Testing the adaptive value of sporulation in budding yeast using experimental evolution

Thomasson, Kelly M.; Franks, Alexander; Teotónio, Henrique; Proulx, Stephen R.

doi:10.1111/evo.14265

Cited by 4 publications

(6 citation statements)

References 34 publications

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“…Higher frequencies of admixed isolates observed in fruits may simply be a result of increased contacts with other lineages. Alternatively, fruits and organisms associated with those fruits such as frugivorous animals and vectors may represent niches that promote hybridization; for instance, sporulation has been suggested to be an adaptation that allows cells to survive in nutrient-depleted conditions such as insects' intestines during experimental passaging (Thomasson et al 2021). Notably, the presence of CHN-VI/VII.2 genetic components in many natural lineages across the world, as well as in admixed isolates found in fruits, raises the possibility that the common ancestors dispersed from East Asia were from this lineage.…”

Section: Discussionmentioning

confidence: 99%

Extensive sampling of Saccharomyces cerevisiae in Taiwan reveals ecology and evolution of predomesticated lineages

Lee

Liu

et al. 2022

Genome Res.

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The ecology and genetic diversity of model yeast Saccharomyces cerevisiae prior to human domestication remain poorly understood. Taiwan is regarded as part of this yeast's geographic birthplace where the most divergent natural lineage was discovered. Here, we extensively sampled the broad-leaf forests across this continental island to probe the ancestral species diversity. We found that S. cerevisiae is distributed ubiquitously at low abundance in the forests. Whole-genome sequencing of 121 isolates revealed nine distinct lineages that diverged from Asian lineages during the Pleistocene, when a transient continental shelf land bridge connected Taiwan to other major landmasses. Three lineages are endemic to Taiwan and six are widespread in Asia, making this region a focal biodiversity hotspot. Both ancient and recent admixture events were detected between natural lineages and a genetic ancestry component associated with isolates from fruits was detected in most admixed isolates. Collectively, Taiwanese isolates harbor genetic diversity comparable to that of the whole Asia continent, and different lineages have coexisted at a fine spatial scale even on the same tree. Patterns of variations within each lineage revealed that S. cerevisiae is highly clonal and predominantly reproduces asexually in nature. We identified different selection patterns shaping the coding sequences of natural lineages and found fewer gene family expansion and contractions which contrast with domesticated lineages. This study establishes that S. cerevisiae has rich natural diversity sheltered from human influences, making it a powerful model system in microbial ecology.

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Section: Discussionmentioning

confidence: 99%

Extensive sampling of Saccharomyces cerevisiae in Taiwan reveals ecology and evolution of predomesticated lineages

Lee

Liu

et al. 2022

Genome Res.

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“…Yeast sporulation tends to be triggered by chemical conditions that correlate with depletion of sugars and crowding of yeast (Neiman, 2005). Natural yeast isolates do vary in their propensity to sporulate (Liti et al, 2009), and vary in their ability to evolve increased sporulation rates (Thomasson et al, 2021). Less is known about how sporulation proceeds under natural conditions and to what extent sporulation represents a facultative program.…”

Section: Discussionmentioning

confidence: 99%

Selection on sporulation strategies in a metapopulation can lead to coexistence

Proulx,

Sakal,

Thomasson

2024

Preprint

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In constant environments the coexistence of similar species or genotypes is generally limited. In a metapopulation context, however, types that utilize the same resource but are distributed along a competition-coexistence trade-off, can coexist. Much thought in this area focuses on a generic trade-off between within-deme competitive ability and between-deme dispersal ability. We point out that the sporulation program in yeasts and other microbes can create a natural trade-off such that strains which initiate sporulation at higher rates suffer in terms of within-deme competition but benefit in terms of between deme dispersal. We develop simple metapopulation models where the within-deme behavior follows simple chemostat dynamics. We first show that the rate of sporulation determines the colonization ability of the strain, with colonization ability increasing with sporulation rate up to a point. Metapopulation stability of a single strain exists in a defined range of sporulation rates. We then use pairwise invasability plots to show that coexistence of strains with different sporulation rates generally occurs, but that the set of sporulation rates that can potentially coexist is smaller than the set that allows for stable metapopulations. We then extend our pairwise results to show how a continuous set of strains can coexist and verify our conclusions with numerical calculations. Our results show that stable variation in sporulation rates is expected under a wide range of ecological conditions.

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“…Alternatively, enhanced sporulation in killer yeast may be an adaptation to predation. Thomasson et al (2021) demonstrated that sporulation is an adaptive trait, and that insect passaging selects for yeasts with higher rates of spore production. Drosophila attraction varies across yeast strains (Buser et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…This would suggest that predation by insects has influenced their evolution (Thomasson et al, 2021).…”

mentioning

confidence: 99%

Infection by dsRNA viruses is associated with enhanced sporulation efficiency in Saccharomyces cerevisiae

Travers-Cook

Skirgaila

Martin

et al. 2022

Ecology and Evolution

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Upon starvation diploid cells of the facultative sexual yeast Saccharomyces cerevisiae undergo sporulation, forming four metabolically quiescent and robust haploid spores encased in a degradable ascus. All endosymbionts, whether they provide net benefits or costs, utilize host resources; in yeast, this should induce an earlier onset of sporulation. Here, we tested whether the presence of endosymbiotic dsRNA viruses (M satellite and L‐A helper) correspond with higher sporulation rate of their host, S. cerevisiae. We find that S. cerevisiae hosting both the M and L‐A viruses (so‐called “killer yeasts”) have significantly higher sporulation efficiency than those without. We also found that the removal of the M virus did not reduce sporulation frequency, possibly because the L‐A virus still utilizes host resources with and without the M virus. Our findings indicate that either virulent resource use by endosymbionts induces sporulation, or that viruses are spread more frequently to sporulating strains. Further exploration is required to distinguish cause from effect.

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Testing the adaptive value of sporulation in budding yeast using experimental evolution

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Cited by 4 publications

References 34 publications

Extensive sampling of Saccharomyces cerevisiae in Taiwan reveals ecology and evolution of predomesticated lineages

Extensive sampling of Saccharomyces cerevisiae in Taiwan reveals ecology and evolution of predomesticated lineages

Selection on sporulation strategies in a metapopulation can lead to coexistence

Infection by dsRNA viruses is associated with enhanced sporulation efficiency in Saccharomyces cerevisiae

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