Handicap principle

The handicap principle was proposed in 1975 by Israeli biologist Amotz Zahavi.[1][2][4] The generality of the phenomenon is the 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.[5][6] Nevertheless, the idea has been very influential, with most researchers in the field believing that the theory explains some aspects of animal communication.[7][8][9]

Johnstone's 1997 graphical representation of a Zahavian handicap. Where ${\displaystyle C_{L}}$ is cost to a low-quality signaller and ${\displaystyle C_{H}}$ is cost to a high-quality signaller. Optimal signalling levels are ${\displaystyle S_{L}^{*}}$ for a low-quality signaller, and ${\displaystyle S_{H}^{*}}$ for a high-quality signaller.[7]

The handicap principle was initially controversial;[10][11][12][13] British biologist John Maynard Smith was a notable early critic of Zahavi's ideas.[14][15][16] However it gained wider acceptance because it is supported by game theory models, most notably Scottish biologist Alan Grafen's signalling game model.[17] This was essentially a rediscovery of Canadian-American economist Michael Spence's job market signalling model,[18] 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—such as the peacock's tail. The signal is reliable if the cost to the signaller of producing it is proportionately lower for higher-quality signallers than for lower-quality ones.[17]

A series of papers by 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, the way humans invest money to increase income in the same currency.[19][20][21][22] This is illustrated in the figures from Johnstone 1997.[7] The validity of this assumption has been contested, in its application to the cost–benefit trade-off that is assumed to mediate 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.[23]

Further formal game theoretical signalling models demonstrated the evolutionary stability of handicapped signals in nestlings' begging calls,[24] in predator-deterrent signals[25] and in threat-displays.[26][27] In the classic handicapped models of begging, 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).[24]

Counter-examples to handicap models predate handicap models themselves. Models of signals (such as threat displays) without any handicapping costs show that conventional signalling may be evolutionarily stable in biological communication.[28] Analysis of some begging models shows that non-communication strategies are not only evolutionarily stable, but lead to higher payoffs for both players.[29][30] Mathematical analyses including Monte Carlo simulations suggest that costly traits used in mate choice by humans should be generally less common and more attractive to the other sex than non-costly traits.[31]

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[32][33] and then in continuous models.[34][35][36] Similar results were obtained in conflict models: threat displays need not be handicaps to be honest and evolutionarily stable.[37]

Dustin J. Penn and Szabolcs Számadó stated in 2019 that there was still no empirical evidence for evolutionary pressure for wasteful biology or acts, and proposed that the handicap principle should be abandoned.[38]

Luxury cars and other "Veblen goods" may be an example of the handicap principle in humans

Zahavi studied in particular the Arabian babbler, a very social bird, with a life-length of 30 years, which was considered to have altruistic behaviors. The helping-at-the-nest behavior often occurs among unrelated individuals, and therefore cannot be explained by kin selection. Zahavi reinterpreted these behaviours according to his signalling theory and its correlative, the handicap principle. The altruistic act is costly to the donor, but may improve its attractiveness to potential mates. The evolution of this condition may be explained by competitive altruism.[40][41][42]

Research by French biologist Patrice David on the stalk-eyed fly species Cyrtodiopsis dalmanni has demonstrated that genetic variation underlies the response to environmental stress, such as variable food quality, or of male sexual ornaments, such as increased eye span. David demonstrated that some male genotypes develop large eye spans under all conditions, whereas other genotypes progressively reduce eye spans as environmental conditions deteriorate. Several non-sexual traits, including female eye span and male and female wing length, also show condition-dependent expression, but their genetic response is entirely explained by scaling with body size. Unlike these characteristics, male eye span still reveals genetic variation in response to environmental stress after accounting for differences in body size. David inferred that these results strongly support the conclusion that female mate choice yields genetic benefits for offspring as eye span acts as a truthful indicator of male fitness. Eye span is therefore not only selected on the basis of attractiveness, but also because it demonstrates good genes in mates.[43]

Impala stotting, a behavior that may signal to predators that a pursuit would be wasted

Signals may be directed at predators, with the function of showing that pursuit will probably be unprofitable. Stotting, for instance, is a form of energetic jumping that certain gazelles do when they sight a predator. As this behavior gives no evident benefit and would seem to waste resources (diminishing the gazelle's head start if chased by the predator), it was a puzzle until handicap theory offered an explanation. According to this analysis, if the gazelle simply invests a little energy to show a lion that it has the fitness necessary to avoid capture, it may not have to evade the lion in an actual pursuit. The lion, faced with the demonstration of fitness, might decide that it will not catch this gazelle, and thus, avoid a wasted pursuit. The benefit to the gazelle is twofold. First, for the small amount of energy invested in the stotting, the gazelle might not have to expend the tremendous energy required to evade the lion. Second, if the lion is in fact capable of catching this gazelle, the gazelle's bluff may lead to its survival that day (in the event the bluff succeeds).[44]

Another example is provided by larks, some of which discourage merlins by sending a similar message: they sing while being chased, telling their predator that they will be difficult to capture.[45]

The theory of immunocompetence handicaps suggests that androgen-mediated traits accurately signal condition due to the immunosuppressive effects of androgens.[46] This immunosuppression may be either because testosterone alters the allocation of limited resources between the development of ornamental traits and other tissues, including the immune system,[47] or because heightened immune system activity has a propensity to launch autoimmune attacks against gametes, such that suppression of the immune system enhances fertility.[48] Healthy individuals can afford to suppress their immune system by raising their testosterone levels, at the same time augmenting secondary sexual traits and displays. A review of empirical studies into the various aspects of this theory found weak support.[49]