Download Eye evolution: Lens and cornea as an upgrade of animal visual system

Seminars in Cell & Developmental Biology 19 (2008) 71–81
Review
Eye evolution: Lens and cornea as an upgrade of animal visual system
Kristyna Jonasova, Zbynek Kozmik ∗
Department of Transcriptional Regulation, Institute of Molecular Genetics, Academy of Sciences of the Czech Republic,
Videnska 1083, CZ-14220, Prague 4, Czech Republic
Available online 13 October 2007
Abstract
Lens-containing eyes are a feature of surprisingly broad spectrum of organisms across the animal kingdom that represent a significant improvement
of simple eye composed of just photoreceptor cells and pigment cells. It is apparent that such an upgrade of animal visual system has originated
numerous times during evolution since many distinct strategies to enhance light refraction through the use of lens and cornea have been utilized. In
addition to having an ancient role in prototypical eye formation Pax transcription factors were convergently recruited for regulation of structurally
diverse crystallins and genes affecting morphogenesis of various lens-containing eyes.
© 2007 Elsevier Ltd. All rights reserved.
Keywords: Eye; Lens; Cornea; Evolution; Crystallin
Contents
1.
2.
3.
4.
5.
6.
Lens and cornea: introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Environmental constraints affecting lens and cornea properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Molecular basis of lens and cornea mediated vision: recruitment of crystallins by a gene sharing strategy . . . . . . . . . . . . . . . . . . . . . . . . . .
Transcriptional control of lens crystallin genes: convergent evolution of Pax regulatory sequences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Building up the lens: a tale of endless diversity and multiple origins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Summary: implication of lens and cornea upgrade for eye evolutionary history . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Lens and cornea: introduction
Vision is one of the most important animal senses. Eyes of
some sort occur in many animal phyla (Fig. 1), but their anatomy,
ontogenetic origin and degree of sophistication vary enormously
[1]. The minimal setting for an eye involves a single photoreceptor in the vicinity of a cell expressing dark shielding pigment [2]
situation found, for example, in Hesse eye cups of amphioxus
[3]. Primitive eyes can only provide information about light
intensity and direction. Adding an optical system such as lens
and cornea that could increase light collection and produce an
image would dramatically improve optical performance. Lenscontaining (camera-type) eyes can simply be defined as those
∗
Corresponding author. Tel.: +420 2 241062110; fax: +420 2 241063125.
E-mail addresses: [email protected] (K. Jonasova),
[email protected] (Z. Kozmik).
1084-9521/$ – see front matter © 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.semcdb.2007.10.005
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with an additional refractive element in front of the photoreceptive layer. The cornea is a transparent layer on the eye periphery
(usually of a convex shape). The cornea can be represented by a
single cell layer (e.g., box jellyfish) but it can also form a complex multilayer organ (e.g., vertebrates). Sometimes it is difficult
to distinguish between lens and cornea which function in similar ways. Eyes where cornea and lens are united as a single
unit (e.g., corneal lens in Drosophila ommatidium) are known
as well as eyes where the cornea has all (e.g., terrestrial vertebrates) or almost no (e.g., underwater animals) refractive power.
Apart from its refractive function, a cornea can serve as protection for the eye, a nutritive device or a light filter [4–6]. The
complex of the cornea and lens is known as a refracton [7].
This review aims to discuss evolution of lens-containing eyes
using a combination of morphological, ontogenetic, optical and
molecular data. We have chosen six model organisms representing distantly related animals (box jellyfish, fruit fly, scallop,
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Fig. 1. Re-occurrence of lens-containing eyes throughout the animal kingdom. A diagram of main animal phyla indicating the presence of lens-containing eyes or
eyes without a lens (in the adult or in the larval stage) within each phylum. An eye is defined here as an organ of spatial vision with a minimum requirement of a
single pigment cell and at least one photoreceptor cell [2]. The representatives with lens-containing eyes in each phylum are shown in Table 1.
squid, zebrafish and mouse) to illustrate different visual strategies. Finally we propose diverse roles of Pax transcription factors
in assembly of prototypical eye and in convergent evolution of
lens-containing eyes.
2. Environmental constraints affecting lens and cornea
properties
Whereas primitive eyes can serve as simple dark/light sensors, sophisticated lens-containing eyes are often able to produce
a sharp image in the desired plane of focus due to light refraction.
Refraction occurs when light rays travel from a medium with a
given refractive index to a medium with another. Therefore, the
optical characteristics of the eye are primarily determined by
whether it is used in air or water (or both) [8]. Terrestrial animals use the refractive power of both cornea and lens because
two interfaces air/cornea and ocular fluid/lens have refractive
indexes sufficiently different to cause relevant refraction. The
aquatic animals mostly use the refractive power of the lens.
Almost no refraction takes place on the water/cornea boundary because they have usually very similar refractive indexes
[1].
The secret to increasing lens efficiency and thereby compensating for the missing function of the cornea in aquatic species
is the small radius of the lens curvature. The spherical shape of
the lens makes it possible to shorten the focal length and maintain an appropriate size of the eye. Unfortunately the spherical
shape (as the almost universal solution for underwater animals)
introduces image aberrations because the properties of the lens
vary sharply between the lens center and periphery and the light
rays behave differently. The rays coming through the peripheral
parts focus onto a different plane than those coming through
the entire lens (spherical aberration) and the rays of different
wavelengths will be focused differently as well (chromatic aberration). The preferred solution to spherical aberration is a graded
refractive index with the maximum in the lens center and minimum on the lens periphery. The light rays break continuously
through the entire lens and a one-step refraction change does
K. Jonasova, Z. Kozmik / Seminars in Cell & Developmental Biology 19 (2008) 71–81
not occur [9]. Graded refractive index is achieved by the concentration gradient of proteins within a lens. Some aquatic lens
centers contain nearly 100% protein (refractive index 1.55) in
contrast to terrestrial animals where the maximum usually is
40% protein. The refractive index decreases towards the lens
periphery to a value of 1.35 close to the 1.34, refractive index
of sea water [10]. A gradient of protein concentration in lens
creates a problem of protein aggregation which can cause light
scattering. A recent study of a large family of proteins encoding variants of glutathione S-transferase present in squid lens
has provided an interesting example of crystallin evolution to
achieve concentration gradient without an apparent aggregation
[10].
Terrestrial species must integrate the output of two refractive
parts of the eye and for this reason many eye designs emerged
during evolution [1]. Although the eyes of terrestrial species
often profit from the high efficiency of the cornea, some terrestrial animals have fish-like spherical lenses with a gradient of
a refractive index, a strategy which maximizes light gathering
and is thus particularly advantageous and common in nocturnal species such as the mouse [11,12]. An unusual example
of cornea and lens diversity is found among the fish Anableps
anableps [13–15]. This fish, living on the air/water interface has
specially optimized eyes where one half (dorsal) is modified for
air environment and second (ventral) for submerged movement.
The aerial and aquatic sections are divided by a pigmented strip
on the cornea and have different attributes. The lens is pyriform with two separate visual axes. Indeed two distinct images
emerge on the retina. The corneas of the dorsal and ventral eye
are very distinct. The dorsal (aerial) cornea is thicker and flatter
and contains more proteins (gelsolin and G-actin). This part has
also been shown to be glycogen rich and with thicker collagen
fibers. The heavily modified upper part (dorsal) of the cornea has
been discussed in the context of desiccation protection (glycogen content) and the increased refractive role (thickness) on air.
It has been suggested that the ventral part is ineffective as underwater corneas used to be and that the longer visual axis of the
lens together with strong accommodation are crucial for aquatic
vision of the Anableps.
3. Molecular basis of lens and cornea mediated vision:
recruitment of crystallins by a gene sharing strategy
The main optical properties of lens and cornea are transparency and refractive power. Proteins that contribute to these
optical properties are collectively called crystallins. Crystallins
were initially thought to be highly characteristic for their optical functions in the lens but instead they turned out to be neither
specialized nor tissue restricted [16]. Crystallins are best defined
as highly abundant, cytoplasmic water-soluble proteins responsible for the optical properties of the lens in both vertebrates and
invertebrates. The abundance parameter is arbitrary: the protein
must simply be present at a sufficient concentration to affect the
refractive properties of the lens in a biologically meaningful way
in order to be called a crystallin. Known crystallins are generally globular proteins present in the lens as monomers (such as
␥-crystallins), dimers (some ␤-crystallins) or tetramers (such as
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␦-crystallins). Vertebrate ␣-crystallins form even higher order
aggregates of variable size with multiple (up to about 50) interacting polypeptides. The crystallins account for up to 90 percent
of the dry weight of the lens although their absolute concentrations vary between species and also with spatial location in the
lens. Crystallin concentrations are generally higher in aquatic
than terrestrial animals and in the center of lens than periphery. In
order to avoid spherical aberrations crystallin concentration has
to decline smoothly from the center to the periphery of spherical
lens to create a gradient in refractive index. Lens transparency
is maintained when the lens lacks discontinuities of refractive
index greater than half the wavelength of the transmitted light.
Large fluctuations in the concentration of closely packed crystallins could cause light scattering and affect the quality of the
resulting image.
In striking contrast to the universal conservation of opsins as
the visual pigments in the photoreceptors, the lens crystallins
are diverse proteins that are often taxon-specific, i.e. different
proteins function as crystallins in different species [17–19]. The
taxon-specificity of crystallins might be a consequence, at least
in some cases, of multiple independent origins of eyes and/or
lenses during evolution. Thus, while there is phylogenetic inheritance of crystallins, such as for example the ␦-crystallins in
birds and reptiles [20], the crystallin composition within the
lens generally does not reflect evolutionary relationships.
The diversity and taxon-specificity of lens crystallins
throughout the animal kingdom is indicative of convergent evolution of crystallin roles. Certain proteins are preferentially
recruited as lens crystallins. Proteins used as lens crystallins are
often related or identical to ubiquitously expressed metabolic
enzymes or physiological stress proteins. All vertebrate lenses
contain the ␣-crystallins belonging to the family of small heat
shock proteins [21,22] and the ␤/␥-crystallins that are related to
microbial stress proteins [23,24]. Vertebrate ␣-crystallins are
effective chaperones that protect partially denatured proteins
from aggregating in the lens [25], thus helping to maintain the
transparency. The co-option of a protein with chaperone-like
activity as a lens crystallin makes sense in light of the lack of
protein turnover in vertebrate lenses. Vertebrate lens continues to
increase in diameter throughout life. As the lens grows the lens
fiber cells differentiate, lose their nuclei and other organelles
and are, therefore, incapable of replacing the aging crystallins.
As a result, the core of the lens contains proteins produced well
before birth that have to last a lifetime. The selective advantage
of recruiting enzyme-crystallins is less clear [16]. First, they
do not fall within a common metabolic category. The catalytic
activities include but are not limited to lactate dehydrogenase
(␧-crystallin), argininosuccinate lyase (␦-crystallin), ␣-enolase
(␶-crystallin) or glyceraldehyde 3-phosphate dehydrogenase (␲crystallin). Furthermore, some enzyme-crystallins have lost
their catalytic activity (e.g. aldehyde dehydrogenase/scallop
-crystallin) suggesting that, unless they have gained a new substrate specificity, their function in lens is limited to the structural
(refractive) role. An interesting group of enzyme-crystallins with
additional putative non-refractive function represent proteins
that bind nicotinamide adenine dinucleotide cofactors (NADbinding enzyme-crystallins). It was proposed that NAD-binding
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enzyme-crystallins present in high amount in lenses could serve
as UV filters to reduce glare and/or to protect against oxidative stress [26]. It is possible that NAD-binding contributed to
frequent recruitment of this group of enzymes as lens crystallins.
There is an intriguing parallel between lens crystallins and
abundant, taxon-specific corneal proteins (e.g. aldehyde dehydrogenase). Although their optical (refractive) function has not
yet been established the close proximity and co-evolution of lens
and cornea, currently viewed as a single unit, the “refracton”,
suggest that these abundant proteins might be considered corneal
crystallins [7].
An important general concept, ‘gene sharing’, has emerged
from crystallin studies [16,19,27]. Gene sharing proposes multiple uses of a single protein encoded in one gene. Thus, the
protein encoded by a single gene may perform two entirely
different functions: a refractive function in the lens as a lens
crystallin and a catalytic or stress function elsewhere (as well
as in the lens). An important implication of gene sharing nicely
illustrated by the example of lens crystallins is that a protein
can evolve a new role, without losing its original function, simply by a change in gene expression [28]. Furthermore the new
function is established in the absence of gene duplication [29].
It has become apparent over time that gene sharing and repeated
use of proteins for new tasks in general represents a common
evolutionary strategy [16].
4. Transcriptional control of lens crystallin genes:
convergent evolution of Pax regulatory sequences
Crystallin protein levels in the lens can be affected by multiple
parameters such as transcriptional rate, translational efficiency,
mRNA or protein stability. However, it appears that the tissuespecific transcriptional regulation plays a key role in recruiting
a gene to become crystallin gene. Remarkably, the high lenspreferred expression of non-homologous crystallin genes is
regulated by a similar set of transcription factors in vertebrates
and invertebrates [30–33]. Many of these transcription factors
are either known regulators of lens (or eye) development (e.g.
Pax, Sox, Maf, Prox1) or transcription factors sensing oxidative
stress (e.g. AP1, CREB) [33].
Perhaps the most remarkable is the widespread conservation
of Pax transcription factors as regulators of eye development and crystallin gene expression (reviewed in [34–38]).
Molecular dissection of crystallin promoters and enhancers identified a number of functional Pax regulatory elements. First
of all, Pax6 can activate or repress many vertebrate crystallin
reporter genes in transfection assays. This appears to be a
direct effect since many Pax6 binding sites were identified
in crystallin regulatory regions by either in vitro or in vivo
(chromatin immunoprecipitation) appproaches. In vertebrates,
Pax6 has been implicated in regulation of chicken and mouse
␣A-crystallin [39–41] mouse ␣B-crystallin [42], ␤B1-crystallin
[43], chicken ␦1-crystallin [44,45], mouse ␥E/␥F-crystallins
[46,47] and taxon-specific guinea pig ␨-crystallin [48]. Much
less is known about Pax6-mediated crystallin gene regulation in
invertebrates. The promoter of the scallop -crystallin gene has
an arrangement of putative cis-control elements, including func-
tional Pax6 binding sites, surprisingly similar to that used for
lens promoter activity of the unrelated ␣A-crystallin genes [31].
Cnidarians who lack a true Pax6 gene [32] have recruited another
member of Pax gene family, designated PaxB, for crystallin activation. PaxB corresponds to an ancestral Pax gene encoding a
paired domain, homeodomain and an octapeptide [49]. The presence of two independent DNA-binding domains is shared by
Pax6 and PaxB. However, specific amino acid changes within
paired domain are responsible for their distinct DNA-binding
specificities. In box jellyfish Tripedalia cystophora possessing well-developed lens-containing eyes PaxB binding sites
were identified in J-crystallin promoters. Furthermore, PaxB
binding sites appeared functional as judged by site-specific
mutagenesis and transfection tests ([32]; Kozmik et al., submitted). The data indicate that modern Pax2 and Pax6 genes
evolved from PaxB ancestor by duplication and diversification
in higher metazoans. Thus the structurally similar yet functionally distinct members of Pax gene family were recruited to
achieve lens-specific crystallin expression in diverse phyla. It
is interesting to note that in all known cases of Pax-mediated
crystallin regulation it is the paired domain and not the homeodomain, which mediates the effect. This situation is reminiscent
of the role of individual domains in general morphogenesis
of animal eyes. At least on the basis of genetic data in vertebrates and flies, the Pax6 paired domain seems to be more
important than is the homeodomain for eye morphogenesis
[50,51].
The presence of similar cis-acting elements for a common
set of transcription factors, especially Pax, in non-homologous
crystallin genes in various animal species is due to convergent evolution. It reflects the situation that the diverse crystallin
genes have been recruited independently during evolution
and hence their regulatory elements to achieve lens-preferred
expression must have been acquired by independent events as
well.
5. Building up the lens: a tale of endless diversity and
multiple origins
The level of sophistication of animal eyes is generally
not correlated with the complexity of animal body plan.
Lens-containing eyes representing a significant improvement
of visual system are sprinkled throughout the animal kingdom
(Fig. 1, Table 1). The first metazoan eyes with lens are found in
the basal phylum Cnidaria. Two out of seven main ecdysozoan’s
phyla developed an eye with a lens. Onychophorans (velvet
worms) possess paired eyes with secreted cuticular cornea
and secreted acellular lens from granular material, with the
whole eye being of epidermal origin [52]. The huge phylum
of arthropods includes mainly species with compound eyes
(either sessile or stalked) or single-chambered eyes with corneal
lens. The lophotrochozoan group includes large phyla such as
mollusks, annelids and plathelminthes. Mollusks are characterized by unusual diversity of their visual system including
sophisticated camera-type (squid) or mirror-containing eyes
(scallop). Within the annelid phylum there are representatives with lens eyes among polychaetes. A simple cup eye,
K. Jonasova, Z. Kozmik / Seminars in Cell & Developmental Biology 19 (2008) 71–81
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Table 1
A table comprising those phyla where lens-containing eye occurs
Phylum
Representative
Lens type
Reference
Cnidaria
Hydrozoa
Cubozoa
Onychophorans
Cladonema radiatum
Tripedalia cystophora
Perpatonder novaezealandiae
Lens bodies
Cellular lens
Non-cellular lens
[101]
[65]
[52]
Porcelio scaber
Portia fimbriata
Craterostigmus tasmanianus
Drosophila melanogaster
Entobdella soleae
Corneal lens and crystalline cone
Corneal lens and secondary retinal lens
Corneal lens
Corneal lens and crystalline cone
Mitochondrial lens
Odontosyllis enopla
Cellular lens
[102]
[103]
[104]
[105] (lens secretion)
[56]
[55]
[53]
Hermissenda crassicornis
Pecten maximus
Loligo opalescens
Ophiocoma wendtii
Ciona intestinalis
Anableps anableps
Non-cellular lens (secreted)
Cellular lens
Non-cellular lens (fused procceses)
Calcitic lens
Three-cell lens
Cellular lens
[107]
[69]
[73]
[58]
[106]
[13]
Arthropods
Crustaceans
Cheliceriformes
Myriapoda
Hexapoda
Plathelminthes
Nemerteans
Annelids
Mollusks
Gastropoda
Bivalvia
Cephalopoda
Echinoderms
Tunicates
Craniates
For each phylum at least one representative with lens type specification and reference is given.
a lensed cup eye (nereid, platynereis) as well as complex
eyes with spherical lens (Vanadis, Odontosyllis) occur in this
diverse class [53–55]. Really peculiar lenses with a likely
mitochondrial origin have been identified within the phylum
Plathelminthes [56,57]. Proteins are not the only refractive
material used for a lens as exemplified by the echinoderm
phylum. Some brittlestars use a unique system of vision
based on calcitic lenses [58]. Similar calcitic lenses have
been discovered also within trilobite fossils [59]. The origin
of vertebrate lens is probably the most interesting question
in relation to our own vision. When we follow the proposed
vertebrate line – cephalochordates (amphioxus)–tunicates
(ciona)–craniata/hyperotreti (hagfish)–vertebrates/hyperoartia
(lamprey)–vertebrates/chondrichtyes
(shark)–vertebrates/teleostomi (fish) – it is possible to see
the development of the concept of lens. It is thought that the
image-forming eye of vertebrates evolved after cephalochordates split [3]. Based on the fossil record of early chordates,
such as pikaya, it appears that those animals did not have
prominent paired eyes. A frontal eye of the amphioxus with
ciliated photoreceptor cells therefore most likely represents an
ancestral condition from which paired bilateral eyes of vertebrates formed rather than a derived (regressed) state. Already
in tunicates which were shown to be closer to vertebrates than
cephalochordates [60], there is an ocellus with three-cell lens in
the larval stage of some species. Study of Ciona ␤␥-crystallin
suggests that chordate ␤␥-crystallin ancestor was already
expressed in a cell-specific manner in derivatives of a primitive
visual system prior to the evolution of the lens in vertebrate
lineage [61]. Hagfish have a poorly developed visual system
(probably as a result of regression) in contrast to lampreys that
previously had relatively small but fish-like eyes with almost
spherical multicellular lens covered closely with a thin cornea
[62]. And finally, the spherical lens with appropriate gradient
of refractive index is the best solution for aquatic animal;
consequently this design is usually maintained among fishes,
the true vertebrates [9].
Diversity of lens-containing eyes is observed at every level
of comparison–structural design, ontogenetic origin or the
crystallin content. Yet the final morphological appearance of
lens-containing eyes is often remarkably similar suggesting
independent origins by convergent evolution. In the following paragraphs we compare and contrast eyes of six organisms
representing distantly related animals (box jellyfish, fruit fly,
scallop, squid, zebrafish and mouse) to illustrate different visual
strategies (Fig. 2).
In box jellyfish (Tripedalia cystophora) very complex structures characteristic of more advanced animals appear such as
the camera-type eye situated within four sensory organs called
rhopalia. Each rhopalium carries six eyes: two pit-shaped, two
slit-shaped and two complex with a cellular lens. The eyes with
lens are covered with a thin cornea, but differ in size, lens shape,
retinal geometry, as well as in gradient of a refractive index [63].
The cornea is de facto a part of a single layer covering the entire
rhopalium and has no refractive capacity. The large biconvex
lens has a homogenous center and a peripheral gradient but the
drop-shaped lens of the small eye has an almost perfect gradient
through the lens correcting its aberrations. The resulting image
produced by the lenses is severely out of focus and, i.e., blurred.
It can be functional as a low-pass filter for this animal which
would not be able to use a more complex image [63]. The
rhopalium develops during metamorphosis of the polyp into the
medusa stage from a dedifferentiated cell derived from fused
polyp tentacles and thus the lenses are originally derived from
myoepithelial cells [64]. None of the Tripedalia crystallins
have a sequence relationship to other crystallins in any other
species [65–68]. Two crystallins, J1 and J2, provide a majority
of crystallins within the lens of both the small and large eye.
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K. Jonasova, Z. Kozmik / Seminars in Cell & Developmental Biology 19 (2008) 71–81
Fig. 2. Lens-containing eyes of selected model organisms. (A) Phylogenetic distances of selected model organisms and their distribution across the animal kingdom.
Splits between clades are indicated in million years (mya). (B) Hematoxylin-eosin stained sections of animal eyes showing differences in lens and cornea shape and
structure. Note the crystalline core of the fish lens (medaka) and an unusual shape of scallop’s lens. L, lens; c, cornea. (C) A schematic diagram illustrating the eye
morphology, crystallin variability and refractive index (n) in the center of the lens of selected model animals [84,63,69,10,100].
K. Jonasova, Z. Kozmik / Seminars in Cell & Developmental Biology 19 (2008) 71–81
The lens in the scallop (Argopecten irradians) eye, unlike
other underwater animals, has a homogenous refractive index
and a hemispheric shape [69]. This is because the image is produced by the mirror on the posterior wall of the eye but not by
the lens. The mirror formed by the layer called argentea or tapetum consists of layers of guanine crystals and has a refractive
index of 1.8 [69]. Light rays coming through the lens reflect
on the distal retina neighboring the mirror. The lens probably
has a role in correcting the spherical aberration of the mirror.
Lens of the bay scallop was described as soft (in contrast to fish)
and filled with one major crystallin (-crystallin) identified as
an aldehyde dehydrogenase and noted ALDH1A9 [31]. The cooption of an ALDH enzyme as a crystallin has occurred several
times in vertebrates or in invertebrates. Scallop -crystallin has
homology to squid and an octopus minor lens -crystallin [70].
-crystallins are enzymatically inactive. It is also expressed in
the cornea and together with other records of corneal crystallin
expression supports the idea of its role as a corneal crystallin
[71].
A squid (Loligo opalescens) possesses an eye with a spherical
lens that has a graded refractive index compensating for spherical
and other aberrations [72]. A cephalopod lens differs markedly
in development compared to vertebrates (although the resulting
lens design of fish and squid is very similar). Vertebrate lenses
develop by invagination or delamination of the surface ectoderm.
The squid lens originates also from the ectoderm but from two
distinguishable parts. Each part is a primordium of one of the
two future halves of the lens. Lentigenic cells of the anterior and
posterior primordium give rise to a bipartite lens which is derived
from ectodermal cellular processes and thus does not have a completely cellular state. The posterior lens primordium arises as the
first and later the anterior forms a smaller plate-like element of
the lens which is thickened during development. The two parts
of the lens are separated by septum, a thin layer of living cells
[73,74]. In addition, the cornea is derived from epithelial tissue.
This tissue from the posterior part of the eye is probably moved
by neighboring muscle cell contractions and migrates over the
eyeball [75]. Modified glutathione S-transferase is a major crystallin (S-crystallin) of the squid ocular lens [76] but aldehyde
dehydrogenase has also been identified as a minor crystallin (crystallin). This enzyme has been further recruited for the lens
of the light organ where it was denoted as L-crystallin [77]. Of
special interest is the fact that there are more than 25 isoforms of
the S-crystallin in the ocular lens of the squid that are differentially expressed to maintain optical performance and clarity of
lens [10]. It has been suggested that gene duplications followed
by mutations to accumulate positive charge in S-crystallin were
essential to achieve concentration gradient without an apparent
aggregation [10].
The compound eye of the fruit fly (Drosophila melanogaster)
consists of hundreds of ommatidia which are composed of
two main refractive parts: corneal lens secreted by underlying
corneagen cells and a four-part crystalline cone (pseudocone)
produced by cone (Semper) cells. The receptive part under the
corneal lens and cones consists of photoreceptors (rhabdomeres)
with rhabdoms. In addition to the refractive and receptive parts
are pigment cells which restrain the receptive field and separate
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ommatidia. The compound eye originates during metamorphosis
from a simple epithelium of the eye disc involving highly complex pattern-creating events. The corneal lens as well as cones
are epithelial derivatives (secreted by cone cells, corneagen cells
and primary pigment cells) and serve as independent surfaces for
multiple refraction [1,55]. A 52 kDa large glycoprotein (known
as drosocrystallin) has been described as a major protein of the
corneal lens [78]. It was shown that drosocrystallin is a homologue of a cuticle protein indicating that a gene-sharing strategy
has been used in arthropods.
The eyes of zebrafish (Danio rerio) are laterally placed and
the protuberant lenses allow for panoramic vision. A zebrafish
lens is spherical having a refractive index gradient with the maximum refractive index in the center of the lens. The whole eye is
developed within first 3 days after fertilization but growth continues for 1 month [79,80]. The development is similar to that of
other vertebrates but important differences have been found. The
lens does not originate from the surface ectoderm by the process
of invagination as known for other vertebrates but a thickened
lens placode undergoes delamination. Thus the lens vesicle rises
as a compact formation and primary fiber cells are formed from
the central cell cluster (and not from posterior epithelial cells)
forming the nucleus of the lens. Three classes of crystallins
(␣-, ␤-, ␥-) typical for vertebrates are expressed in zebrafish
lens. Among those more than sixteen ␥-crystallins have been
found including nine ␥M-crystallins characteristic for aquatic
animals and two ␥N-crystallins which were described as evolutionary hybrids of ␤- and ␥-crystallins [81]. Corneal crystallins
of the gelsolin protein family have been described for zebrafish
[82]. It is a diverged paralogue of the vertebrate scinderin gene
with calcium- and actin-binding and actin-severing capabilities.
Six genes have been cloned and sequenced, three of them with
preferential expression in the cornea [83]. Gelsolin-like proteins were found in zebrafish as well as in Anableps where the
expression varies between ventral and dorsal cornea [14,83].
The nocturnal mouse (Mus musculus) has a large spherical
lens and curved cornea that are ideal for very short focal length
and maximal light gathering capacity [1,84]. Both cornea and
lens function in light focusing in mouse. A critical region of
cornea for refraction is collagen rich stroma where collagen
fiber bundles form a highly ordered three-dimensional network
[85,86]. The lens has an almost spherical shape that suffers from
spherical aberrations and has a smooth gradient of refractive
index [87]. Taken together, mouse is able to gather much more
light than the human eye can, but the quality of the image is
decidedly worse [87]. Mouse lens arises by invagination of
surface ectoderm for which the interaction with optic vesicle
(neural ectoderm) is a key inductive step (for review see [88]).
The corneal epithelium develops at first from anterior surface
ectoderm. Migrating periocular mesenchymal cells (neural crest
and paraxial mesoderm cells) give rise to presumptive corneal
stroma. The posterior part of the cornea differentiates later into
corneal endothelium. As in zebrafish, all three major vertebrate
crystallin classes (␣-, ␤-, ␥-) are present in the mouse lens. ␣Acrystallin is expressed mainly in the lens while ␣B-crystallin
is an ubiquitous protein. The elimination of ␣A-crystallin in
mice leads smaller and opaque lenses [89] while ␣B-crystallin-
78
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defficient mice exhibit more pleiotropic phenotypes associated
primarily with muscles and heart [90,91]. A cluster of six
␥-crystallins (A–F) typical for placental mammals is expressed
within the mouse lens [92]. The main corneal crystallin in mouse
is ALDH3a1 [93,94]. Interestingly, although ALDH3a1 comprises nearly one-half of the water-soluble protein fraction in
the corneal epithelium, the ALDH3a1 knockout mouse contains
no detectable defects in corneal morphology or transparency
[95].
6. Summary: implication of lens and cornea upgrade
for eye evolutionary history
The eye has challenged generations of evolutionary biologists. Whether an eye originated once (monophyletic origin) or
multiple times (polyphyletic origin) still remains a controversial
topic. Despite obvious anatomical, developmental and organizational differences between mouse and Drosophila eyes, genetic
studies have indicated that a homologous gene, Pax6, directs
development of eyes in both species [96,97]. Since then more
evidence has emerged for an almost universal re-deployment of
Pax genes for animal eye development [32,34]. Such common
underlying genetic mechanism provides a powerful argument
for monophyletic eye origin [34] and might reflect an ancient
role of Pax genes in functioning of a “primitive eye” (eye
prototype) composed of a photoreceptor cell and a shielding
pigment cell. A bipartite model proposes that the two independent DNA binding domains within a single Pax transcription
factor have been co-opted for two essential features of the prototypical eye [35] (Fig. 3, top). Production of a dark shielding
pigment (‘pigmentation’ program) has been controlled by paired
domain and production of a photopigment (‘opsin’ program)
by homeodomain. Once such transcriptional regulatory network
was established the two genetic programs being driven by two
independent DNA binding domains within a single transcription
factor became virtually inseparable.
In contrast, the enormous morphological diversity found
among animal eyes seems incompatible with monophyletic
Fig. 3. Diverse roles of Pax transcription factors during eye evolution. All eyes require an assembly of photoreceptor cells (grey) and shielding pigment cells
(black). An almost universal use of Pax genes in eye formation throughout the animal kingdom argues for their ancient role in generation of a prototypical eye as
a photoreceptor/pigment cell combination (top). The bipartite ‘Paxcentric model’ [35] proposed independent functions of paired domain and homeodomain of Pax
transcription factors in regulating either photoreceptor or pigment cell programs. Lens-containing eyes have evolved independently multiple times. Pax transcription
factors are likely involved in the divergent morphogenesis of various types of lens-containing eyes. Convergent evolution of Pax regulatory elements was a driving
force behind the recruitment of lens crystallin genes and eye ‘morphogenesis’ genes. ‘Morphogenesis’ genes are the ones required for eye development in any given
animal. Note that opsin genes are homologous across phylogeny, whereas lens crystallins are encoded by structurally unrelated genes in different species.
K. Jonasova, Z. Kozmik / Seminars in Cell & Developmental Biology 19 (2008) 71–81
origin but is rather consistent with convergent evolution and
multiple independent origins [98]. Theoretical modeling suggested that a camera-type eye can evolve from a flat layer of
photosensitive epithelium in less than 400,000 generations [99].
We can view camera-type (lens-containing) eyes as a significant improvement of primitive eyes that has allowed animals
to gather more light onto their photoreceptors and to obtain
a focused image. Such an upgrade of eyes by addition of a
lens (and cornea) was a milestone during eye evolution. As
described above amazingly broad and distinct strategies of how
to design lens and cornea have been utilized by different animals. It follows that the lens/cornea upgrade of animal eyes has
a polyphyletic origin. It is almost impossible to find anything
uniting corneal lens of jumping spiders and spherical lens of
fish. There is no doubt that even in the case of cellular lenses
with their crucial refractive ability provided by an accumulation
of crystallins it is safe to argue for multiple independent origins
because the genes encoding lens (and corneal) crystallins are
almost always taxon-specific [16]. It is intriguing that the same
transcription factors, especially Pax, were used once again as
key regulators in lens/cornea upgrade. Pax regulatory elements
were essential for convergent recruitment of lens and corneal
crystallins as well as for driving the divergent morphogenesis
of various types of lens-containing eyes (Fig. 3, bottom). In
summary, animal eyes have evolved by convergent mechanisms
a variety of lenses and corneas containing diverse crystallins
and displaying multiple differences for achieving their visual
functions.
Acknowledgements
We would like to thank Jana Ruzickova, Roger Hanlon,
Marek Jindra for providing some animal photographs. Work in
Kozmik’s laboratory is supported by Grant nos. AV0Z50520514
and IAA500520604 from the Academy of Sciences of the
Czech Republic and by Center for Applied Genomics grant no.
1M6837805002 awarded by Ministry of Education, Youths and
Sports of the Czech Republic.
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