How do novel signals originate? The evolution of fairy-wren songs from predator to display contexts

Abstract

Revealing the evolutionary origin of novel traits is a long-standing challenge in evolutionary biology. The dynamics of antipredator signalling and conspecific advertisement provide one framework in which to investigate this phenomenon, because shifts in signal context may lead to new signal functions, novel evolutionary pressures and ultimately novel phenotypes. Several species of fairy-wrens (Maluridae: Malurus) give song-like trills (‘Type II song’) in response to vocalizations of avian predators. Despite this predator context, in some species the trills appear to function as conspecific-directed displays. We investigated two hypotheses for the evolutionary origin of predator-elicited Type II songs: (1) they originated as antipredator signals, then shifted to a display context and subsequently became more elaborate because selection pressures changed; or alternatively (2) they originated as conspecific-directed songs, then shifted to a predator context to exploit an effective communication window. Using predator playbacks and samples of natural dawn chorus recordings, we found that many Malurus species gave trills in response to predators, but only a subset gave unprompted trills during dawn chorus displays, and ancestral state reconstructions suggested that the predator-elicited context evolved first. Additionally, species that used trills more often (in both predator and unsolicited contexts) tended to have longer trills with a faster note rate, suggesting that trills have evolved a higher performance as they became a more important part of the display repertoire. Our results support the hypothesis that trill displays originated through the elaboration of predator context calls and provide an example of a shift in signal context leading to novel signal phenotypes.