Evolution of developmental regulation in a simple multicellular life cycle

The evolution of multicellularity involved a transition in individuality from the level of the cell to the collective, requiring emergence of Darwinian properties at the group-level – most pertinent a mechanism for reproduction. This may be envisioned with a nascent multicellular life cycle that alternates between collective (‘soma’) & individual cell (‘germline’) phases. The bacterial model Pseudomonas fluorescens SBW25 was previously used to demonstrate the experimental evolution of such a life cycle. Though by virtue of using colony morphology (‘wrinkly’ & ‘smooth’) as a proxy for adaptation to each phase, lineages required mutation for phenotypic transitions.

This thesis explores the potential for evolution of developmental regulation of the life cycle. Chapter II characterises an environmentally-responsive strain that changes colony morphology with a shift in temperature, including reconstruction of the mutations necessary for the phenotypic switch. Chapter III then describes the production of a revised experimental regime, with new selective methods based on the traits of collective mat-formation & dispersal by swimming motility. In Chapter IV the results from a large-scale experiment are presented, in which rapid adaptation to the life cycle was observed after only five generations. Sequencing revealed the emergence of various unique strategies for developmental regulation of the life cycle, resulting from specific mutations in the c-di-GMP signalling pathway. For some evolved genotypes an increase in lineage fitness was not associated with a decrease to cell fitness; this trade-off breaking attributed to the capacity to modulate c-di-GMP level in response to the environment. These results shed light on the early origins of multicellularity, evolvability of the c-di-GMP network, and show how development can emerge by the tuning of existing regulatory pathways.

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