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The handicap principle: from erroneous hypothesis to scientific standard

25.11.2019: In a recently published review, Dustin Penn of the Konrad Lorenz Institute of Ethology at Vetmeduni Vienna reveals a widely accepted hypothesis to be a scientific fallacy. The handicap principle is the most widely cited explanation for the evolution of costly and conspicuous signalling systems in the animal world, such as the colourful plumage of peacocks. According to Penn, however, this idea is completely erroneous and can be rejected.

Animals sometimes produce dishonest signals, especially when deception is potentially beneficial, but they can also send out honest and reliable signals – even if deception would appear to be an advantage. One of the central theoretical questions in the evolution of animal communication is: Why is signalling often honest? The most commonly cited explanation has been the handicap principle by Amotz Zahavi, in which he proposed that signals are honest because they are costly to produce. According to this hypothesis, signalling is energetically costly and actually increases the risk of falling prey to a predator.

A critical review of the handicap principle by Dustin Penn of the Konrad Lorenz Institute of Ethology at Vetmeduni Vienna and Szabolcs Számadó (CSS-RECENS, MTA Centre for Social Sciences & Evolutionary Systems Research, Budapest), recently published in the scientific journal Biological Reviews, provides a completely new perspective. This is the first comprehensive review of the handicap hypothesis to examine the various models underlying the principle. The two scientists show that the handicap principle is illogical, non-Darwinian and erroneous, and explain how it has nonetheless gained widespread acceptance within the scientific community.

Peacocks and their costly and conspicuous signals

The large and colourful sexual plumage of peacocks and other birds, with which the male animals attempt to attract females, is often cited as an example for the handicap principle. In 1975 Amotz Zahavi argued that such conspicuous displays were honest indicators of the genetic quality of males because they are costly to produce, and low-quality males would not be able to afford the associated cost. According to the handicap principle, conspicuous signals evolve because they are costly and not despite their cost, as is the case with other traits. This idea was initially very controversial, but it later gained widespread acceptance.

Acceptance of the handicap principle based on mathematical models

In 1990 Alan Grafen published two papers using different mathematical models that he interpreted as confirmation of the handicap principle. His strategic choice signalling model managed to persuade even earlier critics of Zahavi. Ever since, the handicap hypothesis has been widely accepted as a general principle to explain the evolution of reliable signalling systems and is promoted as such in textbooks on animal behaviour and animal communication. In their review, Penn and Számadó state that the acceptance of the handicap principle was based on several misinterpretations of Grafen’s models. Penn and Számadó conclude: “Grafen’s models are consistent with evolutionary life-history theory, but it is time to usher the handicap principle off to an honourable retirement.”

The article “The Handicap Principle: how an erroneous hypothesis became a scientific principle” by Dustin J. Penn and Szabolcs Számadó was published in Biological Reviews.