For the most part, it seems that animals communicate honestly with one another. Individuals use various signals such as elaborate colours or ornaments to convey information to others about their fighting ability or potential value as a mate. Signals are useful, and communication can save time and energy. For example, mismatched rivals can avoid a risky dual if they can communicate their fighting ability, and the weaker opponent cede to the stronger.

The lingering puzzle of animal communication is why animals are honest with one another. On the surface, it would seem beneficial to embellish communication signals. What animal would not want to appear stronger and more attractive? The classic explanation is the ‘handicap hypothesis’, or the hypothesis that the cost of communication signals maintains the honesty of these signals. One common example is the tail of the peacock. This lavish adornment is so cumbersome that only strong males can haul around an impressive tail and still escape from predators.

Simon Lailvaux, Rebecca Gilbert and Jessica Edwards from the University of New Orleans put the handicap hypothesis to the test in a unique way using green anole lizards (Anolis carolinensis). The green anole is an excellent subject for such a study, as male green anoles signal to one another with a brightly coloured dewlap – a flap of skin beneath the jaw that they can extend and retract – and the size of this dewlap is an honest signal of their bite force, an essential trait for fighting. Importantly for the study, the dewlap is developmentally unrelated to the muscles surrounding the jaw that generate bite force, so it is possible for the two traits to vary independently of one another. Lailvaux and his colleagues investigated whether resource limitation would change the honest relationship between dewlap size and bite force. They predicted that if the handicap hypothesis is correct, and the cost of maintaining the bright dewlap maintains the honesty of the signal, then food restriction should limit both dewlap size and bite force. The question is, when the times are tough, do the lizards stay honest?

To answer this question, the authors captured juvenile male green anoles and raised them to sexual maturity in the laboratory, under either food-restricted or plentiful diets. At the end of the study, both dewlap size and bite force were measured. The authors discovered that while lizards with plenty of food developed the typically honest relationship between dewlap size and bite force, the food-restricted males developed the bright dewlaps without developing the corresponding bite force. Therefore, food-deprived lizards were not as honest as their resource-rich counterparts. Moreover, it appears that for green anoles, bite force itself is more costly than the bright dewlap signal.

As the cost of a bright dewlap doesn't keep the lizards honest, what factors maintain dewlap size? The authors suggest several explanations, including the possibility that social feedback might play an important role. In this study, lizards were raised in individual cages, and did not interact with one another. However, in the wild, exaggerating about bite force with a bright dewlap might land a lizard in a fight where he is overmatched and could be injured. While more research is necessary to fully understand the factors that maintain honest communication signals, it seems that, for lizards, honesty is still the best policy.

S. P.
R. L.
J. R.
A performance-based cost to honest signalling in male green anole lizards (Anolis carolinensis)
Proc. R. Soc. B