Despite accumulating evidence for selection within natural systems, the importance of random genetic drift opposing Wright's and Fisher's views of evolution continue to be a subject of controversy. The geographical diversification of aposematic signals appears to be a suitable system to assess the factors involved in the process of adaptation since both theories were independently proposed to explain this phenomenon. In the present study, the effects of drift and selection were assessed from population genetics and predation experiments on poison-dart frogs, Ranitomaya imitator, of Northern Peru. We specifically focus on the transient zone between two distinct aposematic signals. In contrast to regions where high predation maintains a monomorphic aposematic signal, the transient zones are characterized by lowered selection and a high phenotypic diversity. As a result, the diversification of phenotypes may occur via genetic drift without a significant loss of fitness. These new phenotypes may then colonize alternative habitats if successfully recognized and avoided by predators. This study highlights the interplay between drift and selection as determinant processes in the adaptive diversification of aposematic signals. Results are consistent with the expectations of the Wright's shifting balance theory and represent, to our knowledge, the first empirical demonstration of this highly contested theory in a natural system.

Selective predation of aposematic signals is expected to promote phenotypic uniformity. But while uniform within a population, numerous species display impressive variations in warning signals among adjacent populations. Predators from different localities learning to avoid distinct signals while performing intense selection on others are thus expected to maintain such a geographic organization. We tested this assumption by placing clay frog models, representing distinct color morphs of the Peruvian poison-dart frog Ranitomeya imitator and a non conspicuous frog, reciprocally between adjacent localities. In each locality, avian predators were able to discriminate between warning signals; the adjacent exotic morph suffered up to four times more attacks than the local one and two times more than the non conspicuous phenotype. Moreover, predation attempts on the exotic morph quickly decreased to almost nil, suggesting rapid learning. This experiment offers direct evidence for the existence of different predator communities performing localized homogenizing selection on distinct aposematic signals.