Allen Discovery Center at Tufts University, 200 Boston Ave. 334 Research East, Medford, MA, 02155, USA.
Wyss Institute for Biologically Inspired Engineering at Harvard University, 3 Blackfan St., Boston, MA, 02115, USA.
Cell Mol Life Sci. 2023 May 8;80(6):142. doi: 10.1007/s00018-023-04790-z.
A critical aspect of evolution is the layer of developmental physiology that operates between the genotype and the anatomical phenotype. While much work has addressed the evolution of developmental mechanisms and the evolvability of specific genetic architectures with emergent complexity, one aspect has not been sufficiently explored: the implications of morphogenetic problem-solving competencies for the evolutionary process itself. The cells that evolution works with are not passive components: rather, they have numerous capabilities for behavior because they derive from ancestral unicellular organisms with rich repertoires. In multicellular organisms, these capabilities must be tamed, and can be exploited, by the evolutionary process. Specifically, biological structures have a multiscale competency architecture where cells, tissues, and organs exhibit regulative plasticity-the ability to adjust to perturbations such as external injury or internal modifications and still accomplish specific adaptive tasks across metabolic, transcriptional, physiological, and anatomical problem spaces. Here, I review examples illustrating how physiological circuits guiding cellular collective behavior impart computational properties to the agential material that serves as substrate for the evolutionary process. I then explore the ways in which the collective intelligence of cells during morphogenesis affect evolution, providing a new perspective on the evolutionary search process. This key feature of the physiological software of life helps explain the remarkable speed and robustness of biological evolution, and sheds new light on the relationship between genomes and functional anatomical phenotypes.
进化的一个关键方面是在基因型和解剖表型之间运作的发育生理学层。虽然已经有很多工作研究了发育机制的进化和具有新兴复杂性的特定遗传结构的可进化性,但有一个方面尚未得到充分探讨:形态发生问题解决能力对进化过程本身的影响。进化所作用的细胞不是被动的组成部分:相反,它们具有许多行为能力,因为它们来自具有丰富剧目库的祖先单细胞生物。在多细胞生物中,这些能力必须被进化过程驯服并加以利用。具体来说,生物结构具有多层次的能力架构,其中细胞、组织和器官表现出调节可塑性——能够适应外部伤害或内部变化等干扰,仍然能够在代谢、转录、生理和解剖问题空间中完成特定的适应任务。在这里,我将回顾一些例子,说明引导细胞集体行为的生理回路如何赋予作为进化过程基质的代理物质计算属性。然后,我探讨了在形态发生过程中细胞的集体智慧如何影响进化,为进化搜索过程提供了一个新的视角。生命生理软件的这个关键特征有助于解释生物进化的惊人速度和稳健性,并为基因组和功能解剖表型之间的关系提供新的见解。
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