A new look at embryonic development of the visual system in decapod crustaceans: Neuropil formation, neurogenesis, and apoptotic cell death

Abstract

In recent years, comparing the structure and development of the central nervous system in crustaceans has provided new insights into the phylogenetic relationships of arthropods. Furthermore, the structural evolution of the compound eyes and optic ganglia of adult arthropods has been discussed, but it was not possible to compare the ontogeny of arthropod visual systems, owing to the lack of data on species other than insects. In the present report, we studied the development of the crustacean visual system by examining neurogenesis, neuropil formation, and apoptotic cell death in embryos of the American lobster, Homarus americanus, the spider crab, Hyas araneus, and the caridean shrimp, Palaemonetes argentinus, and compare these processes with those found in insects. Our results on the patterns of stem cell proliferation provide evidence that in decapod crustaceans and hemimetabolous insects, there exist considerable similarities in the mechanisms by which accretion of the compound eyes and growth of the optic lobes is achieved, suggesting an evolutionary conservation of these mechanisms. © 1999 John Wiley & Sons, Inc. J Neurobiol 39: 294–306, 1999

Evolution of arthropod visual systems: Development of the eyes and central visual pathways in the horseshoe crabLimulus polyphemusLinnaeus, 1758 (Chelicerata, Xiphosura)

“…In this group of organisms as well as in insects, proliferation zones similar to that described here for the horseshoe crab exist (review in Strausfeld, 2005). One difference is that, in Crustacea and Insecta, this proliferation zone contains asymmetrically dividing stem cells, the neuroblasts (summarized in Harzsch et al, 1999;Harzsch and Walossek, 2001), whereas in L. polyphemus, all mitotic cells that we observed in the optic proliferation zone but also in the ganglion cell layer of the central body had nuclei of a similar size. This finding supports reports on neurogenesis in the L. polyphemus ventral nerve cord (Mittmann, 2002(Mittmann, , 2004 and in other Chelicerata (Stollewerk et al, 2001;Stollewerk, 2002Stollewerk, , 2004) that this taxon does not appear to contain asymmetrically dividing stem cells similar to those in Tetraconata.…”

“…Persistent growth of the eyes and in parallel, persistent postembryonic neurogenesis of the visual interneuron population is also a common feature in decapod crustaceans (discussed in Dawirs, 1995/ 1996;Harzsch et al, 1999). In this group of organisms as well as in insects, proliferation zones similar to that described here for the horseshoe crab exist (review in Strausfeld, 2005).…”

“…Proliferation of cells was monitored by in vivo labeling with the S-phase-specific mitosis marker BrdU (Harzsch et al, 1999). Larvae were incubated in 700 l of BrdU-labeling reagent (Amersham, Cell Proliferation Kit RPN 20) diluted in 10 ml of seawater (0.2 ml BrdU/ml seawater) for 4 hr at room temperature and ambient light condi-tions.…”

“…Thus, we applied the proliferation marker bromodeoxyuridine (BrdU; Harzsch et al, 1999;Harzsch and Walossek, 2001;Wildt and Harzsch, 2002) and immunohistochemistry with photoreceptor-specific markers that have been characterized in adult animals (opsin, visual arrestin, myosin III; Battelle et al, 1998Battelle et al, , 2001). Our analyses focused on embryonic stages shortly before hatching, trilobite larvae, and young juveniles, because the study by French (1980) indicated that this time period includes rapid morphogenetic events.…”

“…Furthermore, in recent years, aspects of eye development emerge as important characters for phylogenetic analyses and, therefore, are examined in a variety of arthropods, including Crustacea (Harzsch et al, 1999;Melzer et al, 2000;Hafner and Tokarski, 2001;Harzsch and Walossek, 2001;Wildt and Harzsch, 2002), Hexapoda (Friedrich et al, 1996;Friedrich and Benzer, 2000;Friedrich, 2003), and Myriapoda . Comparative studies on eye development in insects have also revealed new insights into the molecular developmental changes that occurred during the evolutionary transition from hemimetabolous to holometabolous insects (Friedrich, 2003).…”