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Review
. 2020 Oct 12:11:21.
doi: 10.1186/s13227-020-00165-8. eCollection 2020.

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

Affiliations
Review

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

Juan A Arias Del Angel et al. Evodevo. .

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.

Keywords: Deformable solids; Dictyostelids; Excitable media; Liquid tissues; Myxobacteria.

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Conflict of interest statement

Competing interestsThe authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Life cycles of prokaryotic and eukaryotic aggregative microorganisms. (Upper panel) Life cycle of Myxobacteria xanthus, a representative multicellular myxobacterium. The circle on the left represents the proliferative mode that occurs in a nutrient-replete setting. The oval on the right shows the sequence of stages initiated under conditions of starvation: clockwise, from top left, aggregation, mound formation, fruiting body formation and spore differentiation. Spores can be dispersed and may germinate as single vegetative cells under nutrient-rich conditions. (Lower panel) Life cycle of Dictyostelium discoideum, a representative dictyostelid. The circle on the left represents the proliferative mode that occurs in a nutrient-replete setting. The oval on the right shows the sequence of stages initiated under conditions of starvation (clockwise, from top left: starved amoebae, developing aggregation, late aggregations, migrating slug, developing fruiting body, finished fruiting body with spore mass supported by an erect stalk, amoebae emerging from spores after dispersal)
Fig. 2
Fig. 2
Generic physical effects and agent-like behaviors that contribute to multicellular development in aggregative forms. (Left, top) A selection of generic multicellular properties and their mediators, such as adhesion and extracellular matrix embedment. (Left, bottom) A selection of agent-like effects. Some individual cell behaviors such as oscillation of biochemical state or shape or functional polarity can, when they operate in the multicellular context, mediate global generic effects, like morphogenetic fields in which cell state is coordinated over large distances. (Right) Generic processes can lead to convergent morphologies since they employ the same mesoscale physics despite genetic divergence. Agent-based processes can lead to lineage-specific behaviors and morphological motifs, but also convergent or parallel ones if they act in analogous fashions. See main text for additional examples of generic and agent effects and descriptions of their morphogenetic roles

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