Two-Dimensionality of Yeast Colony Expansion Accompanied by Pattern Formation

Chen, Lin; Noorbakhsh, Javad; Adams, Rhys M.; Samaniego-Evans, Joseph; Agollah, Germaine D.; Nevozhay, Dmitry; Kuzdzal‐Fick, Jennie J.; Mehta, Pankaj; Balázsi, Gábor

doi:10.1371/journal.pcbi.1003979

Cited by 45 publications

(78 citation statements)

References 54 publications

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“…For example, range expansions of microbial populations have revealed the dependence of the invasion velocity on the supply of resources (37) and demographic stochasticity (33). Experiments with microbes have also demonstrated the strong effect of range expansion on competition (38)(39)(40)(41)(42)(43)(44) and neutral evolution via the founder effect or gene surfing (45,46). In this study, we focus on expansions with and without the Allee effect and quantify their differences.…”

Section: Significancementioning

confidence: 99%

Range expansions transition from pulled to pushed waves as growth becomes more cooperative in an experimental microbial population

Gandhi

Yurtsev

Korolev

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

117

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Range expansions are becoming more frequent due to environmental changes and rare long-distance dispersal, often facilitated by anthropogenic activities. Simple models in theoretical ecology explain many emergent properties of range expansions, such as a constant expansion velocity, in terms of organism-level properties such as growth and dispersal rates. Testing these quantitative predictions in natural populations is difficult because of large environmental variability. Here, we used a controlled microbial model system to study range expansions of populations with and without intraspecific cooperativity. For noncooperative growth, the expansion dynamics were dominated by population growth at the low-density front, which pulled the expansion forward. We found these expansions to be in close quantitative agreement with the classical theory of pulled waves by Fisher [Fisher RA (1937) Ann Eugen 7(4):355-369] and Skellam [Skellam JG (1951) Biometrika 38(1-2):196-218], suitably adapted to our experimental system. However, as cooperativity increased, the expansions transitioned to being pushed, that is, controlled by growth and dispersal in the bulk as well as in the front. Given the prevalence of cooperative growth in nature, understanding the effects of cooperativity is essential to managing invading species and understanding their evolution.Allee effect | Fisher wave | biological invasion F rom a local disturbance by an invasive species to the global expansion of the biosphere after an ice age, range expansions have been a major ecological and evolutionary force (1, 2). Range expansions and range shifts are becoming increasingly frequent due to the deliberate introduction of foreign species (3, 4), unintentional introductions caused by global shipping (5), and temperature changes associated with climate change (6, 7). Many invasions disturb ecosystem functions, reduce biodiversity, and impose significant economic costs (8, 9). The interest in invasion forecasting and management resulted in a substantial effort to develop predictive mathematical models of range expansions (4, 10-13), but empirical tests of these models have been less extensive.Species invade new territory through a combination of dispersal and local growth. Mathematically, these dynamics can be described by a variety of models depending on the details of the species ecology or simplifying assumptions (14). For example, the invasion of house finches in North America has been successfully modeled with integrodifference equations (4). Continuous reactiondiffusion equations have been used to describe the expansion of trees following the end of an ice age and the expansion of muskrats from central Europe (15), whereas metapopulation models with disjoint patches of suitable habitat and discrete generations are more appropriate for certain butterflies living in temperate climates (16). One of the great achievements of mathematical ecology is the discovery that all these diverse models of population expansion can be divided into two broad classes of pulled...

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Section: Significancementioning

confidence: 99%

Range expansions transition from pulled to pushed waves as growth becomes more cooperative in an experimental microbial population

Gandhi

Yurtsev

Korolev

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

117

View full text Add to dashboard Cite

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“…Contrary to the classical definition of yeasts as single-celled fungi, some Saccharomyces cerevisiae strains exhibit multicellular phenotypes (Andersen et al, 2014;Cap, Vachova, & Palkova, 2012;Reynolds & Fink, 2001), such as aggregation into flocs (Smukalla et al, 2008), flors (Zara, Zara, Pinna, Marceddu, & Budroni, 2009), and pattern formation on agar plates (Chen et al, 2014;Kuthan et al, 2003;Reynolds & Fink, 2001). Other yeast strains form multicellular "clumps" that differ from flocs and flors in their mechanism of formation and underlying genetics (Li et al, 2013).…”

mentioning

confidence: 97%

Disadvantages and benefits of evolved unicellularity versus multicellularity in budding yeast

Kuzdzal‐Fick

Chen

Balázsi

2019

Ecology and Evolution

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Multicellular organisms appeared on Earth through several independent major evolutionary transitions. Are such transitions reversible? Addressing this fundamental question entails understanding the benefits and costs of multicellularity versus unicellularity. For example, some wild yeast strains form multicellular clumps, which might be beneficial in stressful conditions, but this has been untested. Here, we show that unicellular yeast evolve from clump‐forming ancestors by propagating samples from suspension after larger clumps have settled. Unicellular yeast strains differed from their clumping ancestors mainly by mutations in the AMN1 (Antagonist of Mitotic exit Network) gene. Ancestral yeast clumps were more resistant to freeze/thaw, hydrogen peroxide, and ethanol stressors than their unicellular counterparts, but they grew slower without stress. These findings suggest disadvantages and benefits to multicellularity and unicellularity that may have impacted the emergence of multicellular life forms.

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“…Next, consider range expansion in 2D (e.g. yeast colony expansion [25], 2D melanoma cultures [26,27], where the population grows outward as an expanding circle. In this case, the total population follows the so-called surface growth: N~t 2 .…”

Section: Growth Laws For Neutral Advantageous and Disadvantageous Mmentioning

confidence: 99%

Mutant evolution in spatially structured and fragmented populations

Wodarz

Komarova

2019

Preprint

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Understanding mutant evolution in spatially structured systems is crucially important for a range of biological systems, including bacterial populations and cancer. While previous work has shown that the mutation load is higher in spatially structured compared to well-mixed systems for neutral mutants in the absence of cell death, we demonstrate a significantly higher degree of complexity, using a comprehensive computational modeling approach that takes into account different mutant fitness, cell death, and different population structures. While an agent-based model assuming nearest neighbor interactions predicts a higher abundance of neutral or advantageous mutants compared to well-mixed systems of the same size, we show that for disadvantageous mutants, results depend on the nature of the disadvantage. In particular, if the disadvantage occurs through higher death rates, as opposed to lower reproduction rates, the result is the opposite, and a lower mutation load occurs in spatial compared to mixed systems. Interestingly, we show that in all cases, the same results are observed in fragmented patch models, where individuals can migrate to randomly chosen patches, thus lacking a strict spatial component. Hence, the results reported for spatial models are the consequence of population fragmentation, and not spatial restrictions per se. We further derive growth laws that characterize the expansion of wild type and mutant populations in different dimensionalities. For example, we find that while disadvantageous mutant abundance scales with the total population size, N, neutral mutants grow faster (as N 2 for 1D, as N 3/2 in 2D, and as N 4/3 in 3D). Advantageous mutants scale with the cube of N in 1D and with the square of N in higher dimensions. These laws are universal (as long as mutants remain a minority) and independent of "microscopic" modeling details.

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Two-Dimensionality of Yeast Colony Expansion Accompanied by Pattern Formation

Cited by 45 publications

References 54 publications

Range expansions transition from pulled to pushed waves as growth becomes more cooperative in an experimental microbial population

Range expansions transition from pulled to pushed waves as growth becomes more cooperative in an experimental microbial population

Disadvantages and benefits of evolved unicellularity versus multicellularity in budding yeast

Mutant evolution in spatially structured and fragmented populations

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