Early Vertebrate Colour Vision --.No Oil Droplels ___~--:--~--

SCIENTIFIC CORRESPONDENCE

-- Coloured oil droplets -- Colourless oil droplels Early vertebrate colour vision --.No oil droplels ___~--:--~-- .. Hagfish SIR - A feature of retinae in lizards, edge to include orange. The density of ___------Lampreys turtles and birds is the intercalation of a red droplets is always reduced in regions ...... ---;----- .. Rat fish coloured oil droplet between the inner where orange droplets are present, but ""--~-__:_--_:_-- . Sharks, rays elc. and outer segments of cone photoreceptor there is no reduction in the density of __------. Polyplenus ""--"""'----.,..---: Sturgeons cells l,2. The colour in the droplets absorbs small colourless droplets or cones contain -..,~---- : Bowfin, garpike particular wavelengths of light, thereby ing golden granular pigment. --i---: Teleosts narrowing the spectral sensitivity of the The cone oil droplets in Neoceratodus ------. Coelacanlh four opsins (visual-pigment proteins) that have a larger diameter (6-15 ~m) than ------.. Lungfish are located in the outer segments. The those in turtles (3-10 ~m)8,9 or birds (1-6 ~----- Frogs ~----,: Urodeles result is a tetrachromatic visual system ~m)9,1O. The droplet colours observed in ----'----:' Caecilians with a broad sensitivity that extends from Neoceratodus, as well as colourless drop _--- Crocodiles elc. near-ultraviolet (-350 nm) to infrared lets and cones with a yellow granular ~~--.;..--:: Birds 3 5 (-750 nm) (birds ,4, turtles ,6). The Au pigment in the ellipsoid, are found in ~----': Sphenodon 3 5 --..---. Lizards stralian lungfish, Neoceratodus forsteri, birds ,4,9,10 and turtles ,6,8,9, but not all : Snakes belongs to the order Dipnoi which di colours are present in every species. ----, Turtles verged from the main vertebrate stock in Walls l proposed that coloured oil drop "",--i---,: Monotremes --~--:: Marsupials the early Devonian. N. forsteri fossils have lets appeared very early in vertebrate , Placentals evolution, and that when species adopted I I I I a nocturnal habit, colour was lost from 500 400 300 200 100 their droplets, or the droplets were elimin Million years ated. Once lost, the colours could not be FIG. 2 Approximate origins of the main extant regained, even if the descendants of a vertebrate taxa, based on data in refs 1,2,11. nocturnal animal colonized a diurnal Taxons lacking oil droplets in their cone photo• niche, as has occurred among some mam receptors are indicated in grey, those with mals and frogs. This proposal was not colourless droplets in blue, and those with widely accepted because of the restriction coloured droplets in red. Until now, the dis• tribution of coloured droplets was consistent of coloured oil droplets to a small part of with an origin about 250 million years ago. the vertebrate series. The restricted dis The finding of coloured droplets in lungfish tribution could be explained more simply supports a common origin 400 million years if coloured oil droplets originated about ago. 250 million years ago in the common ancestors of turtles, birds and reptiles advantage when many opsins are present. (Fig. 2). The discovery of coloured oil This perspective favours the idea that droplets in the lungfish provides much Neoceratodus has four cone opsins, and FIG. 1 Photomicrograph showing the array of stronger support for the notion that col raises the possibility that the ancestral coloured oil droplets in the cone photorecep• oured oil droplets were present in the Sarcopterygii had tetrachromatic vision. tors of an unstained Neoceratodus retina. The lobe-finned ancestors of land vertebrates Stephen R. Robinson small colourless droplets are not evident in (Sarcopterygii) more than 400 million Vision, Touch and Hearing Research this plane of focus. Lungfish were deeply years ago (Fig. 2). Centre, anaesthetised, their eyes quickly removed, The number of cone opsins possessed University of Queensland, and the retinae immersed for 24 hours in 4% by Neoceratodus is unknown. However, in Brisbane, paraformaldehyde and 2.5% glutaraldehyde in 0.1 M phosphate buffer (pH 7.4). The all vertebrates that have been studied, Australia 4072 retinae were then flatmounted with the photo• colour vision is achieved through the use receptor layer uppermost, and coverslipped in of two or more different photopigments, 50% glycerol in 0.1 M phosphate buffer. rather than by coloured oil droplets in Visual stability Magnification, x 150. combination with a single opsin-A. The fact that coloured oil droplets are re during eyeblinks been dated at well over 100 million years, stricted to those vertebrates which have making this the oldest extant vertebrate four or more cone opsins4 implies that the SIR - During each eyeblink we lose sight species? Here I show that N. forsteri colour in the droplets only conveys an of the visual world for more than a tenth of has coloured droplets in its cone photo a second without usually perceiving the receptors, suggesting that the common 1. Walls, G.l. The Vertebrate Eye and itsAdaptiveRadiation discontinuity. A suppression of visual 1 2 ancestors of lungfish and land vertebrates (Bloomford Hills, Michigan, 1942). sensitivity during blinks • explains why 2. Crescitelli, F. in Photochemistry of Vision (ed. Dartnall, darkening is not seen but it is not sufficient also had coloured oil droplets and, H.J. A.) 245-363 (Springer, Berlin, 1972). perhaps, tetrachromatic vision. 3. Partridge,J. C.). compo Physiol. A165, 415-426 (1989). to account for the continuity of visual In the eight Neoceratodus retinae that I 4. Bowmaker,J. K. in The Perception ofColour; Vision and perception. Here we report on activation Visual Dysfunction Vol. 6 (ed. Gouras, P.) 108-127 have studied, cones are distributed at (Macmillan, Basingstoke, 1991). of the human parietal lobe after voluntary densities of 2,500-4,600 mm-2 and they 5. Lipetz, l. E. in The Visual System (eds Fein, A. & Levine, J. blinks. The posterior parietal cortex - an S.) 107-132 (Liss, NewYork,1985). compose 50-56% of the photoreceptor 6. Ohtsuka, T.1. compo Neurol. 237,145-154 (1985). essential part of the spatial working mem 3 population, the remainder being rods: 7. Kemp, A. in Vertebrate Palaeontology ofAustralasia (eds ory system - may have a role in main Vickers-Rich, P. et al.) 465-496 (Pioneer Design Studio, 65-75% of cones possess red oil droplets, Melbourne,1991). taining a stable image despite the inter 5 -10% have small colourless droplets, 8. Kolb, H. &Jones, J.). compo Neurol. 209, 331-338 ruption of visual input during blinks. and the rest (15-25%) have a golden (1982). We studied five adult subjects (ages 9. Kawata, A. etal. Photochem. Photobiol. 56,1157-1166 granular pigment at the base of the outer (1992). 27-34 yr; 3 females) with a helmet-shaped segment, instead of an oil droplet (Fig. 1). 10. Cserhilli, P., Szel, A. &Rbhlich, P. Invest. ophthal. Vis. 122-channel SQUID (superconducting Sci. 30, 74--81(1989). In some Neoceratodus the variety of 11. Marshall, C. & Schultze, H.-P.). molec. Evol. 35. quantum interference device) magneto oil droplets increases towards the retinal 93-101 (1992). meter (Neuromag-122™). The subjects

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