Phenotypic plasticity promotes recombination and gene clustering in periodic environments

Abstract

While theory offers clear predictions for when recombination will evolve in changing environments, it is unclear what natural scenarios can generate the necessary conditions. The Red Queen hypothesis provides one such scenario, but it requires antagonistic host–parasite interactions. Here we present a novel scenario for the evolution of recombination in finite populations: the genomic storage effect due to phenotypic plasticity. Using analytic approximations and Monte-Carlo simulations, we demonstrate that balanced polymorphism and recombination evolve between a target locus that codes for a seasonally selected trait and a plasticity modifier locus that modulates the effects of target-locus alleles. Furthermore, we show that selection suppresses recombination among multiple co-modulated target loci, in the absence of epistasis among them, which produces a cluster of linked selected loci. These results provide a novel biological scenario for the evolution of recombination and supergenes.

Genomic Architecture of Phenotypic Plasticity in Response to Water Stress in Tetraploid Wheat

“…This phenomenon may have resulted from pleiotropic and/or epistatic effects in the genetic control of phenotypic plasticity [ 52 ]. Moreover, it was suggested [ 53 ] that co-located effects are the result of the clustering of genes affecting phenotypic plasticity.…”

Ecological diversification in sexual and asexual lineages

“…Our findings may be relevant to understand the paradox of sex, often stated as: why a larger number of eukaryotic species reproduce sexually relative to those that reproduce asexually despite the costs of sex? Most research addressing this problem has focused on identifying multiple mechanisms that enable the maintenance of sex within populations 19,48,[56][57][58][59][60][61][62][63][64][65][66][67][68][69][70][71][72][73][74] . However, differences in diversification rate may also contribute to the relative richness of species with each reproductive mode.…”

Rapid evolution of phenotypic plasticity in patchy habitats

“…Balanced polymorphism represents another venue for the rapid evolution of plastic or non-plastic response, via protected balanced polymorphisms at the plasticity modifier locus. Gulisija et al 13 , 14 offered a plausible scenario for balanced polymorphism and rapid molecular evolution of phenotypic plasticity that requires predictably changing temporally varying environments. However, by the nature of temporal change this scenario is limited predominantly to evolution in seasonally evolving organisms 66 , 67 and makes specific assumptions about genetic architecture and recombination.…”

“…The latter mechanism involves the interaction of loci, such as regulatory loci that affect target expression 10 , and hence constitutes a kind of epistasis. Theoretical studies have explored this type of epistasis using modifier locus models 6 , 13 , 14 . In such models, an allele at the modifier locus, such as a transcription factor or an epigenetic modifier, may affect the expression of a target locus so as to improve the phenotype or fitness in a particular environment.…”

“…Plasticity modifiers, however, might evolve differently from single directly-selected loci due to the distinct way in which plasticity affects fitness. Fitness effects of gene regulation by a modifier are indirect and dependent on both the environment and the target locus 13 , 14 . Plasticity may further come with fitness costs 5 , 15 – 17 , 28 – 30 .…”