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Abstract Interest in the question of when and how species recognition and mate preferences emerge in animals with strong species-typical predispositions has faded since the time of the classical ethologists. In its place, the role of plasticity has surfaced as a central emphasis in the study of animal behavior. Here, I step back and examine the origin and execution of sexual behavior in a tropical frog for which auditory predispositions are key. These experiments challenge assumptions about behavioral development, auditory perception, and stereotyped behavior. First, I illustrate when and how a sex- and speciestypical behavior—conspecific phonotaxis—emerges during development. This study demonstrates that phonotaxis, presumably restricted to mature females, is present in both sexes early in postmetamorphic development—potentially long before such behavior might serve an adaptive function. I place this result in the context of hypotheses regarding the development of learned versus non-learned behaviors, and in light of the potential for perception to be altered by physiological changes occurring concomitantly with ontogeny. Next, I describe a set of dynamic mate choice studies that highlight how decision-making in a relatively simple system is more flexible, and less stereotyped, than was previously assumed. Results here show that frogs temporally update their mate choice decisions in a moment-to-moment fashion as advertisement signals change in real time. By decomposing the decision-making process, I determine the stimulus parameters essential for commitment to an initial phonotactic approach. These studies are followed up by experiments that reveal a high level of individual variation in female choosiness during mate choice. Lastly, I describe a mate choice study that revealed categorical perception in frogs, the first “lower” vertebrate now known to exhibit a perceptual mode previously considered a hallmark of “higher” organisms. Collectively, I make the following arguments: (1) constraints on sensory systems play a larger role in shaping behavior than is generally appreciated, irrespective of the involvement of learning; (2) unstudied sources of variation may contribute significantly to the raw material for sexual selection; and (3) phonotaxis in anurans amphibians is not the simple, stereotyped behavior that has been suggested of it in the past.