Abstract
Filamentous bacteria are the oldest and simplest known multicellular life forms. By using computer simulations and experiments that address cell division in a filamentous context, we investigate some of the ecological factors that can lead to the emergence of a multicellular life cycle in filamentous life forms. The model predicts that if cell division and death rates are dependent on the density of cells in a population, a predictable cycle between short and long filament lengths is produced. During exponential growth, there will be a predominance of multicellular filaments, while at carrying capacity, the population converges to a predominance of short filaments and single cells. Model predictions are experimentally tested and confirmed in cultures of heterotrophic and phototrophic bacterial species. Furthermore, by developing a formulation of generation time in bacterial populations, it is shown that changes in generation time can alter length distributions. The theory predicts that given the same population growth curve and fitness, species with longer generation times have longer filaments during comparable population growth phases. Characterization of the environmental dependence of morphological properties such as length, and the number of cells per filament, helps in understanding the pre-existing conditions for the evolution of developmental cycles in simple multicellular organisms. Moreover, the theoretical prediction that strains with the same fitness can exhibit different lengths at comparable growth phases has important implications. It demonstrates that differences in fitness attributed to morphology are not the sole explanation for the evolution of life cycles dominated by multicellularity.
Highlights
Multicellularity is an organizational characteristic present in the majority of organisms whose size surpasses microbial scales
In order to assure that the experimental dataset and the simulation data are comparable, we indicate with a dotted line the time point where the bacterial populations reach their carrying capacity on each plot of the experimental results
In order to prove the significant increase and decrease of bacterial filament length, we performed an ANOVA test associated with a multiple comparison on the data based on Tukey’s HSD test [69]
Summary
Multicellularity is an organizational characteristic present in the majority of organisms whose size surpasses microbial scales. Phylogenetic inference suggests that evolutionary transitions to multicellularity have occurred several times during the history of life [1 – 6]. Despite its fundamental importance, it is difficult to empirically study the evolutionary and ecological forces that may lead to a transition from single-celled to multicellular organization. One set of theoretical explanations are based on examining the consequences of a shift between units of selection. These approaches consider the changing boundaries of an individual after a transition to multicellularity, and how the different activities of component cells can potentially lead to synergies that increase the fitness. Experimental results concerning social evolution in microbes are largely compatible with this perspective [9 – 14]
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