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Loss of heterozygosity drives adaptation in hybrid yeast

ABSTRACT: CGH arrays for Smukowski Heil, et al MBE 2017. Hybridization is often considered maladaptive, but sometimes hybrids can invade new ecological niches and adapt to novel or stressful environments better than their parents. The genomic changes that occur following hybridization that facilitate genome resolution and/or adaptation are not well understood. Here, we address these questions using experimental evolution of de novo interspecific hybrid yeast Saccharomyces cerevisiae x Saccharomyces uvarum and their parentals. We evolved these strains in nutrient limited conditions for hundreds of generations and sequenced the resulting cultures to identify genomic changes. Analysis of 16 hybrid clones and 16 parental clones identified numerous point mutations, copy number changes, and loss of heterozygosity events, including species biased amplification of nutrient transporters. We focused on a particularly interesting example, in which we saw repeated loss of heterozygosity at the high affinity phosphate transporter gene PHO84 in both intra- and interspecific hybrids. Using allele replacement methods, we tested the fitness of different alleles in hybrid and S. cerevisiae strain backgrounds and found that the loss of heterozygosity is indeed the result of selection on one allele over the other in both S. cerevisiae and the hybrids. This is an example where hybrid genome resolution is driven by positive selection on existing heterozygosity, and demonstrates that even infrequent outcrossing may have lasting impacts on adaptation.

ORGANISM(S): Saccharomyces bayanus Saccharomyces uvarum Saccharomyces cerevisiae Saccharomyces cerevisiae x Saccharomyces uvarum

PROVIDER: GSE95086 | GEO | 2017/02/21

SECONDARY ACCESSION(S): PRJNA376031

REPOSITORIES: GEO

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Project description:Hybrid progeny can enjoy increased fitness and stress tolerance relative to their ancestral species, a phenomenon known as hybrid vigor. Though this phenomenon has been documented throughout the Eukarya, evolution of hybrid populations has yet to be explored experimentally in the lab. To fill this knowledge gap we created a pool of Saccharomyces cerevisiae and S. bayanus homoploid and aneuploid hybrids, and then investigated how selection in the form of incrementally increased temperature or ethanol impacted hybrid genome structure and adaptation. During 500 generations of continuous ammonia-limited, glucose-sufficient culture, temperature was raised from 25C to 46??C. This selection invariably resulted in nearly-complete loss of the S. bayanus genome, although the dynamics of genome loss differed among independent replicates. Temperature-evolved isolates were significantly more thermal tolerant and exhibited greater phenotypic plasticity than parental species and founding hybrids. By contrast, when the same hybrid pool was subjected to increases in exogenous ethanol from 0% to 14%, selection favored euploid S. cerevisiae x S. bayanus hybrids. Ethanol-evolved isolates exhibited significantly greater ethanol tolerance relative only to S. bayanus and one of the founding hybrids tested. Adaptation to thermal and ethanol stress manifested as heritable changes in cell wall structure demonstrated by resistance to zymolyase or micafungin treatment. This is the first study to show experimentally that the fate of interspecific hybrids critically depends on the type of selection they encounter during the course of evolution. Array-CGH was performed on the S. cerevisiae parent strain CEN.PK (GSY2160), the S. bayanus parent strain CBS7001 (GSY2161) and on the F1 interspecific hybrid resulting from mating the 2 parents (GSY2168). Additionally, three rare viable spores obtained after sporulation of the F1 were assayed by array-CGH (F2a, F2b, F2c). A large pool of F2 spores (and probably some number of F1 hybrid cells) were subjected to gradually increasing temperatures, in three independent vessels, with populations sampled at various generation times. Likewise, the same pool was used to found populations in an additional three independent vessels, which were then subjected to gradually increasing ethanol concentrations (at constant temperature). Array-CGH was performed on three different clones from each of the three temperature vessels at the final 500 generation time point (T500 clones). Biological replicates of the T500 clones were performed (T500-new). Two self-self array-CGH hybridization controls were also performed (self-control). Array-CGH was performed on one clone from each of the three ethanol vessels taken at the 400 generation timepoint (EtOH400gen clones).

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Loss of heterozygosity drives adaptation in hybrid yeast

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