Whether or not sexually selected traits consistently exhibit positive allometry (i.e. are disproportionately large in larger individuals) is an ongoing debate. Multiple models and exceptions to this rule suggest that the underlying drivers of sexual trait allometry are nuanced. Here, we compare allometries of sexual and non-sexual traits of a species (Anolis aquaticus) within a well-studied lizard genus to test the competing hypotheses that sexual traits are, or are not, defined by positive allometry. We further consider the relationships of trait functions, which are relatively well understood in the genus Anolis, and allometry to identify potential drivers of allometric patterns. In particular, we explore how trait allometries interact to influence total organism function and generate sexual dimorphism. We quantified size (of targeted traits) and color of a sexual signal (the dewlap) in Anolis aquaticus in the field. The dewlap conveyed information relevant to intra-sexual combat and exhibited positive allometry. Overall, our results suggest that using single-trait allometries as indicators of past selection provides only an incomplete understanding of trait evolution. Although the function of positive allometry in some individual sexual signals (e.g. those conveying "super-honest" information) may be straightforward, we illustrate how scaling relationships interact synergistically to influence the function of phenotypes and propose avenues for future research.