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

Abstract

Despite ongoing interest into the architecture, biochemistry, and physiology of the visual systems of the xiphosuran Limulus polyphemus, their ontogenetic aspects have received little attention. Thus, we explored the development of the lateral eyes and associated neuropils in late embryos and larvae of these animals. The first external evidence of the lateral eyes was the appearance of white pigment spots-guanophores associated with the rudimentary photoreceptors-on the dorsolateral side of the late embryos, suggesting that these embryos can perceive light. The first brown pigment emerges in the eyes during the last (third) embryonic molt to the trilobite stage. However, ommatidia develop from this field of pigment toward the end of the larval trilobite stage so that the young larvae at hatching do not have object recognition. Double staining with the proliferation marker bromodeoxyuridine (BrdU) and an antibody against L. polyphemus myosin III, which is concentrated in photoreceptors of this species, confirmed previous reports that, in the trilobite larvae, new cellular material is added to the eye field from an anteriorly located proliferation zone. Pulse-chase experiments indicated that these new cells differentiate into new ommatidia. Examining larval eyes labeled for opsin showed that the new ommatidia become organized into irregular rows that give the eye field a triangular appearance. Within the eye field, the ommatidia are arranged in an imperfect hexagonal array. Myosin III immunoreactivity in trilobite larvae also revealed the architecture of the central visual pathways associated with the median eye complex and the lateral eyes. Double labeling with myosin III and BrdU showed that neurogenesis persists in the larval brain and suggested that new neurons of both the lamina and the medulla originate from a single common proliferation zone. These data are compared with eye development in Drosophila melanogaster and are discussed with regard to new ideas on eye evolution in the Euarthropoda. Developmental Dynamics 235:2641-2655, 2006.

Arthropod eyes: The early Cambrian fossil record and divergent evolution of visual systems

“…Many publications and modern glossaries confuse eyes of visual systems, as defined above, with light sensitive channels subtending lenses, but which do not supply retinotopic neuropils. The lenses of Onychophora (Strausfeld et al, 2006), the paired median lenses of xiphosurans , single lenslets of Chilopoda , and the lenses of Chelicerata, including Pycnogonida, all supply light to photoreceptor neurons that connect to retinotopic neurons comprising discrete visual neuropils belonging to the protocerebral neuromere of the brain (Strausfeld et al, 2006;Harzsch et al, 2006;Strausfeld, 2012;Lehmann et al, 2012;Lehmann and Melzer, 2013). In contrast, the nauplius eyes of crustaceans and the ocelli of insects, their likely homologues, supply sparse outputs to distributed areas in the central protocerebrum but not to specialized visual neuropils (N€ assel and Hagberg, 1985;Lacalli, 2009;Fritsch and Richter, 2010).…”

Wiring a Periscope – Ocelli, Retinula Axons, Visual Neuropils and the Ancestrality of Sea Spiders

“…Deeper knowledge of, e.g., R-cell projections and visual neuropil architecture is missing, hence there is no stable basis on which to compare visual system features among pycnogonids and to those of their putative arthropod outgroups. In Chelicerata other than Pycnogonida, the visual systems of Limulus polyphemus [15],[16],[17] and Cupiennius salei [18],[19], which are important model organisms in the field of visual neuroscience, are especially well studied. In scorpions the only study of the visual neuropils is that of Hanström [13].…”

Evolution of Insect Eyes: Tales of Ancient Heritage, Deconstruction, Reconstruction, Remodeling, and Recycling

“…2) (Regier et al 2005;Friedrich and Tautz 1995;Hwang et al 2001;Strausfeld 1998). Some myriapod and chelicerate species carry compound eyes as well, but these exhibit less similarity than is observed between insects and crustaceans (Harzsch et al 2007;Harzsch et al 2006). Informatively, of the two synonyms for the super-clade constituting crustaceans and insects, Pancrustacea and Tetraconata, the latter refers to the presence of four cone cells in the ommatidia of insect and crustacean species (Shultz and Regier 2000;Dohle 2001).…”