“The cost of being big: local competition, importance of dispersal, and experimental evolution of reversal to unicellularity”

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María Rebolleda-Gómez and Michael Travisano (Dec 2018)

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Multicellularity (staying-together) did not evolve on land: why? Potentially high competition and dispersal constraints

Multicellularity has evolved independently multiple times, and in many cases, unicellularity has evolved again from multicellular ancestors. Cancers, for example, are evolutionary reversals to unicellularity, in which cells no longer act as part of a larger coordinated whole, but as autonomous entities. Research in multicellularity has focused on these challenges of cooperation. However, cooperation and conflict are not the only challenges faced by multicellular organisms. The appearance of multicellular life is one of the biggest increases in size in the fossil record, and being big comes with challenges of its own.

In this study María Rebolleda-Gómez and Michael Travisano evaluated the costs of multicellularity in recently evolved multicellular phenotypes that evolved in the laboratory as a result of selection for increased size. Combining growth assays, competition experiments, computer simulations, and experimental evolution, they show that costs of resource acquisition and local competition can readily lead to the evolution of reversals to single cells. These costs depend on the size of the multicellular organisms, their ability to disperse and the distribution of resources. In liquid media—where resources are evenly distributed—multicellularity imposes spatial structure and internal cells have less space and/or fewer resources for growth. In contrast, on plates, despite similar growth between multicellular and unicellular isolates (because single cells cannot move away from each other during growth), multicellular isolates are rapidly outcompeted by their unicellular ancestor. In this environment, every time a subset of the population is established in a new plate, unicellular isolates can disperse better and are able to take advantage of more resources. Multicellular individuals are comprised of multiple cells that all compete for the same resources. As a result, selection on plates but not on liquid leads to rapid reversals to unicellularity.

Multicellularity has evolved independently more than 20 times with very different consequences in each of these transitions. A better understanding of the physical and ecological consequences of the morphological changes during the evolution of multicellularity can help us understand this multicellular diversity. Local competition and dispersal limitations may be among the reasons why most multicellular forms that develop through cells staying together have evolved in water, whereas most of the land origins of multicellularity involve single cells coming together temporarily (and often as a means for dispersal). Multicellularity transformed the physical space in which cells interact and this paper provides insight into the physical, ecological, and evolutionary limitations of this major transition.


Abstract

Multicellularity provides multiple benefits. Nonetheless, unicellularity is ubiquitous and there have been multiple cases of evolutionary reversal to a unicellular organization. In this paper, we explore some of the costs of multicellularity as well as the possibility and dynamics of evolutionary reversals to unicellularity. We hypothesize that recently evolved multicellular organisms would face a high cost of increased competition for local resources in spatially structured environments because of larger size and increased cell densities. To test this hypothesis we conducted competition assays, computer simulations, and selection experiments using isolates of Saccharomyces cerevisiae that recently evolved multicellularity. In well-mixed environments, multicellular isolates had lower growth rates relative to their unicellular ancestor due to limitations of space and resource acquisition. In structured environments with localized resources, cells in both multicellular and unicellular isolates grew at a similar rate. Despite similar growth, higher local density of cells in multicellular groups led to increased competition and higher fitness costs in spatially structured environments. In structured environments all of the multicellular isolates rapidly evolved a predominantly unicellular life cycle, while in well-mixed environments reversal was more gradual. Taken together, these results suggest that a lack of dispersal, leading to higher local competition, might have been one of the main constraints in the evolution of early multicellular forms.

El costo de ser grande: competencia local, importancia de dispersión y evolución experimental de reversiones a unicelularidad

Aunque la multicelularidad provee diversos beneficios, la vida unicelular es ubicua y ha habido varios casos de reversiones evolutivas a una forma de organización unicelular. En este artículo exploramos algunos de los costos de la multicelularidad, así como la posibilidad y las dinámicas de reversión a la unicelularidad. Nuestra hipótesis es que, en ambientes con estructura espacial, organismos que evolucionaron multicellularidad recientemente, van a enfrentar mayores costos asociados con una mayor competencia por los recursos locales, debido a que los organismos multicelulares tienen un mayor tamaño y mayores densidades celulares. Para evaluar esta hipótesis, realizamos ensayos de competencia, simulaciones de computadora y evolución experimental con aislados de Saccharomyces cerevisiae que recientemente evolucionaron fenotípos multicelulares. En ambientes con agitación constante, los aislados multicellulares tienen menores tasas de crecimiento que su ancestro unicelular debido a limitaciones de espacio y adqusición de recursos. En ambientes espacialmente estructurados, con recursos localizados, las células de aislados unicelulares y multicelulares crecen a la misma velocidad. Sin embargo, la mayor densidad local de células en grupos multicelulares resultó en mayor competencia y costos de adecuación en ambientes con estructura espacial. En estos ambientes con recursos localizados todos los aislados multicelulares evolucionaron un ciclo de vida principalmente unicelular, mientras que en ambientes con una distribución más homogénea la reversión a unicelularidad fue mucho más gradual. Juntos, estos resultados sugieren que la falta de dispersión, que resulta en una mayor competencia, puede haber sido una de las principales restricciones en la evolución de las primeras formas multicelulares.