School of Biological and Behavioural Sciences, Queen Mary University of London, London, UK.
Faculty of Health and Life Sciences, University of Exeter, Exeter, UK.
Neural Dev. 2024 Feb 21;19(1):3. doi: 10.1186/s13064-024-00180-8.
The evolutionary origins of animal nervous systems remain contentious because we still have a limited understanding of neural development in most major animal clades. Annelids - a species-rich group with centralised nervous systems - have played central roles in hypotheses about the origins of animal nervous systems. However, most studies have focused on adults of deeply nested species in the annelid tree. Recently, Owenia fusiformis has emerged as an informative species to reconstruct ancestral traits in Annelida, given its phylogenetic position within the sister clade to all remaining annelids.
Combining immunohistochemistry of the conserved neuropeptides FVamide-lir, RYamide-lir, RGWamide-lir and MIP-lir with gene expression, we comprehensively characterise neural development from larva to adulthood in Owenia fusiformis.
The early larval nervous system comprises a neuropeptide-rich apical organ connected through peripheral nerves to a prototroch ring and the chaetal sac. There are seven sensory neurons in the prototroch. A bilobed brain forms below the apical organ and connects to the ventral nerve cord of the developing juvenile. During metamorphosis, the brain compresses, becoming ring-shaped, and the trunk nervous system develops several longitudinal cords and segmented lateral nerves.
Our findings reveal the formation and reorganisation of the nervous system during the life cycle of O. fusiformis, an early-branching annelid. Despite its apparent neuroanatomical simplicity, this species has a diverse peptidergic nervous system, exhibiting morphological similarities with other annelids, particularly at the larval stages. Our work supports the importance of neuropeptides in animal nervous systems and highlights how neuropeptides are differentially used throughout development.
动物神经系统的进化起源仍然存在争议,因为我们对大多数主要动物类群的神经发育仍然知之甚少。环节动物 - 一个物种丰富的群体,具有集中的神经系统 - 在关于动物神经系统起源的假说中发挥了核心作用。然而,大多数研究都集中在环节动物树中嵌套深度较深的物种的成虫上。最近,Owenia fusiformis 作为一种信息丰富的物种出现,鉴于其在所有剩余环节动物的姐妹群中的系统发育位置,可以重建环节动物中的祖征。
结合保守神经肽 FVamide-lir、RYamide-lir、RGWamide-lir 和 MIP-lir 的免疫组织化学与基因表达,我们全面描述了 Owenia fusiformis 从幼虫到成体的神经发育。
早期幼虫神经系统包括一个富含神经肽的顶端器官,通过外周神经与原环和刚毛囊相连。原环中有七个感觉神经元。一个双叶大脑在顶端器官下方形成,并与正在发育的幼体的腹神经索相连。在变态期间,大脑压缩,变成环状,并且躯干神经系统发育出几个纵向索和分段的侧神经。
我们的研究结果揭示了 O. fusiformis 生命周期中神经系统的形成和重组,O. fusiformis 是一种早期分支的环节动物。尽管它的神经解剖结构明显简单,但该物种具有多样化的肽能神经系统,在幼虫阶段表现出与其他环节动物的形态相似性。我们的工作支持神经肽在动物神经系统中的重要性,并强调了神经肽在整个发育过程中是如何不同地使用的。