Evolutionary dynamics of nascent multicellular lineages

Abstract

The evolution of multicellular organisms involves the emergence of cellular collectives that eventually become units of selection in their own right. The process can be facilitated by ecological conditions that impose heritable variance in fitness on nascent collectives, with long-term persistence depending on the capacity of competing lineages to transition reliably between soma- and germ-like stages of proto-life cycles. Prior work with experimental bacterial populations showed rapid increases in collective-level fitness, with the capacity to switch between life cycle phases being a particular focus of selection. Here, we report experiments in which the most successful lineage from the earlier study was further propagated for 10 life cycle generations under regimes that required different investments in the soma-like phase. To explore the adaptive significance of switching, a control was included in which reliable transitioning between life cycle phases was abolished. The switch proved central to the maintenance of fitness. Moreover, in a non-switch treatment, where solutions to producing a robust and enduring soma-phase were required, the evolution of mutL-dependent switching emerged de novo. A newly developed computational pipeline (colgen) was used to display the moment-by-moment evolutionary dynamics of lineages, providing rare visual evidence of the roles of chance, history and selection. Colgen, underpinned by a Bayesian model, was further used to propagate hundreds of mutations back through temporal genealogical series, predict lineages and time points corresponding to changes of likely adaptive significance, and in one instance, via a combination of targeted sequencing, genetics and analyses of fitness consequences, the adaptive significance of a single mutation was demonstrated. Overall, our results shed light on the mechanisms by which collectives adapt to new selective challenges and demonstrate the value of genealogy-centred approaches for investigating the dynamics of lineage-level selection.