Ancient and recent origins of shared polymorphisms in yeast

Understanding what a microbial species is and the process of speciation in microbes has been and still is a puzzle with many challenges. But there is now emerging consensus that speciation in microbes does follow certain rules and limitations. Just like in macrobes, it can be driven by divergent natural selection and is maintained by barriers to gene flow, either genetic or ecological in nature. However, whether microbial speciation mirrors that of sexually reproducing eukaryotes is up for debate, as extensive horizontal gene flow can blur patterns and processes. Here, I provide intriguing examples of speciation in bacteria, viruses, and yeast, which are arguably similar to what we see in eukaryotes. I synthesise recent insights from microbial evolutionary genomics, which may mitigate the traditional view that microbes are 'messy' and do not fit eukaryotic species concepts and speciation models. Finally, I highlight the benefits of microbial experimental evolution to answer fundamental questions in speciation research (especially why, how and when speciation occurs). Speciation research with microbes, as opposed to the organisms traditionally used in this field, may suffer less from observational bias and the experimental control we have over selection types, gene flow, and reproductive modes in microbial systems may allow us to determine the mechanisms and timing of ecological divergence, reproductive isolation, and speciation.

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Overview of the Saccharomyces cerevisiae population structure through the lens of 3,034 genomes

Loegler,

Friedrich,

Schacherer

2024

G3: Genes, Genomes, Genetics

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With the rise of high-throughput sequencing technologies, a holistic view of genetic variation within populations—through population genomics studies—appears feasible, although it remains an ongoing effort. Genetic variation arises from a diverse range of evolutionary forces, with mutation and recombination being key drivers in shaping genomes. Studying genetic variation within a population represents a crucial first step in understanding the relationship between genotype and phenotype and the evolutionary history of species. In this context, the budding yeast Saccharomyces cerevisiae has been at the forefront of population genomic studies. In addition, it has a complex history that involves adaptation to a wide range of wild and human-related ecological niches. Although to date more than 3,000 diverse isolates have been sequenced, there is currently a lack of a resource bringing together sequencing data and associated metadata for all sequenced isolates. To perform a comprehensive analysis of the population structure of S. cerevisiae, we collected genome sequencing data from 3,034 natural isolates and processed the data uniformly. We determined ploidy levels, identified single nucleotide polymorphisms (SNPs), small insertion–deletions (InDels), copy number variations (CNVs), and aneuploidies across the population, creating a publicly accessible resource for the yeast research community. Interestingly, we showed that this population captures ∼93% of the species diversity. Using neighbor-joining and Bayesian methods, we redefined the populations, revealing clustering patterns primarily based on ecological origin. This work represents a valuable resource for the community and efforts have been made to make it evolvable and integrable to future yeast population studies.

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Ancient and recent origins of shared polymorphisms in yeast

Cited by 5 publications

References 99 publications

Gain- and loss-of-function alleles within signaling pathways lead to phenotypic diversity among individuals

Gain- and loss-of-function alleles within signaling pathways lead to phenotypic diversity among individuals

A microbial perspective on speciation

Overview of the Saccharomyces cerevisiae population structure through the lens of 3,034 genomes

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