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JCPA-S-19-00140.Pdf This is a post-peer-review, pre-copyedit version of an article published in Journal of Comparative Physiology A. The final authenticated version is available online at: https://doi.org/10.1007/s00359-019-01387-5. Access to this work was provided by the University of Maryland, Baltimore County (UMBC) ScholarWorks@UMBC digital repository on the Maryland Shared Open Access (MD-SOAR) platform. Please provide feedback Please support the ScholarWorks@UMBC repository by emailing [email protected] and telling us what having access to this work means to you and why it’s important to you. Thank you. Journal of Comparative Physiology A Optic lobe organization in stomatopod crustacean species having different degrees of retinal complexity --Manuscript Draft-- Manuscript Number: Full Title: Optic lobe organization in stomatopod crustacean species having different degrees of retinal complexity Article Type: S.I. : Visual Circuits Funding Information: Air Force Office of Scientific Research Dr. Thomas W Cronin (FA9550-18-1-0278) Abstract: Stomatopod crustaceans possess tripartite compound eyes; upper and lower hemispheres are separated by an equatorial midband of several ommatidial rows. The organization of stomatopod retinas is well studied, but their optic lobes are less understood. We used histological staining, immunolabeling, and fluorescent tracer injections to compare optic lobes in two 6-midband-row species, Neogonodactylus oerstedii and Pseudosquilla ciliata , to those in two 2-midband-row species, Squilla empusa and Alima pacifica . Compared to the 6-row species, we found structural simplification in all optic neuropils in both 2-row species. Photoreceptor axons from 2- row midband ommatidia supply two sets of enlarged lamina cartridges, but a gap in the lamina exists at the location where the cartridges of the dorsal four ommatidial rows of 6-row species would appear. The tripartite arrangement and enlarged axonal projections from the two rows of midband ommatidia can be traced throughout the entire optic lobe, but other details of both medullar and lobular neuropils found in 6-row species are lacking. Our results support the hypothesis that 2-row midband species are derived from an 6-row ancestor, and suggest that specializations in the deep medulla and lobula found solely in 6-row species are important for color and polarization analysis. Corresponding Author: Thomas W Cronin University of Maryland Baltimore County Baltimore, Maryland United States Corresponding Author Secondary Information: Corresponding Author's Institution: University of Maryland Baltimore County Corresponding Author's Secondary Institution: First Author: Thomas W Cronin First Author Secondary Information: Order of Authors: Thomas W Cronin Chan Lin, PhD Alice Chou, BS Order of Authors Secondary Information: Author Comments: This paper is for the special issue on "Visual Circuits in Arthropod Brains" Suggested Reviewers: Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporation Manuscript Click here to access/download;Manuscript;Stomatopod optic lobes - Lin et al.docx Click here to view linked References 1 2 3 4 5 1 Optic lobe organization in stomatopod crustacean species 6 7 8 2 having different degrees of retinal complexity 9 10 1,2, 1 1 11 3 Chan Lin , Alice Chou and Thomas W. Cronin 12 13 4 14 15 1 16 5 Department of Biological Sciences, University of Maryland Baltimore County, 17 18 6 Baltimore, Maryland 21250 19 20 2 21 7 Department of Invertebrate Zoology, Smithsonian National Museum of Natural History, 22 23 8 Washington, D.C. 20560 24 25 9 26 27 28 10 29 30 11 31 32 33 12 34 35 13 36 37 38 14 39 40 15 Supporting Grant: Air Force Office of Scientific Research (FA9550-18-1-0278) 41 42 16 43 44 45 17 46 47 18 48 49 50 19 51 52 20 53 54 55 21 56 57 22 58 59 60 23 61 62 63 1 64 65 1 2 3 4 24 5 ABSTRACT 6 7 25 Stomatopod crustaceans possess tripartite compound eyes; upper and lower hemispheres 8 9 10 26 are separated by an equatorial midband of several ommatidial rows. The organization of 11 12 27 stomatopod retinas is well studied, but their optic lobes are less understood. We used 13 14 28 histological staining, immunolabeling, and fluorescent tracer injections to compare optic 15 16 17 29 lobes in two 6 midband-row species, Neogonodactylus oerstedii and Pseudosquilla 18 19 30 ciliata, to those in two 2-midband-row species, Squilla empusa and Alima pacifica. 20 21 22 31 Compared to the 6-row species, we found structural simplification in all optic neuropils 23 24 32 in both 2-row species. Photoreceptor axons from 2-row midband ommatidia supply two 25 26 27 33 sets of enlarged lamina cartridges, but a gap in the lamina exists at the location where the 28 29 34 cartridges of the dorsal four ommatidial rows of 6-row species would appear. The 30 31 35 tripartite arrangement and enlarged axonal projections from the two rows of midband 32 33 34 36 ommatidia can be traced throughout the entire optic lobe, but other details of both 35 36 37 medullar and lobular neuropils found in 6-row species are lacking. Our results support the 37 38 39 38 hypothesis that 2-row midband species are derived from a 6-row ancestor, and suggest 40 41 39 that specializations in the deep medulla and lobula found solely in 6-row species are 42 43 44 40 important for color and polarization analysis. 45 46 41 47 48 49 42 KEYWORDS 50 51 43 Stomatopoda; compound eye; visual system; neuroanatomy; vision 52 53 54 44 55 56 45 INTRODUCTION 57 58 59 60 61 62 63 2 64 65 1 2 3 4 46 Stomatopod crustaceans, known commonly as mantis shrimps, are predatory marine 5 6 7 47 invertebrates considered to possess some of the most complex visual systems known to 8 9 48 biologists, being capable of color vision, ultraviolet vision, motion vision, and both linear 10 11 12 49 and circular polarization vision (Bok et al. 2015; Chiou et al. 2008; Cronin and Marshall 13 14 50 1989a; Cronin et al. 1994; 2003; Kleinlogel and Marshall 2006; Marshall and 15 16 51 Oberwinkler 1999; Marshall 1988; Marshall et al. 1991a,b; 1996; 1999). Approximately 17 18 19 52 400 described species of this order inhabit a diversity of photic environments, most in 20 21 53 shallow, tropical waters, and display a variety of eye designs (Harling 2000; Manning et 22 23 24 54 al. 1984; Marshall et al. 1991a,b). Comprised of thousands of ommatidia, their apposition 25 26 55 compound eyes are divided into three regions with overlapping visual fields (Fig. 1): the 27 28 29 56 upper and lower hemispheres, and a specialized midband region dividing the two (Cronin 30 31 57 1986; Exner 1891; Horridge 1978; Marshall and Land 1993a,b; Marshall et al. 1991a,b). 32 33 34 58 The upper and lower hemispheres are structured much like the eyes of typical 35 36 59 malacostracan crustaceans and are thought to encode luminance, linear polarization 37 38 60 information, and spatial vision (Cronin and Marshall 2004; Marshall et al. 1991a; 2007). 39 40 41 61 The rhabdoms here are split into two tiers, consisting of a distal R8 cell and the 42 43 62 underlying fused R1-R7 cells. 44 45 46 63 The equatorial midband is more complicated, comprised of two, three, or six 47 48 64 parallel rows of enlarged ommatidia (Harling 2000; Manning et al. 1984; Marshall 1988; 49 50 51 65 Marshall et al. 1991a). Modifications within midband ommatidia produce the very 52 53 66 unusual color vision system characteristic of stomatopods. In four stomatopod 54 55 67 superfamilies (Gonodactyloidea, Lysiosquilloidea, Pseudosquilloidea, and 56 57 58 68 Hemisquilloidea), the midband is comprised of six ommatidial rows, within which up to 59 60 61 62 63 3 64 65 1 2 3 4 69 14 morphologically and functionally distinct photoreceptor classes have been 5 6 7 70 documented (Cronin and Marshall 1989a,b; Cronin et al. 1994; Marshall and 8 9 71 Oberwinkler 1999; Marshall 1988; Marshall et al. 1991a,b). The rhabdoms of midband 10 11 12 72 rows 1-4 are uniquely arranged into three distinct tiers formed by subsets of 13 14 73 photoreceptors. This arrangement, together with a system of filtering pigments in rows 2 15 16 74 and 3, allows absorbance of different parts of the color spectrum by the different 17 18 19 75 photoreceptor subsets as the light passes through the entire length of the rhabdom (Cronin 20 21 76 et al. 2014; Cronin and Marshall 1989a,b; Marshall et al. 1991b). Surprisingly, despite 22 23 24 77 the numerous color channels found in 6 midband-row species, these animals perform 25 26 78 poorly in behavioral wavelength discrimination tests (Thoen et al. 2014). In midband 27 28 29 79 rows 5 and 6, the distal photoreceptor R8 cells detect linear polarized light in the UV 30 31 80 range and serve as a quarter-wave retarder for the underlying photoreceptors R1-7, 32 33 34 81 allowing them to detect circularly polarized light (Chiou et al. 2008; Roberts et al. 2009). 35 36 82 Unlike the animals just described, species of the superfamily Squilloidea, which 37 38 83 often live in deeper or more turbid habitats, possess only two midband rows and show no 39 40 41 84 sign of color vision (Cronin 1985; Cronin et al. 1993; Exner 1891; Marshall et al. 1991a; 42 43 85 Schiff 1963). Phylogenetic analyses suggest that this decreased visual complexity is an 44 45 46 86 evolutionary loss (Ahyong and Harling 2000; Ahyong and Jarman 2009; Harling 2000; 47 48 87 Porter et al.
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