Population structure reverses selection of variants with proportionally scaled birth and death rates

Abstract

A frequently observed phenomenon across the kingdom of life is that a higher reproduction rate can be accompanied by higher mortality. During tumor progression, variants emerge that both reproduce and die faster; faster replicating viruses can be characterized by a faster decay rate; and more frequent pregnancy can be accompanied by a higher chance to die due to predation in ecological systems. Variants with proportionally scaled birth and death rates have been called quasi-neutral mutants. Although life-time reproductive success is not changed, such variants are characterized by fixation probabilities that are somewhat lower (higher) than expected for neutral mutants if birth and death rates are proportionally larger (smaller). Studies were performed in the context of well-mixed populations, and despite the deviation from neutrality, quasi-neutral mutants do not have characteristics of disadvantageous or advantageous mutants, as their fixation probabilities still scale with their initial fractions. Here, we report that in deme-or spatially structured populations, variants with proportionally increased (decreased) birth and death rates become truly disadvantageous (advantageous), and calculate their effective fitness. Furthermore, if mutants have a higher life-time reproductive output than the wild-types and are thus advantageous, a proportional increase of birth and death rates can render them strongly disadvantageous, and vice versa. This changes our understanding of how life-time reproductive success correlates with selection, and has implications for evolutionary dynamics across a range of biological systems.