Dramatic examples of right-left asymmetry often inspire adaptive explanations, simply because it is hard to imagine how such forms could not be functionally significant. But are conspicuous morphological asymmetries necessarily adaptive? Surprisingly, in some species where direction of asymmetry is random, asymmetry in bilaterally paired traits may arise as a developmental error in a threshold trait. When cases of asymmetry are rare within a species, they are easily recognized as developmental errors. However, as asymmetrical individuals become more common, or if the asymmetry is in a signaling trait, the temptation to advance an adaptive explanation grows, particularly if the asymmetry is not clearly maladaptive. Several models of the ontogeny of asymmetry are described for both normal and anomalous random asymmetry of bilaterally paired traits. In the absence of selection, each model predicts different expected frequencies of symmetrical and asymmetrical individuals within a species, therefore such frequency distributions can effectively test for different models of development. In normal random asymmetries – where conspicuously asymmetrical individuals predominate – lateral inhibition of one side after the other has transformed appears to be an essential step in development. In anomalous random asymmetries – where conspicuously asymmetrical individuals are relatively rare – no lateral inhibition is required. Other potentially relevant variables include: purely stochastic variation in morphogen levels, use-induced asymmetry, and local (each side independent) versus central (e.g., hormonal) signaling. Examples of normal and anomalous random asymmetries are reviewed for several animal groups. A closer examination of the spectacular forelimb asymmetry in empidid dance flies raises doubts about claims that the asymmetry – both its occurrence and its direction – is adaptive, even though enlargement of the forelimbs likely is. Additional studies are required to conclude that this asymmetry is truly adaptive, as opposed to the outcome of random developmental variation in a threshold trait. This dance-fly leg asymmetry illustrates nicely how alternative hypotheses need to be considered before interpreting such variation as adaptive, even in a signaling trait.