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Phil. Trans. R. Soc. B (2009) 364, 2925–2940
doi:10.1098/rstb.2009.0099
Review
The evolution of early vertebrate
photoreceptors
Shaun P. Collin1,*, Wayne L. Davies2, Nathan S. Hart1 and
David M. Hunt3
1
School of Biomedical Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
2
Nuffield Laboratory of Ophthalmology, University of Oxford, The John Radcliffe Hospital,
Headley Way, Oxford OX3 9DU, UK
3
UCL Institute of Ophthalmology, 11 – 43 Bath Street, London EC1V 9EL, UK
Meeting the challenge of sampling an ancient aquatic landscape by the early vertebrates was crucial to their survival and would establish a retinal bauplan to be used by all subsequent vertebrate
descendents. Image-forming eyes were under tremendous selection pressure and the ability to
identify suitable prey and detect potential predators was thought to be one of the major drivers
of speciation in the Early Cambrian. Based on the fossil record, we know that hagfishes, lampreys, holocephalans, elasmobranchs and lungfishes occupy critical stages in vertebrate evolution,
having remained relatively unchanged over hundreds of millions of years. Now using extant
representatives of these ‘living fossils’, we are able to piece together the evolution of vertebrate
photoreception. While photoreception in hagfishes appears to be based on light detection and
controlling circadian rhythms, rather than image formation, the photoreceptors of lampreys fall
into five distinct classes and represent a critical stage in the dichotomy of rods and cones. At
least four types of retinal cones sample the visual environment in lampreys mediating photopic
(and potentially colour) vision, a sampling strategy retained by lungfishes, some modern teleosts,
reptiles and birds. Trichromacy is retained in cartilaginous fishes (at least in batoids and
holocephalans), where it is predicted that true scotopic (dim light) vision evolved in the
common ancestor of all living gnathostomes. The capacity to discriminate colour and balance
the tradeoff between resolution and sensitivity in the early vertebrates was an important driver
of eye evolution, where many of the ocular features evolved were retained as vertebrates
progressed on to land.
Keywords: photoreception; cones; rods; opsin genes; visual pigments; spectral sensitivity
1. INTRODUCTION
(a) The earliest vertebrates
Lampreys and hagfishes are the sole survivors of the
very early agnathan (jawless) stage in vertebrate evolution (Hardisty 1982). Ancient hagfishes, based on a
single fossil specimen, Myxinikela siroka, found in
similar deposits to fossil lampreys, are thought to
date back to the Cambrian, with M. siroka surviving
until the end of the Triassic era (Bardack 1991,
1998). Extant hagfishes have changed little, and are
considered monophyletic and comprise 60 species
within five genera: Paramyxine, Eptatretus (35 species),
Myxine (19 species), Notomyxine (single species),
Neomyxine (single species) and Nemamyxine (two
species) (Fernholm 1998). These bottom-dwelling,
cartilaginous fishes are found in deep, cold water on
all continents (except Antarctica) and feed on dead or
moribund fish and invertebrates with two sets of laterally
* Author for correspondence ([email protected]).
One contribution of 13 to a Theme Issue ‘The evolution of
phototransduction and eyes’.
everting and biting or scraping teeth or cusps (Fernholm
1998). Hagfishes possess a pair of lateral eyes embedded
beneath an opaque patch of cranial epithelium.
Although the eyes of hagfishes have traditionally been
thought to be degenerate (Holmberg 1970, 1971), lacking a lens and both intra- and extraocular eye muscles,
recent studies consider that they may represent a
‘missing link’ in eye evolution, lying intermediate between
the non-image-forming eyes of tunicates and the
image-forming eyes of lampreys (Lamb et al. 2007, 2008).
Recent studies have shown that lampreys, or their
very close relatives, had already evolved by the Lower
Cambrian period (ca 540 Ma; Xian-Guang et al.
2002; Shu et al. 2003). While all 34 species of Northern Hemisphere (or holarctic) lampreys (Renaud
1997) are placed in a single family (the Petromyzontidae), the four species of Southern Hemisphere
lampreys are separated into either the Geotriidae or
Mordaciidae (Potter 1980). It has been proposed
that both latter families were derived independently
from stocks similar to those of contemporary representatives of the holarctic genus Ichthyomyzon (Hubbs &
Potter 1971; Potter & Hilliard 1987; Gill et al.
2925
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S. P. Collin et al.
Review. Vertebrate photoreceptor evolution
2003). The Geotriidae is represented solely by Geotria
australis, an anadromous species, which is found in
rivers in New Zealand, southern Australia, Tasmania,
Chile and Argentina (Potter & Strahan 1968), while
the Mordaciidae contains two anadromous species
(Mordacia mordax and Mordacia lapicida), restricted
to rivers in eastern Australia and Chile, respectively
(Potter & Strahan 1968; Potter et al. 1978), and a
non-parasitic species, Mordacia praecox. The eyes of
larval lampreys or ammocoetes are similar to those of
hagfishes, i.e. are buried beneath the skin, where
most of the retina is relatively undifferentiated and
possesses a thick neuroblastic layer (Dickson &
Collard 1979; Rubinson & Cain 1989; Rubinson
1990). Recent reviews by Lamb et al. (2007) and
Lamb (2009) suggest that lampreys inherited their
eyes from an ancestor that they had in common with
hagfish, and that this hagfish-like larval eye is present
in the lamprey larva but transforms to a vertebratelike eye in the adult. The eyes of fully metamorphosed
lampreys are certainly prominent and well
differentiated, following closely the design of the
gnathostomatous fishes, with a multi-focal lens,
intra- and extraocular eye muscles and a complex
retina (Collin et al. 1999; Gustafsson et al. 2008).
The class Chondrichthyes is a monophyletic group
with over 1100 extant species occupying a diverse range
of habitats, from shallow, freshwater rivers to marine
environments such as coral reefs and the open ocean
including the deep sea. Extant Chondrichthyes are
divisible into two sister taxa, Holocephali and
Elasmobranchii, with a basal vertebrate lineage dating
back to the Lower Devonian, at least 400 Ma (Grogan
& Lund 2004). Close relatives of extant species today
are found in the fossil record, dating back 150 Myr
(Grogan & Lund 2004; Compagno et al. 2005). The
eyes of both holocephalans and elasmobranchs are
large, image-forming, camera-type eyes with an almost
spherical lens, well-developed intra- and extraocular
eyes muscles and a retina packed with photoreceptive
elements (Gruber & Cohen 1978; Hodgson &
Mathewson 1978; Hueter et al. 2004; Hart et al.
2006a,b).
Sarcopterygian fish gave rise to the first tetrapods
and are represented today by the lungfishes (the
Australian, Neoceratodus forsteri; the African, Protopterus
spp.; and the South American, Lepidosiren paradoxa),
and the coelacanths, Latimeria chalumnae and Latimeria
menadoensis. The relationship between all early Sarcopterygii remains controversial and highly debated despite
the advent of phylogenetic analysis of nucleotide and
amino acid sequences for a variety of diverse genes
(Carroll 1997; Brinkmann et al. 2004; Takezaki et al.
2004). Some molecular analyses of sarcopterygian
phylogeny reveal that the lungfishes are more related
to tetrapods than to the coelacanth, L. chalumnae
(Brinkmann et al. 2004), while others present an unresolved trichotomy between all three groups (Takezaki
et al. 2004). Fossil forms of the Australian lungfish
Ceratodus date back to the Lower Cretaceous Period
135 Ma, making this species more primitive than the
lepidosireniform family of lungfishes and the only
remaining member of one of the oldest extant vertebrate genera (Kemp & Molnar 1981). Therefore,
Phil. Trans. R. Soc. B (2009)
the well-developed visual system of N. forsteri may best
reflect the visual system just prior to the emergence of
land vertebrates in the Devonian period.
These groups of early vertebrates represent critical
periods in vertebrate evolution and studies of their
visual systems in extant species provide a window
into the past. Hagfishes and lampreys are the living
representatives of the agnathan lineage that gave rise
to gnathostomes, and therefore, studies of their eyes
enable us to contemplate the type of light environment
perceived by our vertebrate ancestors and how their
eyes were adapted for vision, thereby laying the foundation for the emergence of jawed vertebrates. The
cartilaginous holocephalans and elasmobranchs represent the basal lineage of jawed vertebrates and are
apex predators, relying on vision in addition to a battery of other senses. The colonization of more dim
light environments may have been one of the main
reasons for the success of this large group, although
more members of the Chondrichthyes need to be
examined and many studies reveal a diversity of
visual adaptations to their light environment, without
the constraints of phylogeny (Hart et al. 2006a,b).
Extant lungfish, on the other hand, represent a period
later in evolution, when vertebrates were about to venture on to land and thereby be exposed to higher light
intensities and a wider range of available wavelengths
of light. For all of these critical groups, colour vision
may have been an important factor in their evolutionary
success in sampling the ancient visual landscape.
(b) The ancient visual landscape
Although the environmental conditions under which
many of the ancestral vertebrates existed are largely
hypothetical, the visual stimuli that would have
driven the random selection of ocular adaptations
can be surmised based on the eyes of extinct and
extant vertebrates. Paleontological evidence from the
Silurian and Devonian periods shows that the lateral
eyes of the ancestral vertebrates were capable of
image formation and were rotated within their orbits
by seven extraocular eye muscles (Young 2008).
These heavily armoured ostracoderms were benthic,
presumably feeding by extracting food in or on the
substrate. Depending on the light environment
encountered by these early vertebrate ancestors, two
theories have been proposed as to how multiple photoreceptor types evolved: (i) those fish that possessed
two visual pigments, one matching the background
and the other offset from the background illumination,
could better detect targets that were spectrally different by enhancement of contrast (Lythgoe 1980;
Hawryshyn 1998) and (ii) the evolution of at least
two spectral classes of photoreceptors would eliminate
the considerable noise associated with the significant
flicker produced by light passing through the surface
ripples in shallow water, thereby enabling the earlier
detection of predators (Maximov 2000).
Both of these theories assume that vision in the
ancestral vertebrates was cone based (photopic), with
colour vision evolving possibly later as a by-product,
following the development of colour adaptation mechanisms via horizontal cells. Despite the absence of any
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Review. Vertebrate photoreceptor evolution
behavioural evidence of colour vision in either the
ancestral or early vertebrates, it is highly likely that
colour vision dates back at least 540 Myr with the
ancestral vertebrates possessing four major types of
vertebrate cone opsins, each presumably sensitive to
different parts of the light spectrum (see below).
Based on molecular genetic analysis of a range of
vertebrate visual pigment genes, it was predicted that
the long wavelength-sensitive/medium wavelengthsensitive (LWS/MWS) opsins evolved first and that
the Rh1 opsins evolved much later, implying that
photopic vision preceded scotopic vision (Yokoyama &
Yokoyama 1990, 1996). Although the selection pressures underlying the origins of colour vision are still
unknown, the early vertebrates lived in a shallow
water environment, which was well lit, based on the
finding of fossilized green algal deposits (Walker &
Laporte 1970), where a broad light spectrum could
be exploited by the evolution of multiple visual
pigments and utilized in observing a range of complex
environments and animals, some of which were
inherently colourful (Parker 1998; Maximov 2000).
In this review, we present a reflection on the evolution of photoreceptors, i.e. rods and cones (or their
predecessors) in early extant vertebrates, based upon
morphological, spectral and molecular criteria. This
includes early strategies for spectral filtering and
tuning and the potential for colour discrimination.
The capacity for photopic (cone-based, bright light
vision) and scotopic (rod-based, dim light vision)
vision will also be discussed within the context of the
ancestral light environment, the visual demands
placed on each group to feed, avoid predation and
reproduce and the need for functional studies on the
photoreceptors (regardless of placing them into
current visual nomenclature) in order to better
understand the evolution of the visual process.
2. EVOLUTION OF EARLY PHOTORECEPTORS
(a) Rods or cones?
Historically, it has been established that the vertebrate
retina, including that of humans, contains two
independent visual systems. Schultze (1866, 1867)
proposed, on the basis of finding predominantly rods
in nocturnal or crepuscular animals and cones in
diurnal animals, that two morphologically distinct
photoreceptor types mediated scotopic and photopic
vision, respectively. Schultze (1867) also recognized
the role of cones in the detection of colour, and by
comparison of the presence or absence of either rods
or cones in a number of different species concluded
that cones evolved from rods. These findings were
later refuted by several authors who identified conelike receptors in the eyes of cyclostomes, i.e. lampreys
(Öhman 1971; Dickson & Graves 1979; Govardovskii &
Lychakov 1984; Tonosaki et al. 1989; Collin et al.
1999; Collin & Trezise 2004), but the characterization
and distinction of rods and cones in the early vertebrates is not at all clear and has been the subject of
great debate for over 150 years (Crescitelli 1972).
The retinae of a number of Northern Hemisphere
(or holarctic) lampreys have been examined morphologically and thought to contain two photoreceptor
Phil. Trans. R. Soc. B (2009)
S. P. Collin et al.
2927
types, a short and a long; putatively a rod and a cone
photoreceptor, respectively (Crescitelli 1956, 1972).
Later, Öhman (1976) classified the two receptors as
‘rods’, and despite both receptors possessing almost
spherical receptor bases with only a few synaptic ribbons, the presence of membranous inclusions within
the retinal pigment epithelium (RPE) and a plasma
membrane surrounding the bulk of the outer segment
discs, there were also cone-associated features apparent. These include tapered outer segments and the
occasional infolding of the plasma membrane. On
the basis of the continuity of the outer segment discs
with the extracellular matrix and a pattern of protein
labelling throughout the outer segment (following
the incorporation of radioactively labelled amino
acids to indicate the process of outer segment disc
renewal), both receptor types were considered cones
in the sea lamprey, Petromyzon marinus (Dickson &
Graves 1979).
The shape of the outer segment (cylindrical in rods
and tapered in cones) has traditionally been used to
characterize receptors, but this has given equivocal
results in many species owing to the similarity of
each receptor type in different regions of the retina,
often a product of variations in receptor size and packing. This ambiguity has been especially difficult to
reconcile in the Southern Hemisphere lamprey,
G. australis, where five morphological types of photoreceptors have been differentiated on criteria as
subtle as the ultrastructural aggregation of short wavelength-absorbing pigment within the myoid (Collin
et al. 1999; Collin & Trezise 2004), a feature that
could easily be overlooked (Meyer-Rochow & Stewart
1996). Based on the continuity of the outer segment
discs with the extracellular matrix in all five morphological photoreceptor types in G. australis, all are
considered cone-like. The short and long receptors of
holarctic lampreys have also been difficult to assign
rod- or cone-like status; authors have variously
considered them both to be rods (Öhman 1971,
1976; Holmberg & Öhman 1976; Dickson & Graves
1982), both cones (Dickson & Graves 1979) or a rod
and a cone, respectively (Crescitelli 1956, 1972;
Govardovskii & Lychakov 1984; Ishikawa et al.
1987; Negishi et al. 1987; Hárosi & Kleinschmidt
1993; Yoshida & Tonosaki 1994). Other morphological
features, which are less ambiguous and underlie
important electrochemical signalling during the phototransduction cascade, e.g. the arrangement of the
plasma membrane surrounding the outer segment
(Cohen 1972), may be better features upon which to
differentiate rods and cones, although these traditional
criteria may not be definitive without taking into account
spectral, molecular and ultimately functional features.
Although spectral analyses may also be ambiguous
because the spectral sensitivity of rods overlaps with
a range of MWS cones, amino acid sequences of the
opsin proteins may hold similar ambiguities. We consider that phototransduction genes may, in fact, hold
vital clues to the identity and/or function of the earliest
photoreceptors. It appears that the RhA and RhB
opsins identified by Collin et al. (2003a,b) in
G. australis may share features in common with the
Rh1 (found in rods) and Rh2 (found in cones)
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S. P. Collin et al.
Review. Vertebrate photoreceptor evolution
(b)
normalized absorbance
(a)
439
359
1.0
492 497
560
359
0.25
(d)
517
1.0
525
555
600
0.75
0.5
0.25
(f)
477 502 504 561
514
normalized absorbance
552 560
0.5
(e)
1.0
0.75
0.5
0.25
(g)
normalized absorbance
497
0.75
(c)
normalized absorbance
439
366–383
479–484
(h)
540 558–584 623–656
479–484
540 558–584 623–656
1.0
0.75
0.5
0.25
300
400
500
wavelength (nm)
600
700
300
400
500
wavelength (nm)
600
700
Figure 1. Schematic representations of the spectral sensitivities of the visual pigments of the different photoreceptor types
found in early vertebrates. (a) The downstream and (b) upstream migrants of the Southern Hemisphere lamprey, G. australis.
The long-wavelength shift (from 492 to 552 nm) of the MWS pigment is caused by the replacement of the yellow myoidal
pigment with an ellipsosome. (c) The river lamprey, L. fluviatilis. (d) The sea lamprey, P. marinus. (e) The Southern Hemisphere lamprey, M. mordax. ( f ) The giant shovelnose ray, G. typus. (g) The juvenile stage of the Australian lungfish, N. forsteri.
(h) The adult stage of N. forsteri. Note the loss of the UVS pigment in the adult lungfish. Data predominantly based on microspectrophotometric (MSP) analyses but spectrophotometric analysis of recombinant pigments regenerated with 11-cis-retinal
have also been included where MSP was not possible. lmax values (indicated) were obtained from Govardovskii & Lychakov
(1984); Hárosi & Kleinschmidt (1993); Collin et al. (2003b, 2004) and Hart et al. (2004, 2008). The dashed lines in (g) and
(h) indicate the long-wavelength shift in absorbance after taking into account the intracellular filtering produced by the oil
droplets and myoidal pigment.
opsins, respectively, of jawed vertebrates (see below).
However, the amino acid sequence of the RhA opsin
in lampreys is intermediate between rod and cone
opsins with a rod-type Glu122 and a cone-type
Pro189 (Imai et al. 2005).
Phil. Trans. R. Soc. B (2009)
The process of capturing a photon and transforming it into a biochemical signal (phototransduction)
is an ancient process involving a diverse range of
chemical reactions that nevertheless shows a striking
similarity in its component parts in both invertebrates
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Review. Vertebrate photoreceptor evolution
human
mouse
platypus
dunnart
chicken
pigeon
frog
green anole
coelacanth
lungfish
40
100
98
100
59
91
99
99
S. P. Collin et al.
87
2929
RhA/Rh1
goldfish
zebrafish
catshark
100
100
dogfish
skate
pouched lamprey
100
99
100
100
Arctic lamprey
99
100
100
100
94
chicken
pigeon
green anole
lungfish
coelacanth
100
100
77
pouched lamprey
chicken
87
pigeon
95
platypus
100
green anole
frog
100
63
lungfish
100
zebrafish
100
goldfish
pouched lamprey
human
100
mouse
100
dunnart
100
96
wallaby
chicken
99
90
81
pigeon
green anole
94
lungfish
frog
100
pouched lamprey
100
goldfish
zebrafish
100
human
97
mouse
dunnart
100
100
wallaby
platypus
97
97
frog
98
lungfish
goldfish
100
97
84
zebrafish
green anole
chicken
98
100
pigeon
RhB/Rh2
goldfish
zebrafish
100
72
0.1
100
SWS2
SWS1
LWS1
pouched lamprey
Arctic lamprey
Figure 2. Phylogeny of visual pigment (opsin) gene families (LWS, SWS1, SWS2, RhB/Rh2 and RhA/Rh1) in vertebrates. The
tree was generated by using a Bayesian probabilistic inference method with a Metropolis Markov chain Monte Carlo algorithm.
A general time-reversal model was used with posterior probability values (represented as a percentage) indicated at the base of
each node. The scale bar indicates the number of nucleotide substitutions per site. The fruitfly Rh4 was used as an outgroup.
Phil. Trans. R. Soc. B (2009)
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S. P. Collin et al.
Review. Vertebrate photoreceptor evolution
and vertebrates. In vertebrates, many of these
component processes (e.g. transducins, arrestin,
phosphodiesterase 6 and the cyclic guanosine monophosphate-gated channels) are encoded by different
cone- or rod-specific isoforms (Hisatomi & Tokunaga
2002). These proteins mediate the reactions at the
different stages of the biochemical cascade. After
photon capture and the isomerization of the chromophore from the 11-cis to all-trans form, the resulting
conformational change in the opsin protein is
converted via the phototransduction cascade to a
biochemical signal recognizable by the other retinal
neurons. Preliminary results for the lamprey G. australis
reveal that, in general, only single isoforms of the
phototransduction genes are present and, with the
exception of transducin-a, the coding sequences are
phylogenetically more cone- than rod-like (Hunt
et al. 2007). Therefore, it may be that at the time in
evolutionary history when the jawed and jawless vertebrates split into two lineages, the eyes of lampreys
possessed a predominantly photopic visual system
based on cone-like photoreceptors. However, at least
one type of receptor was undergoing some sort of
‘transmutation’ to a receptor hybrid, which would
subsequently become a ‘true rod’ with the age of
cartilaginous fishes (Walls 1942; Collin & Trezise
2006; Pisani et al. 2006; Davies et al. 2009).
(b) Spectral sensitivity
The wavelength of maximum absorbance (lmax) of the
visual pigment in a given photoreceptor can be a
useful, but not definitive, criterion for discriminating
between the spectral sensitivity of rods and cones,
although in many species this value can be identical
(Bowmaker 1995, 2008; figure 1).
There has been no microspectrophotometric
analysis of the spectral absorbance of individual photoreceptor types in hagfishes. However, behavioural
experiments have revealed that swimming responses
(preceded by movements of the head or body) to
light stimulation were maximal between 500 and
520 nm, with little or no response above 600 nm
(Steven 1955).
The spectral characterization of photoreceptor
types in lampreys has received more attention. Microspectrophotometric studies of the short and long
photoreceptor types in two Northern Hemisphere
(holarctic) species (the sea lamprey P. marinus and
the river lamprey Lampetra fluviatilis) reveal different
peak spectral sensitivities (lmax) values. These lie at
525 and 600 nm (in upstream P. marinus both receptor
types possess visual pigments that are porphyropsins or
visual pigments that utilize a vitamin-A2 chromophore;
(Hárosi & Kleinschmidt 1993; figure 1d ) and at 517
and 555 nm (in upstream L. fluviatilis both receptor
types possess visual pigments that utilize a vitamin
A1-based chromophore; Govardovskii & Lychakov
1984; figure 1c), respectively. Therefore, it appears
that the short and long photoreceptors in holarctic
lampreys possess an MWS and an LWS visual pigment
within their outer segment, respectively.
In the Southern Hemisphere lamprey, G. australis,
conventional
spectrophotometric
analysis
of
Phil. Trans. R. Soc. B (2009)
recombinant opsins expressed in mammalian cells
reveals five visual pigments with lmax values at 359,
439, 497, 492 and 560 nm (the LWS opsin failed to
generate a functional pigment when expressed as a
recombinant protein so the lmax value was based on
key spectral tuning sites) (Davies et al. 2007;
figure 1a,b). Earlier microspectrophotometric studies
on three of the five photoreceptor types indicated
that that these photoreceptors utilize an A2-based
chromophore on the basis of the goodness of fit of
the mean absorbance spectra to mathematical pigment
templates (Govardovskii et al. 2000; Collin et al. 2003a;
figure 1a).
The lmax of the visual pigment within the outer segment of the single photoreceptor type found in the
retina of the downstream migrant phase of
M. mordax is 514 nm and is, therefore, MWS (Collin
et al. 2004; figure 1e). Based on its lmax, the receptor
type in M. mordax may be homologous to the short
receptors of L. fluviatilis (517 nm, A1; figure 1c) and
P. marinus (525 nm, A2; figure 1d ). The photoreceptors of both downstream and upstream migrants
of the Pacific lamprey, Entosphenous tridentatus, possess
a vitamin-A1-based visual pigment (Crescitelli 1972).
When considered together with the finding of the
entire complement of photoreceptors possessing visual
pigments incorporating a chromophore based on vitamin-A2 in the white sturgeon, Acipenser transmontanus
(an early ray-finned fish with an anadromous life
cycle), it appears that migration between freshwater
and saltwater may not be sufficient to induce a paired
A1/A2 visual pigment system (Whitmore & Bowmaker
1989; Sillman et al. 1995). At this stage, and given
the considerable interspecific variability, it is perhaps
premature to predict whether vitamin A1 or A2 is the
ancestral chromophore in vertebrates. However, it is
interesting to note that only vitamin-A1, and not
vitamin-A2, could be isolated from the liver in
Myxine glutinosa (Steven 1955; Vigh-Teichmann et al.
1984).
Using microspectrophotometry, three species of ray
(Rhinobatos (Glaucostegus) typus, Aptychotrema rostrata
and Dasyatis kuhlii) have been found to possess three
cone types in the short wavelength-sensitive (SWS,
lmax 459 – 477 nm), MWS (lmax 492 – 502 nm) and
long- (lmax 552 – 561 nm) spectral ranges in addition
to a rod (lmax 497 – 504 nm) (Hart et al. 2004;
Theiss et al. 2007; figure 1f ). These findings strongly
suggest the potential for colour discrimination in this
class of vertebrates that was once thought to be
monochromatic, i.e. Chondrichthyes, and support
earlier reports of three peaks in electrophysiologically
recorded spectral sensitivity at 476, 502 and 540 nm
in the closely related stingray, Dasyatis pastinaca, by
Govardovskii & Lychakov (1977).
The retina of the Australian lungfish is duplex,
containing both rod and cone photoreceptors. Microspectrophotometry reveals that juvenile lungfish
possess four types of single cone photoreceptor with
visual pigments maximally sensitive to ultraviolet
(UVS, lmax 366 nm), SWS (lmax 479 nm), MWS
(lmax 558 nm) and LWS (lmax 623 nm) and, therefore, have the potential for tetrachromatic colour
vision (Bailes et al. 2006; Hart et al. 2008;
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Review. Vertebrate photoreceptor evolution
figure 1g,h). UVS cones are the only photoreceptor
type not found in the retina of the adult lungfish.
The retinae of both juveniles and adults also contain
a single type of MWS photoreceptor (lmax 540 nm,
figure 1g,h). On the basis of spectral bandwidth and
the fit of the absorbance spectra to visual pigment templates (Govardovskii et al. 2000), all visual pigments in
the lungfish are considered to use an A2-based chromophore (or porphyropsin), as is typical of many
other freshwater fish (Hart et al. 2008).
(c) Opsins and spectral tuning
Molecular examination of photoreceptor visual pigments is an important and more definitive method of
characterizing rods and cones (especially when combined with in situ hybridization) and assessing the
potential for colour vision. As described previously,
the chromophore that is bound to the visual opsins
of vertebrates is derived from the aldehyde of either
vitamin-A1 or vitamin-A2 to give a rhodopsin or
porphyropsin pigment, respectively. Porphyropsin pigments are spectrally more long-wavelength-shifted
than the corresponding rhodopsin, and this effect
increases progressively at longer wavelengths
(Whitmore & Bowmaker 1989; Hárosi 1994; Parry &
Bowmaker 2000; Temple et al. 2008). Packed into
the membranes of the discs within the outer segments,
these transmembrane proteins comprise a polypeptide
chain of approximately 350 amino acids, which forms
seven transmembrane alpha-helices linked by extraand intracellular loops. Changes in the photoreceptor
spectral sensitivity are mediated primarily by variations
in the amino acid sequence of the opsin protein, each
encoded by a distinct opsin gene and by different ratios
of the two chromophores (Nathans et al. 1986;
Partridge 1995). Vertebrate retinal opsin genes are
classified into five evolutionarily distinct groups:
LWS opsins found in cones (LWS/MWS), SWS 1
opsins found in cones (SWS1), SWS 2 opsins found
in cones (SWS2), MWS opsins found in cones (RhB/
Rh2,), and MWS opsins primarily found in rods
(RhA/Rh1) (Yokoyama 1997; Bowmaker & Hunt
2006; figure 5). Although Rh1 opsin-based pigments
are usually expressed in rods and the remainder in
cones, as indicated previously (and see below), the
closely related RhA opsin has some cone-like
characteristics. Gene duplication, followed by nucleotide substitution, provides the basis of functional
differentiation of the various groups of opsins.
Currently, there are no retinal visual pigments
characterized in hagfishes. However, Hisatomi et al.
(1991) were the first to clone and sequence a fulllength opsin gene from the river lamprey, Lampetra
japonica. The deduced amino acid sequence was
most similar to Rh1 rod opsin sequences of other
vertebrates, showing 78 – 82% identity. The in vitro
expressed lamprey pigment, reconstituted with
11-cis-retinal, showed an absorption maximum of
500 nm and reacted with an anti-bovine rod pigment
(Rh1) antibody, which had previously been found to
recognize the short photoreceptor type in L. japonica
(Hisatomi et al. 1997). Interestingly, and unlike the
rod Rh1 opsins of other vertebrates, this lamprey
Phil. Trans. R. Soc. B (2009)
S. P. Collin et al.
2931
pigment (initially classed as Rh1) bleached gradually
in the presence of hydroxylamine, even in the dark,
which is usually a characteristic of cone pigments
(Okano et al. 1989). Therefore, this pigment has biochemical characteristics intermediate between rod
and cone pigments. Similarly, an opsin gene in the
marine lamprey, P. marinus, has a deduced amino
acid sequence that shows a 92 per cent identity to
the Rh1 opsin gene of the river lamprey, L. japonica
(Zhang & Yokoyama 1997).
The full extent of the palette of visual pigment opsin
genes available to the ancestral vertebrates would
appear to be realized within the Southern Hemisphere
lamprey, G. australis, where all five opsin genes are
expressed within the retina and differentially regulated
during the lamprey life cycle (Collin et al. 2003a;
Davies et al. 2007; figure 2). Based on neighbourjoining, maximum likelihood and Bayesian inference
methods used to reconstruct phylogenetic trees,
opsin genes were identified as the orthologues of the
jawed vertebrate LWS, SWS1 and SWS2 opsin gene
lineages. In addition, two Rh classes of opsin genes
were identified (RhA and RhB), which appear to be
most closely related to the gnathostome Rh1 and Rh2
genes, respectively. This finding suggests that (i) the
most recent common ancestor of the jawed and jawless
vertebrates possessed a single ancestral Rh opsin gene,
the common ancestor of all the Rh opsin genes, as well
as LWS, SWS1 and SWS2 opsin genes, with separate
gene duplications giving rise to the RhA and RhB
opsin genes in jawless (agnathan) vertebrates and the
Rh1 and Rh2 opsin genes in the jawed (gnathostome)
vertebrates (Collin et al. 2003a; Collin & Trezise
2004) or (ii) the RhA opsin found in the two species
of lampreys examined (the pouched lamprey,
G. australis, and the arctic lamprey, Lethenteron japonica)
would appear to be ancestral to the Rh1 class of opsin
and that the RhB opsin in G. australis is ancestral to
the Rh2 opsin group, suggesting that lamprey RhA and
RhB genes share ancestral orthologues with the jawed
vertebrate Rh1 and Rh2 gene classes, respectively
(Pisani et al. 2006; Davies et al. 2009; figure 2).
Holocephalans and elasmobranchs are a large class
of vertebrates that have colonized both deep sea and
shallow water, especially coral reef environments. Up
until recently, only the Rh1 opsin gene had been
isolated and cloned in elasmobranchs, i.e. in the catshark, dogfishes and the skate (O’Brien et al. 1997;
Bozzano et al. 2005). However, an analysis of the
genome of the holocephalan elephant shark, Callorhinus milii, has revealed that a rod (Rh1) and three
cone (Rh2, LWS1 and LWS2) opsin genes are
expressed within the retina, with lmax values of 496
(Rh1), 442 (Rh2), 499 (LWS1) and 548 nm (LWS2)
as determined by in vitro expression (Davies et al.
2009). The research on C. milii represents the first to
reveal the molecular identity of any cone opsin gene
within the Chondrichthyes. Together with the discovery
of three spectrally different cone photoreceptor types in
batoid elasmobranchs (Hart et al. 2004; Theiss et al.
2007), there is now impressive evidence to support the
potential for trichromatic vision in cartilaginous fishes.
All five opsins are also expressed in the retina of the
subadult Australian lungfish (N. forsteri) and a
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S. P. Collin et al.
Review. Vertebrate photoreceptor evolution
(a)
(b)
(c)
(d)
Figure 3. Axial view of the retinal photoreceptor array in a range of early vertebrates viewed using Nomarski optics. (a)
Upstream migrant of the Southern Hemisphere lamprey, G. australis (Agnatha). Photoreceptors are differentiated based on
the presence of an ellipsosome (large circular profiles), the presence or absence of an orange/yellow, myoidal short wavelength-absorbing pigment and size. (b) Downstream migrant of the Southern Hemisphere lamprey, M. mordax (Agnatha).
This species has only one photoreceptor type containing an ellipsosome arranged within a tightly packed hexagonal array
and surrounded by a tapetum housed within the retinal pigment epithelial cells. (c) Epaulette shark, Hemiscyllium ocellatum
(Chondrichthyes, Elasmobranchii). This rod-rich retina has a low proportion of cones differentiated on the basis of their
small size and refractive properties (Litherland & Collin 2008). (d) Australian lungfish, N. forsteri (Osteichthyes, Dipnoi).
Large red oil droplets and orange myoidal pigment (arrowheads) are interspersed with large rods and smaller cones containing
clear oil droplets. Scale bars: (a) 20 mm; (b) 25 mm; (c) 5 mm; (d) 35 mm.
phylogenetic comparison of codon-matched alignments of both nucleotide and deduced amino acid
sequences reveals the presence of LWS, SWS1,
SWS2, Rh2 and Rh1 genes (Bailes et al. 2007;
figure 2). The characterization of four cone opsins
reveals the potential for tetrachromatic vision in lungfish, although behavioural work is needed to verify if
lungfish can discriminate objects based on differences
in chromatic hue, in addition to whether it has
four-dimensional colour space.
(d) Ellipsosomes, oil droplets, myoidal
pigment and tapeta
A photoreceptor’s spectral sensitivity is determined
primarily by the spectral absorbance of the visual pigment(s) it contains. However, many species have also
evolved intra- and extracellular devices to enhance
(filter or tune) the incoming light before it reaches
the visual pigments located within the outer segments
(reviewed by Douglas & Marshall 1999). These filters
come in many forms, including corneal (Collin &
Collin 2001; Siebeck et al. 2003), lenticular
(Heinermann 1985; Siebeck & Marshall 2001) and
retinal, i.e. ellipsosomes (large elliptical inclusions surrounded by mitochondria and lying within the inner
segment) and myoidal pigment situated below the
Phil. Trans. R. Soc. B (2009)
mitochondria (Collin & Potter 2000; Collin et al.
2003b; figures 2a,d and 4a). However, the most
notable are coloured oil droplets (which differ from
ellipsosomes in both their development and biochemistry; Nag & Battacharjee 1995) located within the
ellipsoid of the cone inner segment. These densely pigmented organelles usually act as long-pass cut-off
spectral filters, although the location of the cut-off
wavelength varies depending on the lmax of the
visual pigment (Partridge 1989; Hart 2001; Hart &
Vorobyev 2005; figures 2d and 3e) and even environmental factors such as ambient light intensity (Hart
et al. 2006a,b).
No oil droplets have been identified in the retina of
any species of hagfishes or lampreys examined thus far.
However, an intracellular yellow/orange photostable
pigment is present in the myoid and ellipsoidal regions
of at least three of the five photoreceptor types in the
Southern Hemisphere lamprey G. australis (Collin
et al. 1999; Collin & Trezise 2004; figures 3a and
4c). This yellow-orange pigment, which is perhaps
homologous to that found within one of the cone
photoreceptor types in the Australian lungfish,
N. forsteri (Bailes et al. 2006; figures 3d, 4e and 5)
and also the ornate lizard, Ctenophorus ornatus
(Barbour et al. 2002; figure 5), acts as a spectral
filter by absorbing visible wavelengths below about
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S. P. Collin et al.
Review. Vertebrate photoreceptor evolution
(a)
(b)
2933
(c)
os
os
os
e
m
m
m
m
m
n
C
C/R
C
(d)
yp1
n
yp2
n
n
C/R
m
yp1
n
C/R
n
C
C
C
(e)
os
os
m
od
dm
m
m
C
C
C
R
n
R
od
p
n
p
n
n
yp
m
C
C
od
m
p
n
C
C
Figure 4. Schematic representation of the complement of photoreceptor types in early vertebrates based on morphological criteria. (a) The single receptor type in the lamprey, M. mordax (Mordaciidae). (b) The long and short receptors in the Northern
Hemisphere (holarctic) lampreys (Petromyzontidae). (c) The five receptor types in the lamprey, G. australis (downstream
migrant) (Geotriidae). Note the inclusion of yellow myoidal pigment in three of the receptor types. (d ) The four receptor
types in the giant shovelnose ray, G. typus (Rhinobatidae). (e) The five receptor types in juvenile Australian lungfish, N. forsteri
(Ceratodontidae). Note the yellow myoidal pigment and both red and colourless oil droplets. Receptor identities have been
based on a range of morphological, spectral and molecular studies; C/R, cone/rod hybrid or features that make it difficult
to differentiate; C, cone; R, rod; dm, distended mitochondria; e, ellipsosome; m, mitochondria within the inner segment;
n, nucleus; od, oil droplet; os, outer segment; p, paraboloid; yp (1 and 2), orange/yellow pigment.
550 nm (Collin et al. 2003b). This short-wavelengthabsorbing filter may have evolved originally in a
vertebrate with a similar life history to G. australis, in
response to the need to filter out the potentially damaging short-wavelength (high energy) light to which the
eye is constantly being subjected. A short-wavelengthabsorbing filter may also prevent photostimulation of
the beta-band of the visual pigments and narrow the
spectral sensitivity functions of different cone types,
thereby improving colour discrimination (Vorobyev
2003; Hart et al. 2008). It is also possible that
absorbance of short-wavelength light, at least in
some photoreceptor types, may improve contrast
sensitivity (Walls 1942).
Oil droplets are thought to have evolved early in
vertebrate evolution, predating the emergence of
Phil. Trans. R. Soc. B (2009)
terrestrial vertebrates ca 400 Ma (Robinson 1994).
The Australian lungfish, N. forsteri, a living fossil and
the closest living relative of the first terrestrial vertebrates, possesses oil droplets within three of its four
large cone types (two of which are non-pigmented
and one type in the LWS cone has a dense red pigment; Robinson 1994; Bailes et al. 2006; Hart et al.
2008; Marshall et al. in press; figures 3d, 4e and 5).
Both pigmented and non-pigmented oil droplets have
been retained in diurnal lizards, turtles and birds
(Walls 1942; figure 5). The apparent loss of oil droplets in amphibians, snakes, crocodiles and mammals
(except the marsupials, which have non-pigmented
oil droplets; Arrese et al. 2002), is thought to be the
result of a shift from a diurnal to a nocturnal lifestyle
and may function to improve photon capture and
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2934
S. P. Collin et al.
Review. Vertebrate photoreceptor evolution
focus light onto the outer segment (Walls 1942; Collin
& Potter 2000). Although the more widely accepted
advantages of oil droplets in reducing chromatic aberration and negating the harmful effects of ultraviolet
radiation may still apply (Walls & Judd 1933; Walls
1942; Douglas & Marshall 1999), the improvement
in colour discrimination may have been the driving
force for the evolution of coloured oil droplets in lungfish, especially those living in brightly lit environments
(Vorobyev 2003; Hart et al. 2008). The pigmented oil
droplets act as long-wavelength-pass cut-off filters that
sharpen and shift the spectral sensitivity of the photoreceptor to longer wavelengths in order to improve
spectral discrimination (Kelber et al. 2003; Hart
et al. 2008). Non-pigmented oil droplets may have a
function in improving photon capture and focusing
light on to the outer segment (Hart et al. 2006a,b).
However, we consider that the evolutionary longevity of the visual system of the Australian lungfish may
also lie partly in its ability to balance the trade-off
between resolution and sensitivity. While the large
cone diameters (approx. 15 mm in diameter; Bailes
et al. 2006; figures 3d and 4e) are most probably a
by-product of the reduction in quantal flux in response
to the filtering capacity of the coloured inclusions, its
large rods (approx. 20 mm in diameter; figures 3d
and 4e) will ensure sufficiently high sensitivity to operate in the reportedly low light levels of its crepuscular
and/or nocturnal lifestyle (Kemp 1986).
The presence of ellipsosomes in the photoreceptors
of some lampreys indicates that these early vertebrates
have the capacity to alter the light before it is absorbed
by the visual pigments. These elliptically shaped intracellular organelles span the diameter of the inner
segment (figures 3a,b and 4a) and may be used to
focus light on to a narrow, tapered outer segment
(Young & Martin 1984), in addition to reducing
both photo-oxidative damage (Avery & Bowmaker
1982) and the effects of chromatic aberration (Collin &
Potter 2000). Given that ellipsosomes are present in
two of the extant agnathan families (Geotriidae and
Mordaciidae), it appears likely that ellipsosomes may
have been present in the retina in their most recent
common ancestor (Collin & Potter 2000; Collin et al.
2003b; figures 3a,d, 4a and 5). Whether oil droplets
evolved from such an aggregation of pigment granules
is unknown and may be improbable given the packaging of the pigment: spherical membrane-bound
pigment found in the ellipsoid region (oil droplets)
versus stored secretory material within the endoplasmic
reticulum of the myoid region (Collin et al. 1999).
The presence of a tapetum is an adaptation to
increase sensitivity by reflecting light back through the
photoreceptors after striking a reflective layer situated
either within the retinal pigment epithelial cells or
behind Bruch’s membrane. Depending on the type of
tapetum (specular or diffuse), the wavelengths of light
re-entering the photoreceptor outer segment may also
vary and be tuned to the ambient light environment.
Lampreys, elasmobranchs, lungfishes, as well as teleosts,
all exhibit an eyeshine produced by tapeta (Collin 1988;
Collin & Potter 2000; Bailes et al. 2006; figure 5). The
retina of the Southern Hemisphere lamprey, M.
mordax, possesses a regular hexagonal array of a single
Phil. Trans. R. Soc. B (2009)
type of photoreceptor containing an ellipsoidal ellipsosome (figures 3b and 4a) surrounded by an RPE filled
with two types of tapetal reflector (spheres and needles).
The spherical particles characteristic of the diffuse type
of reflector are most common in the vitread region
surrounding the photoreceptors, whereas the needleshaped particles that are characteristic of the specular
type of reflector are most abundant in the sclerad
region of the RPE. It is evident that the enhanced sensitivity gained from a reflective tapetum was an early
invention and one that was favoured by natural selection
as particular members of each major group escaped
predation by moving into perpetually dim light environments and/or needed to enhance sensitivity during
crepuscular periods of changes in light intensity and
thereby from cone-based to rod-based vision. This scenario is particularly applicable to elasmobranchs, many of
which actively move between different light levels and
possess a reflective choroidal tapetum sitting behind a
retinal array of predominantly rod photoreceptors
(Litherland & Collin 2008; figures 3c, 4d and 5).
3. FUNCTIONAL AND BEHAVIOURAL
IMPLICATIONS FOR EARLY PHOTORECEPTION
The functional divergence of the two receptor types in
Northern Hemisphere lampreys has been examined by
microspectrophotometry (Govardovskii & Lychakov
1984; Hárosi & Kleinschmidt 1993), visual pigment
anion sensitivity (Hárosi & Kleinschmidt 1993),
hydroxylamine sensitivity (Hisatomi et al. 1997) and
electrophysiology (Govardovskii & Lychakov 1984).
In all cases, the results predominantly indicate that
both receptor types are cones but uncertainty still
exists as regards their identity and function. Electroretinographic responses recorded in the river lamprey,
L. fluviatilis, by Govardovskii & Lychakov (1984)
show typical cone responses for both receptor types,
including the short receptors (putative rods), which
do not saturate at high light intensities and contribute
to both photopic and scotopic vision. The short receptors are, however, approximately 100 times more
sensitive than the long receptors and are the only
class of receptor to be active in the dark-adapted
state (Govardovskii & Lychakov 1984). The long
receptors contribute to retinal function only during
intense stimulation and can therefore be regarded as
cones. Moreover, changes in stimulus colour always
produces a large response of a complex form, irrespective of the relative strength of the stimuli, indicating
that under photopic conditions the lamprey retina possesses the ability of colour discrimination. Future
functional studies on the photokinetics of the complement of photoreceptor types in G. australis and
M. mordax will undoubtedly help elucidate the rod/
cone hybrid nature of these photoreceptor types.
No functional studies of the one or two receptor
types hypothesized to exist in hagfish eyes have been
undertaken. However, based on a series of testable
hypotheses, Lamb et al. (2007, 2008) consider the
eyes to be non-image-forming bilateral ‘pineal’
organs that have been retained for over 500 Myr as a
circadian irradiance detector. Similarly, few functional
studies have been undertaken in elasmobranchs.
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Review. Vertebrate photoreceptor evolution
Dowling & Ripps (1972) reveal that, in the pure-rod
skate retina, the rod photoreceptors respond to incremental stimuli up to and including bright light
intensities that would bleach a large fraction of the
visual pigment present, much like typical cones in
other jawed vertebrates. Later research using electroretinograms also confirms that the all-rod retina of the
skate possesses both ON and OFF bipolar cell pathways that are functional (Chappell & Rosenstein
1996).
(a) Colour vision
The detection of all aspects of the aquatic visual scene
including prey, predator or mate is dramatically
improved by the added dimension of chromatic
detail and the large variety of identified photoreceptor
visual pigments in vertebrates indicates that colour
vision offers a substantial selective advantage. In
order to mediate colour vision, multiple sensors
(each providing a means for the differential filtering
of spectral information) and neuronal comparators
(designed to contrast signals originating from these
different sensors) must both be present if the chromatic signal is to elicit a behavioural response
(Jacobs & Rowe 2004).
In vertebrates, molecular phylogenetic analyses
have established that vertebrate visual pigments
evolved along five distinct lines and that these lineages
may have been in place before the divergence of jawed
and jawless fishes (Davies et al. 2009; figure 2). The
five vertebrate visual pigment gene lineages presumably diverged from a single common ancestor that
had evolved prior to the divergence of the protostomes
and deuterostomes, which is thought to have occurred
about 700 Ma (Oota & Saitou 1999). Therefore,
colour vision most probably evolved in the earliest
vertebrates between 400 and 700 Ma. However, our
ability to pinpoint the origins of colour vision or
colour discrimination within this time frame are still
a matter of contention arising from the lack of data
on cephalochordates, tunicates and hagfishes, which
lie at the base of chordate phylogeny.
However, new evidence now suggests that colour
vision evolved between 700 and at least 540 Ma. This
is based on the presence of five types of cone-like photoreceptors in the Southern Hemisphere lamprey,
G. australis (Collin et al. 2003b; Collin & Trezise
2004; figure 4c), three cone types in chondrichthyan
holocephalans and elasmobranchs (Hart et al. 2004;
Theiss et al. 2007; Davies et al. 2009; figure 4d). The
finding of four cone types in the Australian lungfish,
N. forsteri, allows us to make inferences about the
colour vision of the first terrestrial vertebrates (Bailes
et al. 2006; Hart et al. 2008; figure 4e). Molecular
studies in a range of teleost fishes reveal that not only
are these classical cone opsin genes retained in bony
fishes (including an Rh1 opsin; figure 2) but a series
of consecutive gene duplication events within the Rh2
(to produce Rh2a, Rh2Ab and Rh2B in green cones)
and SWS2 (to produce SWS2A and SWS2B in blue
cones) gene lineages have produced up to seven cone
opsin genes, which are functionally expressed in the
retina (Parry et al. 2005; Trezise & Collin 2005;
Phil. Trans. R. Soc. B (2009)
S. P. Collin et al.
2935
Shand et al. 2008). It is proposed that the rapid and
successful speciation of cichlids, which has produced
about a thousand new species, in the African Great
Lakes over the past 250 000 years may have been
partly due to the ability of this group to adapt quickly
to new ecological niches by ‘exploring new genetic
space’ by a series of gene duplications (Carleton et al.
2005; Parry et al. 2005; Trezise & Collin 2005).
Multiple cone opsins found in representatives of all
of the early vertebrate classes, together with a range of
coloured intraocular filtering mechanisms, suggest that
the ancestral vertebrates relied on diurnal vision and
may have utilized colour discrimination to target
prey, avoid predators, communicate and attract
reproductive partners.
(b) The role of vision in early vertebrates
Given the rather simple and poorly organized photoreceptor outer segments of hagfishes, it is of little
surprise that behaviourally they are almost ‘blind’,
and their weak response to light is unaffected by the
removal of the eyes (Newth & Ross 1955). Lamb
et al. (2007, 2008) suggest that the ‘eyes’ of hagfishes
may act more like the pineal of gnathostomes
(hagfishes lack a true pineal).
Unfortunately, there are very few studies examining
visual behaviour in lampreys. The ability to discriminate a broad range of colours and view the world
tetra- (or even penta-) chromatically may be advantageous to extant lampreys living in brightly lit
environments. The countershading patterns of the
Southern Hemisphere lamprey G. australis with a
bright iridescent, blue dorsal surface and a silver ventral surface are unique features within the Agnatha.
Presumably this is an adaptation to its pelagic
marine trophic phase, where it spends much of its
time in the clear, blue surface waters off the coast of
South Georgia feeding parasitically on a range of teleosts. Although parasitic, Nikol’skii (1956) describes
L. japonica as ‘predatory’, gnawing out tissues and
even internal organs with its specialized mouthparts.
Possessing no paired fins and swimming by propagating a laterally directed wave along its eel-like body
(Grillner et al. 1991), lampreys can steer with great
precision towards a specific location in the water
column to locate potential hosts, using visual cues
for orientation during locomotion (Grillner et al.
1991; Ullén et al. 1995). Mordacia mordax are known
to frequent deeper water, diving to depths of up to
1000 m (Bigelow & Schroeder 1953) and, like the
upstream migrants of G. australis, are nocturnal.
Generally, elasmobranch colours tend to be muted
in comparison to the bright colours seen in some teleost fishes (Kemp 1999), although some elasmobranch
species are coloured for camouflage and/or sexual
selection. Until behavioural experiments are carried
out, it will be difficult to understand the functional
existence of up to three cone types and the potential
for trichromatic colour vision in rays and elephant
sharks (Hart et al. 2006a,b; Davies et al. 2009;
figure 4d ). Most elasmobranchs display some degree
of countershading, which tends to be most apparent
in active, pelagic sharks, such as the blue shark,
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2936
S. P. Collin et al.
Review. Vertebrate photoreceptor evolution
od
cod
mp
tp
Tetrapods
coloured oil droplets (od)
lungfishes
od
mp
tp
coelacanth
cod
tp
colourless oil droplets (cod)
cod
el
tp
ray-finned fishes
elasmobranchs
tp
el
mp
tp
lampreys
ellipsosomes (el)
myoidal pigment (mp)
tapeta (tp)
hagfishes
?
Figure 5. Phylogenetic schematic of the major vertebrate groups showing the evolution of tapeta (tp), myoidal short
wavelength-absorbing pigment (mp), ellisosomes (el), colourless oil droplets (cod) and coloured oil droplets (od). Black bars represent the first appearance of each of the morphological traits. The schematic drawings of the photoreceptors on the right-hand
side depict the complement of receptor types within at least one species within that vertebrate class/group. The lists of visual traits
adjacent to these drawings indicate that at least one species possesses this feature. If a particular feature is not listed for a particular clade, it has not been identified (to our knowledge) in any species within that class/group. The phylogeny is based on
that of Meyer & Zardoya (2003). At present, the relationships between hagfishes and lampreys and between lungfishes and
the coelacanth are considered polytomies but have been depicted here as being monophyletic based on other visual characters.
Prionace glauca, and the shortfin mako shark, Isurus
oxyrhinchus, while benthic or bottom-dwelling species
often have characteristic markings that contrast the
background colour and appear as spots, stripes, bars,
blotches or reticulations (Kemp 1999; Hart et al.
2006a,b). In many species, the role of these patterns
has been interpreted as camouflage, although it is
not known whether the animals themselves use
differences in colour and patterning to recognize
conspecifics. In the nurse shark, Ginglymostoma
cirratum, females appear to select larger and darker
coloured males (Pratt & Carrier 2001), suggesting
that body colouration and/or contrast could be used
as a cue by females to select mates in this species.
The Australian lungfish N. forsteri has the potential
for a complex colour vision system based on either trichromacy (adults) or tetrachromacy (juveniles). Also,
Phil. Trans. R. Soc. B (2009)
by reducing the overlap of the spectral sensitivities of
adjacent spectral cone types by long-pass spectral filters (oil droplets), there is an improvement in colour
discrimination, despite the unavoidable reduction in
total photon catch (Vorobyev 1997). Previous studies
have highlighted the theoretical advantages of retinal
spectral filters for colour discrimination in terrestrial
birds and semiaquatic freshwater turtles, but it appears
that this mechanism has its origin within the aquatic
realm (Hart et al. 2008).
4. CONCLUSIONS
In summary, colour vision is inferred to have evolved
in the earliest vertebrates more than 540 Ma, providing the basis for colour discrimination in all extant vertebrate classes found today. The evolution of multiple
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Review. Vertebrate photoreceptor evolution
cone types in the first vertebrates (the lampreys) provides important clues to the basis of visual communication, not only in fishes but in all gnathostomes.
Further studies are required to establish the selective
forces driving the evolution of photoreception in lampreys, hagfishes and other organisms that represent the
invertebrate –vertebrate transition and to increase our
understanding of the phylogenetic basis of the
duplicity theory (or the evolution of the functional
dichotomy of true rod- and cone-based vision) and
early photoreception. It is clear that before
vertebrates ventured onto land, they possessed a
well-developed colour vision system able to balance
the trade-off between resolution and sensitivity.
Multi-disciplinary approaches will continue to identify
the evolutionary constraints placed upon the shape,
light responses, spectral sensitivity and molecular
structure of photoreceptors in early vertebrates and
their role in visual behaviour.
The authors would like to thank Ian Potter, Ann Trezise,
Maree Knight, Justin Marshall, Misha Vorobyev and Helena
Bailes for useful discussions and/or taking part in previous
research forming part of this review. This work was
supported by the Australian Research Council and the UK
Biotechnology and Biological Sciences Research Council.
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