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 the resulting morphological outcomes resemble one another to a remarkable extent despite their independent origins, the evolutionary distance between them and the lack of traceable levels of homology in the molecular mechanisms of the groups. 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, characteristic of the constituent cells. To this effect, we analyze the relative contribution of the generic and agent-like determinants in the main phenomena of myxobacteria and dictyostelid development, and their roles in the emergence of their shared traits. We show that as a consequence of aggregation collective cell-cell contacts mediate the emergence of liquid-like properties, making nascent multicellular masses subject to new sets of patterning and morphogenetic processes. In both lineages, this leads to behaviors such as streaming, rippling, and rounding up, similar to effects observed in non-living fluids. Later the aggregates solidify, leading them to exhibit additional generic properties and motifs. We consider evidence that the morphological phenotypes of the multicellular masses deviate from the predictions of generic physics due to the contribution of agent-like behaviors. These include directed migration, quiescence, and oscillatory signal transduction of the cells mediated by responses to external cues acting through species-specific regulatory and signaling mechanisms reflecting the evolutionary histories of the respective organisms. We suggest that the similar developmental trajectories of Myxobacteria and Dictyostelia are more plausibly due to shared generic physical processes in coordination with analogous agent-type behaviors than to convergent evolution under parallel selection regimes. Finally, we discuss the broader implications of the existence and synergy of these two categories of developmental factors for evolutionary theory.