Frankowski Karina, Miyazaki Katsumi, Brenneis Georg
Zoologisches Institut und Museum, AG Cytologie und Evolutionsbiologie, Universität Greifswald, Soldmannstraße 23, 17489, Greifswald, Germany.
Department of Environmental Science, Faculty of Science, Niigata University, 8050 Ikarashi 2-no-cho, Niigata, 950-2181, Japan.
Front Zool. 2022 Mar 31;19(1):14. doi: 10.1186/s12983-022-00459-8.
Pycnogonida (sea spiders) is the sister group of all other extant chelicerates (spiders, scorpions and relatives) and thus represents an important taxon to inform early chelicerate evolution. Notably, phylogenetic analyses have challenged traditional hypotheses on the relationships of the major pycnogonid lineages (families), indicating external morphological traits previously used to deduce inter-familial affinities to be highly homoplastic. This erodes some of the support for phylogenetic information content in external morphology and calls for the study of additional data classes to test and underpin in-group relationships advocated in molecular analyses. In this regard, pycnogonid internal anatomy remains largely unexplored and taxon coverage in the studies available is limited.
Based on micro-computed X-ray tomography and 3D reconstruction, we created a comprehensive atlas of in-situ representations of the central nervous system and midgut layout in all pycnogonid families. Beyond that, immunolabeling for tubulin and synapsin was used to reveal selected details of ganglionic architecture. The ventral nerve cord consistently features an array of separate ganglia, but some lineages exhibit extended composite ganglia, due to neuromere fusion. Further, inter-ganglionic distances and ganglion positions relative to segment borders vary, with an anterior shift in several families. Intersegmental nerves target longitudinal muscles and are lacking if the latter are reduced. Across families, the midgut displays linear leg diverticula. In Pycnogonidae, however, complex multi-branching diverticula occur, which may be evolutionarily correlated with a reduction of the heart.
Several gross neuroanatomical features are linked to external morphology, including intersegmental nerve reduction in concert with trunk segment fusion, or antero-posterior ganglion shifts in partial correlation to trunk elongation/compaction. Mapping on a recent phylogenomic phylogeny shows disjunct distributions of these traits. Other characters show no such dependency and help to underpin closer affinities in sub-branches of the pycnogonid tree, as exemplified by the tripartite subesophageal ganglion of Pycnogonidae and Rhynchothoracidae. Building on this gross anatomical atlas, future studies should now aim to leverage the full potential of neuroanatomy for phylogenetic interrogation by deciphering pycnogonid nervous system architecture in more detail, given that pioneering work on neuron subsets revealed complex character sets with unequivocal homologies across some families.
海蜘蛛纲（海蜘蛛）是所有其他现存螯肢动物（蜘蛛、蝎子及近亲）的姐妹群，因此是了解早期螯肢动物进化的一个重要分类单元。值得注意的是，系统发育分析对关于主要海蜘蛛类群（科）之间关系的传统假说提出了挑战，表明先前用于推断科间亲缘关系的外部形态特征具有高度的同塑性。这削弱了对外部形态中系统发育信息含量的一些支持，并呼吁研究更多的数据类别，以检验和支持分子分析中所主张的类群内关系。在这方面，海蜘蛛的内部解剖结构在很大程度上仍未被探索，现有研究中的分类单元覆盖范围有限。
基于微计算机断层扫描和三维重建，我们创建了一个全面的图谱，展示了所有海蜘蛛科中枢神经系统和中肠布局的原位表示。除此之外，使用微管蛋白和突触素的免疫标记来揭示神经节结构的选定细节。腹神经索始终具有一系列独立的神经节，但由于神经节段融合，一些类群表现出扩展的复合神经节。此外，神经节间距离和神经节相对于体节边界的位置各不相同，在几个科中出现向前移位。节间神经靶向纵向肌肉，如果纵向肌肉减少则不存在。在所有科中，中肠都有线性的腿部憩室。然而，在海蜘蛛科中，会出现复杂的多分支憩室，这可能在进化上与心脏的减少有关。
一些大体神经解剖特征与外部形态相关，包括节间神经减少与躯干节段融合一致，或神经节前移与躯干伸长/压缩部分相关。在最近的系统发育基因组系统发育树上进行映射显示了这些特征的间断分布。其他特征则没有这种依赖性，并有助于支持海蜘蛛树亚分支中的更紧密亲缘关系，如海蜘蛛科和吻胸蛛科的三联体咽下神经节就是例证。基于这个大体解剖图谱，鉴于对神经元亚群的开创性研究揭示了一些科之间具有明确同源性的复杂特征集，未来的研究现在应该旨在通过更详细地解读海蜘蛛神经系统结构，充分利用神经解剖学在系统发育研究中的潜力。
