Adult neurogenesis in the central olfactory pathway of dendrobranchiate and caridean shrimps: New insights into the evolution of the deutocerebral proliferative system in reptant decapods

Abstract

Persistent neurogenesis in the central olfactory pathway characterizes many reptant decapods such as lobsters, crayfish and crabs. In these animals, the deutocerebral proliferative system generates new neurons which integrate into the neuronal network of the first order processing neuropil of the olfactory system, the deutocerebral chemosensory lobes (also called olfactory lobes). However, differences concerning the phenotype and the mechanisms that drive adult neurogenesis were reported in crayfish versus spiny lobsters. While numerous studies have focussed on these mechanisms and regulation of adult neurogenesis, investigations about the phylogenetic distribution are missing. To contribute an evolutionary perspective on adult neurogenesis in decapods, we investigated two representatives of basally diverging lineages, the dendrobranchiate Penaeus vannamei and the caridean Crangon crangon using the thymidine analogue Bromodeoxyuridine (BrdU) as marker for the S phase of cycling cells. Compared to reptant decapods, our results suggest a simpler mechanism of neurogenesis in the adult brain of dendrobranchiate and caridean shrimps. Observed differences in the rate of proliferation and spatial dimensions are suggested to correlate with the complexity of the olfactory system. We assume that a more complex and mitotically more active proliferative system in reptant decapods evolved with the emergence of another processing neuropil, the accessory lobes. © 2018 Wiley Periodicals, Inc. Develop Neurobiol, 2018.

Adult neurogenesis in crayfish: Origin, expansion, and migration of neural progenitor lineages in a pseudostratified neuroepithelium

“…In contrast to the findings of Song et al () and to results in spiny lobsters and non‐reptant decapod crustaceans (Schmidt, ; Schmidt & Derby, ; Wittfoth & Harzsch, ), we did not detect an enlarged NP in every crayfish DPS studied. In fact, a substantial portion of our 3d‐analyzed samples lacked this morphologically conspicuous cell type (Table ).…”

“…Two decades after the first reports of persistent cell proliferation in the brains of juvenile and adult decapod crustaceans (Harzsch & Dawirs, ; Harzsch, Miller, Benton, & Beltz, ; Schmidt, ; Schmidt & Harzsch, ), this arthropod group has become an intensely studied model taxon for adult neurogenesis. The regions featuring life‐long neurogenesis in the decapod brain are the lateral protocerebrum (optic neuropils and hemiellipsoid body; e.g., Schmidt, ; Sullivan & Beltz, ) and the deutocerebrum (for review, see Sandeman, Bazin, & Beltz, ; Wittfoth & Harzsch, ). In the latter, the deutocerebral proliferative system (DPS; sensu Wittfoth & Harzsch, ) generates adult‐born neurons that integrate into the central olfactory pathway (e.g., Schmidt, ; Sullivan & Beltz, ).…”

“…The regions featuring life‐long neurogenesis in the decapod brain are the lateral protocerebrum (optic neuropils and hemiellipsoid body; e.g., Schmidt, ; Sullivan & Beltz, ) and the deutocerebrum (for review, see Sandeman, Bazin, & Beltz, ; Wittfoth & Harzsch, ). In the latter, the deutocerebral proliferative system (DPS; sensu Wittfoth & Harzsch, ) generates adult‐born neurons that integrate into the central olfactory pathway (e.g., Schmidt, ; Sullivan & Beltz, ). DPS anatomy is best understood in the spiny lobster Panulirus argus (e.g., Schmidt, ; Schmidt & Derby, ) and in crayfish (e.g., Sullivan, Benton, Sandeman, & Beltz, ; Chaves da Silva, Benton, Beltz, & Allodi, ), which have proved suitable for mechanistic studies.…”

Methods to study organogenesis in decapod crustacean larvae II: analysing cells and tissues

“…17). The thymidine analogon 5-bromo-2-deoxyuridine (BrdU) is a wellknown S phase-specific marker to analyse neurogenesis in adult crustacean brains [139,140,[140][141][142][143]. This marker was also applied to study aspects of neurogenesis in late crustacean embryos and larvae such as the development of the ventral nerve cord [144][145][146], the brain [147][148][149] and the compound eyes [150][151][152].…”

“…BrdU-labelling has turned out a robust technique which can be used as a tool to analyse cell proliferation from crustacean embryos (review [1,2]) across the larvae to adult animals [139,140,[140][141][142][143]. However, when interpreting the results of the method presented here it has to be borne in mind that this technique labels DNA synthesis which is not necessarily equivalent to mitosis considering that cells may replicate their DNA without cell division to become polyploid.…”