Exaptation and de novo mutations transcend cryptic variations as drivers of adaptation in yeast

Many organisms live in predictable environments with periodic variation in growth condition which can allow populations to accumulate cryptic genetic variations. Cryptic variations can facilitate adaptation to new environments, as observed in evolution experiments with a ribozyme and a protein. Whether the same holds for cell populations remains unclear. Alternatively, living in a near-constant condition can lead to loss of nonessential cellular functions, which could be maladaptive in new environments. Through laboratory evolution experiments in yeast, we show that populations grown in a predictable nutrient-rich environment for 1000 generations start to lose their ability to respond and adapt to new stressful environments. Growth of yeast populations in the nutrient-rich environment was associated with modest fitness increase in this environment, metabolic remodeling, and increased lipid accumulation. In novel stressful environments, however, these populations generally had reduced fitness, except in salt-stress where lipid accumulation seemed to provide osmotic protection. We further found that adaptation to stressors was primarily driven by de novo mutations, with very little contribution from the mutations accumulated prior to the exposure to stressors. Thus, our work suggests that in the absence of occurrence of new environments, natural populations might not accumulate cryptic variations that could be beneficial for adaptation to these environments. In addition, presence of selection in predictable condition in natural populations may purge away some of the cryptic variations. Taken together, these findings raise questions about persistence of cryptic variations in natural populations and their importance in evolutionary adaptation.