John Harvard Distinguished Science Fellowship Program, Harvard University, Cambridge, MA 02138, USA; Department of Organismic and Evolutionary Biology, Harvard University, Harvard University, Cambridge, MA 02138, USA.
John Harvard Distinguished Science Fellowship Program, Harvard University, Cambridge, MA 02138, USA; Department of Organismic and Evolutionary Biology, Harvard University, Harvard University, Cambridge, MA 02138, USA.
Curr Biol. 2022 Dec 5;32(23):5045-5056.e3. doi: 10.1016/j.cub.2022.10.027. Epub 2022 Nov 9.
Coleoid cephalopods, including squid, cuttlefish, and octopus, have large and complex nervous systems and high-acuity, camera-type eyes. These traits are comparable only to features that are independently evolved in the vertebrate lineage. The size of animal nervous systems and the diversity of their constituent cell types is a result of the tight regulation of cellular proliferation and differentiation in development. Changes in the process of development during evolution that result in a diversity of neural cell types and variable nervous system size are not well understood. Here, we have pioneered live-imaging techniques and performed functional interrogation to show that the squid Doryteuthis pealeii utilizes mechanisms during retinal neurogenesis that are hallmarks of vertebrate processes. We find that retinal progenitor cells in the squid undergo nuclear migration until they exit the cell cycle. We identify retinal organization corresponding to progenitor, post-mitotic, and differentiated cells. Finally, we find that Notch signaling may regulate both retinal cell cycle and cell fate. Given the convergent evolution of elaborate visual systems in cephalopods and vertebrates, these results reveal common mechanisms that underlie the growth of highly proliferative neurogenic primordia. This work highlights mechanisms that may alter ontogenetic allometry and contribute to the evolution of complexity and growth in animal nervous systems.
头足类软体动物,包括鱿鱼、墨鱼和章鱼,拥有大型且复杂的神经系统和高灵敏度的相机型眼睛。这些特征与脊椎动物谱系中独立进化的特征相当。动物神经系统的大小和组成细胞类型的多样性是发育过程中细胞增殖和分化的严格调控的结果。进化过程中发育过程的变化导致了不同的神经细胞类型和可变的神经系统大小,但这些变化的机制还不是很清楚。在这里,我们开创了活体成像技术,并进行了功能研究,结果表明鱿鱼 Doryteuthis pealeii 在视网膜神经发生过程中利用了脊椎动物过程的标志性机制。我们发现鱿鱼的视网膜祖细胞经历核迁移,直到它们退出细胞周期。我们确定了与祖细胞、有丝分裂后细胞和分化细胞相对应的视网膜组织。最后,我们发现 Notch 信号可能调节视网膜细胞周期和细胞命运。鉴于头足类动物和脊椎动物中复杂视觉系统的趋同进化,这些结果揭示了支持高度增殖神经原发生体生长的共同机制。这项工作强调了可能改变个体发生比例的机制,并为动物神经系统的复杂性和生长的进化做出了贡献。