Geometry of environment-to-phenotype mapping: Unifying adaptation strategies in varying environments

Abstract: Biological organisms exhibit diverse strategies for adapting to varying environments. For example, a population of organisms may express the same phenotype in all environments (unvarying strategy'), or follow environmental cues and express alternative phenotypes to match the environment (tracking strategy'), or diversify into coexisting phenotypes to cope with environmental uncertainty (`bet-hedging strategy'). We introduce a general framework for studying how organisms respond to environmental variations, which models an adaptation strategy by an abstract mapping from environmental cues to phenotypic traits. Depending on the accuracy of environmental cues and the strength of natural selection, we find different adaptation strategies represented by mappings that maximize the longterm growth rate of a population. The previously studied strategies emerge as special cases of our model: the tracking strategy is favorable when environmental cues are accurate, whereas when cues are noisy, organisms can either use an unvarying strategy or, remarkably, use the uninformative cue as a source of randomness to bet-hedge. Our model of the environment-to-phenotype mapping is based on a network with hidden units; the performance of the strategies is shown to rely on having a high-dimensional internal representation, which can even be random.