty of documented evidence for parent – parent, as well as parent- offspring conflict. This is seen in genetic imprinting during offspring development. Haig’s Kinship Theory explains that paternal genetic factors regulate offspring gene expression (by epigenetic regulation) to increase demand on mother and ensure survival of offspring; whereas maternal genetic factors work to decrease offspring demand on the mother to increase her own fecundity (Haig, 2000).
A lopsided view of Darwin’s theory has been presented in this paper, and then forcefully negated, by claiming it to be “always mistaken”. It is a well-accepted idea that an individual’s evolutionary interests can sometimes conflict and sometimes coincide with those of its partner (Keller,1999). Darwin explains sexual selection as selection of any trait that confers competitive advantage for access to copulating partners or fertilisation. These traits can allow for a species’ mating system to be led by either sexual conflict or sexual cooperation and thus, social selection theory actually falls as a subcategory under that definition. The reverse however, is not true (Andersson, 1994).
Sexual selection has been a very open-ended theory since its inception because of its great overlap with natural selection. However, it has been extended further and restated many times. Roughgarden et al., asserts cooperation to be superior and driving reproductive fitness but empirical evidence stands against them (Arnqvist and Rowe, 2005; Dall et al., 2006). It is to be remembered that in reproduction, though maximising offspring production is the joint goal, male and female partners have different actions based upon maximising individual fitness. And such a conflict of motives makes the interactions fundamentally competitive, with cooperation being attained under certain ecological conditions. Sexual selection is a much wider theory than social selection, explaining anisogamy; primary, secondary and ecological sex traits, sexual dimorphism and reproductive hierarchy in social groups, which are not addressed by the latter. The same is true for non-cooperative game theory which is wider than, and can accommodate cooperative game theory under certain assumptions. Cooperation certainly exists in reproductive social systems, but cooperative game theory can only model a subset of the reproductive behaviours. Thus, instead of dismissing sexual selection altogether, social selection should be incorporated into it, to understand a wider diversity of structures seen in nature.
Angarika Deb has completed her MSc in Evolutionary and Behavioural Ecology from the University of Exeter (Department of Biosciences), UK.
References
Andersson, M. (1994). Sexual Selection (Princeton Univ. Press, Princeton, NJ).
Arnqvist, G., Rowe, L. (2005). Sexual Conflict (Princeton Univ Press, Princeton, NJ).
Brandenburger, A. (2007). Cooperative game theory. Teaching Materials at New York University.
Replies: Dall, S.R.X., McNamara, J.M., Wedell, N. & Hosken, D.J. (2006). Sexual selection cannot be replaced by cooperative game theory (and it doesn’t need replacing). Science 6 April.
Darwin, C. (1869). ORIGIN OF SPECIES. The Athenaeum, (2174), 861-861.
Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex (London: John Murray).
Haig, D. (2000). The kinship theory of genomic imprinting. Annual review of ecology and systematics, 31(1), 9-32.
Keller, L. (1999). Levels of selection in evolution. Princeton University Press.
Maynard Smith, J. (1972). “Game Theory and The Evolution of Fighting”. On Evolution (Edinburgh University Press).
Maynard Smith, J. (1982). Evolution and the Theory of Games. Cambridge, U.K.: Cambridge University Press.Smith, J. M. (1991). Theories of sexual selection. Trends in Ecology & Evolution, 6(5), 146-151.
Moore, A. J., Haynes, K. F., Preziosi, R. F., & Moore, P. J. (2002). The evolution of interacting phenotypes: genetics and evolution of social dominance. the american naturalist, 160(S6), S186-S197.
Nash, J. (1950). The bargaining problem. Econometrica, 18, 155–162.
Nash, J. (1951). Non-cooperative games. Annals of mathematics, 286-295.
Nash, J. (1953). Two-person cooperative games. Econometrica: Journal of the Econometric Society, 128-140.
Roughgarden J. (2012). Team work, pleasure and bargaining in animal social behaviour. J. Evol. Biol. 25,1454–1462.
Roughgarden, J. (2012). The social selection alternative to sexual selection. Philosophical transactions of the Royal Society B.
Roughgarden, J., Oishi, M. & Akcay, E. (2006). Reproductive social behavior: cooperative games to replace sexual selection. Science, 311, 965–969.
Rubinstein, A. (1982). Perfect equilibrium in a bargaining model. Econometrica: Journal of the Econometric Society, 97-109.
Ryne A.P., Robert M.S., Dorothy L.C. (1997) The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. Anim. Behav., 54, 599.
Wallace, A. R. (1889). Darwinism: An Exposition of the Theory of Natural Selection, with Some of the Applications. Macmillan.
West-Eberhard, M. J. (1979). Sexual selection, social competition, and evolution. Proceedings of the American Philosophical Society, 123(4), 222-234.
West-Eberhard, M. J. (1983). Sexual selection, social competition, and speciation. The Quarterly Review of Biology, 58(2), 155-183.