The cost of honesty and the fallacy of the handicap principle

Honest signalling assumes a correlation between an observable signal and a nonobservable quality. There are many mutually nonexclusive mechanisms that can achieve such a correlation; however, for a long time the handicap principle has been identified as the main solution to this problem. In short, it claims that signals need to be costly to be honest and that honest signallers have to pay this extra cost at the equilibrium (i.e. signals have to be handicaps). Honesty, however, is not maintained by the realized cost paid by honest signallers at the equilibrium but by the potential cost of cheating. Whether this potential cost implies a realized cost for honest signallers depends on the biological details of the system and thus this cost cannot be predicted a priori without knowledge of these details. Accordingly, depending on these details, signals need not be costly to be honest, even under conflict of interest. In other words, handicapping equilibrium signals are not the only way to create a high potential cost of cheating. Here I first review the theoretical models supporting the above conclusion, and then I list mechanisms that can maintain a high potential cost of cheating without imposing extra realized cost (i.e. a handicap) on honest signallers at the equilibrium. Identifying and describing those constraints or the lack of them that might create a connection between these two types of cost should be a major research agenda.

[1]  Joseph B. Williams,et al.  Effects of food supplementation on behavioural decisions of hoopoe-larks in the Arabian Desert: balancing water, energy and thermoregulation , 2002, Animal Behaviour.

[2]  L. Keller,et al.  Pleiotropy in the melanocortin system, coloration and behavioural syndromes. , 2008, Trends in ecology & evolution.

[3]  J. Kotiaho Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence , 2001, Biological reviews of the Cambridge Philosophical Society.

[4]  R. Johnstone Signaling of need, sibling competition, and the cost of honesty. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Peter L. Hurd Communication in discrete action-response games , 1995 .

[6]  D. Kemp,et al.  Gaping Displays Reveal and Amplify a Mechanically Based Index of Weapon Performance , 2006, The American Naturalist.

[7]  P W Taylor,et al.  Body postures and patterns as amplifiers of physical condition , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  R. Freckleton,et al.  Honesty and cheating in cleaning symbioses: evolutionarily stable strategies defined by variable pay-offs , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[9]  R. Johnstone,et al.  Animal signals , 2013, Current Biology.

[10]  A. Zahavi The handicap principle and signalling in collaborative systems , 2008 .

[11]  J. Dale,et al.  Individual recognition: it is good to be different. , 2007, Trends in ecology & evolution.

[12]  H PL. Is Signalling of Fighting Ability Costlier for Weaker Individuals ? , 1996 .

[13]  G. Parker,et al.  Assessment strategy and the evolution of fighting behaviour. , 1974, Journal of theoretical biology.

[14]  Thomas Getty,et al.  Sexually selected signals are not similar to sports handicaps. , 2006, Trends in ecology & evolution.

[15]  M. Roberts,et al.  Testing the immunocompetence handicap hypothesis: a review of the evidence , 2004, Animal Behaviour.

[16]  J. Hurst,et al.  The competing countermarks hypothesis: reliable assessment of competitive ability by potential mates , 1999, Animal Behaviour.

[17]  J. Krebs,et al.  Sexual selection and the handicap principle , 1976, Nature.

[18]  Joan B. Silk,et al.  Cheap talk when interests conflict , 2000, Animal Behaviour.

[19]  M. Hauser Costs of deception: cheaters are punished in rhesus monkeys (Macaca mulatta). , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[20]  A. Grafen Biological signals as handicaps. , 1990, Journal of theoretical biology.

[21]  E. Charnov,et al.  Alternative male life histories in bluegill sunfish. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[22]  F Goller,et al.  The metabolic cost of birdsong production. , 2001, The Journal of experimental biology.

[23]  F. Lutz Mimicry , 1911, The American Naturalist.

[24]  R. Cardé,et al.  Encyclopedia of Insects , 2009 .

[25]  A. Zahavi Mate selection-a selection for a handicap. , 1975, Journal of theoretical biology.

[26]  T. Guilford,et al.  Automimicry destabilizes aposematism: predator sample-and-reject behaviour may provide a solution , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  S. Számadó The validity of the handicap principle in discrete action-response games , 1999 .

[28]  W. Dominey Female mimicry in male bluegill sunfish—a genetic polymorphism? , 1980, Nature.

[29]  M. Enquist Communication during aggressive interactions with particular reference to variation in choice of behaviour , 1985, Animal Behaviour.

[30]  S. Nowicki,et al.  The Evolution of Animal Communication: Reliability and Deception in Signaling Systems: Reliability and Deception in Signaling Systems , 2005 .

[31]  Szabolcs Számadó,et al.  Separating equilibria in continuous signalling games. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[32]  Laasya Samhita The Handicap Principle , 2010 .

[33]  Eric Bonabeau The handicap principle , 1998, Complex..

[34]  J. Dale,et al.  A socially enforced signal of quality in a paper wasp , 2004, Nature.

[35]  T. Amundsen,et al.  Animal signals : signalling and signal design in animal communication , 2000 .

[36]  John Maynard Smith Honest signalling: the Philip Sidney game , 1991, Animal Behaviour.

[37]  T. Guilford,et al.  The corruption of honest signalling , 1991, Animal Behaviour.

[38]  The limits to cost-free signalling of need between relatives , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[39]  D. E. Matthews Evolution and the Theory of Games , 1977 .

[40]  J. P. Mccarty,et al.  The Energetic Cost of Begging in Nestling Passerines , 1996 .

[41]  H. Godfray,et al.  Signalling of need by offspring to their parents , 1991, Nature.

[42]  D. Hughes,et al.  Sociobiology of Communication , 2008 .

[43]  J. Hare,et al.  Effect of hypoxia on opercular displays: evidence for an honest signal? , 2005, Animal Behaviour.

[44]  T. Getty,et al.  Handicap signalling: when fecundity and viability do not add up , 1998, Animal Behaviour.

[45]  J. Dale,et al.  Signaling Individual Identity versus Quality: A Model and Case Studies with Ruffs, Queleas, and House Finches , 2001, The American Naturalist.

[46]  O. Hasson,et al.  Towards a General Theory of Biological Signaling , 1997, Journal of theoretical biology.

[47]  Carl T. Bergstrom,et al.  Signaling among relatives. III. Talk is cheap. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Janice C. Daniel,et al.  Reliability and the adaptive utility of discrimination among alarm callers , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[49]  Edward H. Miller,et al.  Vocal signalling of male southern elephant seals is honest but imprecise , 2007, Animal Behaviour.

[50]  Szabolcs Számadó,et al.  Threat displays are not handicaps. , 2003, Journal of theoretical biology.

[51]  B. Jamieson,et al.  Reproductive biology and phylogeny of birds , 2007 .

[52]  Maynard J. Smith,et al.  Animal Signals: Models and Terminology , 1995 .

[53]  T. Ljungberg,et al.  A test of the sequential assessment game: fighting in the cichlid fish Nannacara anomala , 1990, Animal Behaviour.

[54]  S. Számadó How threat displays work: species-specific fighting techniques, weaponry and proximity risk , 2008, Animal Behaviour.

[55]  A. Zahavi The cost of honesty (further remarks on the handicap principle). , 1977, Journal of theoretical biology.

[56]  M. Enquist,et al.  A strategic taxonomy of biological communication , 2005, Animal Behaviour.

[57]  Carl T. Bergstrom,et al.  Cost and conflict in animal signals and human language , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[58]  G. Moreno-Rueda Is there empirical evidence for the cost of begging? , 2007, Journal of Ethology.

[59]  Carl T. Bergstrom,et al.  Signalling among relatives. II. Beyond the tower of Babel. , 1998, Theoretical population biology.

[60]  F. Walther Communication and Expression in Hoofed Mammals , 1984 .

[61]  J. M. Smith The theory of games and the evolution of animal conflicts. , 1974, Journal of theoretical biology.

[62]  Szamad The validity of the handicap principle in discrete action-response games , 1999, Journal of theoretical biology.

[63]  D. Reby,et al.  Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags , 2003, Animal Behaviour.

[64]  S. Számadó Cheating as a mixed strategy in a simple model of aggressive communication , 2000, Animal Behaviour.