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

Abstract

22Myxobacteria and dictyostelids are prokaryotic and eukaryotic multicellular lineages, 23 respectively, that after nutrient depletion aggregate and develop into structures called fruiting 24 bodies. The developmental processes and the resulting morphological outcomes resemble one 25 another to a remarkable extent despite their independent origins, the evolutionary distance 26 between them and the lack of traceable levels of homology in the molecular mechanisms of the 27 groups. We hypothesize that the morphological parallelism between the two lineages arises as 28 the consequence of the interplay, within multicellular aggregates, between generic processes, 29 physical and physicochemical processes operating similarly in living and non-living matter at the 30 mesoscale (~10 -3 -10 -1 m) and agent-like behaviors, unique to living systems, characteristic of 31 the constituent cells. To this effect, we analyze the relative contribution of the generic and 32 agent-like determinants in the main phenomena of myxobacteria and dictyostelid development, 33and their roles in the emergence of their shared traits. We show that as a consequence of 34 aggregation collective cell-cell contacts mediate the emergence of liquid-like properties, making 35 nascent multicellular masses subject to new sets of patterning and morphogenetic processes. In 36 both lineages, this leads to behaviors such as streaming, rippling, and rounding up, similar to 37 effects observed in non-living fluids. Later the aggregates solidify, leading them to exhibit 38 additional generic properties and motifs. We consider evidence that the morphological 39 phenotypes of the multicellular masses deviate from the predictions of generic physics due to 40 the contribution of agent-like behaviors. These include directed migration, quiescence, and 41 oscillatory signal transduction of the cells mediated by responses to external cues acting 42 through species-specific regulatory and signaling mechanisms reflecting the evolutionary 43 histories of the respective organisms. We suggest that the similar developmental trajectories of 44 Myxobacteria and Dictyostelia are more plausibly due to shared generic physical processes in 45 coordination with analogous agent-type behaviors than to convergent evolution under parallel 46 selection regimes. Finally, we discuss the broader implications of the existence and synergy of 47 these two categories of developmental factors for evolutionary theory.48 49 Key words: myxobacteria; dictyostelids; liquid tissues; deformable solids; excitable 50 media 51 of multicellular structures called fruiting bodies, containing up to 10 5 -10 6 cells, where cell 85 differentiation takes place (Whitworth, 2008). 86The basis of cell differentiation in D. discoideum has been explained in two ways. There are 87 pre-aggregation tendencies among amoebae, stochastic in origin, biased by the environment 88 they experienced during the phases of growth and division, or, cell differentiation is a post-89 aggregation phenomenon based on intercellular inte...

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

“…In this work, we explored how selection acting on single-cell properties affects collective behaviour in cellular populations. Understanding how single-cell properties shape adaptations to collective living is key to explore possible evolutionary scenarios leading from unicellular to multicellular life cycles [9, 40, 41] In our experimental design, selection on cell-substrate adhesion is applied to the ‘social amoeba’ D. discoideum at the unicellular stage of its life cycle, thus it does not act directly on social traits. Two evolved strains were obtained, that have higher (Bottom) and lower (Top) substrate adhesion with respect to their common ancestor.…”

“…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 derived and the Ancestor strains 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-substrate and cell-cell adhesion, and thus access the mechanisms underpinning alternative measures of social performance.…”

The environment topography alters the transition from single-cell populations to multicellular structures inMyxococcus xanthus

“…Various concepts from the field of soft and active matter have already been employed to understand the mechanisms underlying M. xanthus transition to multicellularity (Vicsek & Zafeiris, 2012;Starruß, et al, 2012;Bahar et al, 2014;Thutupalli et al, 2015;Liu et al, 2019, Arias Del Angel et al, 2020. For example, the dynamic formation, shrinkage and growth of cellular aggregates that ultimately produce fruiting bodies has been to some extent described as a droplet formation process in thin liquid films (Bahar et al, 2014) and as a phase separation driven by cells that change their motility over time (Thutupalli et al, 2015;Liu et al, 2019).…”