The evolution of warning coloration in Heliconius butterflies

Many species use conspicuous coloration to advertise their distastefulness to potential predators. The evolution of these warning patterns is a paradox, however, since they are under strong, positive frequency-dependent selection: individuals possessing rare pat terns are more likely to be attacked by predators, thus eliminating the pattern before it can become common. Yet in many warningly colored species, coloration has diversified extensively. In the 50 species of Heliconius butterflies, novel color patterns have evolved at least 400 times and some species are characterized by over two dozen distinct patterns. One mechanism that may account for this diversification is Wright\u27s three-phase shifting balance. Wright envisioned species consisting of small subpopulations that were largely free to explore a fitness landscape . In such subpopulations, adaptive genotypes could drift (phase I) to a high enough frequency for selection to drive it to local fixation (phase II). As subpopulations exchanged migrants, interdemic selection could spread the novel genotype throughout the population (phase III). This shifting balance between selection and drift is in stark contrast to Fisherian evolution, which regards drift as something that hinders adaptation rather than promoting it. Because of the complexity of the shifting balance, its influence on evolutionary systems is difficult to evaluate. To date, no natural system has been shown to exhibit all of the stages of the shifting balance. Thus, I critically evaluated whether Wright\u27s shifting balance or Fisherian selection best explains the pattern of diversification in Heliconius. By conducting mating experiments in greenhouse colonies of Heliconius , I demonstrated that the mating system of these butterflies cannot account for the color pattern diversification of the genus. Other Fisherian hypotheses also fail to account for this diversification. To evaluate the shifting balance, I carried out an intensive study of population structure and behavior in a natural Costa Rican Heliconius community. These data were used to parameterize a sophisticated spatially explicit, individual-based model of Heliconius populations. This model demonstrated the efficiency with which phase III operates in this system, and established the scale over which stochastic events are necessary to drive phases I and II. According to this model, the shifting balance predicts diversification to occur most readily in peripheral populations with low dispersal abilities and high rates of hybridization. This pattern is clearly evident in Heliconius, strongly suggesting a role for Wright\u27s shifting balance in the evolution of warning coloration