Compartmentalization of the precheliceral neuroectoderm in the spider Cupiennius salei: Development of the arcuate body, optic ganglia, and mushroom body

Abstract

Similarly to vertebrates, arthropod brains are compartmentalized into centers with specific neurological functions such as cognition, behavior, and memory. The centers can be further subdivided into smaller functional units. This raises the question of how these compartments are formed during development and how they are integrated into brain centers. We show here for the first time how the precheliceral neuroectoderm of the spider Cupiennius salei is compartmentalized to form the distinct brain centers of the visual system: the optic ganglia, the mushroom bodies, and the arcuate body. The areas of the visual brain centers are defined by the formation of grooves and vesicles and express the proneural gene CsASH1, followed by expression of the neural differentiation marker Prospero. Furthermore, the transcription factor dachshund, which is strongly enriched in the mushroom bodies and the outer optic ganglion of Drosophila, is expressed in the optic anlagen and the mushroom bodies of the spider. The developing brain centers are further subdivided into single neural precursor groups, which become incorporated into the grooves and vesicles but remain distinguishable throughout development, suggesting that they encode spatial information for neural subtype identity. Several molecular and morphological aspects of the development of the optic ganglia and the mushroom bodies are similar in the spider and in insects. Furthermore, we show that the primary engrailed head spot contributes neurons to the optic ganglia of the median eyes, whereas the secondary head spot, which has been associated with the optic ganglia in insects and crustaceans, is absent.

Chelicerata

“…These sites are organised in a grid-like pattern and subsequently simultaneously delaminate from the neuroectoderm when early neurogenesis is complete ( Fig. 5.6 ; Stollewerk et al 2001 ;Mittmann 2002 ;Stollewerk and Chipman 2006 ;Doeffi nger et al 2010 ). In contrast to insects (Vol.…”

“…In arthropods the achaete -scute complex is important in the early stages of neurogenesis. It has been shown that the spider homolog ASH1 has a similar function during the formation of neural precursor cells to that of crustaceans and insects (Doeffi nger et al 2010 ). High levels of ASH1 expression induce the later invagination of regions to form the optic lobes, mushroom bodies, and arcuate body (Doeffi nger et al 2010 ).…”

Evolutionary crossroads in developmental biology: the spiderParasteatoda tepidariorum

“…2A, stage 17). The final stages of embryonic development involve most of the yolk migrating into the opisthosoma while internal organs, such as the heart and digestive tract, develop (Rempel, 1957) and the major brain compartments form (Doeffinger et al, 2010). The embryo gains a typical spider-like appearance as the tissue between the prosoma (see Glossary, Box 1) and opisthosoma constricts ( Fig.…”

Origin ofDrosophilamushroom body neuroblasts and generation of divergent embryonic lineages

“…This peculiar mode of neurogenesis (see also Urbach et al, 2003) parallels that reported for basal arthropods. In chelicerates, the MBs originate from a proneural gene (CsASH1)-expressing, invaginating NE in which all cells are destined to a neural fate (Doeffinger et al, 2010). These similarities might suggest a common evolutionarily origin of a mode of neural progenitor formation that does not rely on lateral inhibition among cells of the NE.…”