Seasonally fluctuating selection can maintain polymorphism at many loci via segregation lift

Abstract

<p id="d13074680e248">A key question in evolutionary biology is: What maintains the abundant genetic variation observed in natural populations? Many organisms experience some seasonality in their habitats, and, if they have multiple generations per year, seasonally fluctuating selection is a potentially powerful mechanism to maintain polymorphism. However, previous research has argued that this occurs rarely. Inspired by recent empirical findings, we reevaluate the potential of seasonally fluctuating selection to simultaneously maintain polymorphism at many loci in the genome. We obtain a more general condition for the maintenance of multilocus polymorphism by seasonally fluctuating selection. This condition may plausibly be satisfied for many species and does not suffer from problems of previous models. </p><p class="first" id="d13074680e251">Most natural populations are affected by seasonal changes in temperature, rainfall, or resource availability. Seasonally fluctuating selection could potentially make a large contribution to maintaining genetic polymorphism in populations. However, previous theory suggests that the conditions for multilocus polymorphism are restrictive. Here, we explore a more general class of models with multilocus seasonally fluctuating selection in diploids. In these models, the multilocus genotype is mapped to fitness in two steps. The first mapping is additive across loci and accounts for the relative contributions of heterozygous and homozygous loci—that is, dominance. The second step uses a nonlinear fitness function to account for the strength of selection and epistasis. Using mathematical analysis and individual-based simulations, we show that stable polymorphism at many loci is possible if currently favored alleles are sufficiently dominant. This general mechanism, which we call “segregation lift,” requires seasonal changes in dominance, a phenomenon that may arise naturally in situations with antagonistic pleiotropy and seasonal changes in the relative importance of traits for fitness. Segregation lift works best under diminishing-returns epistasis, is not affected by problems of genetic load, and is robust to differences in parameters across loci and seasons. Under segregation lift, loci can exhibit conspicuous seasonal allele-frequency fluctuations, but often fluctuations may be small and hard to detect. An important direction for future work is to formally test for segregation lift in empirical data and to quantify its contribution to maintaining genetic variation in natural populations. </p>