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.

Highlights

  • 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 a plausible scenario for the evolution of recombination under changing environments, but it is limited to cases involving coevolution with an antagonistic species, such as a parasite

  • This study introduces a novel scenario for the evolution of recombination under changing environments that does not require antagonistically interacting species or a steady influx of mutations: the genomic storage effect due to phenotypic plasticity

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Summary

Introduction

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 evolution of recombination requires a mechanism to generate constant and considerable diversity in order to sustain LD sufficient for selection to overcome genetic drift. These conditions limit the scenarios that promote recombination in nature to (1) a steady influx of mutations in combination with Hill–Robertson interference[15,16,17] or (2) constantly changing biotic environments under antagonistic coevolution between species[18,19]. The basic idea behind genomic storage is that, when abiotic environments change periodically, alleles can survive periods of adversity by escaping (recombining) to a genetic background that ameliorates the effects of selection, e.g., a modifier background that confers phenotypic plasticity, thereby storing diversity until conditions change. We examine whether or not recombination and balanced polymorphism can evolve simultaneously from a nonrecombining population

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