Individual quality via sensitivity to cysteine availability in a melanin-based honest signaling system

The evolution of honest animal communication is mostly understood through the handicap principle, which is intrinsically dependent on the concept of individual quality: low-quality individuals are prevented from producing high-quality signals because, if they did so, they would pay greater production costs than high-quality individuals. We tested an alternative explanation for the black bib size of male house sparrows, Passer domesticus, an honest signal of quality the expression of which is negatively related to levels of the pigment pheomelanin in the constituent feathers. We previously showed that experimental depletion of cysteine, which participates in pheomelanogenesis, improves the phenotype (bibs larger than in controls) of high-quality males (birds with largest bibs initially) only. Here, we conducted an experiment under opposite conditions, increasing the availability of dietary cysteine, and obtained opposite results: deteriorated phenotypes (bibs smaller than in controls) were only expressed by high-quality birds. Some birds were also treated with the pro-oxidant diquat dibromide, and we found that the cellular resistance to free radicals of high-quality birds benefited more from the antioxidant activity of cysteine against diquat than that of low-quality birds. These findings support the existence of a mechanism uncoupling cysteine and pheomelanin in low-quality birds that confers on them a low sensitivity to variations in cysteine availability. This constitutes an explanation for the evolution of signal honesty that overcomes the limitations of the handicap principle, because it provides a specific definition of individual quality and because costs are no longer required to prevent low-quality individuals from producing large signals.