Embracing Complexity: Yeast Evolution Experiments Featuring Standing Genetic Variation

Burke, Molly K.

doi:10.1007/s00239-023-10094-4

Cited by 5 publications

(3 citation statements)

References 53 publications

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“…We therefore turned to experimental evolution as an alternative approach to improve the hybrids’ fermentative profiles. Experimental evolution across multiple generations, paired with time-series whole genome sequencing, is a powerful tool for studying microbial responses to a selective environment and to understand the fitness effects of de novo mutations (Barrick & Lenski, 2013; Burke, 2023; Cooper, 2018; Maddamsetti et al, 2015). We found that, after 250 generations in a high sugar and ethanol environment, hybrids evolved faster fermentation performance and higher ethanol production compared to both parents and ancestral unevolved hybrids.…”

Section: Discussionmentioning

confidence: 99%

Wild Patagonian yeast improve the evolutionary potential of novel interspecific hybrid strains for Lager brewing

Molinet,

Navarrete,

Villarroel

et al. 2024

Preprint

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Lager yeasts are limited to a few strains worldwide, imposing restrictions on flavour and aroma diversity and hindering our understanding of the complex evolutionary mechanisms during yeast domestication. The recent finding of diverse S. eubayanus lineages from Patagonia offers potential for generating new Lager yeasts and obtaining insights into the domestication process. Here, we leverage the natural genetic diversity of S. eubayanus and expand the Lager yeast repertoire by including three distinct Patagonian S. eubayanus lineages. We used experimental evolution and selection on desirable traits to enhance the fermentation profiles of novel S. cerevisiae x S. eubayanus hybrids. Our analyses reveal an intricate interplay of pre-existing diversity, selection on species-specific mitochondria, de-novo mutations, and gene copy variations in sugar metabolism genes, resulting in high ethanol production and unique aroma profiles. Hybrids with S. eubayanus mitochondria exhibited greater evolutionary potential and superior fitness post-evolution, analogous to commercial Lager hybrids. Using genome-wide screens of the parental subgenomes, we identified genetic changes in IRA2, SNF3, IMA1 and MALX genes that influence maltose metabolism, and increase glycolytic flux and sugar consumption in the evolved hybrids. Functional validation and transcriptome analyses confirmed increased maltose-related gene expression, influencing grater maltotriose consumption in evolved hybrids. This study demonstrates the potential for generating industrially viable Lager yeast hybrids from wild Patagonian strains. Our hybridization, evolution, and mitochondrial selection approach produced hybrids with high fermentation capacity, expands Lager beer brewing options, and deepens our knowledge of Lager yeast domestication.

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Section: Discussionmentioning

confidence: 99%

Wild Patagonian yeast improve the evolutionary potential of novel interspecific hybrid strains for Lager brewing

Molinet,

Navarrete,

Villarroel

et al. 2024

Preprint

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“…Due to the already high species-specific recombination rates (Liu et al 2019), as well as this extra selection for high rates of outcrossing, regions of linked alleles that may potentially respond to experimental evolution are expected to be relatively small in the population (as small as 5-10KB; cf. Burke 2023). The experimental populations featured in this study were then derived from samples of this base population: 20 control replicates (C 1-20 ), 20 moderate ethanol stress replicates (M 1-20 ), and 20 high ethanol stress replicates (H 1-20 ).…”

Section: Methodsmentioning

confidence: 99%

Strength of selection potentiates distinct adaptive responses in an evolution experiment with outcrossing yeast

Phillips

Briar

Scaffo

et al. 2022

Preprint

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Combining experimental evolution with whole-genome sequencing is now a well-established method for studying the genetics of adaptation and complex traits. In this type of work that features sexually-reproducing populations, studies consistently find that adaptation is highly polygenic and fueled by standing genetic variation. Less consistency is observed with respect to general evolutionary dynamics however; for example, investigators remain ambivalent about whether selection produces repeatable versus idiosyncratic responses, or whether small shifts in allele frequencies at many loci drive adaptation, versus selective sweeps at fewer loci. Resolving these open questions is a crucial next step as we move toward extrapolating findings from laboratory evolution experiments to populations inhabiting natural environments. We propose that subtle differences in experimental parameters between studies can influence evolutionary dynamics in meaningful ways, and here we empirically assess how one of those parameters – selection intensity – shapes these dynamics. We subject populations of outcrossing Saccharomyces cerevisiae to zero, moderate, and high ethanol stress for ~200 generations and ask: 1) does stronger selection intensity lead to greater changes in allele frequencies, and a higher likelihood of selective sweeps at sites driving adaptation; and (2) do targets of selection vary with selection intensity? We find some evidence for positive correlations between selection intensity and allele frequency change, but no evidence for more sweep-like patterns at high intensity. While we do find genomic regions that suggest some shared genetic architecture across treatments, we also identify distinct adaptive responses in each selection treatment. Combined with evidence of phenotypic trade-offs between treatments, our findings support the hypothesis that selection intensity might influence evolutionary outcomes due to pleiotropic and epistatic interactions. As such, we conclude that details of a selection regime should be a major point of consideration when attempting to generalize inferences across experimental evolution studies. Finally, our results demonstrate the importance of clearly defined controls when associating genomic changes with adaptation to specific selective pressures. Despite working with a presumably lab-adapted model system, without this element we would not have been able to distinguish between genomic responses to ethanol stress and laboratory conditions.

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“…Performing microbial experiments that include initial genetic variation, allowing for better differentiating the effect of de novo mutations from standing genetic variation after a bottleneck, could improve this understanding. A recent review (Burke, 2023) suggested using yeast evolution experiments with standing genetic variation to study eukaryote adaptation. Indeed, yeast can combine short generation time and easy handling in the lab with sexual reproduction.…”

Section: Prospects For Filling Knowledge Gapsmentioning

confidence: 99%

How bottlenecks shape adaptive potential: from theory and microbiology to conservation biology

Gamblin,

Marrec,

Olazcuaga

2024

Preprint

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Wild populations frequently undergo demographic changes that can destabilize their persistence and, thus, the equilibrium of ecosystems. For instance, habitat loss due to human activities leads to a drastic population size reduction, a process called a bottleneck. By reducing genetic diversity, a bottleneck may prevent a population from adapting to subsequent environmental changes. In the context of climate change, it is crucial to accurately predict how populations evolve after a bottleneck and how it affects their persistence. Mathematical models have provided valuable insights into the impact of bottlenecks on adaptive potential of populations. However, their application to wild populations requires further improvement. Empirical testing of these theoretical predictions is mainly conducted using microbial populations. Thus, it remains unclear what the implications of the results are at the macroscopic scale, although this information is crucial for conservation biology. Here, we aim to determine the extent to which the knowledge acquired through evolutionary theory and experimental microbiology can be applied to wild populations. To achieve this, we address the following questions: (i) What do theory and microbiology experiments tell us about the influence of bottlenecks on the ability of populations to adapt to future environmental changes? (ii) Can these theoretical predictions be applied to wild populations? and (iii) What is missing to better predict the evolution of wild populations after a bottleneck? We analyze how the four main evolutionary processes (mutation, genetic drift, natural selection, and gene flow) influence the outcome of a bottlenecked population. By linking theory, microbial experiments, and empirical studies on natural populations, we identify research directions that could help improve the management of bottlenecked populations and plead for increased communication between these fields.

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Embracing Complexity: Yeast Evolution Experiments Featuring Standing Genetic Variation

Cited by 5 publications

References 53 publications

Wild Patagonian yeast improve the evolutionary potential of novel interspecific hybrid strains for Lager brewing

Wild Patagonian yeast improve the evolutionary potential of novel interspecific hybrid strains for Lager brewing

Strength of selection potentiates distinct adaptive responses in an evolution experiment with outcrossing yeast

How bottlenecks shape adaptive potential: from theory and microbiology to conservation biology

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