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Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity
EvoDevo ( IF 4.1 ) Pub Date : 2020-10-12 , DOI: 10.1186/s13227-020-00165-8
Juan A. Arias Del Angel , Vidyanand Nanjundiah , Mariana Benítez , Stuart A. Newman

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.

中文翻译:

聚合多细胞性平行进化中中尺度物理学和类代理行为的相互作用

粘细菌和双歧硬皮动物分别是原核和真核多细胞谱系,在营养耗尽后聚集并发展成称为子实体的结构。尽管它们的独立起源,它们之间的进化距离以及分子机制中缺乏可追溯的同源性,但它们的发育过程和所产生的形态学结果在很大程度上相似。我们假设这两个谱系之间的形态平行性是多细胞聚集体之间相互作用的结果,该过程是在中尺度(〜10–3–10–1 m )和类似代理的行为,这是生命系统所特有的,并且是组成细胞的特征,被视为在共享环境中根据内部规则行事的自治实体。在这里,我们分析了类固醇决定因子在粘菌和双歧杆菌发育中的贡献及其在它们共同特征产生中的作用。聚集的结果是,细胞间的集体接触介导了液体状特性的出现,使新生的多细胞团块经受了新的模式和形态发生过程。在两个谱系中,这都会导致诸如非生命体中所见的流,波纹和舍入等行为。后来,骨料凝固,导致它们表现出其他一般性质和图案。计算模型表明,由于对外部线索的反应介导的定向迁移,静止和振荡信号转导等细胞的试剂样行为的贡献,多细胞团的形态表型与一般物理学的预测有所不同。这些采用反映各自生物进化历史的信号传导机制。我们提出,粘菌和双歧硬壳动物的相似发展轨迹更多是由于与相似的媒介类型行为协调的共同的通用物理过程,而不是平行选择机制下的趋同进化。这些聚集形式的生物学见解可以使人们对包括动物和植物在内的发育进化有一个统一的认识。
更新日期:2020-10-13
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