Sexually selected signals are not similar to sports handicaps.

The handicap principle is a simple but powerful metaphor that has had a major impact on how biologists study and understand sexual selection. Here, I show that its application to signalling in sexual selection is not a valid generalization from its roots in economics. Although some signalling systems, with additive costs and benefits, have solutions that resemble sports handicaps, the signalling in sexual selection has multiplicative costs and benefits, and solutions that do not resemble sports handicaps. The sports analogy is technically incorrect, metaphorically misleading and a poor guide for empirical research on the signalling in sexual selection. The evolution of sexually selected signals is not a missing piece of Darwin's puzzle; it is an integral piece of the process of evolution by natural selection, and it should be approached with the same tools that we bring to bear on the evolution of other correlated traits involved in social interactions.

[1]  H. Kokko,et al.  The evolution of mate choice and mating biases , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  S. Frank Foundations of Social Evolution , 2019 .

[3]  Arnon Lotem,et al.  From reciprocity to unconditional altruism through signalling benefits , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  Thorstein Veblen,et al.  The theory of the leisure class : an economic study of institutions , 1953 .

[5]  Mark A. Hanson,et al.  Evolution, development and timing of puberty , 2006, Trends in Endocrinology & Metabolism.

[6]  A. Houston,et al.  The sexual selection continuum , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  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.

[8]  T. Pitcher,et al.  Genetic quality and sexual selection: an integrated framework for good genes and compatible genes , 2004, Molecular ecology.

[9]  John G. Riley,et al.  Silver Signals: Twenty-Five Years of Screening and Signaling , 2001 .

[10]  M. Milinski Bill Hamilton, sexual selection, and parasites. , 2001 .

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

[12]  Ranjini Chatterjee,et al.  Directed evolution of metabolic pathways. , 2006, Trends in biotechnology.

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

[14]  D. Schluter,et al.  Sexual selection when the female directly benefits , 1993 .

[15]  P. Parker,et al.  CORRELATIONAL SELECTION LEADS TO GENETIC INTEGRATION OF BODY SIZE AND AN ATTRACTIVE PLUMAGE TRAIT IN DARK‐EYED JUNCOS , 2005, Evolution; international journal of organic evolution.

[16]  A long-term genetic model for the evolution of sexual preference: the theories of Fisher and Zahavi re-examined , 2002, Journal of mathematical biology.

[17]  A. Edlin,et al.  Strict Monotonicity in Comparative Statics , 1998 .

[18]  Troy Day,et al.  Older males signal more reliably , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[19]  Noldeke,et al.  How costly is the honest signaling of need? , 1999, Journal of theoretical biology.

[20]  J. Koella,et al.  Coevolutionary interactions between host and parasite genotypes. , 2006, Trends in parasitology.

[21]  G. Hill,et al.  Choosing mates: good genes versus genes that are a good fit. , 2004, Trends in ecology & evolution.

[22]  THOMAS GETTY Reliable signalling need not be a handicap , 1998, Animal Behaviour.

[23]  A. J. Noordwijk,et al.  Acquisition and Allocation of Resources: Their Influence on Variation in Life History Tactics , 1986, The American Naturalist.

[24]  Oren Hasson,et al.  Phenotypic plasticity and the handicap principle , 1984 .

[25]  A. Houston,et al.  How does an individual's optimal behaviour depend on its quality? An analysis based on relative ability , 2003 .

[26]  Signaling Health versus Parasites , 2002, The American Naturalist.

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

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

[29]  T. W. Fawcett,et al.  Mate choice in the face of costly competition , 2003 .

[30]  T. Day,et al.  THE EVOLUTION OF STATIC ALLOMETRY IN SEXUALLY SELECTED TRAITS , 2003, Evolution; international journal of organic evolution.

[31]  Victor S. Johnston,et al.  Mate choice decisions: the role of facial beauty , 2006, Trends in Cognitive Sciences.

[32]  Tarmo Ketola,et al.  Genetic compatibility and sexual selection. , 2005, Trends in ecology & evolution.

[33]  J. Mattick,et al.  Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. , 2006, Trends in genetics : TIG.

[34]  J. Hirshleifer,et al.  The truthful signalling hypothesis: an explicit general equilibrium model. , 2004, Journal of theoretical biology.

[35]  W. Hamilton,et al.  Heritable true fitness and bright birds: a role for parasites? , 1982, Science.

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

[37]  Jeffrey K. Conner,et al.  A Primer of Ecological Genetics , 2004 .

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