
The handicap principle is a
hypothesis
A hypothesis (: hypotheses) is a proposed explanation for a phenomenon. A scientific hypothesis must be based on observations and make a testable and reproducible prediction about reality, in a process beginning with an educated guess o ...
proposed by the Israeli biologist
Amotz Zahavi
Amotz Zahavi (; August 14, 1928 – May 12, 2017) was an Israeli evolutionary biologist, a Professor in the Department of Zoology at Tel Aviv University, and one of the founders of the Society for the Protection of Nature in Israel. His main work ...
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
Sexual characteristics are physical traits of an organism (typically of a sexually dimorphic organism) which are indicative of or resultant from biological sexual factors. These include both primary sex characteristics, such as gonads, and ...
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
Behavior (American English) or behaviour (British English) is the range of actions of Individual, individuals, organisms, systems or Artificial intelligence, artificial entities in some environment. These systems can include other systems or or ...
, or
morphology
Morphology, from the Greek and meaning "study of shape", may refer to:
Disciplines
*Morphology (archaeology), study of the shapes or forms of artifacts
*Morphology (astronomy), study of the shape of astronomical objects such as nebulae, galaxies, ...
that effectively lowers overall fitness. The central idea is that sexually selected traits function like
conspicuous consumption
In sociology and in economics, the term conspicuous consumption describes and explains the consumer practice of buying and using goods of a higher quality, price, or in greater quantity than practical. In 1899, the sociologist Thorstein Veblen c ...
, 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
Game theory is the study of mathematical models of strategic interactions. It has applications in many fields of social science, and is used extensively in economics, logic, systems science and computer science. Initially, game theory addressed ...
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.
History
Origins
The handicap principle was proposed in 1975 by the
Israeli biologist
Amotz Zahavi
Amotz Zahavi (; August 14, 1928 – May 12, 2017) was an Israeli evolutionary biologist, a Professor in the Department of Zoology at Tel Aviv University, and one of the founders of the Society for the Protection of Nature in Israel. His main work ...
. 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.
Grafen's signaling game model

The handicap principle was initially controversial,
with the British biologist
John Maynard Smith
John Maynard Smith (6 January 1920 – 19 April 2004) was a British mathematical and theoretical biology, theoretical and mathematical evolutionary biologist and geneticist. Originally an aeronautical engineer during the Second World War, he ...
a notable early critic of Zahavi's ideas.
However, the handicap principle gained wider acceptance because it is supported by
game theory
Game theory is the study of mathematical models of strategic interactions. It has applications in many fields of social science, and is used extensively in economics, logic, systems science and computer science. Initially, game theory addressed ...
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
Andrew Michael Spence (born November 7, 1943) is a Canadian-American economist and Nobel laureate.
Spence is the William R. Berkley Professor in Economics and Business at the Stern School of Business at New York University, and the Philip H. Kn ...
'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
Peafowl is a common name for two bird species of the genus '' Pavo'' and one species of the closely related genus '' Afropavo'' within the tribe Pavonini of the family Phasianidae (the pheasants and their allies). Male peafowl are referred t ...
'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.
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).
Cheap talk models without handicaps
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
In game theory, cheap talk is communication between players that does not directly affect the payoffs of the game. Providing and receiving information is free. This is in contrast to signalling (economics), signalling, in which sending certain mess ...
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
Mate choice is one of the primary mechanisms under which evolution can occur. It is characterized by a "selective response by animals to particular stimuli" which can be observed as behavior.Bateson, Paul Patrick Gordon. "Mate Choice." Mate Choi ...
, 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.
Unworkable theory lacking empirical evidence
In 2015, Simon Huttegger and colleagues wrote that the distinction between "indexes" (unfakable signals) and "fakable signals", crucial to the argument for the handicap principle, is an artefact of signalling models. They demonstrated that absent that dichotomy, cost could not be the only factor controlling signalling behaviours, and that indeed it was "probably not the most important" factor acting against deception.
Dustin J. Penn and Szabolcs Számadó stated in 2019 that there was still no
empirical evidence
Empirical evidence is evidence obtained through sense experience or experimental procedure. It is of central importance to the sciences and plays a role in various other fields, like epistemology and law.
There is no general agreement on how the ...
for evolutionary pressure for wasteful biology or acts, and proposed that the handicap principle should be abandoned.
Predictions and interpretations

The handicap principle predicts that a
sexual ornament, or any other signal such as visibly risky behavior, must be costly if it is to accurately advertise a trait of relevance to an individual with conflicting interests. Typical examples of handicapped signals include
bird song
Bird vocalization includes both bird calls and bird songs. In non-technical use, bird songs (often simply ''birdsong'') are the bird sounds that are melodious to the human ear. In ornithology and birding, songs (relatively complex vocalization ...
s, the peacock's tail,
courtship dance
A courtship display is a set of display behaviors in which an animal, usually a male, attempts to attract a mate; the mate Mate choice, exercises choice, so sexual selection acts on the display. These behaviors often include ritualized movement ( ...
s, and
bowerbird
Bowerbirds () make up the bird family Ptilonorhynchidae. They are renowned for their unique courtship behaviour, where males build a structure and decorate it with sticks and brightly coloured objects in an attempt to attract a mate.
The family ...
bowers. American scientist
Jared Diamond
Jared Mason Diamond (born September 10, 1937) is an American scientist, historian, and author. In 1985 he received a MacArthur Genius Grant, and he has written hundreds of scientific and popular articles and books. His best known is '' Guns, G ...
has proposed that certain risky human behaviours, such as
bungee jumping
Bungee jumping (), also spelled bungy jumping, is an activity that involves a person jumping from a great height while connected to a large elastic cord. The launching pad is usually erected on a tall structure such as a building or crane, a ...
, may be expressions of instincts that have evolved through the operation of the handicap principle. Zahavi has invoked the gift-giving
potlatch
A potlatch is a gift-giving feast practiced by Indigenous peoples of the Pacific Northwest Coast of Canada and the United States,Harkin, Michael E., 2001, Potlatch in Anthropology, International Encyclopedia of the Social and Behavioral Scienc ...
ceremony as a human example of the handicap principle in action: the conspicuous generosity is costly. This interpretation of potlatch can be traced to
Thorstein Veblen
Thorstein Bunde Veblen (; July 30, 1857 – August 3, 1929) was an American Economics, economist and Sociology, sociologist who, during his lifetime, emerged as a well-known Criticism of capitalism, critic of capitalism.
In his best-known book ...
's use of the ceremony in his book ''
Theory of the Leisure Class'' as an example of "
conspicuous consumption
In sociology and in economics, the term conspicuous consumption describes and explains the consumer practice of buying and using goods of a higher quality, price, or in greater quantity than practical. In 1899, the sociologist Thorstein Veblen c ...
".
The handicap principle gains further support by providing interpretations for behaviours that fit into a single unifying
gene-centered view of evolution
The gene-centered view of evolution, gene's eye view, gene selection theory, or selfish gene theory holds that adaptive evolution occurs through the differential survival of competing genes, increasing the allele frequency of those alleles wh ...
and making earlier explanations based on
group selection
Group selection is a proposed mechanism of evolution in which natural selection acts at the level of the group, instead of at the level of the individual or gene.
Early authors such as V. C. Wynne-Edwards and Konrad Lorenz argued that the beha ...
obsolete. A classic example is that of ''
stotting
Stotting (also called pronking or pronging) is a behavior of quadrupeds, particularly gazelles, in which they spring into the air, lifting all four feet off the ground simultaneously. Usually, the legs are held in a relatively stiff position. Ma ...
'' in
gazelle
A gazelle is one of many antelope species in the genus ''Gazella'' . There are also seven species included in two further genera; '' Eudorcas'' and '' Nanger'', which were formerly considered subgenera of ''Gazella''. A third former subgenus, ' ...
s. This behaviour consists in the gazelle initially running slowly and jumping high when threatened by a
predator
Predation is a biological interaction in which one organism, the predator, kills and eats another organism, its prey. It is one of a family of common List of feeding behaviours, feeding behaviours that includes parasitism and micropredation ...
such as a
lion
The lion (''Panthera leo'') is a large Felidae, cat of the genus ''Panthera'', native to Sub-Saharan Africa and India. It has a muscular, broad-chested body (biology), body; a short, rounded head; round ears; and a dark, hairy tuft at the ...
or
cheetah
The cheetah (''Acinonyx jubatus'') is a large Felidae, cat and the Fastest animals, fastest land animal. It has a tawny to creamy white or pale buff fur that is marked with evenly spaced, solid black spots. The head is small and rounded, wit ...
. The explanation based on group selection was that such behaviour might be adapted to alerting other gazelle to a cheetah's presence or might be part of a collective behaviour pattern of the group of gazelle to confuse the cheetah. Instead, Zahavi proposed that each gazelle was communicating that it was a fitter individual than its fellows.
Signals to members of the same species
Zahavi studied in particular the
Arabian babbler, a highly social bird, with a life-length of 30 years, which appears to behave
altruistically. Its helping-at-the-nest behavior, where non-parent birds assist in feeding, guarding, and caring for nestlings, often occurs among unrelated individuals. This, therefore, cannot be explained by
kin selection
Kin selection is a process whereby natural selection favours a trait due to its positive effects on the reproductive success of an organism's relatives, even when at a cost to the organism's own survival and reproduction. Kin selection can lead ...
,
natural selection
Natural selection is the differential survival and reproduction of individuals due to differences in phenotype. It is a key mechanism of evolution, the change in the Heredity, heritable traits characteristic of a population over generation ...
acting on genes that close relatives share with the altruistic individual. Zahavi reinterpreted these behaviors 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
Competitive altruism is a possible mechanism for the persistence of cooperative behaviours, specifically those that are performed unconditionally. The theory of reciprocal altruism can be used to explain behaviours that are performed by a donor wh ...
.
French biologist Patrice David showed that in the
stalk-eyed fly
Stalk-eyed flies are insects of the fly family Diopsidae. The family is distinguished from most other flies by most members of the family possessing "eyestalks": projections from the sides of the head with the eyes at the end. Some fly species f ...
species ''
Cyrtodiopsis dalmanni'', genetic variation underlies the response to environmental stress, such as variable food quality, of a male sexual ornament, eye span. He showed that some male
genotypes
The genotype of an organism is its complete set of genetic material. Genotype can also be used to refer to the alleles or variants an individual carries in a particular gene or genetic location. The number of alleles an individual can have in a ...
always develop large eye spans, but others reduce eye span in proportion to environmental worsening. David inferred that female mate choice yields genetic benefits for offspring.
Signals to other species

Signals may be directed at
predators
Predation is a biological interaction in which one organism, the predator, kills and eats another organism, its prey. It is one of a family of common feeding behaviours that includes parasitism and micropredation (which usually do not kill ...
, with the function of showing that pursuit will probably be unprofitable.
Stotting
Stotting (also called pronking or pronging) is a behavior of quadrupeds, particularly gazelles, in which they spring into the air, lifting all four feet off the ground simultaneously. Usually, the legs are held in a relatively stiff position. Ma ...
, 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 appeared likely to be selected against. However, it made sense when seen as a
pursuit deterrence signal to predators. By investing a little energy to show a lion that it has the fitness necessary to avoid capture, a gazelle reduces the likelihood that it will have to evade the lion in an actual pursuit. The lion, faced with the demonstration of fitness, might decide that it would fail to catch this gazelle, and thus choose to avoid a probably 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).
However, the mathematical biologist
John Maynard Smith
John Maynard Smith (6 January 1920 – 19 April 2004) was a British mathematical and theoretical biology, theoretical and mathematical evolutionary biologist and geneticist. Originally an aeronautical engineer during the Second World War, he ...
commented that
other explanations were possible, such as that it was an honest signal of fitness,
or an honest signal that the predator had been detected, and it was hard to see how stotting could be a handicap.
Another example is provided by
lark
Larks are passerine birds of the family Alaudidae. Larks have a cosmopolitan distribution with the largest number of species occurring in Africa. Only a single species, the horned lark, occurs in North America, and only Horsfield's bush lark occ ...
s, some of which discourage
merlins by sending a similar message: they
sing
Singing is the art of creating music with the voice. It is the oldest form of musical expression, and the human voice can be considered the first musical instrument. The definition of singing varies across sources. Some sources define singi ...
while being chased, telling their predator that they will be difficult to capture.
Immunocompetence handicaps
The theory of
immunocompetence
In immunology, immunocompetence is the ability of the body to produce a normal immune response following exposure to an antigen. Immunocompetence is the opposite of immunodeficiency (also known as ''immuno-incompetence'' or being ''immuno-compro ...
handicaps suggests that
androgen
An androgen (from Greek ''andr-'', the stem of the word meaning ) is any natural or synthetic steroid hormone that regulates the development and maintenance of male characteristics in vertebrates by binding to androgen receptors. This includes ...
-mediated traits accurately signal condition due to the
immunosuppressive
Immunosuppression is a reduction of the activation or efficacy of the immune system. Some portions of the immune system itself have immunosuppressive effects on other parts of the immune system, and immunosuppression may occur as an adverse react ...
effects of androgens. This immunosuppression may be either because
testosterone
Testosterone is the primary male sex hormone and androgen in Male, males. In humans, testosterone plays a key role in the development of Male reproductive system, male reproductive tissues such as testicles and prostate, as well as promoting se ...
alters the allocation of limited resources between the development of
ornamental traits and other tissues, including the
immune system
The immune system is a network of biological systems that protects an organism from diseases. It detects and responds to a wide variety of pathogens, from viruses to bacteria, as well as Tumor immunology, cancer cells, Parasitic worm, parasitic ...
, or because heightened immune system activity has a propensity to launch autoimmune attacks against
gametes
A gamete ( ) is a haploid cell that fuses with another haploid cell during fertilization in organisms that reproduce sexually. Gametes are an organism's reproductive cells, also referred to as sex cells. The name gamete was introduced by the Ge ...
, such that suppression of the immune system enhances
fertility
Fertility in colloquial terms refers the ability to have offspring. In demographic contexts, fertility refers to the actual production of offspring, rather than the physical capability to reproduce, which is termed fecundity. The fertility rate ...
. 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.
See also
*
Aposematism
Aposematism is the Advertising in biology, advertising by an animal, whether terrestrial or marine, to potential predation, predators that it is not worth attacking or eating. This unprofitability may consist of any defenses which make the pr ...
*
Costly signaling theory in evolutionary psychology
*
Fisherian runaway
Fisherian runaway or runaway selection is a sexual selection mechanism proposed by the mathematical biologist Ronald Fisher in the early 20th century, to account for the evolution of ostentatious male ornamentation by persistent, directional f ...
*
Multiple sexual ornaments
Many species have multiple sexual ornaments, whereby females select mating partners using several cues instead of only one cue. Whereas this phenomenon is self-evident and hence long recognized, adaptive explanations of why females use several in ...
*
Parasite-stress theory
Parasite-stress theory, or pathogen-stress theory, is a theory of human evolution proposing that Parasitism , parasites and diseases encountered by a species shape the development of species' values and qualities, proposed by researchers Corey Fin ...
*
Sacrifice
Sacrifice is an act or offering made to a deity. A sacrifice can serve as propitiation, or a sacrifice can be an offering of praise and thanksgiving.
Evidence of ritual animal sacrifice has been seen at least since ancient Hebrews and Gree ...
References
External links
''Honest Signalling Theory: A Basic Introduction'' By Carl T. Bergstrom, University of Washington, 2006.
{{DEFAULTSORT:Handicap Principle
Signalling theory
Animal communication
Ethology
Selection
Sexual selection