Chromosomal duplication is a transient evolutionary solution to stress

Abstract

Aneuploidy, an abnormal number of chromosomes, is a widespread phenomenon found in unicellulars such as yeast, as well as in plants and in mammalians, especially in cancer. Aneuploidy is a genomescale aberration that imposes a severe burden on the cell, yet under stressful conditions specific aneuploidies confer a selective advantage. This dual nature of aneuploidy raises the question of whether it can serve as a stable and sustainable evolutionary adaptation. To clarify this, we conducted a set of laboratory evolution experiments in yeast and followed the long-term dynamics of aneuploidy under diverse conditions. Here we show that chromosomal duplications are first acquired as a crude solution to stress, yet only as transient solutions that are eliminated and replaced by more efficient solutions obtained at the individual gene level. These transient dynamics of aneuploidy were repeatedly observed in our laboratory evolution experiments; chromosomal duplications gained under stress were eliminated not only when the stress was relieved, but even if it persisted. Furthermore, when stress was applied gradually rather than abruptly, alternative solutions appear to have emerged, but not aneuploidy. Our findings indicate that chromosomal duplication is a first evolutionary line of defense, that retains survivability under strong and abrupt selective pressures, yet it merely serves as a "quick fix," whereas more refined and sustainable solutions take over. Thus, in the perspective of genome evolution trajectory, aneuploidy is a useful yet short-lived intermediate that facilitates further adaptation.evolutionary dynamics | environmental stress | heat tolerance | pH tolerance

Role of chromosomal instability in cancer progression

“…In addition, it is thought that chromosomal instability can act as an adaptive mechanism to allow cancer cells to widely sample a range of genotypes and phenotypes during periods of stress. This concept has been clearly demonstrated in single-celled organisms (Rancati et al 2008, Selmecki et al 2009, Pavelka et al 2010, Yona et al 2012, Chang et al 2013, however, demonstrating this in human cells has been more challenging. There is evidence that aneuploid human cells, although generally appearing less fit than their euploid counterparts under 'standard' conditions (Williams et al 2008, Thompson & Compton 2010 display advantages under selective conditions (Rutledge et al 2016) and that aneuploidy of pluripotent stem cells promotes their efficient adaptation to culture conditions (Barbaric et al 2014, Na et al 2014.…”

Single cell sequencing reveals low levels of aneuploidy across mammalian tissues

“…Indeed a positive role for aneuploidy is well documented in experimental evolution studies in microorganisms (27,28). The reports of high levels of aneuploidy in the brain and liver thus raised the exciting possibility that these organs somehow avoid the adverse Significance Aneuploidy refers to the gain or loss of individual chromosomes within a cell.…”

Fate of a mutation in a fluctuating environment

“…For example, drug resistance mutations often carry a cost when the dosage of the drug decays (1), and seasonal variations in climate can differentially select for certain alleles in the summer or winter (2). Similarly, laboratory adaptation to specific temperatures (3,4) or particular nutrient sources (5,6) often leads to declines in fitness in other conditions. Related trade-offs apply to any specialist phenotype or regulatory system that incurs a general cost to confer benefits in specific environmental conditions (7).…”