Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations

Abstract

Laboratory experimental evolution provides a window into the details of the evolutionary process. To investigate the consequences of long-term adaptation, we evolved 205 Saccharomyces cerevisiae populations (124 haploid and 81 diploid) for ~10,000 generations in three environments. We measured the dynamics of fitness changes over time, finding repeatable patterns of declining adaptability. Sequencing revealed that this phenotypic adaptation is coupled with a steady accumulation of mutations, widespread genetic parallelism, and historical contingency. In contrast to long-term evolution in E. coli, we do not observe long-term coexistence or populations with highly elevated mutation rates. We find that evolution in diploid populations involves both fixation of heterozygous mutations and frequent loss-of-heterozygosity events. Together, these results help distinguish aspects of evolutionary dynamics that are likely to be general features of adaptation across many systems from those that are specific to individual organisms and environmental conditions.

Adaptation in outbred sexual yeast is repeatable, polygenic, and favors rare haplotypes

“…Further, after 50,000 generations of purely asexual evolution, (Tenaillon et al, 2016) found an average fitness increase of ~1.7-fold amongst all replicate Escherichia coli populations during adaptation to nutrient limitation. These comparisons suggest that the presence of recombination and high levels of standing variation lead to much larger fitness gains than are normally seen in experiments with less variation and/or no recombination, at least over short bursts of evolution in a novel environment, consistent with early studies that have more directly made this observation (Johnson et al, 2021).…”

“…Under this asexual isogenic paradigm forces such as historical contingency (Toprak et al, 2011), genetic parallelism at the level of genes but not (except for rare exceptions, see (Toprak et al, 2011)) specific mutations (Tenaillon et al, 2012;Toprak et al, 2011), and diminishing returns epistasis (Toprak et al, 2011;Wang et al, 2016) matter a great deal to the evolutionary process. Similar studies in asexual isogenic diploids have shown that ploidy can influence the dynamics of adaptation, with diploids often adapting more slowly than haploids, likely due to the effects of Haldane's sieve (Fisher et al, 2018;Gerstein et al, 2014;Johnson et al, 2021;Marad et al, 2018;Sellis et al, 2016;Sellis et al, 2011;Zeyl et al, 2003). Diploids also appear to accumulate more potentially deleterious mutations (increased mutational load), and continue to adapt longer than haploids, likely due to the effects of mitotic recombination (Forche et al, 2011;Gerstein et al, 2014;Johnson et al, 2021).…”

“…Similar studies in asexual isogenic diploids have shown that ploidy can influence the dynamics of adaptation, with diploids often adapting more slowly than haploids, likely due to the effects of Haldane's sieve (Fisher et al, 2018;Gerstein et al, 2014;Johnson et al, 2021;Marad et al, 2018;Sellis et al, 2016;Sellis et al, 2011;Zeyl et al, 2003). Diploids also appear to accumulate more potentially deleterious mutations (increased mutational load), and continue to adapt longer than haploids, likely due to the effects of mitotic recombination (Forche et al, 2011;Gerstein et al, 2014;Johnson et al, 2021). Despite these differences, general aspects of adaptation are shared with asexual haploids, including clonal interference and the fixation of beneficial mutations.…”

Seven Years at High Salinity—Experimental Evolution of the Extremely Halotolerant Black Yeast Hortaea werneckii

“…Kozela and Johnston [8] examined the effects of growth-limiting salt stress on mutational variation and the mutation rate. Johnson et al [9] performed a large-scale evolutionary experiment in three environments and identified several features of adaptation thought to be common across many species. Other fungal species are rarely used in experimental evolution, although fungi, especially microfungi, are generally good experimental subjects due to their relatively short generation times, compact genomes, and large effective population sizes compared to other eukaryotes.…”

Joint effects of genes underlying a temperature specialization tradeoff in yeast

“…Whether the multiple unlinked genes underlying a complex adaptation depend on each other to this degree is less well understood. Laboratory evolution has allowed genomic surveys (Blount et al, 2012; Good et al, 2017; Johnson et al, 2021; Kryazhimskiy et al, 2014) and, in some cases, experimental validation (Chou et al, 2011; Khan et al, 2011) of interactions between adaptive genes. Testing these principles in the context of evolution from the wild has posed a key challenge (although see Marcusson et al, 2009).…”