Birdsong is a complex, learned vocal communication signal that functions in reproduction. Many aspects of the neural mechanisms underlying this behavior remain unknown, with respect to both song production and perception. The work described here investigates these issues from different levels of analysis. Nearly every aspect of song is characterized by immense interspecific diversity. In particular, species range from those that learn a single syllable to others that produce hundreds or thousands, but neither the ultimate nor proximate causes for this variability have been identified. Chapter 2 uses comparative analyses across a wide phylogeny of songbirds to address these questions. Syllable repertoire size is positively and strongly correlated with the degree of convergence along the descending motor pathway, suggesting that the level of top-down control rather than motor circuit size per se is more closely associated with the complexity of behavioral output. Repertoire size is not related to the sizes of other brain regions, however. Chapter 3 describes general evolutionary patterns of functional neural circuits and tests predictions made by two models of brain evolution. Interestingly, support was found for both. Nuclei that develop late in ontogeny possess larger allometric slopes than those that develop early, which is consistent with a developmental conservation model in which a general stretching of neurogenetic schedules underlies increases in brain size. Functional circuits evolve in concert and do so independently of others, however, supporting a mosaic pattern. Finally, chapter 4 examines the function of the caudomedial nidopallium (NCM), a region of the auditory forebrain, in adult females. Numerous correlative studies suggest that NCM is important for song learning. Consistent with this, inactivation of NCM eliminates female preferences for familiar songs but has much more modest effects on their preferences for high quality songs. Together, these experiments are the first to relate evolutionary changes in behavioral capacities to those in its underlying circuit, to document the coordinated evolution of functional circuits, and to demonstrate a causative role for the auditory forebrain in song perception.