Crossing the valley of non-intimidating conspicuousness: evolution of warning coloration through the lens of fitness landscapes

Abstract

The initial evolution of conspicuous aposematism is a longstanding evolutionary paradox: while the benefits of conspicuousness in aposematic signals have been demonstrated, they rely on predators being familiar with the conspicuous signals and avoiding them. In a system dominated by naïve predators, the appearance of conspicuousness would be expected to increase detection and attack rate by the predators. Hence, it is unclear how such signals could become established in a naïve community. We suggest that this problem may usefully be framed in the terms of fitness landscapes, an idea used for conceptualizing the mapping between genotype/phenotype and fitness. The evolution of conspicuousness can be thought of as a special case of valley crossing, which concerns the transition of populations between fitness peaks, when such a transition imposes an initial decrease in fitness. Crypsis may be regarded as a local fitness peak, hindering predators’ ability to detect prey; for an unpalatable species, conspicuous aposematism may constitute a higher-still fitness peak, preventing predation attempts altogether and allowing access to niches unavailable to species encumbered by the necessity to remain concealed from predators. However, in order to reach this higher peak, the population must first cross the valley of non-intimidating conspicuousness, in which the prey is conspicuous but the predators are not yet deterred. Using terms borrowed from the concept of fitness landscapes, we categorize several solutions suggested previously in the literature as either concerning changes in the fitness landscape or as illuminating possible ridges connecting the two peaks, which emerge from unconsidered dimensions of the fitness landscape. We suggest that considering this question through the lens of fitness landscapes not only facilitates useful categorization of previously suggested solutions but may also prove useful for thinking about novel ones.