title: The dynamics of diverse segmental amplifications in populations of Saccharomyces cerevisiae adapting to strong selection.
abstract: Population adaptation to strong selection can occur through the sequential or parallel accumulation of competing beneficial mutations. The dynamics, diversity, and rate of fixation of beneficial mutations within and between populations are still poorly understood. To study how the mutational landscape varies across populations during adaptation, we performed experimental evolution on seven parallel populations of Saccharomyces cerevisiae continuously cultured in limiting sulfate medium. By combining quantitative polymerase chain reaction, array comparative genomic hybridization, restriction digestion and contour-clamped homogeneous electric field gel electrophoresis, and whole-genome sequencing, we followed the trajectory of evolution to determine the identity and fate of beneficial mutations. During a period of 200 generations, the yeast populations displayed parallel evolutionary dynamics that were driven by the coexistence of independent beneficial mutations. Selective amplifications rapidly evolved under this selection pressure, in particular common inverted amplifications containing the sulfate transporter gene SUL1. Compared with single clones, detailed analysis of the populations uncovers a greater complexity whereby multiple subpopulations arise and compete despite a strong selection. The most common evolutionary adaptation to strong selection in these populations grown in sulfate limitation is determined by clonal interference, with adaptive variants both persisting and replacing one another.
authors.affiliation: Department of Genome Sciences, University of Washington, Seattle, Washington 98195.
authors.forename: Celia
authors.initials: C
authors.lastname: Payen
authors.forename: Sara C
authors.initials: SC
authors.lastname: Di Rienzi
authors.forename: Giang T
authors.initials: GT
authors.lastname: Ong
authors.forename: Jamie L
authors.initials: JL
authors.lastname: Pogachar
authors.forename: Joseph C
authors.initials: JC
authors.lastname: Sanchez
authors.forename: Anna B
authors.initials: AB
authors.lastname: Sunshine
authors.forename: M K
authors.initials: MK
authors.lastname: Raghuraman
authors.forename: Bonita J
authors.initials: BJ
authors.lastname: Brewer
authors.forename: Maitreya J
authors.initials: MJ
authors.lastname: Dunham
mesh_terms: D000220:Adaptation, Biological; D027321:Anion Transport Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D004271:DNA, Fungal / Q000737:chemistry / Q000302:isolation & purification; D059014:High-Throughput Nucleotide Sequencing; D007700:Kinetics; D009154:Mutation; D009690:Nucleic Acid Conformation; D012441:Saccharomyces cerevisiae / Q000235:genetics*; D029701:Saccharomyces cerevisiae Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA; D000076988:Sulfate Transporters
chemical_list: D027321:Anion Transport Proteins; D004271:DNA, Fungal; C094656:SUL1 protein, S cerevisiae; D029701:Saccharomyces cerevisiae Proteins; D000076988:Sulfate Transporters
keywords: clonal interference; evolutionary genomics; experimental evolution; gene amplification; inverted triplication; whole genome sequencing