Genotype networks of 80 quantitative Arabidopsis thaliana phenotypes reveal phenotypic evolvability despite pervasive epistasis.

Gabriel Schweizer,Andreas Wagner,Björn Usadel

doi:10.1371/journal.pcbi.1008082

Gabriel Schweizer, Andreas Wagner + Show 1 more

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https://doi.org/10.1371/journal.pcbi.1008082

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Abstract

We study the genotype-phenotype maps of 80 quantitative phenotypes in the model plant Arabidopsis thaliana, by representing the genotypes affecting each phenotype as a genotype network. In such a network, each vertex or node corresponds to an individual’s genotype at all those genomic loci that affect a given phenotype. Two vertices are connected by an edge if the associated genotypes differ in exactly one nucleotide. The 80 genotype networks we analyze are based on data from genome-wide association studies of 199 A. thaliana accessions. They form connected graphs whose topography differs substantially among phenotypes. We focus our analysis on the incidence of epistasis (non-additive interactions among mutations) because a high incidence of epistasis can reduce the accessibility of evolutionary paths towards high or low phenotypic values. We find epistatic interactions in 67 phenotypes, and in 51 phenotypes every pairwise mutant interaction is epistatic. Moreover, we find phenotype-specific differences in the fraction of accessible mutational paths to maximum phenotypic values. However, even though epistasis affects the accessibility of maximum phenotypic values, the relationships between genotypic and phenotypic change of our analyzed phenotypes are sufficiently smooth that some evolutionary paths remain accessible for most phenotypes, even where epistasis is pervasive. The genotype network representation we use can complement existing approaches to understand the genetic architecture of polygenic traits in many different organisms.

Highlights

Understanding how genotypes are linked to phenotypes and to fitness is of central interest for evolutionary biology, because genotypic changes in the form of DNA mutations cause heritable variation in phenotypes, on which natural selection acts
We study the genotype-phenotype maps of 80 quantitative phenotypes in the model plant Arabidopsis thaliana, by representing the genotypes affecting each phenotype as a genotype network
How genotypic change relates to phenotypic change is a fundamental problem in evolutionary biology

Summary

Introduction

Understanding how genotypes are linked to phenotypes and to fitness is of central interest for evolutionary biology, because genotypic changes in the form of DNA mutations cause heritable variation in phenotypes, on which natural selection acts. While many early studies used computational approaches, genotype-phenotype maps are increasingly studied experimentally, for instance in a transfer RNA [12], a ribozyme [13], a small nucleolar RNA [14], a green fluorescent protein [15], and the antibiotic resistance beta-lactamase TEM-1 [16] Both empirical and experimental studies of such maps address fundamental evolutionary questions, for example about the implications of pleiotropy for the evolvability of complex organisms [17], the robustness and persistence of bet-hedging [18], the role of epistasis in evolution [19], or the influence of genetic correlations on mutational robustness and evolvability [20]

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