Noncovarying storage effect: balancing and positive directional selection on mutant alleles that amplify random fitness and demographic fluctuations

Temporally variable environments in natural populations generate fluctuations in not only the population size but also the fitness effects of mutant alleles. The theory of storage effect, a species/allelic diversity-promoting mechanism discovered in ecology, predicts that rare mutants with fluctuating fitness can be positively selected and then maintained in balanced polymorphism if the population is subdivided into two parts that are respectively exposed to and protected from fluctuating environment. Recent study found that, under pre-exisiting oscillation in population size, the mutant is positively selected to fixation if its fitness change correlates with the rate of population growth, which further amplifies population size oscillation. To further understand these eco-evolutionary dynamics and elucidate their generality in natural populations, this study built more realistic models that assume randomly, not cyclically, fluctuating selection and common demographic features, including heterogeneous ecological patches or an age-structured population. Mathematical analysis revealed that this novel evolutionary force is generated when the size of the subpopulation subject to weak selection does not covary with that of the other subpopulation. Simulations showed that this noncovarying storage effect is robust to various perturbations in the model. Multi-locus simulations revealed that oscillatory polymorphism at many loci can be simultaneously maintained and that positive feedback between demography and selection can accelerate the sequential fixations of fluctuation-amplifying mutations and thus lead to a drastic amplification of population size fluctuation. These results suggest that the noncovarying storage effect is a potentially prevalent evolutionary force in nature for maintaining genetic variation and causing large demographic fluctuations. ARTICLE SUMMARYNatural populations experience rapid environmental changes that cause fluctuations in the fitness of genetic variants and population size. This study investigates how evolutionary changes due to fitness differences interact with concurrent demographic changes. The theory of the storage effect, which is a mechanism for promoting genetic diversity, was extended to add random population size fluctuation with heterogeneous environmental patches or in a population divided into different age classes. A novel evolutionary force that either increases genetic variation or drives evolution toward further amplification of population size fluctuation, an unconventional contributor to large demographic fluctuations in nature, was identified and analyzed.