Vroomans, R. M. | Search bioRxiv

bioRxiv2022

Evolution of selfish multicellularity: collective organisation of individual spatio-temporal regulatory strategies

BackgroundThe unicellular ancestors of modern-day multicellular organisms were remarkably complex. They had an extensive set of regulatory and signalling genes, an intricate life cycle and could change their behaviour in response to environmental changes. At the transition to multicellularity, some of these behaviours were co-opted to organise the development of the nascent multicellular organism. Here, we focus on the transition to multicellularity before the evolution of stable cell differentiation, to reveal how the emergence of clusters affects the evolution of cell behaviour. ResultsWe construct a computational model of a population of cells that can evolve the regulation of their behavioural state - either division or migration - in a unicellular or multicellular context. They compete for reproduction and for resources to survive in a seasonally changing environment. We find that the evolution of multicellularity strongly determines the co-evolution of cell behaviour, by altering the competition dynamics between cells. When adhesion cannot evolve, cells compete for survival by rapidly migrating towards resources before dividing. When adhesion evolves, emergent collective migration alleviates the pressure on individual cells to reach resources. This allows cells to selfishly maximise replication. Migrating adhesive clusters display striking patterns of spatio-temporal cell state changes that visually resemble animal development. ConclusionsOur model demonstrates how emergent selection pressures at the onset of multicellularity can drive the evolution of cellular behaviour to give rise to developmental patterns.

evolutionary biology↗

bioRxiv2021

Evolution of genome fragility enables microbial division of labor

Division of labor can evolve when social groups benefit from the functional specialization of its members. Recently, a novel means of coordinating division of labor was found in the antibiotic-producing bacterium Streptomyces coelicolor, where functionally specialized cells are generated through large-scale genomic re-organization. Here, we investigate how the evolution of a genome architecture enables such mutation-driven division of labor, using a multi-scale mathematical model of bacterial evolution. We let bacteria compete on the basis of their antibiotic production and growth rate in a spatially structured environment. Bacterial behavior is determined by the structure and composition of their genome, which encodes antibiotics, growth-promoting genes and fragile genomic loci that can induce chromosomal deletions. We find that a genomic organization evolves that partitions growth-promoting genes and antibiotic-coding genes to distinct parts of the genome, separated by fragile genomic loci. Mutations caused by these fragile sites mostly delete growth-promoting genes, generating antibiotic-producing mutants from non-producing (and weakly-producing) progenitors, in agreement with experimental observations. Mutants protect their colony from competitors but are themselves unable to replicate. We further show that this division of labor enhances the local competition between colonies by promoting antibiotic diversity. These results show that genomic organization can co-evolve with genomic instabilities to enable reproductive division of labor. Motivation of current workDivision of labor can evolve if trade-offs are present between different traits. To organize a division of labor, the genome architecture must evolve to enable differentiated cellular phenotypes. Cell differentiation may be coordinated through gene regulation, as occurs during embryonic development. Alternatively, when mutation rates are high, mutations themselves can guide cell and functional differentiation; however, how this evolves and is organized at the genome level remains unclear. Here, using a model of antibiotic-producing bacteria based on multicellular Streptomyces, we show that if antibiotic production trades off with replication, genome architecture can evolve to support a mutation-driven division of labor. These results are consistent with recent experimental observations and may underlie division of labor in many bacterial groups.

evolutionary biology↗