Phenotypic plasticity promotes balanced polymorphism in periodic environments by a genomic storage effect

Abstract

Phenotypic plasticity is known to evolve in perturbed habitats, where it alleviates the deleterious effects of selection. But the effects of plasticity on levels of genetic polymorphism, an important precursor to adaptation in temporally varying environments, are unclear. Here we develop a haploid, two-locus population-genetic model to describe the interplay between a plasticity modifier locus and a target locus subject to periodically varying selection. We find that the interplay between these two loci can produce a "genomic storage effect" that promotes balanced polymorphism over a large range of parameters, in the absence of all other conditions known to maintain genetic variation. The genomic storage effect arises as recombination allows alleles at the two loci to escape more harmful genetic backgrounds and associate in haplotypes that persist until environmental conditions change. Using both Monte Carlo simulations and analytical approximations we quantify the strength of the genomic storage effect across a range of selection pressures, recombination rates, plasticity modifier effect sizes, and environmental periods.KEYWORDS balanced polymorphism; phenotypic plasticity; temporally varying selection; storage effect B ALANCED polymorphism fosters adaptation in changing environments. As populations continuously adapt from one environment to the other, genetic polymorphism provides a readily available reservoir of adaptive alleles that selection can act upon and, thus, promotes population persistence (Lande and Shannon 1996;Barrett and Schluter 2008). Despite their role in persistence, evolutionary mechanisms that help maintain genetic polymorphism in temporally changing environments remain poorly understood.Empirical studies have revealed cases of polymorphism that are subject to temporally varying selection (e.g., Lynch 1987;Cain et al. 1990;Turelli et al. 2001;Bergland et al. 2014). However, the underlying mechanisms maintaining genetic polymorphism in these cases are unclear. Theoretical possibilities that predict balanced polymorphism in varying environments include heterozygous advantage [geometric mean overdominance, which cannot occur in haploids (Dempster 1955;Haldane and Jayakar 1963;Gillespie 1973Gillespie , 1974], overlapping generations with age-/stage-specific selection or seed banks (Ellner and Hairston 1994;Turelli et al. 2001;Svardal et al. 2011), density regulation with resource competition (Dean 2005;Yi and Dean 2013), or these mechanisms in combination with spatial heterogeneity in selection (Gillespie 1974(Gillespie , 1975Ewing 1979;Gulisija and Kim 2015;Svardal et al. 2015). Despite these developments, balancing selection due to temporally varying selection has not been widely accepted in population genetic literature probably because early models were criticized due to their failure to maintain polymorphism under genetic drift (Hedrick 1976).The storage effect, initially recognized in studies of species coexistence in community ecology (Chesson and Warner 1981;Chesson 1985Chesso...