Data from: Owenia fusiformis - a basally branching annelid suitable for studying ancestral features of annelid neural development

Background-Comparative investigations on bilaterian neurogenesis shed light on conserved developmental mechanisms across taxa. With respect to annelids, most studies focus on taxa deeply nested within the annelid tree, while investigations on early branching groups are almost lacking. According to recent phylogenomic data on annelid evolution Oweniidae represent one of the basally branching annelid clades. Oweniids are thought to exhibit several plesiomorphic characters, but are scarcely studied - a fact that might be caused by the unique morphology and unusual metamorphosis of the mitraria larva, which seems to be hardly comparable to other annelid larva. In our study, we compare the development of oweniid neuroarchitecture with that of other annelids aimed to figure out whether oweniids may represent suitable study subjects to unravel ancestral patterns of annelid neural development. Our study provides the first data on nervous system development in basally branching annelids. Results-Based on histology, electron microscopy and immunohistochemical investigations we show that development and metamorphosis of the mitraria larva has many parallels to other annelids irrespective of the drastic changes in body shape during metamorphosis. Such significant changes ensuing metamorphosis are mainly from diminution of a huge larval blastocoel and not from major restructuring of body organization. The larval nervous system features a prominent apical organ formed by flask-shaped perikarya and circumesophageal connectives that interconnect the apical and trunk nervous systems, in addition to serially arranged clusters of perikarya showing 5-HT-LIR in the ventral nerve cord, and lateral nerves. Both 5-HT-LIR and FMRFamide-LIR are present in a distinct nerve ring underlying the equatorial ciliary band. The connections arising from these cells innervate the circumesophageal connectives as well as the larval brain via dorsal and ventral neurites. Notably, no distinct somata with 5-HT -LIR in the apical organ are detectable in the larval stages of Owenia. Most of the larval neural elements including parts of the apical organ are preserved during metamorphosis and contribute to the juvenile nervous system. Conclusions-Our studies in Owenia fusiformis strongly support that early branching annelids are comparable to other annelids with regard to larval neuroanatomy and formation of the juvenile nervous system. Therefore, Owenia fusiformis turns out to be a valuable study subject for comparative investigations and unravelling ancestral processes in neural development in Annelida and Bilateria in general.背景——针对两侧对称动物（Bilateria）神经发生的比较研究，可为揭示不同类群间保守的发育机制提供关键见解。就环节动物（Annelida）而言，现有研究多聚焦于系统发育树中深度嵌套的类群，而针对早期分支类群的探索几乎空白。基于近期环节动物演化的系统基因组学数据，欧文虫科（Oweniidae）属于最早分支的环节动物支系之一。欧文虫类被认为具有诸多祖征，但相关研究极少——这一现状可能源于其帽状幼虫（mitraria larva）独特的形态与罕见的变态过程，该幼虫与其他环节动物幼虫几乎无可比性。本研究将欧文虫类的神经结构发育与其他环节动物进行对比，旨在明确欧文虫类是否可作为合适的研究对象，以解析环节动物神经发育的祖先模式。本研究首次提供了早期分支环节动物的神经系统发育数据。结果——基于组织学、电子显微镜术与免疫组织化学分析，本研究发现：尽管变态过程中体形发生剧烈变化，但帽状幼虫的发育与变态过程与其他环节动物存在诸多共通之处。这类由变态引发的显著形态变化主要源于大型幼虫囊胚腔（blastocoel）的缩减，而非身体组织结构的大规模重构。幼虫神经系统具有如下特征：由烧瓶状胞体（perikarya）构成的显著顶器（apical organ）、连接顶器与躯干神经系统的围食道神经连合（circumesophageal connectives），以及腹神经索（ventral nerve cord）中呈系列排列的5-羟色胺样免疫反应性（5-HT-LIR）胞体簇与侧神经。在赤道纤毛带（equatorial ciliary band）下方的特殊神经环中，同时存在5-HT-LIR与FMRF酰胺样免疫反应性（FMRFamide-LIR）。这些细胞发出的神经突通过背侧与腹侧神经突支配围食道神经连合与幼虫脑。值得注意的是，在欧文虫属（Owenia）的幼虫阶段，顶器中未检测到具有5-HT-LIR的明确胞体。多数幼虫神经结构（包括顶器的部分区域）在变态过程中得以保留，并参与构建幼体神经系统。结论——本研究针对纺锤形欧文虫（Owenia fusiformis）开展的实验充分证实：早期分支环节动物在幼虫神经解剖结构与幼体神经系统形成方面，与其他环节动物具有较高的可比性。因此，纺锤形欧文虫成为开展比较研究、解析环节动物乃至整个两侧对称动物神经发育祖先过程的优质研究对象。