Development and Evolution: The Physics Connection

Newman, Stuart A.

doi:10.1007/978-94-017-9412-1_19

Cited by 5 publications

(1 citation statement)

References 111 publications

(92 reference statements)

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“…Properties shared by cellular masses with (as the case may be) non-living liquids, solids, or semisolid materials have been termed “generic” [ 42 ], and we adopt that term here. The physical forces, effects and processes inherent to such materials enable and constrain developmental outcomes in multicellular masses, leading to the conclusion that homoplasy (the same form, independently evolved) is expected to be common, and some morphological motifs should be recurrent and predictable [ 37 , 39 ]. Physical determinants, in this view, are complementary to the regulatory dynamics within cells.…”

Section: Introductionmentioning

confidence: 99%

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

Angel

Nanjundiah

Benítez

et al. 2020

EvoDevo

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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.

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Section: Introductionmentioning

confidence: 99%

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

Angel

Nanjundiah

Benítez

et al. 2020

EvoDevo

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D’Arcy Thompson and Synthetic Biology—Then and Now

Davies

2024

Biol Theory

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Though often presented as a recent scientific endeavor, synthetic biology began in the 19th century and was a particularly active field in the years preceding the publication of D’Arcy Thompson’s On Growth and Form. Much synthetic biology of the era was devoted to the construction of nonliving chemical systems that would undergo morphogenesis or dynamic behaviors which had been observed in living organisms. The point was to show that “life-like” structure and behavior could be generated by physicochemical laws and required no vitalist element. D’Arcy Thompson’s careful analysis of physicochemical morphogenetic mechanisms as possible explanations of organic form links closely to this way of thinking. In the modern era, when we can genetically engineer cells to undergo specific behaviors, and program cells to undergo simple morphogenetic behaviors of the kind that Thompson and others felt might underly natural morphogenesis, it is possible to test whether they will in fact produce a predictable multicellular shape. This addresses essentially the same questions about the morphogenetic role of physicochemical forces, such as surface tension, but does so “the other way round”: physicochemical mechanisms are not being used as models for morphogenesis by natural cells but rather as a means to engineer cells to make designed forms.

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A work in progress: William Bateson’s vibratory theory of repetition of parts

Rushton

2024

HPLS

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Development and Evolution: The Physics Connection

Cited by 5 publications

References 111 publications

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

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

D’Arcy Thompson and Synthetic Biology—Then and Now

A work in progress: William Bateson’s vibratory theory of repetition of parts

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