A general condition for adaptive genetic polymorphism in temporally and spatially heterogeneous environments

Abstract

Both evolution and ecology have long been concerned with the impact of variable environmental conditions on observed levels of genetic diversity within and between species. We model the evolution of a quantitative trait under selection that fluctuates in space and time, and derive an analytical condition for when these fluctuations promote genetic diversification. As ecological scenario we use a generalized island model with soft selection within patches in which we incorporate generation overlap. We allow for arbitrary fluctuations in the environment including spatio-temporal correlations and any functional form of selection on the trait. Using the concepts of invasion fitness and evolutionary branching, we derive a simple and transparent condition for the adaptive evolution and maintenance of genetic diversity. This condition relates the strength of selection within patches to expectations and variances in the environmental conditions across space and time. Our results unify, clarify, and extend a number of previous results on the evolution and maintenance of genetic variation under fluctuating selection. Individual-based simulations show that our results are independent of the details of the genetic architecture and whether reproduction is clonal or sexual. The onset of increased genetic variance is predicted accurately also in small populations in which alleles can go extinct due to environmental stochasticity.

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

“…The evolutionary dynamic between a plasticity modifier and a target allele generates an effect analogous to that in previous models of storage (Chesson and Warner 1981;Chesson 1985;Ellner and Hairston 1994;Turelli et al 2001;Svardal et al 2011Svardal et al , 2015Gulisija and Kim 2015). Modifier and nonmodifier genetic backgrounds provide subpopulations in which alleles at the target locus experience different magnitudes/direction of fitness effects and between which alleles "migrate" by recombination.…”

“…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 1985Chesson , 2000, presents a key mechanism underlying balanced genetic polymorphism in populations with overlapping generations and stage-specific selection or in combination with spatial heterogeneity (Ellner and Hairston 1994;Turelli et al 2001;Gulisija and Kim 2015;Svardal et al 2015). The basic idea is that a fraction of the population, in a specific life stage or a patch of habitat where adverse effects of selection are diminished, can "store" polymorphism until conditions change.…”

“…The basic idea is that a fraction of the population, in a specific life stage or a patch of habitat where adverse effects of selection are diminished, can "store" polymorphism until conditions change. Although the storage effect was originally studied in a deterministic framework, Svardal et al (2011Svardal et al ( , 2015 demonstrated a storage effect in finite populations experiencing overlapping generations and fluctuating selection, while Gulisija and Kim (2015) demonstrated balanced polymorphisms in finite populations under periodic selection and discrete generations, where a portion of a population is exposed to a decreased magnitude of environmental oscillation. Moreover, Gulisija and Kim (2015) showed that the effect arises even in the presence of geometric mean selective advantage/disadvantage between the competing alleles.…”

“…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 1985Chesson , 2000, presents a key mechanism underlying balanced genetic polymorphism in populations with overlapping generations and stage-specific selection or in combination with spatial heterogeneity (Ellner and Hairston 1994;Turelli et al 2001;Gulisija and Kim 2015;Svardal et al 2015). The basic idea is that a fraction of the population, in a specific life stage or a patch of habitat where adverse effects of selection are diminished, can "store" polymorphism until conditions change.…”