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

View ORCID ProfileJuan A. Arias Del Angel, View ORCID ProfileVidyanand Nanjundiah, Mariana Benítez, View ORCID ProfileStuart A. Newman
doi: https://doi.org/10.1101/2020.06.03.133025
Juan A. Arias Del Angel
1Laboratorio Nacional de Ciencias de la Sostenibilidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad de México, México
2Centro de Ciencias de la Complejidad, Universidad Nacional Autónoma de México, Ciudad de México, México
3Department of Cell Biology and Anatomy, New York Medical College, Valhalla, NY 10595, USA
4Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México, México
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Vidyanand Nanjundiah
5Centre for Human Genetics, Electronic City (Phase I), Bengaluru 560100, India
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Mariana Benítez
1Laboratorio Nacional de Ciencias de la Sostenibilidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad de México, México
2Centro de Ciencias de la Complejidad, Universidad Nacional Autónoma de México, Ciudad de México, México
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Stuart A. Newman
3Department of Cell Biology and Anatomy, New York Medical College, Valhalla, NY 10595, USA
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  • For correspondence: newman@nymc.edu
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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.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵† d. 2019

  • Contact: mbenitez{at}iecologia.unam.mx (MB); vidyan{at}alumni.iisc.ac.in (VN); newman{at}nymc.edu (SAN)

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 04, 2020.
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Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity
Juan A. Arias Del Angel, Vidyanand Nanjundiah, Mariana Benítez, Stuart A. Newman
bioRxiv 2020.06.03.133025; doi: https://doi.org/10.1101/2020.06.03.133025
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Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity
Juan A. Arias Del Angel, Vidyanand Nanjundiah, Mariana Benítez, Stuart A. Newman
bioRxiv 2020.06.03.133025; doi: https://doi.org/10.1101/2020.06.03.133025

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