Direct Selection on Genetic Robustness Revealed in the Yeast Transcriptome

Abstract

BackgroundEvolutionary theory predicts that organisms should evolve the ability to produce high fitness phenotypes in the face of environmental disturbances (environmental robustness) or genetic mutations (genetic robustness). While several studies have uncovered mechanisms that lead to both environmental and genetic robustness, we have yet to understand why some components of the genome are more robust than others. According to evolutionary theory, environmental and genetic robustness will have different responses to selective forces. Selection on environmental robustness for a trait is expected to be strong and related to the fitness costs of altering that trait. In contrast to environmental robustness, selection on genetic robustness for a trait is expected to be largely independent of the fitness cost of altering the trait and instead should correlate with the standing genetic variation for the trait that can potentially be buffered. Several mechanisms that provide both environmental and genetic robustness have been described, and this correlation could be explained by direct selection on both forms of robustness (direct selection hypothesis), or through selection on environmental robustness and a correlated response in genetic robustness (congruence hypothesis).Methodology/Principal FindingsUsing both published and novel data on gene expression in the yeast Saccharomyces cerevisiae, we find that genetic robustness is correlated with environmental robustness across the yeast genome as predicted by the congruence hypothesis. However, we also show that environmental robustness, but not genetic robustness, is related to per-gene fitness effects. In contrast, genetic robustness is significantly correlated with network position, suggesting that genetic robustness has been under direct selection.Conclusions/SignificanceWe observed a significant correlation between our measures of genetic and environmental robustness, in agreement with the congruence hypothesis. However, this correlation alone cannot explain the co-variance of genetic robustness with position in the protein interaction network. We therefore conclude that direct selection on robustness has played a role in the evolution of genetic robustness in the transcriptome.

Spontaneous Mutations Decrease Sensitivity of Gene Expression to Random Environmental Variation in Caenorhabditis elegans

“…Similar result were previously reported for Drosophila melanogaster [18] and Saccharomyces cerevisiae [19]. The positive association of V E with V G is consistent with the idea that genetic and environmental canalization may have common underlying mechanisms [20], [21], [22]. The positive association between V M and V E has an important implication, because theory predicts that genetic robustness is much more likely to evolve via correlated responses to selection for environmental robustness than via direct selection [11], [20].…”

Epigenetics Decouples Mutational from Environmental Robustness. Did It Also Facilitate Multicellularity?

“…Previous studies, using gene regulatory network models, have shown that networks will evolve robustness to genetic mutations under conditions of stabilizing selection [13], [14]. This result has been experimentally verified in RNA viruses [15], yeast [16], [17], and in the process of RNA folding [18]. In addition to genetic mutations, organisms are exposed to environmental changes.…”

Phenotypic robustness can increase phenotypic variability after nongenetic perturbations in gene regulatory circuits

“…A system is robust to genetic or nongenetic perturbations if its phenotype does not change when perturbed. Mutational robustness and robustness to nongenetic perturbations are correlated with one another in many cases (Rutherford & Lindquist, 1998;Ancel & Fontana, 2000;Meiklejohn & Hartl, 2002;de Visser et al, 2003;Ciliberti et al, 2007b;Proulx et al, 2007;Lehner, 2010), although exceptions exist (Cooper et al, 2006;Masel & Siegal, 2009;Fraser & Schadt, 2010). The ability to produce evolutionary innovation is linked to the robustness of a biological system (Ancel & Fontana, 2000;Wagner, 2005;Ciliberti et al, 2007a;Wagner, 2008b;Draghi & Wagner, 2009).…”