The Handicap Principle Is an Artifact

The handicap principle is one of the most influential ideas in evolutionary biology. It asserts that when there is conflict of interest in a signaling interaction signals must be costly in order to be reliable. While in evolutionary biology it is a common practice to distinguish between indexes and fakable signals, we argue this dichotomy is an artifact of existing popular signaling models. Once this distinction is abandoned, we show one cannot adequately understand signaling behavior by focusing solely on cost. Under our reframing, cost becomes one—and probably not the most important—of a collection of factors preventing deception.

[1]  D. Harper,et al.  The evolution of aggression: can selection generate variability? , 1988, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[2]  Elliott O. Wagner,et al.  The Dynamics of Costly Signaling , 2013, Games.

[3]  Sandra L. L. Gaunt,et al.  Is singing costly ?. Author's reply , 1996 .

[4]  A. Grafen,et al.  The evolution of index signals to avoid the cost of dishonesty , 2014, Proceedings of the Royal Society B: Biological Sciences.

[5]  D. Weary,et al.  Oxygen consumption during crowing by roosters: talk is cheap , 1995, Animal Behaviour.

[6]  Y. Iwasa,et al.  Handicap signalling: loud and true? , 1998 .

[7]  M. Zuk,et al.  Energy cost of an avian vocal display: crowing in red junglefowl , 1995, Animal Behaviour.

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

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

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

[11]  R. Kirk.  CONVENTION: A PHILOSOPHICAL STUDY , 1970 .

[12]  J M Smith,et al.  Evolution and the theory of games , 1976 .

[13]  David Lewis.  Convention: A Philosophical Study , 1986 .

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

[15]  Carl T. Bergstrom,et al.  Signalling among relatives. I. Is costly signalling too costly , 1997 .

[16]  M. Naguib,et al.  The evolution of animal communication , 2013 .

[17]  D. Emlen,et al.  A Mechanism of Extreme Growth and Reliable Signaling in Sexually Selected Ornaments and Weapons , 2012, Science.

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

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

[20]  Kevin J. S. Zollman,et al.  Between cheap and costly signals: the evolution of partially honest communication , 2013, Proceedings of the Royal Society B: Biological Sciences.

[21]  Kenneth Webb,et al.  Evolution of Communication Simulation of Adaptive Behavior – Project Report , 2004 .

[22]  David G. Haskell.  Experimental evidence that nestling begging behaviour incurs a cost due to nest predation , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  Josef Hofbauer,et al.  Evolutionary Games and Population Dynamics , 1998 .

[24]  R. Persaud.  Philosophy of science , 1992, The Lancet.

[25]  Kevin J. S. Zollman,et al.  Dynamic stability and basins of attraction in the Sir Philip Sidney game , 2010, Proceedings of the Royal Society B: Biological Sciences.

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

[27]  L. Holman.  COSTS AND CONSTRAINTS CONSPIRE TO PRODUCE HONEST SIGNALING: INSIGHTS FROM AN ANT QUEEN PHEROMONE , 2012, Evolution; international journal of organic evolution.

[28]  Nicholas Allott,et al.  Game Theory and Communication , 2006 .

[29]  A. Kodric‐Brown.  Female preference and sexual selection for male coloration in the guppy (Poecilia reticulata) , 1985, Behavioral Ecology and Sociobiology.

[30]  Amots Zehavi,et al.  The Handicap Principle: A Missing Piece of Darwin's Puzzle , 1997 .

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

[32]  G Borgia.  The Cost of Display in the Non-Resource-Based Mating System of the Satin Bowerbird , 1993, The American Naturalist.

[33]  W. A. Frankino,et al.  New perspectives on the evolution of exaggerated traits , 2013, BioEssays : news and reviews in molecular, cellular and developmental biology.

[34]  Jonathan Grose,et al.  Modelling and the fall and rise of the handicap principle , 2011 .

[35]  Marcella J. Kelly,et al.  Tail-flagging and other antipredator signals in white-tailed deer: new data and synthesis , 1995 .

[36]  J M Smith,et al.  Sexual selection, handicaps and true fitness. , 1985, Journal of theoretical biology.

[37]  Kevin J. S. Zollman,et al.  An Evolutionary Comparison of the Handicap Principle and Hybrid Equilibrium Theories of Signaling , 2015, PloS one.

[38]  A. Kodric‐Brown.  Dietary carotenoids and male mating success in the guppy: an environmental component to female choice , 1989, Behavioral Ecology and Sociobiology.

[39]  M. Hauser.  The Evolution of Communication , 1996 .

[40]  M. Spence.  Job Market Signaling , 1973 .

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

[42]  Szabolcs Számadó,et al.  The cost of honesty and the fallacy of the handicap principle , 2011, Animal Behaviour.

[43]  Kevin J. S. Zollman,et al.  Methodology in Biological Game Theory , 2013, The British Journal for the Philosophy of Science.