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

Abstract

The Pycnogonida or sea spiders are cryptic, eight-legged arthropods with four median ocelli in a ‘periscope’ or eye tubercle. In older attempts at reconstructing phylogeny they were Arthropoda incertae sedis, but recent molecular trees placed them as the sister group either to all other euchelicerates or even to all euarthropods. Thus, pycnogonids are among the oldest extant arthropods and hold a key position for the understanding of arthropod evolution. This has stimulated studies of new sets of characters conductive to cladistic analyses, e.g. of the chelifores and of the hox gene expression pattern. In contrast knowledge of the architecture of the visual system is cursory. A few studies have analysed the ocelli and the uncommon “pseudoinverted” retinula cells. Moreover, analyses of visual neuropils are still at the stage of Hanström's early comprehensive works. We have therefore used various techniques to analyse the visual fibre pathways and the structure of their interrelated neuropils in several species. We found that pycnogonid ocelli are innervated to first and second visual neuropils in close vicinity to an unpaired midline neuropil, i.e. possibly the arcuate body, in a way very similar to ancestral euarthropods like Euperipatoides rowelli (Onychophora) and Limulus polyphemus (Xiphosura). This supports the ancestrality of pycnogonids and sheds light on what eyes in the pycnogonid ground plan might have ‘looked’ like. Recently it was suggested that arthropod eyes originated from simple ocelli similar to larval eyes. Hence, pycnogonid eyes would be one of the early offshoots among the wealth of more sophisticated arthropod eyes.

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).…”

The visual system of harvestmen (Opiliones, Arachnida, Chelicerata) – a re-examination

“…In this region, groups of axons are just interwoven with their neighbours. Hence, a primitive form of retinotopic projection arrangement of these nerve bundles occurs, resembling that in Pycnogonida [14]. All nerve fibres from the eye are bundled and a re-assortment of the single axons takes place.…”

“…Besides Opiliones, the basal Pycnogonida and Solifugae possess only median eyes, and Pseudoscorpiones possess only lateral eyes. However, examined in detail are only the visual systems of Pycnogonida, Xiphosura ( Limulus ), Scorpiones, and Araneae [14–24, 31]. Concerning the R-cell projections and neuropil arrangement, two different configurations have been described, with Pycnogonida, Xiphosura, and Scorpiones on the one side and Araneae on the other.…”

“…In both taxa the R-cell axons have collaterals in two target regions, in a first visual neuropil (or ocellar ganglion) and in a second visual neuropil near the arcuate body [14, 20]. In Scorpiones the cells of the median eye retina are also linked to two visual neuropils: the photoreceptor cells to a first visual neuropil, and the arhabdomeric cells to a second neuropil.…”

“…However, this approach has proven fruitful in recent comparative analyses of the visual systems of Pycnogonida and Scorpiones [9, 14–16]. Concerning other chelicerate taxa, recent data exist only for the xiphosuran, Limulus polyphemus [17–20], an important species well investigated in the field of visual neuroscience, and for Araneae [21–24].…”