Increased time sampling in an evolve‐and‐resequence experiment with outcrossing <i>Saccharomyces cerevisiae</i> reveals multiple paths of adaptive change

Phillips, Mark; Kutch, Ian C.; Long, Anthony D.; Burke, Molly K.

doi:10.1111/mec.15687

Cited by 14 publications

(22 citation statements)

References 76 publications

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“…Most E&R experiments with sexually-reproducing model organisms use Drosophila 10 – 19 . However, outcrossing S. cerevisiae populations have emerged as an attractive alternative due to shorter generation times, ease of replication, the ability to freeze and “resurrect” samples taken from different timepoints, and comparable genetic resources 20 , 21 . As such, we have chosen to focus our efforts on determining how to best construct populations of outcrossing S. cerevisiae for use in E&R studies with respect to maximizing standing genetic variation and haplotype diversity.…”

Section: Introductionmentioning

confidence: 99%

“…As S. cerevisiae populations isolated from natural or industrial settings typically lack genetic heterogeneity, generating laboratory populations with standing genetic variation requires crossing distinct isogenic strains. These “synthetic recombinant” or multiparent populations have traditionally been used for QTL mapping 22 , 23 , but they can also serve as the ancestral population in evolution experiments 20 , 21 . Notably, synthetic recombinant populations have also been used for E&R in other model organisms such as D. melanogaster (e.g.…”

Section: Introductionmentioning

confidence: 99%

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Crossing design shapes patterns of genetic variation in synthetic recombinant populations of Saccharomyces cerevisiae

Phillips

Kutch

McHugh

et al. 2021

Sci Rep

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Abstract“Synthetic recombinant” populations have emerged as a useful tool for dissecting the genetics of complex traits. They can be used to derive inbred lines for fine QTL mapping, or the populations themselves can be sampled for experimental evolution. In the latter application, investigators generally value maximizing genetic variation in constructed populations. This is because in evolution experiments initiated from such populations, adaptation is primarily fueled by standing genetic variation. Despite this reality, little has been done to systematically evaluate how different methods of constructing synthetic populations shape initial patterns of variation. Here we seek to address this issue by comparing outcomes in synthetic recombinant Saccharomyces cerevisiae populations created using one of two strategies: pairwise crossing of isogenic strains or simple mixing of strains in equal proportion. We also explore the impact of the varying the number of parental strains. We find that more genetic variation is initially present and maintained when population construction includes a round of pairwise crossing. As perhaps expected, we also observe that increasing the number of parental strains typically increases genetic diversity. In summary, we suggest that when constructing populations for use in evolution experiments, simply mixing founder strains in equal proportion may limit the adaptive potential.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Crossing design shapes patterns of genetic variation in synthetic recombinant populations of Saccharomyces cerevisiae

Phillips

Kutch

McHugh

et al. 2021

Sci Rep

Self Cite

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show abstract

“…Cubillos et al 2013;Linder et al 2020), but they can also serve as the ancestral population in evolution experiments (e.g. Burke et al 2014;Phillips et al 2020). Notably, synthetic recombinant populations have also been used for E&R in other model organisms such as D. melanogaster (e.g the Drosophila Synthetic Population Resource cf.…”

Section: Introductionmentioning

confidence: 99%

“…Teotónio et al 2012). In this context, having clearly defined founder genotypes enables the estimation of haplotype frequencies in evolved populations from "Pool-SEQ" data (Michalak et al 2018, Linder et al 2020, Phillips et al 2020. And this ability to detect haplotypes responding to selection, as opposed to individual markers, allows for better characterization of linkage and genetic hitchhiking in evolved populations than is possible in studies where founder genotypes are unknown (e.g.…”

Section: Introductionmentioning

confidence: 99%

“…As S. cerevisiae populations isolated from natural or industrial settings typically lack genetic heterogeneity, generating laboratory populations with standing genetic variation requires crossing distinct isogenic strains. These “synthetic recombinant” or multiparent populations have traditionally been used for QTL mapping 22–23 , but they can also serve as the ancestral population in evolution experiments 20–21 . Notably, synthetic recombinant populations have also been used for E&R in other model organisms such as D. melanogaster (e.g the Drosophila Synthetic Population Resource cf .…”

Section: Introductionmentioning

confidence: 99%

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Crossing design shapes patterns of genetic variation in synthetic recombinant populations ofSaccharomyces cerevisiae

Phillips

Kutch

Burke

2021

Preprint

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Multiparent or synthetic recombinant populations those created by combining distinct isogenic founders to establish a single recombinant background have emerged as a useful tool for dissecting the genetics of complex traits. Synthetic recombinant populations can be used to derive inbred lines in which quantitative traits can be mapped, or the recombinant populations themselves can be sampled for experimental evolution. Especially for the latter application, investigators generally value maximizing genetic variation in a recombinant population; in other words, a population harboring relatively equal contributions of the genetic backgrounds of each isogenic founder strain is a desirable resource. It is well-documented that in evolution experiments initiated from recombinant or outbred ancestral populations, the subsequent adaptation that occurs in evolved populations is driven by standing genetic variation, rather than de novo mutations. Despite the demonstrated importance of initial genetic variation to the adaptive process, little has been done to systematically evaluate methods of constructing a synthetic recombinant population, for creating resources for evolution experiments. Here we seek to address this issue by comparing patterns of genetic variation in different synthetic recombinant populations of Saccharomyces cerevisiae created using one of two combination strategies: pairwise crossing of isogenic strains or simple mixing of strains in equal proportion. We also explore the impact of the varying the number of parental strains used in each strategy. We find that more genetic variation is initially present and subsequently maintained over generations when population construction includes a round of pairwise crossing. We also observe that when using a given crossing strategy, increasing the number of parental strains typically increases genetic diversity. In summary, we suggest that when creating recombinant populations for use in experimental evolution studies, simply mixing founder strains in equal proportion may limit the adaptive potential of that population.

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Loss of Heterozygosity and Its Importance in Evolution

Heil

2023

J Mol Evol

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Loss of heterozygosity (LOH) is a mitotic recombination event that converts heterozygous loci to homozygous loci. This mutation event is widespread in organisms that have asexual reproduction like budding yeasts, and is also an important and frequent mutation event in tumorigenesis. Mutation accumulation studies have demonstrated that LOH occurs at a rate higher than the point mutation rate, and can impact large portions of the genome. Laboratory evolution experiments of heterozygous yeasts have revealed that LOH often unmasks beneficial recessive alleles that can confer large fitness advantages. Here, I highlight advances in understanding dominance, fitness, and phenotypes in laboratory evolved heterozygous yeast strains. I discuss best practices for detecting LOH in intraspecific and interspecific evolved clones and populations. Utilizing heterozygous strain backgrounds in laboratory evolution experiments offers an opportunity to advance our understanding of this important mutation type in shaping adaptation and genome evolution in wild, domesticated, and clinical populations.

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Increased time sampling in an evolve‐and‐resequence experiment with outcrossing Saccharomyces cerevisiae reveals multiple paths of adaptive change

Cited by 14 publications

References 76 publications

Crossing design shapes patterns of genetic variation in synthetic recombinant populations of Saccharomyces cerevisiae

Crossing design shapes patterns of genetic variation in synthetic recombinant populations of Saccharomyces cerevisiae

Crossing design shapes patterns of genetic variation in synthetic recombinant populations ofSaccharomyces cerevisiae

Loss of Heterozygosity and Its Importance in Evolution

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