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

Temporally variable environments in natural populations generate fluctuations in both the fitness of mutant alleles and population size. The theory of storage effect predicted that balanced polymorphism emerges if a population is subdivided into two parts that are respectively exposed to and protected from the selective effect of fluctuating environment. Recently, adding cyclic fluctuation in population size to the model of storage effect was found to generate a novel force of positive selection on fitness-amplifying mutants that are eventually maintained in oscillatory polymorphism or fixed in the population. The latter particularly has an effect of amplifying 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 structure with overlapping generations. Mathematical analysis revealed that this novel evolutionary force is generated when the size of the subpopulation subject to weak selection does not covary with the rest of the population. 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.