Looking like Limulus? – Retinula axons and visual neuropils of the median and lateral eyes of scorpions

Abstract

BackgroundDespite ongoing interest in the neurophysiology of visual systems in scorpions, aspects of their neuroanatomy have received little attention. Lately sets of neuroanatomical characters have contributed important arguments to the discussion of arthropod ground patterns and phylogeny. In various attempts to reconstruct phylogeny (from morphological, morphological + molecular, or molecular data) scorpions were placed either as basalmost Arachnida, or within Arachnida with changing sister-group relationships, or grouped with the extinct Eurypterida and Xiphosura inside the Merostomata. Thus, the position of scorpions is a key to understanding chelicerate evolution. To shed more light on this, the present study for the first time combines various techniques (Cobalt fills, DiI / DiO labelling, osmium-ethyl gallate procedure, and AMIRA 3D-reconstruction) to explore central projections and visual neuropils of median and lateral eyes in Euscorpius italicus (Herbst, 1800) and E. hadzii Di Caporiacco, 1950.ResultsScorpion median eye retinula cells are linked to a first and a second visual neuropil, while some fibres additionally connect the median eyes with the arcuate body. The lateral eye retinula cells are linked to a first and a second visual neuropil as well, with the second neuropil being partly shared by projections from both eyes.ConclusionsComparing these results to previous studies on the visual systems of scorpions and other chelicerates, we found striking similarities to the innervation pattern in Limulus polyphemus for both median and lateral eyes. This supports from a visual system point of view at least a phylogenetically basal position of Scorpiones in Arachnida, or even a close relationship to Xiphosura. In addition, we propose a ground pattern for the central projections of chelicerate median eyes.

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

“…11). Even the visual system of Onychophora may not be an exception because it reveals a central organization of optic neuropils that is almost identical to that in chelicerates (Strausfeld et al, 2006;Lehmann and Melzer, 2013).…”

“…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

“…8Comparison of the results of this study (a) with other taxa (b, c) and with previous studies (d–f). a Opiliones, this study, note region, that in previous studies (d–f) is described as M1, is indeed eye nerve and M1 lies deeper in the protocerebrum; b Scorpiones ( Euscorpius italicus , E. hadzii ; after Lehmann & Melzer [15]); c Araneae ( Cupiennius salei ; after Strausfeld et al [22]); d Opiliones, after Saint Remy [25]; e Opiliones, after Hanström [29], note M2 subdivided into three layers (layer C, B, and C, see text) by Hanström; f Opiliones, after Breidbach & Wegerhoff [30], note M2 subdivided into two layers (internal and external, see text) by Breidbach & Wegerhoff. EN, eye nerve; L, lateral eye visual neuropil; LEN, lateral eye nerve; M, median eye visual neuropil; M/L2, region where M2 and L2 overlap; MEN, median eye nerve …”

“…The R‐cells of the lateral eyes are linked to a first and a second visual neuropil as well. Furthermore, the second median and the second lateral eye visual neuropils overlap each other; this means that there is a region with axon terminals from both eye types [15, 31]. A similar situation is found in the normal median and lateral eyes of Xiphosura [17, 18, 20], indicating close evolutionary relationships, at least of the visual systems.…”

Sense organs in Pycnogonida: A review

“…Of interest for reconstruction of arthropod phylogeny and evolution of visual systems, however, might be the results presented by Lehmann et al (2012) and Lehmann, Heß, Wanner, et al (2014) on pycnogonid visual neuropils. In their analysis of the general layout of the visual system, they show that sea spiders exhibit features corresponding well with those of Xiphosura (median rudimentary eyes) and even Onychophora but to a lesser extent with those of scorpions, harvestmen and spiders (Lehmann, Lodde-Bensch, Melzer, & Metz, 2016;Lehmann & Melzer, 2013;Lehmann et al, 2012). Similarities to Onychophora and Xiphosura are the presence of paired median eye nerves and two visual neuropils, one of them being located in the neighbourhood of an unpaired midline neuropil, namely the arcuate body (given that these neuropils are homologous in Onychophora, Xiphosura and Pycnogonida; see also Strausfeld, Strausfeld, Stowe, Rowell, and Loesel (2006)).…”