|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
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
Early evolution of multifocal optics for well-focused colour vision in vertebrates
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
* Author for correspondence (e-mail: Ola.Gustafsson{at}cob.lu.se)
Accepted 10 March 2008
 |
Summary |
|---|
 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Key words: longitudinal spherical aberration, longitudinal chromatic aberration, lens, multifocal, colour vision, evolution, lamprey
|
INTRODUCTION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
). This
longitudinal chromatic aberration (LCA) leads to chromatic blur that degrades
image quality. In manufactured optical systems, LCA is minimized by using a
combination of several lenses composed of different refractive materials
(Hecht, 2002). The biological solution to LCA is the multifocal lens. Such a lens has several distinct zones that focus monochromatic light of a particular wavelength at different distances. Since the refractive power of the multifocal lens is also a function of the wavelength of light, each of the zones of different focal length for monochromatic light focuses a different band of wavelengths on the same plane in the retina. A sharp colour image is created on the background of defocused light. This solution seems at first sight to be inferior to the technical solution, but has the important advantage that the optical system is considerably smaller, which is of energetic benefit to the animal.
Multifocal lenses were first discovered in the African cichlid fish
Astatotilapia (formerly Haplochromis) burtoni
(Kröger et al., 1999),
where each of the three focal lengths of the lens focuses wavelengths that
closely match the wavelength of maximum absorbance (
max) of
one of the three cone photoreceptor types present in the retina. Multifocal
lenses are now known to be present in other species of bony fish
(Malkki and Kröger, 2005;
Karpestam et al., 2007) and
this mechanism for minimizing LCA was retained when the cornea came into play
as a refractive element during the evolutionary transition from aquatic to
terrestrial life. The success of this optical design is reflected in the
multifocal systems present in a variety of amphibians, reptiles and mammals
(including primates) (Malmström and
Kröger, 2006). The evolutionary origins of this lens design,
however, are unknown.
It is known that the ability to discriminate between different wavelengths
of light (colour vision) evolved very early. The southern hemisphere lamprey
Geotria australis possesses five photopigments with
max of 359 nm, 439 nm, 497 nm, 492 nm and 560 nm
(Davies et al., 2007). At least
three of the five visual pigments [long wavelength sensitive (LWS), and short
wavelength sensitive types 1 and 2 (SWS1 and SWS2)] are orthologous to the
visual pigments in jawed vertebrates
(Collin et al., 2003a).
Although rod opsin-like opsin type A (RhA) and type B (RhB) of lampreys share
similarities with the rod opsin (Rh1) and Rh1-like cone opsin (Rh2) of jawed
vertebrates, respectively (Collin et al.,
2003b; Collin and Trezise,
2004; Pisani et al.,
2006; Collin and Trezise,
2006), the functional identity of the receptors housing these
visual pigments remains elusive. It has, however, been suggested that all five
photoreceptors in G. australis have close affinities to those of
cones in gnathostomes [jawed vertebrates
(Lamb et al., 2007)].
Lampreys and hagfishes are the only extant jawless fishes (Agnatha) and
they most closely resemble the earliest stage in vertebrate evolution. Fossils
of similar animals have been found in layers dating from the early Cambrian
[about 540 million years ago (MYA)] (Shu
et al., 2003). The separation of agnathans from the main
vertebrate lineage is thought to have occurred at least 500 MYA
(Gess et al., 2006). Although
the eyes of hagfishes are rudimentary, they may hold important clues about the
early evolution of the vertebrate eye
(Lamb et al., 2007). However,
since they lack a lens and further research is required to assess the
differentiation of the retinal photoreceptor types
(Holmberg, 1977), an analysis
of the eyes of adult lampreys, which possess well-developed eyes that closely
follow the eye design of jawed vertebrates
(Walls, 1942;
Duke-Elder, 1958), may hold
more promise in tracing the origin of multifocal optical systems.
In order to investigate whether the early evolution of a wide range of
chromatic sampling at the level of the photoreceptors
(Collin et al., 2003b) was
paralleled by the optical system of the eye, we studied lens optics in four
species of lamprey (Fig. 1).
The 38 known species of lampreys have an anti-tropical distribution with 34
species occurring in the northern hemisphere and four species in the southern
hemisphere (Gill et al.,
2003). We studied two species from the northern hemisphere:
Lampetra fluviatilis and Petromyzon marinus, and two species
from the southern hemisphere: Mordacia praecox and Geotria
australis. This covered all three extant families of lamprey
(Petromyzontidae, Mordaciidae and Geotriidae).
|
Lampreys spend several years as larvae (ammocoetes) buried in river beds,
filter-feeding and with their developing eyes covered by pigmented skin. The
eyes then rapidly become functional at the end of the larval period. Some
lampreys are anadromous, i.e. after metamorphosis they migrate from their
natal freshwater river into the sea to return years later and ascend the river
for breeding. The adults of these lamprey species parasitize bony fishes,
digesting blood and/or flesh from their hosts using horny teeth housed within
their specialized mouthparts. About half of the extant species of lampreys do
not have a parasitic stage, but spawn directly after transformation from
ammocoete to adult (Hardisty and Potter,
1971) and some populations have become land-locked in freshwater
systems.
The complement of photoreceptor types in the retina of each species of
lamprey examined is predicted to be an important factor in the selection
pressures underlying the evolution of multifocal lenses. In G.
australis there are five morphologically distinct photoreceptors (all
with cone-like characteristics), each expressing a different photopigment
(Davies et al., 2007). The
holarctic lampreys L. fluviatilis and P. marinus each
possess two morphological types [both considered to be cones by Dickson and
Graves (Dickson and Graves,
1979)] with max values of 525 nm and 600 nm,
and 517 nm and 555 nm, respectively
(Govardovskii and Lychakov,
1984; Harosi and Kleinschmidt,
1993). Only one morphological type (seemingly a hybrid between a
rod and a cone) has been described for M. mordax, which is the
parasitic homologue of M. praecox, with a max of
514 nm (Collin et al., 2004).
Presumably being a monochromat, M. praecox might do best with a
monofocal lens, whereas in the other species the spectral separation between
visual pigments housed within the outer segments of the different
photoreceptor types is wide enough to make multifocal lenses advantageous.
|
MATERIALS AND METHODS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
|
Three complementary methods were used to study the optical properties of
the crystalline lenses: eccentric slope-based infrared photoretinoscopy,
schlieren photography and laser scanning
(Malkki and Kröger,
2005).
Photoretinoscopy
The animals were lightly anaesthetized with 3-aminobenzoic acid ethyl ester
(MS-222, 100 mg l–1; Sigma, St Louis, MO, USA) in a small
water-filled aquarium at 10°C. After allowing the lamprey to acclimatize
for about 5 min, each eye was videotaped with a retinoscope for approximately
1–1.5 min and some typical frames exported to a computer using Adobe
Premiere 6.0 software. Developed by Schaeffel and coworkers
(Schaeffel et al., 1987;
Schaeffel et al., 1993),
eccentric slope-based infrared photoretinoscopy
(Fig. 2A) provided an
indication of the distance, relative to the camera, at which the eye is
focused. If an eye has multiple focal lengths, ring-like patterns varying in
brightness appear in the pupil. Infrared light was used to avoid interference
with the animals.
|
).
Laser scanning
We used a 537 nm diode-pumped solid-state laser in a scanning setup
(Fig. 2C) to determine
quantitatively the longitudinal spherical aberration (LSA) of the lens
(Campbell and Hughes, 1981;
Sivak, 1982;
Kröger et al., 1994;
Malkki and Kröger, 2005).
Polystyrene microbeads (diameter 100 nm) were added to the Ringer solution to
enhance the visibility of the laser beam. The beam was focused in front of the
lamprey lens using a lens with a focal length of 50 mm, to reduce beam
diameter, and scanned through a meridional plane of the lamprey lens. Each
lens was scanned twice and the scans were videotaped from above with a digital
camera (Sony DCR-TRV 730E PAL). After the optical experiments had been carried
out, lens diameter was measured with callipers to the nearest 0.1 mm. The
entire procedure for both lenses of an animal lasted between 45 and 60
min.
From the video sequence of each scan, 200 frames were exported using Adobe
Premiere 6.0. From these frames, the LSA was determined by using
custom-written software (Malkki and
Kröger, 2005). We were only interested in spherical
aberration, which is a symmetrical aberration, and therefore we averaged the
LSA curves across the optical axis over both halves of each lens. Each lens
was treated as an independent measurement since intra-animal variance is
higher than inter-animal variance using this technique
(Kröger et al., 2001).
The results were compared with schlieren images in which variation in focal
length is indicated by variation in colour
(Fig. 3C–F). Mean focal
lengths normalized to lens radius (R) were calculated as weighted
means [
(BCD·BEP)/BEP] with
0.01
BEP0.95R (BCD, back centre distance; BEP, beam entrance
position). These limits were used because the laser-scanning method has low
accuracy for small BEPs (Malkki and
Kröger, 2005) and most of the energy is reflected for BEPs
larger the 0.95R (Sroczynski,
1977).
|
|
RESULTS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Schlieren photography confirmed the photoretinoscopic results from the holarctic lampreys (Fig. 3C,D) and indicated that the southern hemisphere lampreys also have multifocal lenses (Fig. 3E,F). The findings were clearest for the holarctic lampreys, where several zones of different focal lengths were present, including a peripheral zone of long focal length that appeared dark on schlieren photographs and may be used to focus ultraviolet light on the retina. Schlieren photographs of M. praecox lenses revealed three well-defined zones (Fig. 3E). In G. australis, the zones were more diffusely demarcated, but equally different in focal length (Fig. 3F). M. praecox and G. australis lenses had zones of short focal length in the periphery.
The averaged results from laser scanning show that each species has a specific LSA curve, with sufficient variation in focal length across the aperture of the lens (Fig. 4) that all lenses can be classified as multifocal. The 90% confidence intervals of the LSA curves are separated at several places (arrowheads in Fig. 4), which means that the curves are significantly different at P<0.05.
|
|
DISCUSSION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
),
was not possible. The dispersive properties of lamprey lenses are currently
unknown and measuring LCA with several lasers of different wavelengths was
beyond the scope of this study. All lenses studied were small
(Table 1), which led to large
uncertainties in the mean LSA curves. Furthermore, only a few lenses could be
studied in the southern hemisphere lampreys.
A monofocal lens has little variation in back centre distance (BCD) as a
function of beam entrance position (BEP)
(Kröger and Gislén,
2004) and would appear unicoloured on schlieren images. A
homogenous spherical lens would have such severe spherical aberration that no
useful image would be created. A lens poorly corrected for LSA would focus
long wavelengths with its periphery and short wavelengths with its central
region. Furthermore, the LSA curve would have continually decreasing BCDs for
increasing BEPs. Such results were not obtained from any of the lenses
studied, which strongly suggests that all species studied possess multifocal
lenses.
The findings are clearest in the holarctic species. The small lens sizes of the southern hemisphere lampreys (Table 1) prohibited the use of photoretinoscopy and limited the spatial and spectral resolutions of the results obtained with schlieren photography and laser scanning. Small lens size is probably the main reason for the somewhat diffuse results obtained from the southern hemisphere species. There may, however, also be biological reasons for these results. Firstly, photoreceptor diameter is large relative to focal length in a small eye. This means that depth of focus is long, which in turn reduces the necessity to compensate for LCA. Secondly, small lenses consist of few cell layers, such that it may not be possible to accommodate several sharply bordered regions of different focal lengths within the lens diameter. This effect would be expected to be most severe in G. australis that has five spectrally different photopigments and this may explain why the most diffuse results were obtained from this species. However, both M. praecox and G. australis lenses show sufficient variation in BCD across the aperture (Fig. 4) to be considered multifocal.
As in the lampreys studied, teleost lenses may also have various
combinations of refractive zones. Diurnal planktivores of the Red Sea [three
species studied by Karpestam et al.
(Karpestam et al., 2007)] and
the crucian carp [Carassius carassius
(Malkki and Kröger,
2005)] have outer zones of long focal lengths, similar to the
lenses of L. fluviatilis and P. marinus. Several rings
alternating between two colours (Fig.
3C,D) have been observed in teleost lenses (unpublished results),
but are unusual. Three species of diurnal herbivores and two predatory species
of the Red Sea were found to have outer zones of long focal lengths
(Karpestam et al., 2007), as
in the lenses of M. praecox and G. australis. Interestingly,
schlieren images of M. praecox lenses could easily be confused with
schlieren images obtained from the diurnal planktivores of the Red Sea. The
LSA curves, however, reveal an important difference: the outer, almost
invisible zones have long focal lengths in the planktivores and are thought to
be used to focus UV light (Karpestam et
al., 2007), the corresponding zone in M. praecox lenses
has short focal length and its functional significance is unclear. Sensitivity
to infra-red (IR) light is unlikely, and even if it were present, there is
little difference in focal length of the lens between long visible and near-IR
wavelengths. Instead, for optical reasons, the zone may come about by
constraints on the cellular compositions of these small lenses.
The lenses of P. marinus, M. praecox and G. australis have in common that back centre distance increases with decreasing beam entrance position below 0.4R (Figs 3 and 4). This means that light passing through the central region of the lens is defocused. However, the effects on image quality are minor, since the area of the central region is small, such that little light passes through it. Furthermore, because of the small diameter of the region, depth of focus is long such that the tolerable amount of defocus is higher than in more peripheral regions of the lens.
The holarctic lampreys L. fluviatilis and P. marinus each
possess two morphological types of photoreceptor with different
max values
(Govardovskii and Lychakov,
1984; Harosi and Kleinschmidt,
1993) and although controversy still surrounds the identity of
these two receptor types (for a review, see
Collin and Trezise, 2006), the
molecular basis for colour discrimination is certainly present. Only one
morphological type has been described for M. mordax
(Collin and Potter, 2000;
Collin et al., 2004), which is
somewhat surprising, given that our results suggest that the sister species
M. praecox has some form of colour vision. G. australis,
with five types of photoreceptor characterized by anatomical, spectral and
molecular criteria would be predicted to possess the most advanced level of
colour discrimination of the four species examined here
(Collin et al., 2003b;
Collin and Trezise, 2004;
Collin and Trezise, 2006;
Davies et al., 2007). However,
in the small eyes that we could study, complex multifocal lenses may not be
necessary because of limited spatial resolution and thus long depth of focus
of such eyes. The long normalized focal lengths of G. australis
lenses (Table 1) increase depth
of focus even further. Fully developed multifocal lenses with sharply
demarcated zones of different focal lengths may therefore become necessary
first when the eyes have grown larger.
The mean normalised focal lengths of the lenses are 2.31R in both
L. fluviatilis and P. marinus, and 2.32R in M.
praecox. This is in the lower range of the focal lengths typical for
teleost lenses (2.2–2.8R)
(Matthiessen, 1882;
Kröger and Campbell,
1996), whereas the focal length of the lens is considerably longer
in G. australis (3.04R). The adults of M. praecox
(found in downstream regions of rivers), L. fluviatilis (Baltic Sea)
and P. marinus (Lake Michigan) live in deep or turbid waters, whereas
G. australis occurs close to the surface in clear water (Southern
Ocean) (Potter and Hilliard,
1987; Collin et al.,
2003b). It is therefore not surprising that G. australis
has the most advanced system of colour vision with five different visual
pigments and the longest focal length relative to lens size. Long focal length
increases image magnification and thus resolution, while it decreases light
gathering ability and thus sensitivity
(Land and Nilsson, 2002).
The evolution of multifocality
The presence of multifocal lenses in the eyes of lampreys confirms the
early origins of colour vision in vertebrates, and suggests that other aquatic
vertebrates and tetrapods have retained this optical feature, the latter
despite the transition from an aquatic environment to a terrestrial habitat,
where the cornea comes into play as an additional refractive element.
Therefore, in vertebrates, multifocal optical systems seem to be
evolutionarily older than monofocal systems. Monofocality is present mainly in
diurnal tetrapods, such as humans, which have pupils that are small relative
to the focal length of the eye
(Malmström and Kröger,
2006). In such an eye, depth of focus is long and LCA produces
little chromatic blur (Kröger,
2000; Land and Nilsson,
2002).
However, there are interesting examples of well-developed camera-type eyes
with large pupils that possess monofocal lenses, such as in cephalopods
(Land and Nilsson, 2002). The
firefly squid Watasenia scintillans is one of the few cephalopods
known to have the molecular basis for colour vision (Seidou, 1990) and
possesses a monofocal lens. The problem of chromatic defocus is solved instead
by a banked retina (Kröger and
Gislén, 2004). The presence of multifocal lenses in
representatives of all vertebrate classes studied thus far and their absence
in cephalopods suggests a monophyletic origin for this lens design. Convergent
evolution in so many vertebrate lineages is unlikely.
The evolution of camera-type eyes capable of forming an image and providing
directional information from a distance
(Nilsson, 1996;
Land and Nilsson, 2002) is
thought to have been an important factor in the `explosion' in species
diversity, i.e. the sudden appearance of many highly motile species with hard
skeletons (Budd, 2003) in the
Cambrian period (about 540 MYA). The presence of at least four visual pigments
[long wavelength sensitive (LWS), short wavelength sensitive type 1 and 2
(SWS1, SWS2) and an rod opsin (Rh) class of visual pigment
(Collin et al., 2003a)] in the
last common ancestor of jawed and jawless vertebrates suggests that the
earliest vertebrates were able to sample a rich spectral light environment and
enjoy the many advantages of colour vision. Our findings suggest that the eyes
of these ancient animals were capable of forming well-focused colour images.
This visual ability may have been critical for the evolutionary success of the
lineage leading to gnathostomes at a time when optimizing the visualization of
either food or predator had become of utmost importance.
LIST OF ABBREVIATIONS
max
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Budd, G. E. (2003). The Cambrian fossil record
and the origin of the phyla. Integr. Comp. Biol.
43,157
-165.
Campbell, M. C. W. and Hughes, A. (1981). An analytic, gradient index schematic lens and eye for the rat which predicts aberrations for finite pupils. Vision Res. 21,1129 -1148.[CrossRef][Medline]
Collin, S. P. and Potter, I. C. (2000). The ocular morphology of the southern hemisphere lamprey Mordacia mordax Richardson with special reference to a single class of photoreceptor and a retinal tapetum. Brain Behav. Evol. 55,120 -138.[CrossRef][Medline]
Collin, S. P. and Trezise, A. E. (2004). The origins of colour vision in vertebrates. Clin. Exp. Optom. 87,217 -223.[Medline]
Collin, S. P. and Trezise, A. E. O. (2006). Molecular evidence for dim-light vision in the last common ancestor of the vertebrates – response. Curr. Biol. 16, R320.[CrossRef]
Collin, S. P., Knight, M. A., Davies, W. L., Potter, I. C., Hunt, D. M. and Trezise, A. E. O. (2003a). Ancient colour vision: multiple of opsin genes in the ancestral vertebrates. Curr. Biol. 13,R864 -R865.[CrossRef][Medline]
Collin, S. P., Hart, N. S., Shand, J. and Potter, I. C. (2003b). Morphology and spectral absorption characteristics of retinal photoreceptors in the southern hemisphere lamprey (Geotria australis). Vis. Neurosci. 20,119 -130.[CrossRef][Medline]
Collin, S. P., Hart, N. S., Wallace, K. M., Shand, J. and Potter, I. C. (2004). Vision in the southern hemisphere lamprey Mordacia mordax: spatial distribution, spectral absorption characteristics, and optical sensitivity of a single class of retinal photoreceptor. Vis. Neurosci. 21,765 -773.[Medline]
Davies, W. L., Cowing, J. A., Carvalho, L. S., Potter, I. C.,
Trezise, A. E., Hunt, D. M. and Collin, S. P. (2007).
Functional characterization, tuning, and regulation of visual pigment gene
expression in an anadromous lamprey. FASEB J.
21,2713
-2724.
Dickson, D. H. and Graves, D. A. (1979). Fine structure of the lamprey photoreceptors and retinal pigment epithelium (Petromyzon marinus L.). Exp. Eye Res. 29, 45-60.[CrossRef][Medline]
Duke-Elder, W. S. (1958). The Eye in Evolution: System of Ophthalmology, Vol.1. St Louis, London: Mosby, Kimpton.
Gess, R. W., Coates, M. I. and Rubidge, B. S. (2006). A lamprey from the Devonian period of South Africa. Nature 443,981 -984.[CrossRef][Medline]
Gill, H. S., Renaud, C. B., Chapleau, F., Mayden, R. L. and Potter, I. C. (2003). Phylogeny of living parasitic lampreys (Petromyzontiformes) based on morphological data. Copeia 2003,687 -703.[CrossRef]
Govardovskii, V. I. and Lychakov D. V. (1984). Visual cells and visual pigments of the lamprey, Lampetra fluviatilis L. J. Comp. Physiol. 154A,279 -286.[CrossRef]
Hardisty, M. W. and Potter, I. C. (1971). The Biology of Lampreys. London, New York: Academic Press.
Harosi, F. I. and Kleinschmidt, J. (1993). Visual pigments in the sea lamprey, Petromyzon marinus. Vis. Neurosci. 10,711 -715.[Medline]
Hecht, E. (2002). Optics. San Francisco: Addison Wesley.
Holmberg, K. (1977). The cyclostome retina. In Handbook of Sensory Physiology: The Visual System in Vertebrates (ed. F. Crescitelli), pp.47 -66. New York: Springer-Verlag.
Karpestam, B., Gustafsson, J., Shashar, N., Katzir, G. and
Kröger, R. H. H. (2007). Multifocal lenses in coral reef
fishes. J. Exp. Biol.
210,2923
-2931.
Kröger, R. H. H. (2000). Optical and developmental constraints on colour vision with lens eyes. J. Opt. A Pure Appl. Opt. 2,R39 -R43.[CrossRef]
Kröger, R. H. H. and Campbell, M. C. W. (1996). Dispersion and longitudinal chromatic aberration of the crystalline lens of the African cichlid fish Haplochromis burtoni.J. Opt. Soc. Am. A 13,2341 -2347.[CrossRef]
Kröger, R. H. H. and Gislén, A. (2004). Compensation for longitudinal chromatic aberration in the eye of the firefly squid, Watasenia scintillans. Vision Res. 44,2129 -2134.[CrossRef][Medline]
Kröger, R. H. H., Campbell, M. C. W., Munger, R. and Fernald, R. D. (1994). Refractive index distribution and spherical aberration in the crystalline lens of the African cichlid fish Haplochromis burtoni. Vision Res. 34,1815 -1822.[CrossRef][Medline]
Kröger, R. H. H., Campbell, M. C., Fernald, R. D. and Wagner, H. J. (1999). Multifocal lenses compensate for chromatic defocus in vertebrate eyes. J. Comp. Physiol. A 184,361 -369.[CrossRef][Medline]
Kröger, R. H. H., Campbell, M. C. W. and Fernald, R. D. (2001). The development of the crystalline lens is sensitive to visual input in the African cichlid fish, Haplochromis burtoni.Vision Res. 41,549 -559.[CrossRef][Medline]
Lamb, T. D., Collin, S. P. and Pugh, E. N., Jr (2007). Evolution of the vertebrate eye: opsins, photoreceptors, retina and eyecup. Nat. Rev. Neurosci. 8, 960-975.[CrossRef][Medline]
Land, M. F. and Nilsson, D.-E. (2002). Animal Eyes. Oxford, New York: Oxford University Press.
Malkki, P. E. and Kröger, R. H. H. (2005). Visualization of chromatic correction of fish lenses by multiple focal lengths. J. Opt. A Pure Appl. Opt. 7, 691-700.[CrossRef]
Malmström, T. and Kröger, R. H.
(2006). Pupil shapes and lens optics in the eyes of terrestrial
vertebrates. J. Exp. Biol.
209, 18-25.
Matthiessen, L. (1882). Ueber die Beziehungen, welche zwischen dem Brechungsindex des Kerncentrums der Krystalllinse und den Dimensionen des Auges bestehen. Pflügers Arch. Gesamte Physiol. Menschen Tiere 27,510 -523.[CrossRef]
Nilsson, D.-E. (1996). Eye ancestry: old genes for new eyes. Curr. Biol. 6, 39-42.[CrossRef][Medline]
Pisani, D., Mohun, S. M., Harris, S. R., McInerney, J. O. and Wilkinson, M. (2006). Molecular evidence for dim-light vision in the last common ancestor of the vertebrates. Curr. Biol. 16,R318 -R319; author reply R320.[CrossRef][Medline]
Potter, I. C. and Hilliard, R. W. (1987). A proposal for the functional and phylogenetic significance of differences in the dentition of lampreys (agnatha: petromyzontiformes). J. Zool. Lond. 212,713 -738.
Schaeffel, F., Farkas, L. and Howland, H. C. (1987). Infrared photoretinoscope. Appl. Optics 26,1505 -1509.
Schaeffel, F., Wilhelm, H. and Zrenner, E.
(1993). Inter-individual variability in the dynamics of natural
accommodation in humans: relation to age and refractive errors. J.
Physiol. 461,301
-320.
Seidou, M., Sugahara, M., Uchiyama, H., Hiraki, K., Hamnaka, T., Michinomae, M., Yoshihara, K. and Kito, Y. (1990). On the three visual pigments in the retina of the firefly squid, Watasenia scintillans. J. Comp. Physiol. A 166,769 -773.
Shu, D. G., Morris, S. C., Han, J., Zhang, Z. F., Yasui, K., Janvier, P., Chen, L., Zhang, X. L., Liu, J. N., Li, Y. et al. (2003). Head and backbone of the Early Cambrian vertebrate Haikouichthys. Nature 421,526 -529.[CrossRef]
Sivak, J. G. (1982). Optical properties of a cephalopod eye (the short finned squid, Illex illecebrosus). J. Comp. Physiol. A 147,323 -327.[CrossRef]
Sroczynski, S. (1977). Spherical aberration of crystalline lens in the roach, Rutilus rutilus. J. Comp. Physiol. A 121,135 -144.[CrossRef]
Walls, G. L. (1942). The Vertebrate Eye and its Adaptive Radiation. Bloomfield Hills, MI: Cranbrook Institute of Science.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  F. D. Hanke, R. H. H. Kroger, U. Siebert, and G. Dehnhardt Multifocal lenses in a monochromat: the harbour seal J. Exp. Biol., October 15, 2008; 211(20): 3315 - 3322. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O. E. Lind, A. Kelber, and R. H. H. Kroger Multifocal optical systems and pupil dynamics in birds J. Exp. Biol., September 1, 2008; 211(17): 2752 - 2758. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
