Song and genetic divergence within a subspecies of white-crowned sparrow (Zonotrichia leucophrys nuttalli).

Animal culture evolves alongside genomes, and the two modes of inheritance-culture and genes-interact in myriad ways. For example, stable geographic variation in culture can act as a reproductive barrier, thereby facilitating genetic divergence between "cultural populations." White-crowned sparrows (Zonotrichia leucophrys) are a well-established model species for bird song learning and cultural evolution, as they have distinct, geographically discrete, and culturally transmitted song types (i.e., song dialects). In this study, we tested the hypothesis that divergence between culturally transmitted songs drives genetic divergence within Nuttall's white-crowned sparrows (Z. l. nuttalli). In accordance with sexual selection theory, we hypothesized that cultural divergence between mating signals both preceded and generated genetic divergence. We characterized the population structure and song variation in the subspecies and found two genetically differentiated populations whose boundary coincides with a major song boundary at Monterey Bay, California. We then conducted a song playback experiment that demonstrated males discriminate between songs based on their degree of divergence from their local dialect. These results support the idea that discrimination against non-local songs is driving genetic divergence between the northern and southern populations. Altogether, this study provides evidence that culturally transmitted bird songs can act as the foundation for speciation by sexual selection.

Acoustic adaptation to city noise through vocal learning by a songbird.

Anthropogenic noise imposes novel selection pressures, especially on species that communicate acoustically. Many animals-including insects, frogs, whales and birds-produce sounds at higher frequencies in areas with low-frequency noise pollution. Although there is support for animals changing their vocalizations in real time in response to noise (i.e. immediate flexibility), other evolutionary mechanisms for animals that learn their vocalizations remain largely unexplored. We hypothesize that cultural selection for signal structures less masked by noise is a mechanism of acoustic adaptation to anthropogenic noise. We test this hypothesis by presenting nestling white-crowned sparrows (Zonotrichia leucophyrs) with less-masked (higher-frequency) and more-masked (lower-frequency) tutor songs either during playback of anthropogenic noise (noise-tutored treatment) or at a different time from noise playback (control treatment). As predicted, we find that noise-tutored males learn less-masked songs significantly more often, whereas control males show no copying preference, providing strong experimental support for cultural selection in response to anthropogenic noise. Further, noise-tutored males reproduce songs at higher frequencies than their tutor, indicating a distinct mechanism to increase signal transmission in a noisy environment. Notably, noise-tutored males achieve lower performance songs than their tutors, suggesting potential costs in a sexual selection framework.

Ecological drivers of song evolution in birds: Disentangling the effects of habitat and morphology.

Environmental differences influence the evolutionary divergence of mating signals through selection acting either directly on signal transmission ("sensory drive") or because morphological adaptation to different foraging niches causes divergence in "magic traits" associated with signal production, thus indirectly driving signal evolution. Sensory drive and magic traits both contribute to variation in signal structure, yet we have limited understanding of the relative role of these direct and indirect processes during signal evolution. Using phylogenetic analyses across 276 species of ovenbirds (Aves: Furnariidae), we compared the extent to which song evolution was related to the direct influence of habitat characteristics and the indirect effect of body size and beak size, two potential magic traits in birds. We find that indirect ecological selection, via diversification in putative magic traits, explains variation in temporal, spectral, and performance features of song. Body size influences song frequency, whereas beak size limits temporal and performance components of song. In comparison, direct ecological selection has weaker and more limited effects on song structure. Our results illustrate the importance of considering multiple deterministic processes in the evolution of mating signals.

Correlated evolution of beak morphology and song in the neotropical woodcreeper radiation.

Mating signals may diversify as a byproduct of morphological adaptation to different foraging niches, potentially driving speciation. Although many studies have focused on the direct influence of ecological and sexual selection on signal divergence, the role of indirect mechanisms remains poorly understood. Using phenotypic and molecular datasets, we explored the interplay between morphological and vocal evolution in an avian radiation characterized by dramatic beak variation, the Neotropical woodcreepers (Dendrocolaptinae). We found evidence of a trade-off between the rate of repetition of song syllables and frequency bandwidth: slow paced songs had either narrow or wide frequency bandwidths, and bandwidth decreased as song pace increased. This bounded phenotypic space for song structure supports the hypothesis that passerine birds face a motor constraint during song production. Diversification of acoustic characters within this bounded space was correlated with diversification of beak morphology. In particular, species with larger beaks produced slower songs with narrower frequency bandwidths, suggesting that ecological selection on beak morphology influences the diversification of woodcreeper songs. Because songs in turn mediate mate choice and species recognition in birds, these results indicate a broader role for ecology in avian diversification.