Handicap principle

The handicap principle is a hypothesis proposed by the Israeli biologist Amotz Zahavi in 1975. It is meant to explain how "signal selection" during mate choice may lead to "honest" or reliable signalling between male and female animals which have an obvious motivation to bluff or deceive each other. The handicap principle suggests that secondary sexual characteristics are costly signals which must be reliable, as they cost the signaller resources that individuals with less of a particular trait could not afford. The handicap principle further proposes that animals of greater biological fitness signal this through handicapping behaviour, or morphology that effectively lowers overall fitness. The central idea is that sexually selected traits function like conspicuous consumption, signalling the ability to afford to squander a resource. Receivers then know that the signal indicates quality, because inferior-quality signallers are unable to produce such wastefully extravagant signals.

The handicap principle is supported by game theory modelling representing situations such as nestlings begging for food, predator-deterrent signalling, and threat displays. However, honest signals are not necessarily costly, undermining the theoretical basis for the handicap principle, which remains unconfirmed by empirical evidence.

The handicap principle was proposed in 1975 by the Israeli biologist Amotz Zahavi. He argued that mate choice involving what he called "signal selection" would lead to "honest" or reliable signalling between male and female animals, even though they have an interest in bluffing or deceiving each other. The handicap principle asserts that secondary sexual characteristics are costly signals, which are reliable indicators of the signaller's quality, since they cost the signaller resources that lower-quality individuals could not afford. The generality of the phenomenon is a matter of some debate and disagreement, and Zahavi's views on the scope and importance of handicaps in biology have not been accepted by the mainstream. Nevertheless, the idea has been very influential, with most researchers in the field believing that the theory explains some aspects of animal communication.

The handicap principle was initially controversial, with the British biologist John Maynard Smith a notable early critic of Zahavi's ideas. However, the handicap principle gained wider acceptance because it is supported by game theory models, most notably the Scottish biologist Alan Grafen's 1990 signalling game model. This was essentially a rediscovery of the Canadian-American economist Michael Spence's job market signalling model, where the job applicant signals their quality by declaring a costly education. In Grafen's model, the courting male's quality is signalled by investment in an extravagant trait—similar to the peacock's tail. The signal is reliable if the marginal cost to the signaller is proportionately lower for higher-quality signallers than for lower-quality ones: the cost can be lower or the benefit higher, or both.

A series of papers by the American biologist Thomas Getty showed that Grafen's proof of the handicap principle depends on the critical, simplifying assumption that signallers trade off costs for benefits in an additive fashion, analogous to the way humans invest money to increase income in the same currency. This is illustrated in the figures from Johnstone 1997, which show that the optimum signalling levels are different for low- and high-quality signallers. The validity of the assumption that costs and benefits are additive has been contested, in its application to the evolution of sexually selected signals. It can be reasoned that since fitness depends on the production of offspring, this is a multiplicative rather than additive function of reproductive success.

Further game theoretical models demonstrated the evolutionary stability of handicapped signals in nestlings' begging calls, in predator-deterrent signals and in threat-displays. In the classic handicap models of begging in game theory, all players are assumed to pay the same amount to produce a signal of a given level of intensity, but differ in the relative value of eliciting the desired response (donation) from the receiver. The hungrier the baby bird, the more food is of value to it, and the higher the optimal signalling level (the louder its chirping).

Counter-examples to handicap models predate handicap models themselves. Models of signals (such as threat displays) without any handicapping costs show that what biologists call cheap talk may be an evolutionarily stable form of communication. Analysis of some begging models shows that non-communication strategies are not only evolutionarily stable, but lead to higher payoffs for both players. In human mate choice, mathematical analyses including Monte Carlo simulations suggest that costly traits ought to be more attractive to the other sex and much rarer than non-costly traits.

It was soon discovered that honest signals need not be costly at the honest equilibrium, even under conflict of interest. This conclusion was first shown in discrete models and then in continuous models. Similar results were obtained in conflict models: threat displays need not be handicaps to be honest and evolutionarily stable.