Differential encoding of signals and preferences by noradrenaline in the anuran brain

Social preferences enable animals to selectively interact with some individuals over others. One influential idea for the evolution of social preferences is that preferred signals evolve because they elicit greater neural responses from sensory systems. However, in juvenile Plains spadefoot toad (Spea bombifrons), a species with condition-dependent mating preferences, responses of the preoptic area, but not of the auditory midbrain, mirror adult social preferences. To examine whether this separation of signal representation from signal valuation generalizes to other anurans, we compared the relative contributions of noradrenergic signalling in the preoptic area and auditory midbrain of S. multiplicata, a close relative to S. bombifrons. We manipulated body condition in juvenile toads by controlling diet and used high pressure liquid chromatography to compare call-induced levels of noradrenaline and its metabolite MHPG in the auditory midbrain and preoptic area of the two species. We found that noradrenaline and MHPG levels in the auditory system differed between species' calls, with higher levels measured in both species for the more energetic S. bombifrons call. In contrast, noradrenaline levels in the preoptic area mirrored patterns of social preferences in both S. bombifrons and S. multiplicata. That is, noradrenaline levels were higher in response to the preferred calls within each species and were modified by diet in S. bombifrons (with condition-dependent preferences) but not S. multiplicata (without condition-independent preferences). Our results are consistent with a potentially important role for preoptic noradrenaline in the development of social preferences and indicate that it could be a target of selection in the evolution of condition-dependent social preferences.