Positive and negative frequency-dependent selection acting on polymorphism in a palatable moth

Camouflage and warning signals are contrasted prey strategies reducing predator attack, which offer an excellent opportunity to study the evolutionary forces acting on prey appearance. Edible prey are often inconspicuous and escape predation by remaining undetected. Predators learn to find the most common ones, leading to apostatic selection (advantage to rare morphs) enhancing variation in cryptic prey. By contrast, defended prey are often conspicuous and escape predation by using warning colorations identifying them as unprofitable. Predators avoid the ones they are most familiar with, leading to positive frequency-dependence and warning signal uniformity. It is less clear, however, what happens when two morphs of the same species vary strongly in conspicuousness, and how to explain the maintenance of cryptic and conspicuous morphs within populations, in the case of profitable prey. Using the white and melanic morphs of the invasive Box Tree Moth (Cydalima perspectalis) presented at three different frequencies, we investigate whether a) caterpillars and adult moths are palatable for birds, b) the less conspicuous, melanic morph experiences lower predation rates and b) whether frequency-dependence balances morph frequencies. Our results suggest that the melanic morph enjoys a survival advantage owing to a lower visibility. However, our experiments show that, unexpectedly, the two color morphs experience opposite patterns of frequency-dependent predation, despite being both fully palatable to birds. The melanic morph is under apostatic selection, whereas the conspicuous, white morph is subject to positive frequency-dependence (safety in numbers). Our experiments also show some level of unpalatability in the caterpillars. These results offer novel insight into how predation triggers contrasting evolutionary patterns in a palatable, polymorphic species within two morphs that differ markedly in conspicuousness and within two different life stages. Lay summaryUnderstanding the factors influencing character variation in natural populations is a key question in evolutionary ecology. Predation is one of the main drivers of color evolution in prey communities and prey usually mitigate predation using camouflage or warning colors. Camouflage evolves because it lowers the probability of being detected by predators. Since predators are more efficient at finding prey which they are familiar with, prey which display a rare phenotype are favoured (negative frequency-dependent selection). By contrast, aposematism is defined by conspicuous appearance in toxic or otherwise unprofitable prey, and evolves because birds identify defended prey by learning to use their appearance as a warning signal. The most common signals are usually best identified and avoided (positive-frequency dependent selection). It is not clear, however, how these two forces combine when predators are facing cryptic and conspicuous morphs of the same species, and how to explain their coexistence. Here we investigate this question in a laboratory experiment, by presenting wild birds with a melanic and a white morph of the same moth. Unexpectedly, our results show that despite being both fully palatable to birds, the two color morphs are subject to very different types of selection depending on their frequencies. The melanic morph is favored when it is rare, the conspicuous white morph as it gets common. The simultaneous action of these forces may contribute to maintain color polymorphism in natural populations. We also show that caterpillars of this species are unpalatable and chemically defended, whereas adults are not, showing opposite strategies of predator defense in different life stages of the same species.