Genetic variation in adaptability and pleiotropy in budding yeast.

Elizabeth R Jerison,James Kameron Mitchell,Leonid Kruglyak,Joshua S Bloom,Sergey Kryazhimskiy,Michael M Desai

doi:10.7554/elife.27167

Abstract

Evolution can favor organisms that are more adaptable, provided that genetic variation in adaptability exists. Here, we quantify this variation among 230 offspring of a cross between diverged yeast strains. We measure the adaptability of each offspring genotype, defined as its average rate of adaptation in a specific environmental condition, and analyze the heritability, predictability, and genetic basis of this trait. We find that initial genotype strongly affects adaptability and can alter the genetic basis of future evolution. Initial genotype also affects the pleiotropic consequences of adaptation for fitness in a different environment. This genetic variation in adaptability and pleiotropy is largely determined by initial fitness, according to a rule of declining adaptability with increasing initial fitness, but several individual QTLs also have a significant idiosyncratic role. Our results demonstrate that both adaptability and pleiotropy are complex traits, with extensive heritable differences arising from naturally occurring variation.

Highlights

All organisms can evolve in the face of environmental perturbations
Genetic modifiers that create these differences in evolvability are subject to natural selection, and the potential consequences of secondary selection on evolvability has been the subject of extensive theoretical work
Note that here we use the term ‘pleiotropy’ in a sense that is common in experimental evolution but not in the genetics literature: it reflects how mutations that affect one trait influence other traits. We address these gaps by measuring genetic variation in adaptability among 230 haploid S. cerevisiae genotypes (‘founders’) derived from a cross between two substantially diverged parental strains (Bloom et al, 2013)

Summary

Introduction

All organisms can evolve in the face of environmental perturbations. Yet even closely-related individuals may differ in how quickly and effectively they adapt (Kirschner and Gerhart, 1998; Masel and Trotter, 2010; Lauring et al, 2013). Other empirical work has shown that alleles that modify recombination rates can speed the rate of adaptation or help purge deleterious load (Zeyl and Bell, 1997; Colegrave, 2002; Goddard et al, 2005; Cooper, 2007; Becks and Agrawal, 2012; Gray and Goddard, 2012; McDonald et al, 2016; Xiao et al, 2016). Mutations can affect evolvability in more subtle ways, through epistatic interactions that shape the future directions that evolution can take.

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Conclusion