The overlooked signaling component of nonsignaling behavior

The handicap principle (Zahavi, 1975, 1987; Zahavi and Zahavi, 1997) is now widely used to explain the evolution of conspicuous signals such as tail ornaments, courtship displays, and nestling begging (Godfray, 1991; Grafen, 1990a,b; Johnston, 1997; Maynard Smith and Harper, 1995). The essence of the model is that signals must be costly to be honest. Females have evolved preferences for males with longer tails or brighter plumage, for example, because only males of high quality can survive and perform with handicapping ornaments. Despite the general acceptance that the handicap principle explains extravagant morphological and behavioral signals, the model’s mechanism has not been broadly applied to explain a host of other behaviors. Here we suggest that the selection on animal behavior to be performed differently when observed by other animals can lead to significant quantitative changes in behavior. Although such changes in the level or intensity of a behavior may not justify calling the behavior a signal, they can evolve as signaling components to behaviors whose primary function is not signaling (i.e., they can shift the level of the behavior from its nonsignaling optimum). We call this idea the overlooked signaling component of behavior. We explore this issue using three examples: (1) prey fleeing a predator; (2) human behavior in the presence of others; and (3) parental care behavior. We then apply the overlooked signaling component to reexamine Zahavi’s (1977, 1995) suggestion that altruism is a signal of social prestige. Whereas Zahavi presents his ‘‘prestige hypothesis’’ as an alternative to kin selection, we show how both theories can work together. We suggest that helping behavior among kin, which increases inclusive fitness, may also eventually evolve into signals of individual quality, condition or need. We conclude by suggesting ways to test for signaling components of animal behaviors.