Variations on a theme: Morphological variation in the secondary eye visual pathway across the order of Araneae

Abstract

Spiders possess a wide array of sensory-driven behaviors and therefore provide rich models for studying evolutionary hypotheses about the relationship between brain morphology, sensory systems, and behavior. Despite this, only a handful of studies have examined brain variation across the order of Araneae. In this study, I present descriptions of the gross brain morphology for 19 families of spiders that vary in eye morphology. Spiders showed the most variation in the secondary eye visual pathway. Based on this variation, spiders could be categorized into four groups. Group 1 spiders had small, underdeveloped laminae, no medullae, and no mushroom bodies. Group 2 spiders had large laminae, no medullae and large mushroom bodies. Group 3 spiders had laminae and some evidence of reduced medullae and mushroom bodies. Group 4 spiders had the most complex systems, with large laminae, medullae formed from optical glomeruli, and robust mushroom bodies. Within groups, there was large variation in the shape and size of individual regions, indicating possible variation in neuronal organization. The possible evolutionary implications of the loss of a dedicated olfactory organ in spiders and its effects on the mushroom body are also discussed.

The central nervous system of whip spiders (Amblypygi): Large mushroom bodies receive olfactory and visual input

“…This has also been described for several other, visually advanced spider genera by Long (2020). The diameters of the spider medulla glomeruli (when present) range from 5 to 10 μm in different spider genera (Long, 2020), similar to the small calycal glomeruli in Amblypygi. Long (2020) discusses these spider glomeruli in the context of small‐field movement detection.…”

“…In spiders, the arcuate body receives direct input from the principal eye medulla (Long, 2020; Strausfeld, Weltzien, & Barth, 1993), which is homologous to the amblypygid medium eye secondary visual neuropil in Figure 5b. The arrangement and location of amblypygid visual centers and the arcuate body is very similar to that of spiders (Long, 2020), which makes it likely that the amblypygid arcuate body may receive visual input at its lateral tips [in addition to massive input along its entire length from other protocerebral regions, similar to the situation in spiders (Loesel, Seyfarth, Bräunig, & Agricola, 2011)]. However, in the absence of specific tracing of visual fibers potentially connecting the secondary visual neuropil and the arcuate body we cannot confirm such a connection.…”

“…Situated at the posterior edge of the protocerebrum (Figures 2c, 5b, and 6b), the arcuate body is similar to that of spiders (Babu & Barth, 1984;Long, 2020), but thinner and more rod-shaped ( Figure 2c).…”

“…In spiders, the arcuate body receives direct input from the principal eye medulla (Long, 2020;Strausfeld, Weltzien, & Barth, 1993), which is homologous to the amblypygid medium eye secondary visual neuropil in Figure 5b. The arrangement and location of amblypygid visual centers and the arcuate body is very similar to that of spiders (Long, 2020), which makes it likely that the amblypygid arcuate body may receive F I G U R E 3 Horizontal sections (anterior is top) of the fused postoral ganglia of Damon diadema at different dorso-ventral depths from ventral surface (indicated in Figure 1e; a: 150 μm; b: 250 μm; d: 300 μm; e, g: 400 μm; f: 500 μm); osmium-stained material except for Golgiimpregnated (c). (a) Overview of the ventral regions of the fused ganglia showing the neuromeres of the pedipalp (Pe) and the legs 1 to 4 and the ventromedian neuropil vmN as well as the opisthosomal (abdominal) neuropil (Op).…”

“…Photoreceptor axons project from the median and lateral eyes to respective first and a second order visual neuropils situated at the lateral edge of the protocerebrum next to the cell body rind (Figure 5b,c and Lehmann & Melzer, 2018). In analogy to spiders (Long, 2020;Steinhoff et al, 2017), we refer to these small neuropils as lamina and medulla, F I G U R E 7 Summarizing sketch of mushroom body input pathways. Left side shows visual input, right side olfactory input.…”