Editing Handicap principle

{{good article}}
{{Short description|Hypothesis in evolutionary biology}}
[[File:Peacock Flying.jpg|thumb|300px|right|The peacock tail in flight, a classic example of what [[Amotz Zahavi]] proposed was a handicapped signal of male quality.<ref name="Grafen 1990"/>|alt=Photo of a peacock with its enormous tail]]

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 [[Signalling theory|"honest" or reliable signalling]] between male and female animals which have an obvious motivation to bluff or deceive each other.<ref name="Zahavi 1975 pp. 205–214">{{cite journal |last=Zahavi |first=Amotz |author-link=Amotz Zahavi |title=Mate selection—A selection for a handicap |journal=Journal of Theoretical Biology |publisher=Elsevier BV |volume=53 |issue=1 |year=1975 |issn=0022-5193 |doi=10.1016/0022-5193(75)90111-3 |pages=205–214|pmid=1195756 |bibcode=1975JThBi..53..205Z }}</ref><ref name="Zahavi 1977 pp. 603–605">{{cite journal |last=Zahavi |first=Amotz |author-link=Amotz Zahavi |title=The cost of honesty |journal=Journal of Theoretical Biology |publisher=Elsevier BV |volume=67 |issue=3 |year=1977 |issn=0022-5193 |doi=10.1016/0022-5193(77)90061-3 |pages=603–605|pmid=904334 |bibcode=1977JThBi..67..603Z }}</ref><ref name="Zahavi Zahavi 1997">{{cite book |last1=Zahavi |first1=Amotz |author1-link=Amotz Zahavi |last2=Zahavi |first2=Avishag |title=The handicap principle: a missing piece of Darwin's puzzle |publisher=Oxford University Press |location=New York |year=1997 |isbn=978-0-19-510035-8 |oclc=35360821 |url=http://eprints.soton.ac.uk/261475/1/10.1.1.40.3266.pdf}}</ref> 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 [[fitness (biology)|biological fitness]] signal this through handicapping [[ethology|behaviour]], or [[Morphology (biology)|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.<ref name="Davis 1976" /><ref name="Eshel 1978" /><ref name="Kirkpatrick 1986" /><ref name="Pomiankowski 1987" /><ref name="Maynard Smith 1976" />   

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.

== History ==

=== Origins ===

The handicap principle was proposed in 1975 by the [[Israel|Israeli]] biologist [[Amotz Zahavi]]. He argued that mate choice involving what he called "signal selection" would lead to [[honest signalling|"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.<ref name="Zahavi 1975 pp. 205–214"/><ref name="Zahavi 1977 pp. 603–605"/><ref name="Zahavi 1997">{{cite book |last=Zahavi |first=Amotz |title=The handicap principle: a missing piece of Darwin's puzzle |publisher=Oxford University Press |location=New York |year=1997 |isbn=978-0-19-510035-8 |oclc=35360821 |url-access=registration |url=https://archive.org/details/handicapprincipl0000zeha}}</ref> 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.<ref>{{cite journal |last1=Grose |first1=Jonathan |title=Modelling and the fall and rise of the handicap principle |journal=Biology & Philosophy |date=7 June 2011 |volume=26 |issue=5 |pages=677–696 |doi=10.1007/s10539-011-9275-1 |s2cid=84600072 }}</ref><ref>Review by {{cite journal |first1=Andrew |last1=Pomiankowski |last2=Iwasa |first2=Y. |year=1998 |title=Handicap Signaling: Loud and True? |journal=[[Evolution (journal)|Evolution]] |volume=52 |issue=3 |pages=928–932 |doi=10.2307/2411290 |jstor=2411290 |s2cid=53060420 |url=https://semanticscholar.org/paper/9fd8edb7b18bd5e6666e798e5c7679b2b4b0993b }}</ref> Nevertheless, the idea has been very influential, with most researchers in the field believing that the theory explains some aspects of animal communication.<ref name="Johnstone97">{{cite journal |last=Johnstone |first=R. A. |year=1995 |title=Sexual selection, honest advertisement and the handicap principle: reviewing the evidence |journal=[[Biological Reviews]] |volume=70 |issue=1 |pages=1–65 |doi=10.1111/j.1469-185X.1995.tb01439.x |pmid=7718697 |s2cid=40322800 }}</ref><ref>{{cite book |last=Johnstone |first=Rufus A. |year=1997 |chapter=The Evolution of Animal Signals |title=Behavioural Ecology: An Evolutionary Approach |url=https://archive.org/details/behaviouralecolo00kreb |url-access=limited |edition=4th |editor-first=J. R. |editor-last=Krebs |editor2-first=N. B. |editor2-last=Davies |publisher=Blackwell |pages=[https://archive.org/details/behaviouralecolo00kreb/page/n164 155]–178 |isbn=978-0865427310 }}</ref><ref>{{cite book |last1=Maynard Smith |first1=John |author1-link=John Maynard Smith |last2=Harper |first2=David |author2-link=David Harper (biologist) |year=2003 |chapter=The theory of costly signalling |title=Animal Signals |publisher=[[Oxford University Press]] |pages=16–31 |isbn=978-0-19-852685-8}}</ref>

=== Grafen's signaling game model ===

{{further|Signaling game}}

[[File:Handicap-signal-of-quality.png|thumb|upright=1.5|Graph based on Johnstone's 1997 graphical representation of a Zahavian handicap. Where <math>C_L</math> is cost to a low-quality signaller and <math>C_H</math> is cost to a high-quality signaller. Optimal signalling levels are <math>S^*_L</math> for a low-quality signaller, and <math>S^*_H</math> for a high-quality signaller.<ref name="Johnstone97"/>|alt=Graph showing mathematically how a handicap would in theory work]]

The handicap principle was initially controversial,<ref name="Davis 1976">{{cite journal |last1=Davis |first1=J. W. F. |last2=O'Donald |first2=P. |year=1976 |title=Sexual selection for a handicap: A critical analysis of Zahavi's model |journal=Journal of Theoretical Biology |volume=57 |issue=2 |pages=345–354 |doi=10.1016/0022-5193(76)90006-0 |pmid=957664 |bibcode=1976JThBi..57..345D }}</ref><ref name="Eshel 1978">{{cite journal |last=Eshel |first=I. |year=1978 |title=On the Handicap Principle—A Critical Defence |journal=Journal of Theoretical Biology |volume=70 |issue=2 |pages=245–250 |doi=10.1016/0022-5193(78)90350-8 |pmid=633919 |bibcode=1978JThBi..70..245E }}</ref><ref name="Kirkpatrick 1986">{{cite journal |last=Kirkpatrick |first=M. |year=1986 |title=The handicap mechanism of sexual selection does not work |journal=[[American Naturalist]] |volume=127 |issue=2 |pages=222–240 |doi=10.1086/284480|jstor=2461351 |s2cid=83984463 }}</ref><ref name="Pomiankowski 1987">{{cite journal |last=Pomiankowski |first=A. |year=1987 |title=Sexual selection: The handicap principle does work sometimes |journal=[[Proceedings of the Royal Society B]] |volume=231 |issue=1262 |pages=123–145 |doi=10.1098/rspb.1987.0038 |bibcode=1987RSPSB.231..123P |s2cid=144837163 }}</ref> with the British biologist [[John Maynard Smith]] a notable early critic of Zahavi's ideas.<ref name="Maynard Smith 1976">{{cite journal |last=Maynard Smith |first=John |author-link=John Maynard Smith |year=1976 |title=Sexual selection and the handicap principle |journal=Journal of Theoretical Biology |volume=57 |issue=1 |pages=239–242 |doi=10.1016/S0022-5193(76)80016-1 |pmid=957656 |bibcode=1976JThBi..57..239S }}</ref><ref>{{cite journal |last=Maynard Smith |first=John |author-link=John Maynard Smith |year=1978 |title=The Handicap Principle—A Comment |journal=Journal of Theoretical Biology |volume=70 |issue=2 |pages=251–252 |doi=10.1016/0022-5193(78)90351-X |pmid=633920 |bibcode=1978JThBi..70..251S }}</ref><ref>{{cite journal |last=Maynard Smith |first=John |author-link=John Maynard Smith |year=1985 |title=Mini Review: Sexual Selection, Handicaps and True Fitness |journal=Journal of Theoretical Biology |volume=115 |issue=1 |pages=1–8 |doi=10.1016/S0022-5193(85)80003-5 |pmid=4033159 }}</ref> 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.<ref name="Grafen 1990">{{cite journal |last=Grafen |first=A. |year=1990 |title=Biological signals as handicaps |journal=Journal of Theoretical Biology |volume=144 |issue=4 |pages=517–546 |doi=10.1016/S0022-5193(05)80088-8 |pmid=2402153|bibcode=1990JThBi.144..517G }}</ref> This was essentially a rediscovery of the Canadian-American economist [[Michael Spence]]'s [[Signaling (economics)|job market signalling model]],<ref>{{cite journal |last=Spence |first=A. M. |year=1973 |title=Job Market Signaling |journal=[[Quarterly Journal of Economics]] |volume=87 |issue=3 |pages=355–374 |doi=10.2307/1882010 |jstor=1882010 }}</ref> 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 cost to the signaller of producing it is proportionately lower for higher-quality signallers than for lower-quality ones.<ref name="Grafen 1990"/>

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.<ref>{{cite journal |last=Getty |first=T. |year=1998a |title=Handicap signalling: when fecundity and viability do not add up |journal=[[Animal Behaviour (journal)|Animal Behaviour]] |volume=56 |issue=1 |pages=127–130 |doi=10.1006/anbe.1998.0744 |pmid=9710469|s2cid=36731320 }}</ref><ref>{{cite journal |last=Getty |first=T. |year=1998b |title=Reliable signalling need not be a handicap |journal=Anim. Behav. |volume=56 |issue=1 |pages=253–255 |doi=10.1006/anbe.1998.0748 |pmid=9710484 |s2cid=34066689 }}</ref><ref>{{cite journal |last=Getty |first=Thomas |year=2002 |title=Signaling health versus parasites |journal=[[American Naturalist]] |volume=159 |issue=4 |pages=363–371 |doi=10.1086/338992 |jstor=338992 |pmid=18707421 |s2cid=12598696 }}</ref><ref name="Getty 2006">{{cite journal |last=Getty |first=T. |year=2006 |title=Sexually selected signals are not similar to sports handicaps |journal=[[Trends in Ecology & Evolution]] |volume=21 |issue=2 |pages=83–88 |doi=10.1016/j.tree.2005.10.016 |pmid=16701479 }}</ref> This is illustrated in the figures from Johnstone 1997, which show that the optimum signalling levels are different for low- and high-quality signallers.<ref name="Johnstone97"/> The validity of the assumption that costs and benefits are additive has been contested, in its application to the evolution of [[signalling theory|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.<ref>{{cite journal |last1=Nur |first1=N. |last2=Hasson |first2=O. |year=1984 |title=Phenotypic plasticity and the handicap principle |journal=J. Theor. Biol. |volume=110 |issue=2 |pages=275–297 |doi=10.1016/S0022-5193(84)80059-4 |bibcode=1984JThBi.110..275N }}</ref>

Further game theoretical models demonstrated the [[Evolutionarily stable strategy|evolutionary stability]] of handicapped signals in nestlings' begging calls,<ref name="Godfray 1991">{{cite journal |last=Godfray |first=H. C. J. |year=1991 |title=Signalling of need by offspring to their parents |journal=[[Nature (journal)|Nature]] |volume=352 |issue=6333 |pages=328–330 |doi=10.1038/352328a0 |bibcode=1991Natur.352..328G |s2cid=4288527 }}</ref> in predator-deterrent signals<ref>{{cite journal |last=Yachi |first=S. |year=1995 |title=How can honest signalling evolve? The role of the handicap principle |journal=[[Proceedings of the Royal Society B]] |volume=262 |issue=1365 |pages=283–288 |doi=10.1098/rspb.1995.0207 |s2cid=85339637 }}</ref> and in threat-displays.<ref>{{cite journal |last1=Adams |first1=E. S. |last2=Mesterton-Gibbons |first2=M. |year=1995 |title=The cost of threat displays and the stability of deceptive communication |journal=Journal of Theoretical Biology |volume=175 |issue=4 |pages=405–421 |doi=10.1006/jtbi.1995.0151 |bibcode=1995JThBi.175..405A |doi-access=free }}</ref><ref>{{cite journal |last=Kim |first=Y-G. |year=1995 |title=Status signalling games in animal contests |journal=Journal of Theoretical Biology |volume=176 |issue=2 |pages=221–231 |doi=10.1006/jtbi.1995.0193 |pmid=7475112 |bibcode=1995JThBi.176..221K }}</ref> 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).<ref name="Godfray 1991"/>

=== Cheap talk models without handicaps ===

{{further|Cheap talk}}

Counter-examples to handicap models predate handicap models themselves. Models of signals (such as [[Deimatic behaviour|threat displays]]) without any handicapping costs show that what biologists call [[cheap talk]] may be an evolutionarily stable form of communication.<ref>{{cite journal |last=Enquist |first=M. |year=1985 |title=Communication during aggressive interactions with particular reference to variation in choice of behaviour |journal=Animal Behaviour |volume=33 |issue=4 |pages=1152–1161 |doi=10.1016/S0003-3472(85)80175-5 |s2cid=53200843 }}</ref> Analysis of some begging models shows that non-communication strategies are not only evolutionarily stable, but lead to higher payoffs for both players.<ref>{{cite journal |last1=Rodriguez-Girones |first1=M. A. |last2=Cotton |first2=P. A. |last3=Kacelnik |first3=A. |year=1996 |title=The evolution of begging: signaling and sibling competition |journal=[[Proceedings of the National Academy of Sciences of the United States of America]] |volume=93 |issue=25 |pages=14637–14641 |doi=10.1073/pnas.93.25.14637|pmid=8962106 |pmc=26187 |bibcode=1996PNAS...9314637R |doi-access=free }}</ref><ref>{{cite journal |last1=Lachmann |first1=M. |author-link2=Carl Bergstrom |last2=Bergstrom |first2=C. T. |year=1998 |title=Signalling among relatives. II. Beyond the tower of babel |journal=Theoretical Population Biology |volume=54 |issue=2 |pages=146–160 |doi=10.1006/tpbi.1997.1372 |pmid=9733656|doi-access=free |bibcode=1998TPBio..54..146L }}</ref> In human [[mate choice]], mathematical analyses including [[Monte Carlo method|Monte Carlo simulations]] suggest that costly traits ought to be more attractive to the other sex and much rarer than non-costly traits.<ref>{{cite journal |last=Kock |first=N. |year=2011 |url=http://cits.tamiu.edu/kock/Pubs/journals/2011JournalJEP/Kock_2011_JEP_EvoMateChTrts.pdf |title=A mathematical analysis of the evolution of human mate choice traits: Implications for evolutionary psychologists |journal=Journal of Evolutionary Psychology |volume=9 |issue=3 |pages=219–247 |doi=10.1556/jep.9.2011.3.1}}</ref>

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 modelling|discrete models]]<ref>{{Cite journal |last=Hurd |first=Peter L. |date=May 1995 |title=Communication in discrete action-response games |url=http://dx.doi.org/10.1006/jtbi.1995.0093 |journal=Journal of Theoretical Biology |volume=174 |issue=2 |pages=217–222 |doi=10.1006/jtbi.1995.0093 |bibcode=1995JThBi.174..217H |issn=0022-5193|url-access=subscription }}</ref><ref>{{Cite journal |last=Számadó |first=Szabolcs |date=June 1999 |title=The Validity of the Handicap Principle in Discrete Action–Response Games |url=http://dx.doi.org/10.1006/jtbi.1999.0935 |journal=Journal of Theoretical Biology |volume=198 |issue=4 |pages=593–602 |doi=10.1006/jtbi.1999.0935 |pmid=10373357 |bibcode=1999JThBi.198..593S |issn=0022-5193|url-access=subscription }}</ref> and then in [[Continuous modelling|continuous models]].<ref>{{Cite journal |last1=Lachmann |first1=Michael |last2=Számadó |first2=Szabolcs |last3=Bergstrom |first3=Carl T. |date=2001-10-30 |title=Cost and conflict in animal signals and human language |journal=Proceedings of the National Academy of Sciences |volume=98 |issue=23 |pages=13189–13194 |doi=10.1073/pnas.231216498 |pmid=11687618 |issn=0027-8424|pmc=60846 |doi-access=free |bibcode=2001PNAS...9813189L }}</ref><ref>{{Cite journal |last1=Számadó |first1=Szabolcs |last2=Czégel |first2=Dániel |last3=Zachar |first3=István |date=2017-12-28 |title=One problem, too many solutions: How costly is honest signalling of need? |journal=PLOS ONE |volume=14 |issue=1 |pages=e0208443 |doi=10.1371/journal.pone.0208443|doi-access=free |biorxiv=10.1101/240440 |pmid=30633748 |pmc=6329501 }}</ref><ref>{{Cite journal |last1=Számadó |first1=Szabolcs |last2=Zachar |first2=István |last3=Czégel |first3=Dániel |last4=Penn |first4=Dustin J. |date=2023-01-08 |title=Honesty in signalling games is maintained by trade-offs rather than costs |journal=BMC Biology |volume=21 |issue=1 |page=4 |doi=10.1186/s12915-022-01496-9 |pmid=36617556 |issn=1741-7007|pmc=9827650 |doi-access=free }}</ref> Similar results were obtained in [[Conflict theories|conflict models]]: threat displays need not be handicaps to be honest and evolutionarily stable.<ref name="Számadó 2003 pp. 327–348">{{cite journal |last=Számadó |first=Szabolcs |title=Threat Displays are not Handicaps |journal=Journal of Theoretical Biology |publisher=Elsevier |volume=221 |issue=3 |year=2003 |issn=0022-5193 |doi=10.1006/jtbi.2003.3176 |pages=327–348|pmid=12642112 |bibcode=2003JThBi.221..327S }}</ref>

=== 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.<ref name="Huttegger Bruner Zollman 2015">{{cite journal |last1=Huttegger |first1=Simon M. |last2=Bruner |first2=Justin P. |last3=Zollman |first3=Kevin J. S. |title=The Handicap Principle Is an Artifact |journal=Philosophy of Science |volume=82 |issue=5 |date=2015 |issn=0031-8248 |doi=10.1086/683435 |pages=997–1009 |jstor=10.1086/683435 |url=https://figshare.com/articles/journal_contribution/6492797 }}</ref>

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.<ref name="Penn Számadó 2019 pp. 267–290">{{cite journal |last1=Penn |first1=Dustin J. |last2=Számadó |first2=Szabolcs |title=The Handicap Principle: how an erroneous hypothesis became a scientific principle |journal=Biological Reviews |publisher=Wiley |volume=95 |issue=1 |date=23 October 2019 |issn=1464-7931 |doi=10.1111/brv.12563 |pages=267–290|doi-access=free |pmid=31642592 |pmc=7004190 }}</ref>

== Predictions and interpretations ==

[[File:SC06 2006 Rolls-Royce Phantom.jpg|thumb|Luxury cars and other "[[Veblen goods]]" may be an example of the handicap principle in humans.<ref name="White 2016">{{cite book |last1=White |first1=Richard C. |title=Relational Red Flags: Detecting Undesirable Qualities in Initial Romantic EncountersRomantic Encounters |date=2016 |publisher=Louisiana State University (PhD thesis) |doi=10.31390/gradschool_dissertations.1171 |id=etd-04052016-153947 |url=https://repository.lsu.edu/gradschool_dissertations/1171}}</ref>|alt=Photo of a Rolls-Royce car]]

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]]s, the peacock's tail, [[courtship dance]]s, and [[bowerbird]] bowers. American scientist [[Jared Diamond]] has proposed that certain risky human behaviours, such as [[bungee jumping]], may be expressions of instincts that have evolved through the operation of the handicap principle. Zahavi has invoked the gift-giving [[potlatch]] 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]]'s use of the ceremony in his book ''[[Theory of the Leisure Class]]'' as an example of "[[conspicuous consumption]]".<ref>{{cite journal |last1=Bliege Bird |first1=R. |last2=Smith |first2=E. A. |year=2005 |title=Signalling theory, strategic interaction, and symbolic capital |journal=[[Current Anthropology]] |volume=46 |issue=2 |pages=221–248 |jstor=427115 |doi=10.1086/427115 |s2cid=13946731 }}</ref>

The handicap principle gains further support by providing interpretations for behaviours that fit into a single unifying [[gene-centered view of evolution]] and making earlier explanations based on [[group selection]] obsolete. A classic example is that of ''[[stotting]]'' in [[gazelle]]s. This behaviour consists in the gazelle initially running slowly and jumping high when threatened by a [[predator]] such as a [[lion]] or [[cheetah]]. 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.<ref name="Zahavi Zahavi 1997"/>

=== Signals to members of the same species ===

<!--[[File:Babblers, Ardon Creek, Ramon Makhtesh, Negev, Israel (cropped).jpg|thumb|[[Arabian babbler]] are highly social, helping to care for nestlings of unrelated individuals.<ref name=Zahavi1990/>]]
-->
Zahavi studied in particular the [[Arabian babbler]], a highly social bird, with a life-length of 30 years, which appears to behave [[altruism|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]], [[natural selection]] 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]].<ref name=Zahavi1974>{{cite journal |last=Zahavi |first=Amotz |author-link=Amotz Zahavi |year=1974 |title=Communal nesting by the Arabian Babbler: A case of individual selection |journal=Ibis |volume=116 |pages=84–87 |doi=10.1111/j.1474-919X.1974.tb00225.x}}</ref><ref>{{cite journal |last1=Anava |first1=A. |last2=Kam |first2=M. |last3=Shkolnik |first3=A. |last4=Degen |first4=A.A. |year=2001 |jstor=4089815 |title=Does group size affect field metabolic rate of Arabian Babbler (''Turdoides squamiceps'') nestlings? |journal=[[The Auk]] |volume=118 |issue=2 |pages=525–528 |url=http://sora.unm.edu/node/131937 |doi=10.1642/0004-8038(2001)118[0525:DGSAFM]2.0.CO;2 |s2cid=38680548 |doi-access=free }}</ref><ref name=Zahavi1990>{{cite book |last=Zahavi |first=Amotz |author-link=Amotz Zahavi |year=1990 |chapter=Arabian Babblers: The quest for social status in a cooperative Breeder |pages=105–130 |title=Cooperative Breeding in Birds |editor1-first=P. B. |editor1-last=Stacey |editor2-first=W. D. |editor2-last=Koenig |publisher=[[Cambridge University Press]]}}</ref>

French biologist Patrice David showed that in the [[stalk-eyed fly]] 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 [[Genotype|genotypes]] 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.<ref name="david">{{cite journal |first1=P. |last1=David |author2=T. Bjorksten |author3=K. Fowler |author4=A. Pomiankowski |year=2000 |title=Condition-dependent signalling of genetic variation in stalk-eyed flies |journal=[[Nature (journal)|Nature]] |volume=406 |pages=186–188 |doi=10.1038/35018079 |pmid=10910358 |issue=6792|bibcode=2000Natur.406..186D |s2cid=4425172 }}</ref>

=== Signals to other species ===

{{further|Anti-predator adaptation}}

[[File:Stotting gazelle.jpg|thumb|Impala [[stotting]], a behavior that may serve as a [[pursuit deterrence]] signal to predators.<ref name="Caro"/>|alt=Photo of an impala jumping high in the African bush]]

Signals may be directed at [[Predation|predators]], with the function of showing that pursuit will probably be unprofitable. [[Stotting]], for instance, is a form of energetic jumping that certain [[Gazelle|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).<ref name="Caro">{{cite journal |last=Caro |first=Tim M. |author-link=Tim Caro |title=The functions of stotting in Thomson's gazelles: Some tests of the predictions |journal=Animal Behaviour |year=1986 |volume=34 |issue=3 |pages=663–684 |doi=10.1016/S0003-3472(86)80052-5 |s2cid=53155678 }}</ref> However, the mathematical biologist [[John Maynard Smith]] commented that [[Stotting#Possible explanations|other explanations were possible]], such as that it was an honest signal of fitness,<ref name="Maynard Smith 2003 p61"/> or an honest signal that the predator had been detected,<ref>{{cite journal |last1=FitzGibbon |first1=C. D. |last2=Fanshawe |first2=J. H. |title=Stotting in Thomson's gazelles: an honest signal of condition |journal=Behavioral Ecology and Sociobiology |date=August 1988 |volume=23 |issue=2 |pages=69–74 |doi=10.1007/bf00299889 |bibcode=1988BEcoS..23...69F |s2cid=2809268 }}</ref> and it was hard to see how stotting could be a handicap.<ref name="Maynard Smith 2003 p61">{{cite book |last1=Maynard Smith |first1=John |author1-link=John Maynard Smith |last2=Harper |first2=David |title=Animal Signals |publisher=Oxford University Press |year=2003 |pages=61–63 |isbn=978-0-19-852685-8 |url=https://books.google.com/books?id=SUA51MeG1lcC&pg=PA61}}</ref>

Another example is provided by [[lark]]s, some of which discourage [[merlin (bird)|merlins]] by sending a similar message: they [[Bird vocalization|sing]] while being chased, telling their predator that they will be difficult to capture.<ref>{{cite journal |last=Cresswell |first=Will |title=Song as a pursuit-deterrent signal, and its occurrence relative to other anti-predation behaviours of skylark (Alauda arvensis) on attack by merlins (Falco columbarius) |journal=Behavioral Ecology and Sociobiology |date=March 1994 |volume=34 |issue=3 |pages=217–223 |doi=10.1007/BF00167747 |bibcode=1994BEcoS..34..217C |s2cid=25608814}}</ref>

=== Immunocompetence handicaps ===

The theory of [[immunocompetence]] handicaps suggests that [[androgen]]-mediated traits accurately signal condition due to the [[Immunosuppression|immunosuppressive]] effects of androgens.<ref>{{cite journal |last1=Folstad |first1=I. |last2=Karter |first2=A. K. |year=1992 |title=Parasites, bright males, and the immunocompetence handicap |journal=American Naturalist |volume=139 |issue=3 |pages=603–622 |jstor=2462500 |doi=10.1086/285346|s2cid=85266542 }}</ref>  This immunosuppression may be either because [[testosterone]] alters the allocation of limited resources between the development of [[Secondary sex characteristic|ornamental traits]] and other tissues, including the [[immune system]],<ref>{{cite journal |last1=Wedekind |first1=C. |last2=Folstad |first2=I. |year=1994 |title=Adaptive or non-adaptive immunosuppression by sex hormones? |journal=American Naturalist |volume=143 |issue=5 |pages=936–938 |jstor=2462885 |doi=10.1086/285641|s2cid=84327543 }}</ref> or because heightened immune system activity has a propensity to launch autoimmune attacks against [[gametes]], such that suppression of the immune system enhances [[fertility]].<ref>{{cite journal |last1=Folstad |first1=I. |last2=Skarstein |first2=F. |year=1996 |title=Is male germ line control creating avenues for female choice? |journal=[[Behavioral Ecology (journal)|Behavioral Ecology]] |volume=8 |issue=1 |pages=109–112 |doi=10.1093/beheco/8.1.109 |doi-access=free }}</ref> 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.<ref>{{cite journal |last1=Roberts |first1=M. L. |last2=Buchanan |first2=K. L. |last3=Evans |first3=M. R. |year=2004 |title=Testing the immunocompetence handicap hypothesis: a review of the evidence |journal=Animal Behaviour |volume=68 |issue=2 |pages=227–239 |doi=10.1016/j.anbehav.2004.05.001 |s2cid=9549459 }}</ref>

== See also ==

* [[Aposematism]]
* [[Costly signaling theory in evolutionary psychology]]
* [[Fisherian runaway]]
* [[Multiple sexual ornaments]]
* [[Parasite-stress theory]]
* [[Sacrifice]]

== References ==

{{reflist|30em}}

== External links ==

* [https://web.archive.org/web/20150224083708/http://octavia.zoology.washington.edu/handicap/ ''Honest Signalling Theory: A Basic Introduction'']. By Carl T. Bergstrom, University of Washington, 2006.

{{Evolution}}
{{Signalling theory}}


{{DEFAULTSORT:Handicap Principle}}
[[Category:Signalling theory]]
[[Category:Animal communication]]
[[Category:Ethology]]
[[Category:Selection]]
[[Category:Sexual selection]]