School of Life Sciences, University of Nevada Las Vegas, Las Vegas, NV 89154, USA.
The Francis Crick Institute, London NW1 1AT, UK.
Genes (Basel). 2024 Nov 14;15(11):1472. doi: 10.3390/genes15111472.
The evolution of complex multicellularity in land plants represents a pivotal event in the history of life on Earth, characterized by significant increases in biological complexity. This transition, classified as a Major Evolutionary Transition (MET), is best understood through the framework of Evolutionary Transitions in Individuality (ETIs), which focuses on formerly independent entities forming higher-level units that lose their reproductive autonomy. While much of the ETI literature has concentrated on the early stages of multicellularity, such as the formation and maintenance stages, this paper seeks to address the less explored transformation stage. To do so, we apply an approach that we call Transitions in Structural Complexity (TSCs), which focuses on the emergence of new units of organization via the three key evolutionary processes of modularization, subfunctionalization, and integration to the evolution of land plants. To lay the groundwork, we first explore the relationships between sex, individuality, and units of selection to highlight a sexual life cycle-based perspective on ETIs by examining the early stages of the transition to multicellularity (formation) in the sexual life cycle of the unicellular common ancestor of land plants, emphasizing the differences between the transition to multicellularity in eumetazoans and land plants. We then directly apply the TSC approach in this group, identifying key evolutionary events such as the distinct evolutionary innovations like shoot, root, vascular systems, and specialized reproductive structures, arguing that bringing these under the broader rubric of TSCs affords a degree of explanatory unification. By examining these evolutionary processes, this paper provides a new perspective on the evolution of multicellularity in land plants, highlighting both parallels and distinctions with the animal kingdom.
陆地植物中复杂多细胞生物的进化代表了地球生命史上的一个关键事件,其特点是生物复杂性的显著增加。这种转变被归类为主要进化转变(MET),通过个体进化转变(ETIs)的框架来更好地理解,该框架侧重于以前独立的实体形成失去生殖自主性的更高层次的单位。虽然 ETI 文献的很大一部分集中在多细胞生物的早期阶段,如形成和维持阶段,但本文旨在解决研究较少的转变阶段。为此,我们应用了一种称为结构复杂性转变(TSC)的方法,该方法侧重于通过模块化、次功能化和整合这三个关键进化过程来出现新的组织单位,从而研究陆地植物的进化。为了奠定基础,我们首先探讨了性别、个体性和选择单位之间的关系,通过研究陆地植物单细胞共同祖先的有性生命周期中的多细胞生物早期过渡(形成),强调有性生命周期中 ETIs 的性周期观点,强调后生动物和陆地植物向多细胞生物过渡的区别。然后,我们在这个群体中直接应用 TSC 方法,确定了关键的进化事件,如独特的进化创新,如芽、根、维管系统和专门的生殖结构,认为将这些归入 TSC 的更广泛范畴提供了一定程度的解释统一性。通过研究这些进化过程,本文为陆地植物多细胞生物的进化提供了一个新的视角,突出了与动物王国的相似之处和区别。