The ways in which animals sense the world around them change throughout development. Young of many species have absent or limited visual capabilities, but still make complex decisions about individuals with whom they interact. Poison frog tadpoles display complex social behaviors that have been suggested to rely on vision despite a century of research indicating tadpoles have poorly-developed visual systems. Here, we examined visual system development in tadopoles of the Mimetic Poison Frog (Ranitomeya imitator) that use begging displays to stimulate egg feeding from their mothers. Neural activation in the retina increased in begging metamorphic tadpoles, but not in begging pre-metamorphic tadpoles. Molecular profiling of active eye neurons during begging identified numerous differentially expressed development-related transcripts, suggesting that developmental stage, not begging, was driving gene expression profiles. Using the neural tracer neurobiotin, we found that connections between the eye and brain proliferate during metamorphosis, with little retinotectal connections in recently-hatched tadpoles. To assess visual capabilities of tadpoles, we used a light/dark preference assay in early, middle, and late stages. All tadpoles showed a preference for the dark side, but the strength of preference increased with developmental stage and eyes were not required for this behavior. Taken together, these data indicate visual ontology of poison frog tadpoles is similar to that of other frogs, with poor visual capabilities at hatching and immense morphological and physiological changes occurring during metamorphosis. More broadly, this highlights the importance of multimodal cues, including photodetection via the pineal structure, in tadpole social interactions.

Altricial young of many species beg parents for the nutrients required for healthy development. From human crying to begging chicks, young expend precious energy reserves to communicate their hunger. Despite repeated independent evolutionary origins, the neural basis of parent-directed communication by infants is unknown. Here, we examined the sensory and neural basis of begging behavior in tadpoles of the monogamous and biparental Mimetic poison frog (Ranitomeya imitator). In this species, tadpoles beg parents for egg meals by dancing. We used this robust motor display to determine that tadpoles use multimodal cues for caregiver recognition, where olfactory cues are necessary for caregiver recognition while visual cues provide an orientation goal. We found that dopamine related brain regions have higher neural activity in begging tadpoles and that dopamine signaling had opposing modulatory effects through D1 and D2 family receptors, similar to swimming behavior in other tadpole species. We then identified caudal posterior tuberculum dopamine neurons as more active during begging behavior and sensitive to caregiver olfactory cues. Projections of these dopaminergic neurons to the spinal accessory motor nucleus are required for begging displays. These findings support the idea that dopamine regulates olfactory-guided parental recognition in young and opens many avenues for studying how new communication behaviors can evolve from ancestral motor circuits.