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The evolution of phototransduction and eyes
Trevor D. Lamb, Detlev Arendt and Shaun P. Collin
Phil. Trans. R. Soc. B 2009 364, 2791-2793
doi: 10.1098/rstb.2009.0106
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Phil. Trans. R. Soc. B (2009) 364, 2791–2793
doi:10.1098/rstb.2009.0106
Introduction
The evolution of phototransduction
and eyes
Charles Darwin was acutely aware of the need to
account for the evolution of ‘organs of extreme
perfection’ such as the eye and, in particular, of
the importance of demonstrating that numerous
gradations in complexity have existed, with each intermediate stage having provided some kind of advantage
to its possessor (Darwin 1859). In recent years, there
has been remarkable progress in understanding how
the eyes of invertebrate and vertebrate animals have
evolved, and in this Theme Issue leading figures in
the field draw together our current understanding.
Eyes of one kind or another are present in perhaps 95
per cent of all animal species (Land & Nilsson 2002),
indicating that imaging vision provides a great
advantage in numerous environments. The spatial
acuity (or optical resolving power) of these eyes ranges
from spectacularly high in the camera-style eyes of
vertebrates and cephalopods, through moderate in the
compound eyes of arthropods, to very low in the eyes
(or eye-spots) of certain ‘primitive’ invertebrate species.
Indeed, it is a matter of semantics as to what comprises an eye. Common parlance usually adopts a fairly
stringent definition, requiring optical imaging capabilities, as, for example, in a camera-style eye or a
compound eye. However, in the eye evolution field,
a looser definition has often been adopted, encompassing any light-sensitive organ that provides clues to the
direction of illumination; an extreme definition would
include as an eye a single photoreceptor cell shielded
to some degree by dark pigment. The intended
meaning is usually clear in context, though ambiguity
can be avoided by using terms such as ‘imaging eye’,
‘proto-eye’ or ‘eye spot’.
The paths by which eyes in different phyla
have evolved are steadily becoming clearer, although
uncertainties still abound. What is undeniable is that
photoreceptor cells employing rhodopsin-like photopigments linked to G-protein cascades had already
evolved prior to the divergence of cnidaria (e.g. jellyfish and anemones) from our own bilaterian line,
possibly more than 600 Myr ago.
One question that has attracted interest over the
last several decades is the number of times that
eyes have evolved independently in animals. In
their classic survey of photoreceptors and eyes,
von Salvini-Plawen & Mayr (1977) concluded that
One contribution of 13 to Theme Issue ‘The evolution of
phototransduction and eyes’.
eyes had evolved on at least 40 (and possibly up to
65) separate occasions. However, it is now clear that
deep homologies exist between the components of
eyes in different phyla. For example, the photoreceptor
cells of vertebrates and invertebrates are not as distinct
from each other as has sometimes been suggested.
Likewise, the opsin photopigments in the photoreceptors of all animal eyes derive from a common
ancestral opsin, even though the commonly known
animal opsins fall into two distinct groups: rhabdomeric and ciliary. Furthermore, despite the apparent
major differences in the structure of photosensitive
organs across phyla (for example, compound eyes
versus camera-style eyes), the genes that underlie eye
development are in most cases quite clearly related.
As a result, determining the number of times that
eyes have evolved independently depends to a considerable extent on one’s definition of ‘independence’
in this context and also on the level of comparison—
i.e. whether one is comparing molecules, cell types
or organs—and at present a clear-cut answer to the
question remains elusive. At the molecular level, it
has been established that a great many of the components now employed by extant species, either as
crucial elements in phototransduction or elsewhere in
their eyes (e.g. as screening pigments or optical
elements) or as factors controlling the ontogenetic
development of their eyes, were already present as precursors in metazoan animals by the time that cnidaria
diverged. Accordingly, there can be problems in specifying which of the subsequent specializations of eye
construction were genuinely independent of those
that occurred in other eyes and which might better
be construed as variations on a theme.
In recent years, there has been an enormous increase
in the amount of genetic information that is available
and relevant to the evolution of photoreceptors and
eyes, and this has resulted in a considerable shift in
the knowledge base upon which our understanding of
eye evolution is currently founded. This genetic
emphasis is reflected in the content of many of the
articles that follow, as is particularly evident in the
breadth of analyses of the phylogeny of opsin genes.
The papers in this Theme Issue cover a wide range of
topics in the evolution of phototransduction and eyes,
ranging from the origins of light-sensing mechanisms
in ancient single-celled organisms, through the
acquisition of dedicated photoreceptor cells in early
metazoans, to the evolution of proto-eyes and to the
subsequent evolution of sophisticated imaging eyes in
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This journal is # 2009 The Royal Society
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2792
T. D. Lamb et al.
Introduction. Evolution of phototransduction and eyes
both invertebrates and vertebrates. Our sequence of
presentation of the articles follows this general
organization.
The Theme Issue opens with a review of the origin
of the mechanisms of phototaxis that have evolved in
eukaryotes (Jékely 2009). Organisms first evolved
spiral swimming and thereafter acquired photopigments of diverse kinds (often by horizontal transfer
from prokaryotes), which were able to modulate ciliary
activity. Arendt et al. (2009) then present a new model,
coined ‘division of labour’, which accounts for the
evolution of photoreceptor cells and the various
specializations needed to construct ‘proto-eyes’ and
visual circuits. Their model is based on the concept
that the separate functions of an ancestral multifunctional metazoan cell became distributed between
the different members of its descendant cell types.
Vopalensky & Kozmik (2009) analyse the finding
that only a restricted set of transcription factors (e.g.
Pax, Six, Eya, Otx and Mitf ) has been deployed in
the evolution of disparate eyes across phyla, thereby
providing support for the notion that the regulatory
controls for essential photoreceptor genes had already
been established in the ancestral metazoan photoreceptor cell. Nilsson (2009) next analyses the way in
which entire visual systems may have evolved, through
the sequential addition of capabilities (i.e. innovations
such as efficient photopigments, screening pigments
and optics), to produce proto-eyes and thereafter
eyes capable of image formation. For instance, the
evolution of membrane stacking is seen as a prerequisite for the transition from directional photoreception
to the first imaging eyes.
The later articles in the Theme Issue concentrate on
the evolution of vertebrate eyes. Peirson et al. (2009)
review the recently discovered system of inner retinal
photoreceptors in the vertebrate eye, comprising a
subset of retinal ganglion cells that express the photopigment melanopsin and that provide the signals for
circadian synchronization. Melanopsin is a rhabdomeric opsin, and vertebrate retinal ganglion cells
appear homologous to the rhabdomeric photoreceptors of protostomes. At the base of the vertebrate
lineage, two rounds of whole genome duplication
occurred. The remnant signature features of these tetraploidizations, in the paralagon (i.e. quadruplicate)
arrangement of genes, are reviewed by Larhammar
et al. (2009) for the case of 10 families of genes
involved in phototransduction. Shichida & Matsuyama
(2009) explore the evolution of opsin photopigments;
they concentrate on the opsins of vertebrate cone
and rod photoreceptors and they contrast the molecular properties that these alternative proteins contribute
to phototransduction.
Kusakabe et al. (2009) examine the evolution of the
biochemical pathway for the dark resynthesis of 11-cisretinal that is unique to vertebrates, and they provide
indications for the existence of a proto-RPE65 isomerase in an early chordate ancestor of vertebrates. Next,
Lamb (2009) argues that the advent of this biochemical pathway, together with the ability of ciliary opsins
to release their all-trans-retinal, provided a selective
advantage at the very low light levels encountered in
deeper waters, which led not only to the adoption of
Phil. Trans. R. Soc. B (2009)
ciliary rather than rhabdomeric photoreceptors, but
also to the ‘inside-out’ organization of the retina, in
the early vertebrate eye. Subsequent stages in the evolution of vertebrate photoreception are addressed by
Collin et al. (2009), who describe the emergence of
five classes of retinal photoreceptor with cone-like
specializations, using five classes of cone opsin,
presumably for daylight vision and very possibly
underlying colour vision.
The final two articles trace the evolution of colour
vision in birds and mammals. Birds retain four classes
of cone pigment and are generally considered to be tetrachromats; mammals retain only two classes of cone
pigment, the short-wavelength-sensitive (SWS1) and
long-wavelength-sensitive opsins, and are therefore
usually dichromats. Hunt et al. (2009) follow the
evolution of spectral tuning of vertebrate visual
pigments, paying particular attention to those residues
that tune the SWS1 pigments in different groups of
both birds and mammals. In the last article, Jacobs
(2009) traces the evolution of colour vision in mammals and considers the loss and gain of opsin classes
leading to di- and monochromacy, as well as the
special case of trichromacy, which is regained in
some groups of primates. He also examines the possible role of rods and rhodopsin in colour vision in
some species of mammal.
For further reviews of eye evolution aimed at a more
general audience, the reader is referred to Gregory
(2008) and to the other papers in the same issue of
that volume.
Trevor D. Lamb1,*, Detlev Arendt2 and
Shaun P. Collin3
1
ARC Centre of Excellence in Vision Science, and Eccles
Institute of Neuroscience, John Curtin School of Medical
Research, The Australian National University, Canberra,
ACT 0200, Australia
2
European Molecular Biology Laboratory,
Meyerhofstrasse 1, 69012 Heidelberg, Germany
3
School of Biomedical Sciences, The University of
Queensland, Brisbane 4072, Queensland, Australia
*Author for Correspondence
([email protected]).
REFERENCES
Arendt, D., Hausen, H. & Purschke, G. 2009 The
‘division of labour’ model of eye evolution. Phil.
Trans. R. Soc. B 364, 2809–2817. (doi:10.1098/rstb.
2009.0104)
Collin, S. P., Davies, W. L., Hart, N. S. & Hunt, D. M. 2009
The evolution of early vertebrate photoreceptors. Phil.
Trans. R. Soc. B 364, 2925–2940. (doi:10.1098/rstb.2009.
0099)
Darwin, C. 1859 On the origin of species by means of natural
selection, or the preservation of favoured races in the struggle
for life. London, UK: John Murray.
Gregory, T. R. 2008 The evolution of complex organs. Evol.
Edu. Outreach 1, 358– 389. (doi:10.1007/s12052-0080076-1)
Hunt, D. M., Carvalho, L. S., Cowing, J. A. & Davies, W. L.
2009 Evolution and spectral tuning of visual pigments in
Downloaded from rstb.royalsocietypublishing.org on October 6, 2012
Introduction. Evolution of phototransduction and eyes T. D. Lamb et al.
birds and mammals. Phil. Trans. R. Soc. B 364, 2941–
2955. (doi:10.1098/rstb.2009.0044).
Jacobs, G. H. 2009 Evolution of colour vision in mammals.
Phil. Trans. R. Soc. B 364, 2957– 2967. (doi:10.1098/rstb.
2009.0039)
Jékely, G. 2009 Evolution of phototaxis. Phil. Trans. R.
Soc. B 364, 2795–2808. (doi:10.1098/rstb.2009.0072)
Kusakabe, T. G., Takimoto, N., Jin, M. & Tsuda, M. 2009
Evolution and the origin of the visual retinoid cycle in
vertebrates. Phil. Trans. R. Soc. B 364, 2897 –2910.
(doi:10.1098/rstb.2009.0043)
Lamb, T. D. 2009 Evolution of vertebrate retinal photoreception. Phil. Trans. R. Soc. B 364, 2911–2924. (doi:
10.1098/rstb.2009.0102)
Land, M. F. & Nilsson, D. E. 2002 Animal eyes. Oxford, UK:
Oxford University Press.
Larhammar, D., Nordström, K. & Larsson, T. A. 2009 Evolution of vertebrate rod and cone phototransduction genes.
Phil. Trans. R. Soc. B (2009)
2793
Phil. Trans. R. Soc. B 364, 2867–2880. (doi:10.1098/rstb.
2009.0077)
Nilsson, D.-E. 2009 The evolution of eyes and visually
guided behaviour. Phil. Trans. R. Soc. B 364, 2833–
2847. (doi:10.1098/rstb.2009.0083)
Peirson, S. N., Halford, S. & Foster, R. G. 2009 The
evolution of irradiance detection: melanopsin and the
non-visual opsins. Phil. Trans. R. Soc. B 364, 2849–
2865. (doi:10.1098/rstb.2009.0050)
von Salvini-Plawen, L. & Mayr, E. 1977 On the evolution of
photoreceptors and eyes. Evol. Biol. 10, 207–263.
Vopalensky, P. & Kozmik, Z. 2009 Eye evolution: common
use and independent recruitment of genetic components. Phil. Trans. R. Soc. B 364, 2819–2832.
(doi:10.1098/rstb.2009.0079)
Shichida, Y. & Matsuyama, T. 2009 Evolution of opsins and
phototransduction. Phil. Trans. R. Soc. B 364, 2881–
2895. (doi:10.1098/rstb.2009.0051)