Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity

Abstract

Myxobacteria and dictyostelids are prokaryotic and eukaryotic multicellular lineages, respectively, that after nutrient depletion aggregate and develop into structures called fruiting bodies. The developmental processes and resulting morphological outcomes resemble one another to a remarkable extent despite their independent origins, the evolutionary distance between them and the lack of traceable homology in molecular mechanisms. We hypothesize that the morphological parallelism between the two lineages arises as the consequence of the interplay within multicellular aggregates between generic processes, physical and physicochemical processes operating similarly in living and non-living matter at the mesoscale (~10–3–10–1 m) and agent-like behaviors, unique to living systems and characteristic of the constituent cells, considered as autonomous entities acting according to internal rules in a shared environment. Here, we analyze the contributions of generic and agent-like determinants in myxobacteria and dictyostelid development and their roles in the generation of their common traits. Consequent to aggregation, collective cell–cell contacts mediate the emergence of liquid-like properties, making nascent multicellular masses subject to novel patterning and morphogenetic processes. In both lineages, this leads to behaviors such as streaming, rippling, and rounding-up, as seen in non-living fluids. Later the aggregates solidify, leading them to exhibit additional generic properties and motifs. Computational models suggest that the morphological phenotypes of the multicellular masses deviate from the predictions of generic physics due to the contribution of agent-like behaviors of cells such as directed migration, quiescence, and oscillatory signal transduction mediated by responses to external cues. These employ signaling mechanisms that reflect the evolutionary histories of the respective organisms. We propose that the similar developmental trajectories of myxobacteria and dictyostelids are more due to shared generic physical processes in coordination with analogous agent-type behaviors than to convergent evolution under parallel selection regimes. Insights from the biology of these aggregative forms may enable a unified understanding of developmental evolution, including that of animals and plants.

The Shared Origins of Embodiment and Development

“…The organization that characterizes nonliving unities is not autopoietic, thus precluding them from having a perspective in the sense of the biological phenomenology of living systems that arises through their inherent autopoietic self-specification. This line of thinking remains an important background framework for studying the emergence of agency and autonomy in living systems, including research that probes the interface of mesoscale physical and physiochemical processes that are common to nonliving and living things and agentive behaviors of cellular systems that are unique to living organisms (Arias Del Angel et al, 2020).…”

Unicellular–multicellular evolutionary branching driven by resource limitations

“…Along with agent-like features of living cells, these generic properties associated with mesoscale physics (i.e. involving a spatial range of scales ∼10 −3 –10 −1 m) might be fundamental to understand the common evolutionary paths found in some types of MC [50].…”

Evolving social behaviour through selection of single-cell adhesion in Dictyostelium discoideum

“…Direct selection of a quantitative cell trait allowed us to factor out the effects of modified adhesion from those of broader genetic differences that occur in natural strains, and, unlike in mutagenized strains, to connect trait difference to their generative selection process. Chimeras containing the evolved lines and the Ancestor strain were used to assess the extent to which social behaviour can evolve as a byproduct of evolution of cell-level physical properties [40, 43]. We could interpret the resulting patterns of cell sorting based on associated variations in cell-substratum and cell-cell adhesion, and thus access the mechanisms underpinning alternative measures of social performance.…”