Abstract

Understanding how and why cells cooperate to form multicellular organisms is a central aim of evolutionary biology. Multicellular groups can form through clonal development (where daughter cells stick to mother cells after division) or by aggregation (where cells aggregate to form groups). These different ways of forming groups directly affect relatedness between individual cells, which in turn can influence the degree of cooperation and conflict within the multicellular group. It is hard to study the evolution of multicellularity by focusing only on obligately multicellular organisms, like complex animals and plants, because the factors that favour multicellular cooperation cannot be disentangled, as cells cannot survive and reproduce independently. We support the use of Saccharomyces cerevisiae as an ideal model for studying the very first stages of the evolution of multicellularity. This is because it can form multicellular groups both clonally and through aggregation and uses a family of proteins called ‘flocculins’ that determine the way in which groups form, making it particularly amenable to laboratory experiments. We briefly review current knowledge about multicellularity in S. cerevisiae and then propose a framework for making predictions about the evolution of multicellular phenotypes in yeast based on social evolution theory. We finish by explaining how S. cerevisiae is a particularly useful experimental model for the analysis of open questions concerning multicellularity.

Highlights

  • Multicellular organisms dominate the world we see around us, and yet they are formed from millions of individual cells that specialize on different tasks and cooperate to form a cohesive body

  • We briefly review current knowledge about group formation and multicellularity in S. cerevisiae and propose a framework for making predictions about the evolution of multicellular phenotypes in yeast based on social evolution theory

  • There has been a wealth of research on multicellularity in yeast on mechanisms [28,29,30] and social evolution [4,15,23,63,64]

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Summary

Introduction

Multicellular organisms dominate the world we see around us, and yet they are formed from millions of individual cells that specialize on different tasks and cooperate to form a cohesive body. The slime mould Dictyostelium discoideum and other species that form groups through aggregation remain able to switch between unicellularity and multicellularity, making them facultatively multicellular (figure 1) As a consequence, they have a lower number of cell types and are generally smaller, compared to species that form multicellular groups through clonal development [7]. We propose bakers yeast, Saccharomyces cerevisiae, as an ideal model for studying the very first stages of the evolution of multicellularity as a major evolutionary transition in individuality (figure 1) This is because: (i) it is able to switch between unicellularity and multicellularity, (ii) it can do this 2 through both modes of group formation (clonal development and aggregation), and (iii) it is a well-studied, genetically tractable model organism. We suggest terminology that is general and useful, and we finish by suggesting outstanding questions and potentially fruitful avenues for future research

Why is group formation important?
Multicellularity in yeast: a major evolutionary transition?
How does Saccharomyces cerevisiae become multicellular?
Multicellularity and susceptibility to cheating
Facultative multicellularity in Saccharomyces cerevisiae
Saccharomyces cerevisiae in the laboratory
Experimental evolution of multicellularity
Concluding remarks
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