Many evolutionary forces can shape the evolution of communicative signals, and the long-term impact of each force may depend on relative timing and magnitude. We use a phylogenetic analysis to infer the history of blue belly patches of Sceloporus lizards, and a detailed spectrophotometric analysis of four species to explore the specific forces shaping evolutionary change. We find that the ancestor of Sceloporus had blue patches. We then focus on four species; the first evolutionary shift (captured by comparison of S. merriami and S. siniferus) represents an ancient loss of the belly patch by S. siniferus, and the second evolutionary shift, bounded by S. undulatus and S. virgatus, represents a more recent loss of blue belly patch by S. virgatus. Conspicuousness measurements suggest that the species with the recent loss (S. virgatus) is the least conspicuous. Results for two other species (S. siniferus and S. merriami) suggest that over longer periods of evolutionary time, new signal colours have arisen which minimize absolute contrast with the habitat while maximizing conspicuousness to a lizard receiver. Specifically, males of the species representing an ancient loss of blue patch (S. siniferus) are more conspicuous than are females in the UV, whereas S. merriami males have evolved a green element that makes their belly patches highly sexually dimorphic but no more conspicuous than the white bellies of S. merriami females. Thus, our results suggest that natural selection may act more immediately to reduce conspicuousness, whereas sexual selection may have a more complex impact on communicative signals through the introduction of new colours.