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 both population size and 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 one part of the population, the 'field', is exposed to and the other, the 'refuge', is protected from fluctuating selection. A recent study found that oscillation in population size modifies the storage effect such that positive selection on a rare mutant occurs if its fitness and the size of the field change in the same directions. By this new version of storage effect, mutants with even smaller geometric mean fitness than the wild-type can be selected to intermediate frequencies and remain in balanced polymorphism or reach fixation. To further understand these eco-evolutionary dynamics and test 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 elucidated that whether balanced polymorphism or fixation occurs depends on the relative magnitudes of demographic versus fitness fluctuations and that both results require the discordant oscillation in the population sizes of the field and refuge. Therefore this novel evolutionary force is called 'noncovarying storage effect (NSE)'. Multi-locus simulations revealed that oscillatory polymorphism can be maintained simultaneously or reach fixations at many loci. The latter occurs in a wider range of parameters and, if the fitness effects of mutations change the mean absolute fitness of the population, leads to positive feedback between demography and selection that causes a drastic amplification of population size fluctuation. These results suggest that the NSE is a potentially prevalent evolutionary force in nature for maintaining genetic variation or causing large demographic fluctuations.