It is a familiar idea in evolutionary biology that sexual selection may produce some trait despite its being disadvantageous to general fitness. The peacock’s tail is a classic example.
The Handicap Principle goes a step further by claiming that some traits are selected precisely because they are disadvantageous. The HP was first put forward by the Israeli zoologist Amotz Zahavi in the 1970s. For a long time it was resisted by other biologists, but since about 1990 it has been more widely accepted.
I recently read Amotz and Avishag Zahavi’s book The Handicap Principle: a Missing Piece of Darwin’s Puzzle (1997). This is the most interesting book on evolutionary biology I have read for a long time. The Zahavis apply the HP not only to sexual selection but to a wide range of other animal and human traits. Some of their ideas are far-fetched, but always stimulating.
The Zahavis argue that the HP comes into play whenever an animal trait conveys information to other animals (of the same or different species), where it is in the interests of both sender and receiver that the information should be honest, but where it would be advantageous to other animals to ‘cheat’ by sending false information. The only way to deter cheating is for the ‘signal’ to be so expensive to produce that it is not worth while to cheat. Since animal signals do exist, and in many cases it would be advantageous to cheat if this could be done without cost, it seems to follow that signals must have evolved to be expensive to produce, and this is just another way of stating the Handicap Principle.
It is one thing to show that the HP must apply, but another to show how ‘handicaps’ evolve. The reason why biologists resisted the idea was that the Zahavis offered no mathematical models to show how a gene promoting a handicap could be selected, and other biologists who tried to devise such models found that they did not work. The problem is that such a gene starts by reducing fitness, and it is difficult to see how it can get a sufficient advantage from ‘honesty’ to offset this until it has already become common in the population. At this point it becomes advantageous for the ‘receivers’ (e.g. females, in the case of mating behaviour) to evolve a strong preference for it. This would explain how a handicap can be maintained by selection, but not how it evolves in the first place.
This seems to be still a weak point in the Zahavis’ arguments, and they are very vague about the process by which handicaps evolve, and the conditions under which this can occur. Mathematical biologists have however done a lot to clarify this, notably Alan Grafen in two papers in 1990. As Grafen explains it, the key condition for a handicap to evolve is that the marginal cost of producing a signal (e.g. the peacock growing a longer tail) must be greater for a low-quality animal than for a high-quality one, so that the low-quality animal stands to lose more by trying to ‘cheat’ than it gains. It is plausible that this condition often applies. For analogy, suppose that men can obtain sexual partners by lifting heavier weights than their rivals. It may be that with sufficient training and practice any man can lift the heaviest weight available, but it will still be easier for the biggest and strongest men to reach the position of being able to lift any given weight. The contest will therefore be a reliable test of strength.
The Handicap Principle can also be applied to cultural and economic phenomena such as conspicuous expenditure, initiation rites and tests, extreme sports and contests, artistic skill, and fashions in dress. Here we do not suppose that each cultural trait has been produced by biological selection. It sufficient that humans should have a general-purpose ability to detect cheating. If the only honest signal is a costly signal, then culture will spontaneously select signals which impose costs on the signallers. This principle seems capable of explaining a great deal in human behaviour that otherwise seems perverse and wasteful. Of course, in one way this is a rather pessimistic conclusion. But it does also offer the hope that by understanding the roots of behaviour we may consciously change it.
DAVID BURBRIDGE
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