Evolution of bird communication signals: transference between signals mediated by sensory drive

Abstract

Animals communicate using signals perceived via multiple sensory modalities but usually invest more heavily in one of type of signal. This pattern, observed by Darwin1 and many researchers since, led to development of the transfer hypothesis (see also transferal effect2 and tradeoff hypothesis3,4), which predicts a negative relationship between investment in different signaling modalities dictated by the relative costs and benefits of each. One factor that influences costs and benefits, and is central to the sensory drive hypothesis5 posed to account for signal evolution, is the suitability of the environment for different types of signals. Movement into a dark habitat, for example, should favor investment in acoustic over visual signals. We use phylogenetic comparative methods to analyze the joint effect of transfer and sensory drive on plumage and song variation in 52 species of a large radiation of passerine birds, the New World warblers (Parulidae), and to estimate temporal patterns in the accumulation of differences in visual and vocal signals and habitat along the evolutionary history of this lineage. We found evidence for the predicted negative correlations between a variety of song and plumage traits that vary with habitat type. Plumage contrast to background and chromatic diversity were both negatively related to syllable variety when vegetation structure was a covariate: birds with a greater variety of song syllables and less colorful plumages live in closed or darker habitats. Also as predicted, achromatic or brightness diversity was related to vegetation structure. In addition, disparity-through-time analyses showed that when one set of traits (i.e. songs or colors) diversified at a relatively high rate the other did not, as predicted by the transfer hypothesis. Our results show that sensory drive influences the transfer of investment between traits in different sensory modalities. This interaction between mechanisms shaping signals may be a major determinant in the evolution of animal communication.