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First published online May 2, 2008
Journal of Experimental Biology 211, 1559-1564 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016048

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Early evolution of multifocal optics for well-focused colour vision in vertebrates

O. S. E. Gustafsson^1,*, S. P. Collin² and R. H. H. Kröger¹

¹ Department of Cell and Organism Biology, Lund University, Helgonavägen 3, 223 62 Lund, Sweden
² Marine Neurobiology Laboratory, School of Biomedical Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia

View larger version (77K): [in this window] [in a new window]   Fig. 1. Images of the four species of lamprey used in this study. (A) Lampetra fluviatilis (river lamprey). (B) Petromyzon marinus (sea lamprey). (C) Mordacia mordax [the parasitic homologue of the non-parasitic Mordacia praecox, from Collin et al. (Collin et al., 2004)]. (D) Geotria australis (pouched lamprey) [from Collin et al. (Collin et al., 2003b)]. Scale bars, 20 mm. Note that the eyes are well developed in all species.

View larger version (14K): [in this window] [in a new window]   Fig. 2. Schematic representations of the three methods used to study the optical properties of the lamprey eyes. (A) Photoretinoscopy. The lower half of the objective of an infrared-sensitive digital camera is covered by a black occluder holding an array of infrared light-emitting diodes (LEDs). Light reflected back towards the camera from the fundus of the eye is spatially filtered by the occluder, which leads to a light upper half of the pupil if the eye is focused behind the camera and a light lower half of the pupil if the eye is focused in front of the camera. Multifocal optical systems lead to alternating light and dark regions in the pupil. (B) Schlieren photography (setup seen from above). White light is reflected via a beam splitter onto the lamprey lens. The light is focused by the lamprey lens onto a diffuse reflector. Reflected light is focused by the lamprey lens onto a small aperture (pinhole) mounted in front of a digital colour camera. Only light that has passed through the pinhole can be used to take a photograph of the lamprey lens. (C) Laser scanning. The beam of a green laser is focused to reduce beam diameter and scanned through a meridional plane of the lens. Beam paths are recorded with a digital video camera. Longitudinal spherical aberration (LSA) is determined from exported frames by a custom-written program.

View larger version (91K): [in this window] [in a new window]   Fig. 3. Retinoscopic photographs (A,B) and comparisons of longitudinal spherical aberration (LSA) curves with schlieren photographs for individual lamprey lenses (C–F). (C) Comparisons between the LSA curve and a schlieren photograph of a representative L. fluviatilis lens. The grey line is the mean LSA curve of 21 lenses from Astatotilapia burtoni, the species in which multifocal lenses were discovered (Kröger et al., 1999). The A. burtoni curve was scaled for easier comparison and shows less variation because averaging smoothes the data somewhat. The graph (LSA) shows the axial distance between the centre of the lens and where the beam intercepts the optical axis (back centre distance, BCD) as a function of the lateral distance between the optical axis and the undeflected entrance beam (beam entrance position; BEP) in units of lens radius (R). The curves were terminated at 0.95R because most of the energy incident on a fish lens at higher BEPs is reflected (Sroczynski, 1977). Close to the optical axis the laser-scanning method has low accuracy (Malkki and Kröger, 2005). (D) Comparisons as in C for P. marinus. (E) Comparisons as in C for M. praecox. (F) Comparisons as in C for G. australis. Note that the BCDs are short for BEPs corresponding to radial positions in the lens with reddish areas in the schlieren photographs. By contrast, the BCDs peak at positions corresponding to bluish areas in the schlieren photographs. The results obtained with both methods therefore consistently indicate that lamprey lenses are multifocal and compensate for LCA. Zones that are dark on the schlieren photographs may focus either infrared (short BCDs) or ultraviolet (long BCDs) light. Note that the scale of the y axis is different for G. australis. Scale bars, 1 mm.

View larger version (16K): [in this window] [in a new window]   Fig. 4. Mean longitudinal spherical aberration (LSA) curves with 90% confidence intervals for the four species of lamprey and the mean curve of A. burtoni (grey line). Averaging the results from several lenses (for numbers see Table 1) leads to some smoothing of the curves (compare with curves in Fig. 3). Note that the confidence intervals do not overlap in some regions (arrowheads), which means that the curves are different at the P<0.05 level. The laser-scanning method has low accuracy for small beam entrance positions (BEPs; close to the optical axis) because of technical reasons (Malkki and Kröger, 2005). This leads to very large error margins. All curves have been terminated at 0.95R (see Fig. 3 legend). The A. burtoni curve has been scaled for easier comparison. Note that the LSA curves of the lampreys have at least as much variation in back centre distance (BCD) as the curve of A. burtoni lenses (grey line) which are known to be multifocal. (1) The LSA curve of L. fluviatilis is different from all other curves. (2) The M. praecox curve is different from all other curves. (3) G. australis lenses had longer normalized focal lengths than the lenses of all other species studied, which is indicated by the vertical shift of the LSA curve of G. australis.

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