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

Abstract

BackgroundStudies 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.ResultsWe 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.ConclusionsEmbryonic 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.

Chelicerata

“…In a second step, in pycnogonids, however, larger neural stem cells with high mitotic activity differentiate from the precursor groups and form ganglion cells by asymmetric cell divisions ( Fig. 5.6 ; Brenneis et al 2013 ).…”

“…Whether the pycnogonid neural stem cells have evolved convergently or, alternatively, chelicerates and myriapods have lost this cell type will, according to Brenneis et al ( 2013 ), require studies of the molecular mechanisms of neurogenesis in pycnogonids, as well as detailed reinvestigation of neurogenesis in other arthropod groups. It is interesting to note that some authors of classical literature have noted the existence of neural stem cells within a few chelicerates (Anderson 1973 ).…”

“…5.6 ; Brenneis et al 2013 ). Like the euchelicerates, neurogenesis in pycnogonids is initiated by formation of post-mitotic neuronal precursor groups that form cell internalisation sites.…”

“…Two groups that diverge from the general chelicerate segmentation pattern are (1) the katoikogenic scorpions, in which the mesosoma (the fi rst eight embryonic segments of the opisthosoma in scorpions) is precociously segmented, with each segment bearing a pair of dorsolateral protrusions that supplement exchange surfaces with the mother, whereas the prosoma is segmented much later, and (2) the pycnogonids, which form a freeswimming larva that usually only possesses the cheliforal and two larval appendages (Vilpoux and Waloszek 2003 ;Machner and Scholtz 2010 ;Brenneis et al 2013 ).…”

A flexible genetic toolkit for arthropod neurogenesis

“…However, the division pattern has not been analysed in detail and it is not known if the neural precursors within a group are related by lineage. Interestingly, sea spiders, which are most probably the sister group of all other chelicerates (euchelicerates), show a combination of asymmetrically dividing neural progenitors and neural precursor groups [78]. However, in this case, neural precursor groups are generated before the neural progenitors appear.…”