Embryonic neurogenesis in Pseudopallene sp. (Arthropoda, Pycnogonida) includes two subsequent phases with similarities to different arthropod groups.

PMID 24289241


Studies on early neurogenesis have had considerable impact on the discussion of the phylogenetic relationships of arthropods, having revealed striking similarities and differences between the major lineages. In Hexapoda and crustaceans, neurogenesis involves the neuroblast, a type of neural stem cell. In each hemi-segment, a set of neuroblasts produces neural cells by repeated asymmetrical and interiorly directed divisions. In Euchelicerata and Myriapoda, neurogenesis lacks neural stem cells, featuring instead direct immigration of neural cell groups from fixed sites in the neuroectoderm. Accordingly, neural stem cells were hitherto assumed to be an evolutionary novelty of the Tetraconata (Hexapoda + crustaceans). To further test this hypothesis, we investigated neurogenesis in Pycnogonida, or sea spiders, a group of marine arthropods with close affinities to euchelicerates. We studied neurogenesis during embryonic development of Pseudopallene sp. (Callipallenidae), using fluorescent histochemical staining and immunolabelling. Embryonic neurogenesis has two phases. The first phase shows notable similarities to euchelicerates and myriapods. These include i) the lack of morphologically different cell types in the neuroectoderm; ii) the formation of transiently identifiable, stereotypically arranged cell internalization sites; iii) immigration of predominantly post-mitotic ganglion cells; and iv) restriction of tangentially oriented cell proliferation to the apical cell layer. However, in the second phase, the formation of a central invagination in each hemi-neuromere is accompanied by the differentiation of apical neural stem cells. The latter grow in size, show high mitotic activity and an asymmetrical division mode. A marked increase of ganglion cell numbers follows their differentiation. Directly basal to the neural stem cells, an additional type of intermediate neural precursor is found. Embryonic neurogenesis of Pseudopallene sp. combines features of central nervous system development that have been hitherto described separately in different arthropod taxa. The two-phase character of pycnogonid neurogenesis calls for a thorough reinvestigation of other non-model arthropods over the entire course of neurogenesis. With the currently available data, a common origin of pycnogonid neural stem cells and tetraconate neuroblasts remains unresolved. To acknowledge this, we present two possible scenarios on the evolution of arthropod neurogenesis, whereby Myriapoda play a key role in the resolution of this issue.