Dynamics of Adaptation in Experimental Yeast Populations Exposed to Gradual and Abrupt Change in Heavy Metal Concentration

Abstract

Directional environmental change is a ubiquitous phenomenon that may have profound effects on all living organisms. However, it is unclear how different rates of such change affect the dynamics and outcome of evolution. We studied this question using experimental evolution of heavy metal tolerance in the baker's yeast Saccharomyces cerevisiae. To this end, we grew replicate lines of yeast for 500 generations in the presence of (1) a constant high concentration of cadmium, nickel, or zinc or (2) a gradually increasing concentration of these metals. We found that gradual environmental change leads to a delay in fitness increase compared with abrupt change but not necessarily to a different fitness of evolutionary endpoints. For the nonessential metal cadmium, this delay is due to reduced fitness differences between genotypes at low metal concentrations, consistent with directional selection to minimize intracellular concentrations of this metal. In contrast, for the essential metals nickel and zinc, different genotypes are selected at different concentrations, consistent with stabilizing selection to maintain constant intracellular concentrations of these metals. These findings indicate diverse fitness consequences of evolved tolerance mechanisms for essential and nonessential metals and imply that the rate of environmental change and the nature of the stressor are crucial determinants of evolutionary dynamics.

Local Fitness Landscapes Predict Yeast Evolutionary Dynamics in Directionally Changing Environments

“…Our previous findings (Gorter et al 2016(Gorter et al , 2017 are consistent with the predictions from our G 3 E framework, but do not provide direct evidence for it. Specifically, for Cd, we found mutations in the same genes in response to both gradual and abrupt change, and this suggests magnitude G 3 E. Conversely, for Ni and Zn, we found mutations in different genes in response to gradual and abrupt change, and this suggests reranking G 3 E. We also repeatedly found mutations in specific combinations, suggesting that epistasis was important within the context of adaptation to all three metals.…”

“…The above findings may be explained within a G 3 E framework that we envisioned previously, which relies on the distinction between magnitude G 3 E and reranking G 3 E (Gorter et al 2016). This framework makes predictions about evolutionary dynamics and outcomes in changing environments based on the nature of the selection pressure, and can, in principle, be applied to any selection pressure or scenario of environmental change.…”

“…We previously evolved replicate populations of Saccharomyces cerevisiae for 500 generations in the presence of either gradually increasing or constant high concentrations of the heavy metals cadmium (Cd), nickel (Ni), and zinc (Zn; Gorter et al 2016). While Cd is toxic already at comparatively low concentrations, Ni and Zn are toxic at high concentrations only.…”

Dynamics of molecular evolution in RNA virus populations depend on sudden versus gradual environmental change

“…; Gorter et al. ). Here we examined Sindbis virus (SINV), the type species for positive‐sense ssRNA Alphaviruses, which include mosquito‐borne pathogens such as chikungunya virus and Eastern equine encephalitis virus.…”

Secondary environmental variation creates a shifting evolutionary watershed for the methyl-parathion hydrolase enzyme

“…Can they be re-shaped or altered by variation in "secondary" environmental factors, such as temperature, salinity, pH, the presence of other proteins, or cofactor availability such as metals? These factors do not necessarily define the novel adaptive function but they can nonetheless impact the fitness of a genotype; 11,12 can they also impact the direction of their evolution (Figure 1B)? [13][14][15] Several enzyme studies have addressed the impact of "primary" environments (i.e., different substrates or ligands) on the topology of the adaptive landscapes, 16,17 the degree to which the secondary environmental factors can alter evolutionary outcomes even under the same primary selective pressure remains poorly understood 11,18 ).…”