Bingham Emma P, Ratcliff William C
School of Physics, Georgia Institute of Technology. Atlanta, Georgia 30332, USA.
Interdisciplinary Graduate Program in Quantitative Biosciences, Georgia Institute of Technology. Atlanta, Georgia 30332, USA.
bioRxiv. 2023 Nov 13:2023.11.11.566713. doi: 10.1101/2023.11.11.566713.
"Complex multicellularity", conventionally defined as large organisms with many specialized cell types, has evolved five times independently in eukaryotes, but never within prokaryotes. A number hypotheses have been proposed to explain this phenomenon, most of which posit that eukaryotes evolved key traits (., dynamic cytoskeletons, alternative mechanisms of gene regulation, or subcellular compartments) which were a necessary prerequisite for the evolution of complex multicellularity. Here we propose an alternative, non-adaptive hypothesis for this broad macroevolutionary pattern. By binning cells into groups with finite genetic bottlenecks between generations, the evolution of multicellularity greatly reduces the effective population size () of cellular populations, increasing the role of genetic drift in evolutionary change. While both prokaryotes and eukaryotes experience this phenomenon, they have opposite responses to drift: mutational biases in eukaryotes tend to drive genomic expansion, providing additional raw genetic material for subsequent multicellular innovation, while prokaryotes generally face genomic erosion. These effects become more severe as organisms evolve larger size and more stringent genetic bottlenecks between generations- both of which are hallmarks of complex multicellularity. Taken together, we hypothesize that it is these idiosyncratic lineage-specific mutational biases, rather than cell-biological innovations within eukaryotes, that underpins the long-term divergent evolution of complex multicellularity across the tree of life.
“复杂多细胞性”，传统上定义为具有多种特化细胞类型的大型生物体，在真核生物中已独立进化了五次，但在原核生物中从未进化过。已经提出了许多假设来解释这一现象，其中大多数假设认为真核生物进化出了关键特征（如动态细胞骨架、基因调控的替代机制或亚细胞区室），这些是复杂多细胞性进化的必要前提。在这里，我们针对这种广泛的宏观进化模式提出了一种替代性的、非适应性的假设。通过将细胞分组，使世代之间存在有限的遗传瓶颈，多细胞性的进化极大地降低了细胞群体的有效种群大小（Ne），增加了遗传漂变在进化变化中的作用。虽然原核生物和真核生物都会经历这种现象，但它们对漂变有相反的反应：真核生物中的突变偏向往往会驱动基因组扩张，为随后的多细胞创新提供额外的原始遗传物质，而原核生物通常面临基因组侵蚀。随着生物体进化出更大的体型和世代之间更严格的遗传瓶颈，这些影响会变得更加严重——这两者都是复杂多细胞性的标志。综上所述，我们假设正是这些特定谱系的独特突变偏向，而非真核生物内部的细胞生物学创新，支撑了生命之树上复杂多细胞性的长期分歧进化。
