Physiology, physics, and ecological interactions can generate trade-offs within species, but may also shape divergence among species. We tested whether signal divergence in Oecanthus tree crickets is shaped by acoustic, energetic, and behavioral trade-offs. We found that species with faster pulse rates, produced by opening and closing wings up to twice as many times per second, did not have higher metabolic costs of calling. The relatively constant energetic cost across species is explained by trade-offs between the duration and repetition rate of acoustic signals – species with fewer stridulatory teeth closed their wings more frequently such that the number of teeth struck per second of calling and the resulting duty cycle were relatively constant across species. Further trade-offs were evident in relationships between signals and body size. Calling was relatively inexpensive for small males, permitting them to call for much of the night, but at low amplitude. Large males produced much louder calls, reaching up to four times more area, but the energetic costs increased substantially with increasing size and the time spent calling dropped to only 20% of the night. These trade-offs indicate that the trait combinations that arise in these species represent a limited subset of conceivable trait combinations.