Inevitability of Red Queen evolution driven by organismic complexity and simple feedback via environmental modification

Abstract

Evolution in complex high-dimensional phenotype spaces can be very different than the caricature of uphill evolutionary trajectories in a low-dimensional fitness landscape. And slight modifications of the environment can have large consequences for the future evolution. Here, the simplest approximation of evolution, an almost-always clonal population evolving by small effect mutations under deterministic "adaptive" dynamics, is studied. The complexities of organisms and their interactions with their environments are caricatured by population growth rates being smoothly varying random functions in very high dimensional phenotype spaces. In a fixed environment, there are huge numbers of fitness maxima, yet evolutionary trajectories wander around amongst saddles, gradually slowing down but still wandering widely and without committing to any maximum. But with even very small changes of the environment caused by the phenotypic changes, after an initial transient the evolution continues forever without further slowing down. In this Red Queen "phase" the apparent rate of increase of the fitness saturates (at a feedback strength-dependent rate) and the trajectories perpetually wander over large phenotypic distances. Organismic complexities, caricatured by a large number of constraints on the molecular-level phenotype, together with the simplest possible interactions of the organisms with their environment, are shown to be sufficient to cause such Red Queen dynamics. Arguments are made for the ubiquity of such behavior.