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Gecko Vision—Retinal Organization, Foveae and Implications for Binocular Vision

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Gecko Vision—Retinal Organization, Foveae and Implications for Binocular Vision CORE Metadata, citation and similar papers at core.ac.uk Provided by Elsevier - Publisher Connector Vision Research 41 (2001) 2043–2056 www.elsevier.com/locate/visres Gecko vision—retinal organization, foveae and implications for binocular vision Beate Ro¨ll* Lehrstuhl fu¨r Tierphysiologie, Fakulta¨t fu¨r Biologie, Ruhr-Uni6ersita¨t Bochum, D-44780 Bochum, Germany Received 11 August 2000; received in revised form 16 February 2001 Abstract Geckos comprise both nocturnal and diurnal genera, and between these categories there are several transitions. As their retinae have definitely to be classified as pure cone retinae, they provide an especially attractive model for comparison of organization and regional specializations adapted to very different photic environments. While the visual cells themselves show clear adaptations to nocturnal or diurnal lifestyles, the overall retinal organization is more related to that of diurnal vertebrates. Nocturnal geckos have lost any foveae of their diurnal ancestors, but they have retained a low convergence ratio and a high visual cell density. To enhance visual sensitivity, they exploit binocular — but not necessarily stereoscopic — vision. Diurnal species have retained binocular vision. Most diurnal species have developed new foveae, which are consequently located not in the central but in the temporal region of the retina. © 2001 Elsevier Science Ltd. All rights reserved. Keywords: Geckos; Retinal organization; Binocular vision; Foveae; Evolution 1. Introduction of the retinal neurons (Rodieck, 1973). Typically, these retinae are provided with regional specializations, e.g. The basic structure of vertebrate retinae comprises visual streaks, areae or foveae, which show higher three cellular and three neural layers. From sclerad to densities of visual and/or ganglion cells compared with vitread the nuclei of the visual cells, which form the the unspecialized regions. outer nuclear layer, are followed by the outer plexi- Most lizards are strictly diurnal. Their retinae usually form, inner nuclear, inner plexiform, ganglion cell and lack rods and are generally characterized by centrally optic nerve fiber layers. However, both the visual cells located foveae. Pure-cone retinae appear to be common and the other retinal neurons tend to vary in size, in lizards like iguanids, chameleonids, agamids, scin- shape, number and arrangement among vertebrate cids, lacertids, anguids, pygopodids and varanids (De- groups. These variations reflect habits and habitats of twiler & Laurens, 1920; Verrier, 1933; Underwood, the different groups. Most striking are retinal adapta- 1951, 1957, 1970; Anh, 1968, 1969; Crescitelli, 1972; tions to nocturnality and diurnality. Young, 1977; Armengol, Prada, Ambrosiani, & Genis- Visual cells of vertebrates are usually categorized into Galvez, 1988; Ro¨ll, 1998; Ro¨ll & Horn, 1999). Their rods and cones, which operate maximally at low and foveae are convexiclivate in eyes of chameleonids, high light intensities, respectively. Accordingly, retinae iguanids and agamids or more concaviclivate or shal- of strictly nocturnal vertebrates are dominated by rods. low in eyes of lacertids, scincids and varanids (Detwiler In contrast, retinae of diurnal vertebrates have high & Laurens, 1920; Verrier, 1933; Walls, 1942; Vilter, numbers of cones, while the population of rods is small 1949; Williams, Colley, Anderson, Farber, & Fisher, or completely absent. Furthermore, retinae of diurnal 1986; Lanuza, Martı´nez-Marcos, Font, & Martı´nez- animals are characterized by thick inner nuclear and Garcı´a, 1996; Ro¨ll, 1998). The eyes of anoline iguanids inner plexiform layers due to the connectivity patterns are unique among reptiles in that they are bifoveate with both a convexiclivate central and a shallow tempo- * Tel.: +49-234-3224327; fax: +49-234-3214185. ral fovea (Makaretz & Levine, 1980; Fite & Lister, E-mail address: [email protected] (B. Ro¨ll). 1981). 0042-6989/01/$ - see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0042-6989(01)00093-1 2044 B. Ro¨ll / Vision Research 41 (2001) 2043–2056 However, the majority of the Gekkonidae, the sec- species and the ultrastructure of foveal visual cells is ond largest extant lizard family, is nocturnal. Geckos unknown. In this study, retinae of different diurnal and are small to moderate-sized, agile lizards occurring nocturnal geckos are investigated with emphasis on worldwide in tropical and subtropical regions. Only 15 retinal organization and occurrence and structure of genera out of approximately 90 are diurnal, and be- foveae. tween the categories ‘nocturnal’ and ‘diurnal’ there are several transitions. With regard to their evolution, the Gekkonidae are unique among lizards. According to 2. Materials and methods Walls (1934, 1942), nocturnal geckos are supposed to have descended from primarily diurnal lizard ancestors 2.1. Materials with pure cone-retinae possessing coloured oil droplets. Thus, the rod-like visual cells of extant nocturnal Animals were housed in glass terraria under a 12 h geckos have transmuted from cones. However, they light/dark cycle; temperatures ranged from 21–23°Cat generally lack oil droplets (Walls, 1942; Underwood, night to 28–34°C during the day. The geckos were fed 1951, 1970; Ro¨ll, 2000a). Regarding nocturnality as a a variety of insects and their larvae; drinking water was derived character, Walls designated geckos as ‘secon- enriched with calcium, phosphate and vitamins. Several darily’ nocturnal. Several genera have reverted from species were reared in the laboratory; of a few species nocturnal to diurnal habits again, designated as ‘tertiar- only one or two specimens have been available. ily’ diurnal by Walls. Their visual cells have undergone Retinae of the following species were examined: (1) a second transmutation from superficially rod-like vi- diurnal species (Gonatodes albogularis, G. 6ittatus, sual cells back to cones, most of which also lack oil Lygodactylus picturatus, L. chobiensis, Phelsuma an- droplets. However, the visual cells of both nocturnal damanensis, P. dubia, Pristurus rupestris, Quedenfeldtia and diurnal geckos exhibit characteristics of cones at all trachyblepharus, Rhoptropus barnardi ); crepusculo-diur- levels of their ultrastructure (Ro¨ll, 2000b). The bio- nal species (Sphaerodactylus elegans, S. glaucus); noc- chemical compositions of gekkonid eye lenses and ge- turno-diurnal species (Phelsuma guentheri ); (2) netics of the visual pigments strongly support this nocturnal species (Paroedura pictus, Phyllopezus polli- notion. The lenses of diurnal geckos contain a specific caris, Stenodactylus sthenodactylus, Tropiocolotes nat- ultraviolet filter consisting of vitamin A2 bound to tereri, Uroplatus phantasticus) and diurno-nocturnal i-crystallin, which is identical with the cellular retinol- species (Ailuronyx seychellensis, Lepidodactylus lugu- binding protein type I (Ro¨ll, Amons, & de Jong, 1996; bris). The experiments were performed in compliance Ro¨ll & Schwemer, 1999). The visual pigments both of with the current laws of the Federal Republic of nocturnal and diurnal geckos show greatest similarities Germany. to those of cone opsins (Kojima, Okano, Fukada, Shichida, Yoshizawa, & Ebrey, 1992; Taniguchi, 2.2. Electron microscopy Hisatomi, Yoshida, & Tokunaga, 1999). Geckos appar- ently have a trichromatic visual system with absorption Light- and/or dark-adapted (minimum of 4 h) ani- maxima in the violet, blue and green wavelength range mals were anaesthetized by chilling to 4°C, killed by (e.g. Crescitelli, 1972; Ro¨ll, 1996a; Loew, Govardoskii, decapitation and enucleated. The eyes were either fixed Ro¨hlich, & Sze´l, 1996). whole or after removal of cornea, iris, lens and vitreous. Geckos are a distinct phylogenetic group of lizards Both whole eyes and eye cups were marked by small depending mainly on their visual sense for prey capture, incisions at the dorsal and nasal retinal margins for regardless of their activity periods. As their retinae are reconstruction of the orientation of the preparations. pure cone retinae, both scotopic and photopic vision in Samples were fixed for 2–4 h in 2% paraformaldehyde, geckos is performed by one basic visual cell type. Thus, 2.5% glutaraldehyde in phosphate buffered saline at pH their retinae provide an especially attractive model for 7.2. Some of the specimens were fixed for 4 h in 4% comparison of organization and regional specializations paraformaldehyde, 3% glutaraldehyde, 6% acrolein, adapted to very different photic environments. 10% dimethylsulphoxide at pH 7.2 in 0.1 M cacodylate Up to now, regional specializations typical for reti- buffer. After rinsing, the preparations were postfixed in nae of predatory vertebrates have been mentioned in 2% osmium tetroxide for 2 h and dehydrated through a the eyes of the neotropical diurnal gekkonid genera graded ethanol series (range 30–100%). The samples Gonatodes and Sphaerodactylus and in one representa- were passed through propyleneoxide or acetone and tive of the Madagascan genus Phelsuma: retinae of embedded in Epon or Spurr’s epoxy resin, respectively. these genera are provided with foveae (Underwood, Eye cups were carefully oriented before polymerization 1951; Tansley, 1964). The fovea of the Phelsuma species so that longitudinal or tangentional sections through is described as being shallow and poorly developed. the fovea could be obtained. Serial semithin sections Both the morphology of the foveae of other diurnal were stained with toluidene
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