Significance The process by which new complex traits evolve has been a persistent conundrum throughout the history of evolutionary inquiry. How multiple physiological changes at the organism level and genetic changes at the molecular level combine is still unclear for many traits. Here, we studied the displays of manakins, who beat their wings together at nearly twice the speed of other songbirds to produce a loud “snap” that attracts mates. We simultaneously analyzed evolution of gene expression levels and gene sequences to identify key genes related to muscle contractions and tissue regeneration after stress. Our results show how innovative behavioral traits evolve as a layered process where recent molecular shifts build on ancestral genetic evolutionary changes.