Embryonic and postembryonic neurogenesis in the ventral nerve cord of the freshwater crayfish Cherax destructor

Abstract

Previous studies of neurogenic activity in the thoracic neuromeres of indirect developing crustaceans indicated that the temporal patterns of neurogenesis can be correlated with the appearance of the thoracic appendages during larval and metamorphic development. To test further the idea that the temporal patterns of neurogenesis in crustaceans are related to their life histories, we examined neurogenesis in the ventral nerve cord of a direct developing crustacean, the freshwater crayfish Cherax destructor, whose life history contains neither larval stages nor metamorphoses. Neurogenesis was examined using the in vivo incorporation of bromodeoxyuridine into DNA. During late embryonic development the thoracic neuromeres of the crayfish contain arrays of mitotically active neuroblasts similar to those previously described in the spider crab and lobster. The arrays in the crayfish abdomen are, however, greatly reduced compared with those of the thorax. On hatching, both the thoracic and abdominal appendages of C. destructor are capable of movement. The pleopods, however, do not beat rhythmically until the second postembryonic stage whereas the pereiopods are not used in coordinated walking movements until the third stage. An examination of the time course of neurogenesis in the ventral nerve cord revealed that neurogenic activity in each neuromere ceases during or before the moult to the developmental stage in which its segmental appendage is first used in coordinated movements. These findings indicate that the patterns of neurogenesis in crustaceans are indeed related to the maturation of the segmental appendages and, in particular, to the maturation of motor behaviours.

“Crustacea”: Decapoda – Astacida

“…By experiments using the S-phase-specifi c proliferation marker BrdU during late embryogenesis (E80 % to hatching), these authors labelled an average number of 5-6 neuroblasts per thoracic hemineuromere in a 4-h pulse of BrdU at 21 °C. Their experiments also showed that in the thoracic and pleonal ganglia, the neurogenic activity in each neuromere ceases during or before the moult to the developmental stage in which its segmental appendage is fi rst used in coordinated movements (Sullivan and Macmillan 2001 ). These results suggest that the patterns of neurogenesis in the ventral ganglia of decapod crustaceans are intimately related to the development of the segmental appendages and maturation of motor behaviours (discussed in Harzsch 2003a ).…”

“…The presence of segmentally arranged midline neuroblasts in the developing thoracic ganglia has been reported in several malacostracans including crayfi sh: Cherax destructor (Scholtz 1992 ;Sullivan and Macmillan 2001 ), Homarus araneus (Harzsch and Dawirs 1994 ), H. americanus (Harzsch et al 1998 ), as well as Porcellio scaber and Orchestia cavimana Scholtz 1999 , 2001 ). The cell division pattern of midline precursor cells was explored in great detail in the amphipod O. cavimana Scholtz 1999 , 2001 ; reviewed in Scholtz and Gerberding 2002 ).…”

“…However, there is evidence now from the American lobster Homarus americanus that ganglion mother cells in the embryonic crustacean brain undergo not just one but multiple divisions and this may also be the case in other crustaceans. Sullivan and MacMillan ( 2001 ) have examined neurogenesis in late embryonic stages of C. destructor , whose life history, being a characteristic representative of crayfi sh, contains neither free-living, pelagic larval stages nor metamorphosis. By experiments using the S-phase-specifi c proliferation marker BrdU during late embryogenesis (E80 % to hatching), these authors labelled an average number of 5-6 neuroblasts per thoracic hemineuromere in a 4-h pulse of BrdU at 21 °C.…”

“…A monoclonal antibody (4D9) against the protein of the segment polarity gene engrailed was instrumental for understand-ing the process of segmentation during germband formation in embryonic Procambarus clarkii (Patel et al 1989 ). Cell proliferation, specifi cally the generation of new neurons, was analysed in late embryos and larvae of selected decapod crustaceans by in vivo incorporation of the S-phasespecifi c proliferation marker bromodeoxyuridine (BrdU) and subsequent immunohistochemical detection with antisera directed against BrdU (Harzsch and Dawirs 1994 ;Harzsch et al 1998 ;Harzsch 2001 ;Sullivan and Macmillan 2001 ). Later phases of neurogenesis involve that neurons differentiate and synthesise a neurotransmitter (for reviews, see Beltz 1999 ;Spindler et al 2000 ;Harzsch 2002 ).…”

Engrailed-like immunoreactivity in the embryonic ventral nerve cord of the Marbled Crayfish (Marmorkrebs)

“…Neurogenesis in malacostracan crustaceans typically is driven by neuroblasts which repeatedly undergo unequal divisions to produce ganglion mother cells, which later divide again to give birth to ganglion cells (e.g. Dohle 1970Dohle , 1972Scholtz 1990Scholtz , 1992Harzsch and Dawirs 1994;Harzsch et al 1998;Gerberding and Scholtz 2001;Harzsch 2001;Sullivan and MacMillan 2001;Ungerer and Scholtz 2007;reviews Harzsch 2003a, b;Dohle et al 2004;Whitington 2004). This mode of neurogenesis in principal shares many similarities with that in insects (reviews, e.g.…”