The ocular skeleton through the eye of evo-devo
Post on 11-Jun-2016
The Ocular Skeleton Throughthe Eye of Evo-DevoTAMARA ANNE FRANZ-ODENDAAL
Biology Department, Mount Saint Vincent University, Halifax, Nova Scotia, Canada
An evolutionary developmental (evo-devo) approach to understanding the evolution, homology, anddevelopment of structures has proved important for unraveling complex integrated skeletal systemsthrough the use of modules, or modularity. An ocular skeleton, which consists of cartilage andsometimes bone, is present in many vertebrates; however, the origin of these two componentsremains elusive. Using both paleontological and developmental data, I propose that the vertebrateocular skeleton is neural crest derived and that a single cranial neural crest module divided early invertebrate evolution, possibly during the Ordovician, to give rise to an endoskeletal component and anexoskeletal component within the eye. These two components subsequently became uncoupled withrespect to timing, placement within the sclera and inductive epithelia, enabling them to evolveindependently and to diversify. In some extant groups, these two modules have become reassociatedwith one another. Furthermore, the data suggest that the endoskeletal component of the ocularskeleton was likely established and therefore evolved before the exoskeletal component. This studyprovides important insights into the evolution of the ocular skeleton, a region with a long evolutionaryhistory among vertebrates. J. Exp. Zool. (Mol. Dev. Evol.) 316:393401, 2011. & 2011 Wiley-Liss, Inc.
How to cite this article: Franz-Odendaal TA. 2011. The ocular skeleton through the eye ofevo-devo. J. Exp. Zool. (Mol. Dev. Evol.) 316:393401.
The ocular skeleton of vertebrates is well known among
paleontologists as enigmatic structures within the eye whose
function, origin, and homology are not well understood. The
ocular skeleton can consist of bone and/or cartilage. Two general
morphologies are recognized: (i) a multi-component ring of
several scleral ossicles with a separate scleral cartilage cup
supporting the eyeball (e.g. in reptiles) (Fig. 1); or (ii) two scleral
ossicles joined by scleral cartilage (e.g. in advanced teleosts)
(Fig. 2). Importantly, the relationship between the scleral ossicles
and the scleral cartilage is different in each of these morphologies
(Franz-Odendaal and Hall, 2006a).
In 1929, Dr. Tilly Edinger published the first comparative
study on the scleral ossicles of both fossil and modern vertebrates
in an attempt to try and resolve some of these complexities
(Edinger, 29). More recently, Franz-Odendaal and Hall (2006a)
provided an updated assessment of the presence and absence of
scleral ossicles and scleral cartilage within the eyes of extant
vertebrates. From this analysis, we concluded that the ocular
skeleton(s) of extant teleosts and reptiles differs morphologically
and in their mode of ossification. Furthermore, presuming a
common ancestral ocular skeleton, we hypothesized that the
scleral ossicles of extant reptiles and extant teleosts cannot be
assumed to be homologous to one another (Franz-Odendaal and
The evolution of ocular skeleton is particularly complex to
resolve because at various time points (and/or in various
lineages) during vertebrate evolution one or both components
may be absent. There is also a large variability in the morphology
of the ocular skeleton specifically with respect to its overall
structure (a capsule or a ring of plates/ossicles), and with respect
to the individual ossicles within the sclerotic ring, which can be
variable in shape, size, and number, both among different
vertebrate groups and within taxa (Franz-Odendaal and Hall,
2006a; Franz-Odendaal, 2011) (Figs. 1 and 2). Together, this
variability in the ocular skeletal morphology significantly
complicates any attempt at an evolutionary assessment. Here,
I attempt to resolve the evolutionary history of the ocular
skeleton by reassessing its morphology in the jawless vertebrates.
Published online 19 April 2011 in Wiley Online Library (wileyonline
library.com). DOI: 10.1002/jez.b.21415
Received 25 October 2010; Revised 22 February 2011; Accepted 24 March
Grant Sponsor: Natural Sciences and Engineering Research Council, Canada;
Grant number: DG ] 328376.Correspondence to: Tamara Anne Franz-Odendaal, Biology Department,
Mount Saint Vincent University, Halifax, Nova Scotia, Canada B3M 2J6.
J. Exp. Zool.(Mol. Dev. Evol.)316:393401, 2011
& 2011 WILEY-LISS, INC.
PERSPECTIVE AND HYPOTHESIS
Figure 1. Schematics showing some of the variation in scleral ossicle shape and size, the amount of cartilage support and the size of the eye
aperture within Reptilia. (A) The European green lizard Lacerta viridis, (B) the legless lizard, Anguis fragilis, (C) the gecko Gehyra mutilata, and
the chicken Gallus gallus. The cartilage support in D is very large compared with the very reduced cartilage element in A and C (a cup vs. a
disk). Shaded regions show scleral cartilage; unshaded regions indicate scleral ossicles.
Figure 2. Schematic of teleost scleral ossicles and scleral cartilage, lateral view of the eye with the ossicles situated anterior and posteriorly
within the eye. (A) Two large ossicles as seen in salmon, Salmo salar, for example; (B) the two small ossicles of the pike, Esox; and (C) the
complete scleral cartilage ring of the American eel, Anguilla rostrata. For phylogentic distribution, see Franz-Odendaal et al. (2008b). Shaded
regions show scleral cartilage; unshaded regions indicate scleral ossicles.
J. Exp. Zool. (Mol. Dev. Evol.)
I then apply the evolutionary developmental (evo-devo) concept
of modularity (described below) to this data set and discuss the
evolutionary origin of these elements.
Endoskeleton or Exoskeleton?
Within the paleontological field, ossifications within the eye have
been reported as one of two morphologies; either as scleral
ossicles (a series of dermal bones) and/or as an ossified
endoskeletal scleral capsule within the eye (e.g. in Donoghue
et al., 2000). This is an important distinction. Although many
agree that the presence of scleral ossicles is a unifying character
of gnathostomes and Osteostraci (Maisey, 86; Donoghue et al.,
2000), the presence of an additional endoskeletal scleral capsule
is less certain. Several authors, for example, code Osteostraci as
having both scleral ossicles and an ossified endoskeletal scleral
capsule encapsulating the eyeball (Donoghue et al., 2000; Gess
et al., 2006). Others do not make this distinction (Zhu et al., 99).
I have reassessed the ocular skeleton at major nodes of
vertebrate evolution based on the published literature. However,
before discussing these data, we should examine the use of the
term endoskeletal vs. exoskeletal. Most of the vertebrate skeleton
of extant animals consists of bone and cartilage, is internal and is
considered endoskeletal. The exoskeleton arose as denticles in
association with ectoderm, and consists of bone and dentine with
no cartilage components. During vertebrate evolution, the
exoskeleton has been greatly reduced. The endoskeletal cartilage
on the other hand either persisted as permanent cartilage, or as
mineralized cartilage (as in sharks) or was replaced by bone (via
endochondral ossification; Smith and Hall, 90). With respect to
germ layer origins, the endoskeleton is mesodermal or neural
crest derived, whereas the exoskeleton is always neural crest
derived. The neural crest cells migrate out of the neural folds
during neural tube formation and are considered derivatives of
the neural ectoderm.
Regarding the ocular skeleton, the scleral ossicles of extant
reptiles are induced by ectoderm and do not preform in cartilage,
and therefore should be considered exoskeletal; the scleral
cartilage cup situated more posteriorly in the eye, however, is a
permanent or persistent cartilage and should be considered
endoskeletal. In advanced teleosts, in which two scleral ossicles
are joined by scleral cartilage, the situation is different. Here, the
scleral ossicles develop via a form of endochondral ossification
from a cartilage template (Franz-Odendaal et al., 2007). Both
components in extant teleosts should therefore be considered
endoskeletal. In summary, only the scleral ossicles of extant
reptiles are exoskeletal, whereas all the other components of the
ocular skeleton of extant vertebrates are endoskeletal.
A Phylogenetic Assessment
In addition to the differences in the terminology used to describe
the ocular skeleton, this region of the skeleton has been character
coded in inconsistent ways with respect to the number of
elements. Zhu et al. (99) coded the number of scleral plates/
ossicles: 0 for four or less plates; 1 for greater than four plates. In
contrast, Donoghue et al. (2000) coded the ocular skeleton in two
characters. One character for scleral ossicles, regardless of
number of elements: 0 if the ossicles were absent; 1 if they were
present. The second character was the ossified endoskeletal
sclera: 0 if absent; 1 if present. Other paleontologists are less
clear, for example, figures given in Luksevics and Vin (2001),
describe the ocular skeleton of Asterolepis (a placoderm) as a
scleral capsule yet the figure shows a ring and is labeled as
Sclr for sclerotic ring.
A re-coding of the ocular skeleton at major nodes of
vertebrate evolution based on the published literature is needed
and should help to unravel this data; ultimately it should help us
to understand the evolution of the ocular skeleton (Fig. 3). We
have previously hypothesized about the homology of the
components of the ocular skeleton based on data from extant
actinopterygians and extant sarcopterygians. The focus in this
manuscript is to go further back in vertebrate history and to
examine the ocular skeleton of jawless vertebrates. To do this, the
ocular skeleton as a single entity was assessed as present or
absent in each group, regardless of the number of elements, the
type of ossification, the shape (capsule vs. ring), or skeletal type
(endoskeleton vs. exoskeleton). Second, the (endoskeletal vs.
exoskeletal) components were coded, regardless of their mor-
phology. These data are presented and summarized in Figure 3.
The ocular skeleton is present in extant gnathostomes
(Sarcopterygii, Actinopterygii, and Chondrichthyes) as well as
in basal gnathostomes such as placoderms (Table 1, Fig. 3). Most
placoderms have scleral ossicles and some have dermal
ornamentation on these bones (Burrow et al., 2005). However
in one placoderm (Jagorina) the ocular skeleton has been
described as an ossified capsule fused to a sclerotic ring of bones
(Stensio, 50; Luksevics and Vin, 2001); that is both components
of the ocular skeleton are present. In acanthodians, a sclerotic
ring is described in some forms (Acanthodes, Homalacanthus)
while others (Climatius, Ptomacanthus, Euthacanthus, Brachya-
canthus, Cassidiceps) possess circumorbital plates (Gagnier, 96).
Watson (37) however, considered the ring in all these
acanthodians as circumorbital plates. Friedman and Brazeau
(2010) note that no acanthodian has both a sclerotic ring and
circumorbital plates, begging the question of their homology. To
unravel this status, these groups should be re-examined (see
recent work by Burrow et al., 2011); however, this is not the focus
of the current review. To summarize, the fossil record of jawed
vertebrates provides evidence for an ocular skeleton in all groups
(placoderms, acanthodians, Osteichthyes, and Chondichthyes).
Within jawless vertebrates, no ocular skeleton is known from
Eriptychius; however, this fossil is known from fragmentary
elements only. An ocular skeleton is described in Osteostraci as
an endoskeletal capsule with scleral ossicles (Edinger, 29; Walls,
63; Donoghue et al., 2000; Gess et al., 2006). The ocular skeleton
SCLERAL OSSICLE EVOLUTION 395
J. Exp. Zool. (Mol. Dev. Evol.)
is absent in Galeaspids, Heterostraci, Anaspida, Jamoytius,
Euphanerops, and Loganellia (Edinger, 29; Gess et al., 2006).
Interestingly, there is evidence for an ocular skeleton in the
Ordovician before the evolution of the above groups; both
Astraspis and Arandaspida have an ocular skeleton (Gess et al.,
2006). Astraspis has an ossified endoskeletal capsule without
scleral ossicles, whereas Arandaspida has both an ossified
endoskeletal capsule and (exoskeletal) scleral ossicles. The
identification of both scleral ossicles and an endoskeletal capsule
within the eye of Arandaspida is based on a single observation by
Gagnier (93), but has been confirmed by Donoghue et al. (2000).
Groups without an ocular skeleton may have had, and most likely
had, unmineralised connective tissue within the sclera (e.g. as
described in conodonts and as is evident in some extant
vertebrates such as placental mammals; Walls, 63).
This known evolutionary history, places the origin for the
ocular skeleton before the evolution of Astraspis and Arandas-
pida (dating to Ordovician 480440 million years ago; Fig. 3).
Hence, both exoskeletal and endoskeletal components had
evolved at this time. Given that the exoskeletal component is
never found without an endoskeletal component and given that
Astraspis possesses the endoskeletal component alone, the most
likely hypothesis is that the endoskeletal component (the
cartilage-based component) was established first (i.e. before the
exoskeletal component). Interestingly, 480 million years ago is
shortly after the proposed origin of bone and dentine, cartilage
having arose earlier (between 540 and 525 million years ago)
(Donoghue et al., 2008; Fig. 3).
In terms of cellular origins, the exoskeleton is neural crest
derived, whereas the endoskeleton has a mixed origin of neural
crest and mesoderm. It is also well known that the entire avian
ocular skeleton is neural crest derived (Couly et al., 93; Franz-
Odendaal and Vickaryous, 2006). Other data using a sox10-green
fluorescent protein-tagged transgenic zebrafish line indicates that
the ocular skeleton of teleosts is also neural crest derived
(unpublished observation). Regarding fossil specimens, Donoghue
and colleagues have also shown that the neural crest evolved in the
Cambrian, and that the molecular tools required to specify the
neural crest were also present in early vertebrates (hagfishes and
lampreys) (Donoghue et al., 2000, 2008). In summary, the neural
crest was well-established at the time of the origin of the ocular
skeleton and the opportunity to pattern this cell population was
presumably also present. Indeed, the tissue responsible for inducing
the scleral cartilage, the retinal pigmented epithelium, was present
Figure 3. Phylogenetic distribution of the presence and absence of the ocular skeleton within vertebrates. The status of the ocular skeleton
regardless of origin, morphology, or development is denoted by the terms, present, absent, or unknown. This is followed by a coding for the
type of ocular skeleton. The first value in parentheses indicates endoskeletal elements; the second value indicates exoskeletal elements.
15 presence, 05 absence of character. The evolution of neural crest specifiers and effectors from Donoghue et al. (2008) are shown by
means of a red star. The green circle shows the latest time point when the cranial neural crest module possibly subdivided. Phylogeny
modified from Donoghue et al. (2000) and Maddison and Schulz (2007).
J. Exp. Zool. (Mol. Dev. Evol.)
in protochordates (Lamb et al., 2007). In addition, based on the
above evidence from both extant and fossil investigations, it is very
likely that the vertebrate ocular skeleton is neural crest derived.
With this conclusion, we are now in a position to ask how the
cranial neural crest cell population evolved into the ocular
skeletons we see in extant vertebrates today.
Table 1. Analysis of the ocular skeleton of fossil specimens within major vertebrate groups, extant information is provided where relevant.
Order/Family/Genus Ocular skeleton References
Myxinoidea/Myxinikela None Gess et al. (2006)
Myxinoidea/Gilpichthys None Donoghue et al. (2000)
Hyperoartia/Mesomyzon None Gess et al. (2006)
Hyperoartia/Priscomyzon None Gess et al. (2006)
Hyperoartia/Mayomyzon None Gess et al. (2006)
Euconodonta None Gess et al. (2006)
Pteraspidomorphi/Astraspis Ossified endoskeletal capsule only Gess et al. (2006)
Pteraspidomorphi/Arandaspida Scleral ossicles present and ossified
Gess et al. (2006)
Pteraspidomorphi/Heterostraci/Protopterus None Edinger (29)
Thelodonti/Loganellia None Gess et al. (2006)
Anaspida/Jamoytius None Gess et al. (2006)
Anaspida/Euphanerops None Gess et al. (2006)
Galaespida None Gess et al. (2006)
Osteotraci/Cephalaspidea Scleral ossicles present Edinger (29)
Osteotraci/Tremataspis Scleral ossicles present Edinger (29)
Osteotraci Ossicles and endoskeletal capsule Gess et al. (2006),
Donoghue et al. (2000),
Gnathostomes/Actinopterygii/Aspidorhynchus Two bones Edinger (29)
Gnathostomes/Actinopterygii/Guildayichthyiformes Scleral ossicles present Lund (2000)
Gnathostomes/Actinopterygii/Palaeonisciformes/Cyranorhis Scleral ossicles present Lund (2000)
Gnathostomes/Actinopterygii/Palaeonisciformes/Wendyichthys Scleral ossicles present Lund (2000)
Gnathostomes/Actinopterygii/Palaeonisciformes/Moythomasia Scleral ossicles present Lund (2000)
Gnathostomes/Actinopterygii/Palaeonisciformes/Cheirolepis Scleral ossicles present Lund (2000), Edinger (29)
Gnathostomes/Actinopterygii/Semionotiformes/Lepidosteus None de Beer (37)
Gnathostomes/Actinopterygii/Chondrosteus Scleral ossicles present Edinger (29)
Gnathostomes/Acanthodii/Acanthodes Scleral ossicles present Moy-Smith and Miles (71)
Gnathostomes/Sarcopterygii/Osteolepis Scleral ossicles present Edinger (29)
Gnathostomes/Sarcopterygii/Coelacanthiformes Scleral ossicles present Underwood (70)
Gnathostomes/Sarcopterygii/Eusthenopteron Scleral ossicles present Zhu et al. (99)
Gnathostomes/Sarcopterygii/Osteolepis Scleral ossicles present Zhu et al. (99)
Gnathostomes/Sarcopterygii/Acanthostega Scleral ossicles present Cloutier and Ahlberg (96)
Gnathostomes/Chondrichthyes (extant forms) Mineralized cup with tesserae
in some forms
Pilgrim and Franz-Odendaal (2009)
Gnathostomes/Chondrichthyes/Cladoselache Scleral ossicles present Pilgrim and Franz-Odendaal (2009)
Gnathostomes/Placodermi/Selenosteus Scleral ossicles present Pilgrim and Franz-Odendaal (2009)
Gnathostomes/Placodermi/Titanichthys Scleral ossicles present Pilgrim and Franz-Odendaal (2009)
Gnathostomes/Placodermi/Gymnotrachleus Scleral ossicles present Pilgrim and Franz-Odendaal (2009)
Gnathostomes/Placodermi/Heintzichthys Scleral ossicles present Pilgrim and Franz-Odendaal (2009)
Gnathostomes/Placodermi/Dunkleosteus Scleral ossicles present Pilgrim and Franz-Odendaal (2009)
Gnathostomes/Placodermi/Asterolepis Sclerotic capsule Luksevics and Vin (2001)
Gnathostomes/Placodermi/Jagorina Ossified capsule fused to sclerotic
ring of ornamental bones
SCLERAL OSSICLE EVOLUTION 397
J. Exp. Zool. (Mol. Dev. Evol.)
Modules in the Ocular Skeleton
Applying the concept of modularity to understand the evolu-
tionary history of complex structures or organisms has proved
useful in many systems (e.g. limbs: Raff, 96; fins: Mabee
et al., 2002; cavefish: Franz-Odendaal and Hall, 2006b; skulls:
Schoch, 2006, etc). A module is a functional, morphological, or
morphogenetic unit of an organism and is the cellular resource
for developmental construction and evolutionary variability
(Atchley and Hall, 91; Raff, 96; Gass and Bolker, 2003; Gass
and Hall, 2008). Modules are hierarchical and as such can have
modules nested within them. They are also dynamic and may
undergo modifications and/or transformations (including dupli-
cation and divergence). Here, I consider developmental modules,
which have a unique and intrinsic set of patterning mechanisms
(Hall, 2005). Similar to the manner in which populations of cells
can subdivide, so to can modules (Raff, 96). These new modules
are integrated and able to interact with other modules (Atchley
and Hall, 91; Gass and Bolker, 2003; Franz-Odendaal and Hall,
2006b). Recently, Gass and Hall (2008) provided a detailed and
thoughtful discussion on multicellular modules and concluded
that each of the four subpopulations of the neural crest cells (i.e.
cranial, cardiac, trunk, and vagal/sacral) can be considered as
four separate modules.
A hypothesis: Following this, one can consider the neural
crest population that migrates into the eye region (specifically
into the periocular mesenchyme) as a developmental module. At
some point during evolution, this population of cells or this
module subdivided into two modules that could evolve
independently and at different rates to give rise to the scleral
cartilage and the scleral ossicle components we see today (Fig. 4).
One module was positioned posteriorly in the eye and became the
scleral cartilage (the endoskeletal component) and the other was
positioned more anteriorly and developed directly into dermal
bone (the exoskeletal component). Although these two modules
were uncoupled in the past, they are once again closely
associated in some extant forms (e.g. in reptiles). The alternative
hypothesis is that the neural crest population within the eye did
not subdivide, and that the two components of the ocular
skeleton we observe today evolved together and dependently.
Testing the Hypothesis
Extant sarcopterygians (incl. birds) have two distinct components
of the ocular skeletonthe scleral cartilage and the scleral ossicles.
These two components are morphologically, developmentally
(timing and induction), and perhaps functionally distinct. Both
the inductive epithelia and the timing of induction of the scleral
cartilage and the scleral ossicles are distinctly different from one
another (Franz-Odendaal and Hall, 2006a). In chickens, scleral
ossicles are induced by the conjunctival epithelium several days
after the scleral cartilage is induced by the retinal pigment
epithelium (Coulombre, 65; Newsome, 72; Franz-Odendaal,
2008a; Thompson et al., 2010). Both of these inductions involve
epithelial to mesenchymal signaling but their timing and inductive
tissues are distinct. Therefore, the latter hypothesis that the two
Figure 4. Schematic showing the cranial neural crest cell (NCC) modules within the eye. (A) Sarcopterygians. A single neural crest
submodule subdivides. One module evolves to form the scleral cartilage (endoskeletal component) and the other evolves into scleral ossicles
(i.e. bone via intramembranous ossification) (the exoskeletal component). These modules may be lost over the course of evolution.
(B) Actinopterygians. The single neural crest module subdivides into two modules. One module is lost, whereas the other evolves into an
endoskeletal element that may ossify in some teleosts. The ancestral neural crest module is the same module population of cells in A and B,
and is drawn separately in this schematic for clarity.
J. Exp. Zool. (Mol. Dev. Evol.)
modules evolved together and dependently is not supported by
data from the developmental biology field and can be rejected. The
alternative hypothesis that the two developmental modules
evolved independently is discussed below.
From an evolutionary perspective, one should consider these
two developmental modules as uncoupled with respect to
inducing epithelia and timing of induction, despite their close
association in extant forms today. Because these two modules
were likely uncoupled for millions of years, the more posterior
module (that gives rise to the endoskeletal component, the scleral
cartilage) could have evolved to respond to different epithelia (and
epithelial signals) and at different times compared with the more
anterior module (that gives rise to the exoskeletal scleral ossicles
or the sclerotic ring). This ability to respond to epithelia and to
then be induced is termed tissue competency and requires a
distinct change in the activated/inhibited genes. The paleontolo-
gical data suggest that the subdivision of the neural crest module
took place before 480440 million years ago (first appearance of
Astraspis and Arandaspida) and after the Cambrian when the
neural crest evolved (Donoghue et al., 2000, 2008).
The hypothesis that the two modules evolved independently is
further supported by data from extant sarcopterygians in which
some taxa have secondarily lost one module but maintained the
other (Walls, 63; Franz-Odendaal and Hall, 2006a) (Fig. 4A). For
example, snakes only have the endoskeletal module destined to
form scleral cartilage, and have lost the exoskeletal module destined
to form scleral ossicles. Other sarcopterygians, such as mammals,
have lost both modules and still others, such as birds, have retained
both modules. The mechanism for the complete loss of a module, or
population of cells, could be via programmed cell death (apoptosis)
in situations where the cells have become unresponsive to the
inducing tissues (i.e. lost their competency to respond to inducing
signals from the epithelium). Changing tissue competency is
considered to be a major force in the evolution of development
(Hall, 2000). Alternatively, the neural crest cells may have taken on
a new (unknown) non-skeletogenic function (neofunctionalisation)
after leaving the neural tube and before reaching their final
destination. Most importantly, to date no extant or fossil group has
retained the exoskeletal component (anterior module) and lost only
the endoskeletal component (posterior module).
Furthermore within sarcopterygians, the number of inductive
events and hence the number of scleral ossicles varies in different
taxa. Basal sarcopterygians, for example, had many more scleral
ossicles than living forms therefore the most parsimonious
explanation is that a reduction in the number of inductive events
within the anterior module has also taken place over the course
of evolution (Franz-Odendaal and Hall, 2006a). Epigenetic factors
that influence condensation sizes and boundaries and hence the
shape of skeletal elements (Hall and Miyake, 2000; Franz-
Odendaal, 2011) likely also evolved and changed at this time.
Consequently, with the ancestral neural crest module subdivid-
ing early in vertebrate evolution, basal actinopterygians would also
have had two neural crest-derived modules present within their
eyes. Teleost scleral ossicles develop via scleral cartilage replace-
ment (Franz-Odendaal et al., 2007) and these elements are
endoskeletal (discussed above). Following this logic, the more
posterior neural crest module persisted within teleosts while the
anterior module did not evolve further and was probably lost
before teleost evolution (via apoptosis or neofunctionalisation, as
described above) (Fig. 4B). Having lost the anterior module (which
had the potential to directly ossify) teleosts have succeeded in
ossifying the more posterior endoskeletal component perhaps as
functional demands required. To date, there is no evidence of
dermal scleral ossicles arising as an atavistic structure within
Teleostei. Interestingly, in the sister group to Osteichthyes, we have
observed ossified plates (tesserae) within the scleral cartilage of
several extant sharks (Pilgrim and Franz-Odendaal, 2009) and have
documented sclerotic rings in fossil Chondrichthyes (Pilgrim and
Franz-Odendaal, 2009). These findings suggest that Chondrichthyes
independently evolved a mechanism to strengthen their scleral
tissue; these mechanism(s) warrant further investigation.
From the evidence presented above, the scleral ossicles in
sarcoptergyians and the scleral ossicles in actinopterygians
cannot be homologous (one is exoskeletal and one is endoske-
letal). The scleral cartilage elements in each group (and possibly
all vertebrates) are likely to be homologous since both are derived
from the posterior module and share a common neural crest
origin. Although we do not know the induction mechanism in
each case, it is generally accepted that developmental processes
themselves can evolve (Hall, 99). In chicken embryos, the retinal
pigmented epithelium (RPE) has been shown to regulate the
development of the scleral cartilage (Thompson et al., 2010) and
these authors suggest that the RPE might direct fate choices
within the neural crest-derived sclera. In addition, this group
suggest an intriguing link between the development of pigmen-
tation in the RPE and cartilage differentiation in the sclera
(Thompson et al., 2010). In mouse embryos, Pitx2 is necessary to
specify the fate of the neural crest-derived corneal endothelium,
corneal stroma, and sclera (Evans and Gage, 2005) and its
expression is induced by retinoic acid from the optic cup (Gage
and Zacharias, 2009; Kumar and Duester, 2010). Pitx2 is also
required for the development of ocular blood vessels, which are
critical for the formation of chondro- and osteogenic condensa-
tions (Evans and Gage, 2005). Another gene, Indian hedgehog
(from blood vessels) has recently been shown to be required for
the development of the sclera and the RPE in mouse embryos
(Dakubo et al., 2008). Furthermore, recent findings in humans
and rats have shown that the mammalian sclera has retained the
ability to calcify or form cartilage (but not bone) in pathological
situations or in response to aging (OSteen and Brodish 90; Seko
et al., 2008). The above findings point to a shared mechanism of
scleral cartilage induction among vertebrates.
If the homology of the scleral cartilage across all vertebrates is
accepted, then the different shapes of the scleral cartilage
SCLERAL OSSICLE EVOLUTION 399
J. Exp. Zool. (Mol. Dev. Evol.)
(cartilage cup vs. cartilage ring) might simply reflect different
expression patterns of cartilage inhibitory molecules or different
inductive potentials of the RPE (Thompson et al., 2010).
The different mechanisms by which vertebrates have suc-
ceeded in strengthening the ocular skeleton (e.g. birds: evolved a
separate strengthening tissue, namely the sclerotic ring; sharks:
evolved tesserae on their cartilage; fish: evolved a mechanism for
perichondral ossification of the scleral cartilage) might also
reflect evolutionary convergence.
SUMMARY AND CONCLUSIONSThe findings presented above support our previous hypothesis that
the scleral ossicles of teleosts are not homologous to the scleral
ossicles of reptiles (Franz-Odendaal and Hall, 2006a). In addition,
it further suggests that the scleral cartilage (the endoskeletal
component of the eye) of all gnathostomes is homologous.
The paleontological data place the earliest origin of the ocular
skeleton to the Ordovician. Furthermore, research on the origin of
the neural crest indicates that neural crest specifiers were present at
this time. The developmental data conclude that the ocular skeleton
is neural crest derived and that the endoskeletal and exoskeletal
components of the ocular skeleton evolved independently. In
extant reptiles, which have both exoskeletal scleral ossicles and
endoskeletal scleral cartilage, these two independently evolving
components have been reassociated with one another anatomically.
Therefore considering this data, it is likely that the population
of neural crest cells that migrates to the periocular mesenchyme
surrounding the eye subdivided during vertebrate evolution and
subsequently evolved independently into two distinct compo-
nents. This subdivision occurred sometime shortly after the
evolution of dentine and bone since the oldest known fossil
evidence of the ocular skeleton dates to Ordovician 480440
million years ago. This early subdivision made it possible for the
modules to evolve independently into the diverse ocular
skeletons we see today. In addition, since there is evidence in
the fossil record for the presence of an ocular endoskeletal
component alone (without the exoskeletal component) and since
the primordial pigmented epithelium (that induces the scleral
cartilage) evolved before the conjunctival epithelium (Lamb et al.,
2007), it is highly probable that the endoskeletal component
within the eye was established before the exoskeletal component.
In conclusion, one should consider that the components of the
ocular skeleton (cartilage and bone) likely evolved independently
from the neural crest and that each component was patterned and
induced by different tissues. It is especially important when
character coding the ocular skeleton of fossil vertebrates that
accurate terminology is used to describe this region of the skeleton.
The problems that arise with inadequate documentation of known
fossils was recently raised by Friedman and Brazeau (2010). The
application of concepts such as modularity to understanding
complex systems provides us with novel insight into their
evolution; this insight is not immediately apparent when examin-
ing either the paleontological or developmental literature alone.
ACKNOWLEDGMENTSThe author thanks the Natural Science and Engineering Research
Council of Canada (TFO, Discovery Grant) for funding this research
and Mount Saint Vincent University who provided a student
assistantship to Jonathon Sproul (MSVU) to collate the fossil data.
I extend my thanks to Kathryn Knorr (MSVU) for translating the
Edinger (1929) text from German into English. I am also extremely
grateful to Brian Hall (Dalhousie University, Canada) for
encouragement with this manuscript and for insightful comments.
I also thank M. I. Coates, M. Laubichler, and P. Donoghue for
reading earlier drafts of this manuscript. Comments from
anonymous reviewers were very valuable and greatly appreciated.
LITERATURE CITEDAtchley WR, Hall BK. 1991. A model for development and evolution of
complex morphological structures. Biol Rev Camb Philos Soc 66:
Burrow CJ, Jones AS, Young GC. 2005. X-ray microtomography of 410
million year-old optic capsules from placoderm fishes. Micron 36:
Burrow CJ, Newman MJ, Davidson RG, Den Blaauwen JL. 2011.
Sclerotic plates or circumorbital bones in early jawed fishes?
Cloutier R, Ahlberg PE. 1996. Morphology, characters, and inter-
relationships of basal sarcopterygians. In: Stiassny MLJ, Parenti LR,
Johnson GD, editors. Interrelationships of fishes. San Diego, London:
Academic Press. p 445479.
Coulombre AJ. 1965. The eye. In: De Haan RL, Ursprung H, editors.
Organogenesis. New York: Holt. p 219251.
Couly GF, Coltey PM, Le Douarin NM. 1993. The triple origin of skull in
higher vertebrates: a study in quail-chick chimeras. Development
Dakubo GD, Mazerolle C, Furimsky M, Yu C, St-Jaques B, McMahon A,
Wallace VA. 2008. Indian hedgehog signaling from endothelial cells
is required for sclera and retinal pigment epithelium development
in the mouse eye. Dev Biol 320:242255.
de Beer GR. 1937. The development of the vertebrate skull. Chicago:
University of Chicago Press.
Donoghue PCJ, Forey PL, Aldridge RJ. 2000. Conodont affinity and
chordate phylogeny. Biol Rev 75:191251.
Donoghue PCJ, Graham A, Kelsh RN. 2008. The origin and evolution of
the neural crest. BioEssays 30:530541.
Edinger T. 1929. Uber knocherne Scleralringe. Zool Jahrb 51:163226.
Evans AL, Gage PJ. 2005. Expression of the homeobox gene Pitx2 in
neural crest is required for optic stalk and ocular anterior segment
development. Hum Mol Genet 14:33473359.
J. Exp. Zool. (Mol. Dev. Evol.)
Franz-Odendaal TA. 2008a. Towards understanding the development
of scleral ossicles in the chicken, Gallus gallus. Dev Dyn 237:
Franz-Odendaal TA. 2008b. The scleral ossicles of Teleostei: evolu-
tionary and developmental trends. Anat Rec 291:161168.
Franz-Odendaal TA. 2011. Epigenetics in bone and cartilage
development. In: Hallgrmsson B, Hall BK, editors. Epigenetics:
linking genotype and phenotype in development and evolution.
San Francisco: University of California Press.
Franz-Odendaal TA, Hall BK. 2006a Skeletal elements within teleost
eyes and a discussion of their homology. J Morphol 267:13261337.
Franz-Odendaal TA, Hall BK. 2006b. Modularity and sense organs in
the blind cavefish, Astyanax mexicanus. Evol Dev 8:94100.
Franz-Odendaal TA, Vickaryous MK. 2006. Skeletal elements in the
vertebrate eye and adnexa: morphological and developmental
perspectives. Dev Dyn 235:12441255.
Franz-Odendaal T, Ryan K, Hall B. 2007. Developmental and
morphological variation in the teleost craniofacial skeleton reveals
an unusual mode of ossification. J Exp Zool (Mol Dev Evol) 308B:
Friedman M, Brazeau MD. 2010. A reappraisal of the origin and basal
radiation of the Osteichthyes. J Vertebr Paleontol 30:3656.
Gage PJ, Zacharias AL. 2009. Signaling cross-talk is integrated by
transcription factors in the development of the anterior segment in
the eye. Dev Dyn 238:21492162.
Gagnier P-Y. 1993. Sacabambaspis janvieri, vertebre ordovician de
bolivie: I: analyse morphologique. Ann Paleontol 79:1951.
Gagnier P-Y. 1996. Early Devonian acanthodians from northern
Canada. Paleontology 39:241258.
Gass GL, Bolker JA. 2003. Modularity. In: Hall BK, Olson WM, editors.
Keywords and concepts in evolutionary developmental biology.
Cambridge: Harvard University Press. p 260267.
Gass GL, Hall BK. 2008. Modularity and cell sociology. In: Stephens C,
Matthen M, editors. Handbook of the philosophy of biology.
Gess R, Coates MI, Rubidge BS. 2006. A lamprey from the Devonian
period of South Africa. Nature 443:981984.
Hall BK. 1999. Evolutionary developmental biology, 2nd edition. The
Netherlands: Kluwer Academic Publishers.
Hall BK. 2000. The neural crest as a fourth germ layer and vertebrates
as quadroblastic not triploblastic. Evol Dev 2:13.
Hall BK. 2005. Bones and cartilage. Developmental and evolutionary
skeletal biology. London: Elsevier.
Hall BK, Miyake T. 2000. All for one and one for all: condensations and
the initiation of skeletal development. BioEssays 22:138147.
Janvier P. 1996. Early vertebrates. Oxford: Oxford University Press.
Kumar S, Duester G. 2010. Retinoic acid signaling perioptic
mesenchyme represses Wnt signaling via induction of Pitx2 and
Dkk2. Dev Biol 340:6774.
Lamb T, Collin S, Pugh Jr E. 2007. Evolution of the vertebrate eye:
opsins, photoreceptors, retina and eye cup. Nat Rev Neurol 8:960.
Luksevics ER, Vin S. 2001. The orbito-nasal area of Asterolepis ornata,
a middle Devonian placoderm fish. J Vert Paleontol 21:687692.
Lund R. 2000. The new Actinopterygian order Guildayuchthyiformes
from the lower Carboniferous of Montana (USA). Geodiversitas 22:
Mabee PM, Crotwell PL, Bird NC, Burke AC. 2002. Evolution of median
fin modules in the axial skeleton of fishes. J Exp Zool (Mol Dev Evol)
Maddison DR, Schulz K-S, editors. 2007. The tree of life web project.
Available at: http://tolweb.org.
Maisey JG. 1986. Heads and tails: a chordate phylogeny. Cladistics 2:
Moy-Smith JA, Miles RS. 1971. Palaeozoic fishes. Philadelphia:
WB Saunders Co.
Newsome DA. 1972. Cartilage induction by retinal pigmented
epithelium of chick embryos. Dev Biol 27:575579.
OSteen WK, Brodish A. 1990. Scleral calcification and photoreceptor
cell death during aging and exposure to chronic stress. Am J Anat
Pilgrim BL, Franz-Odendaal TA. 2009. A comparative study of the
ocular skeleton of fossil and modern chondrichthyes. J Anat 214:
Raff RA. 1996. The shape of life. genes, development, and the
evolution of animal form. Chicago: The University of Chicago Press.
Schoch RR. 2006. Skull ontogeny: developmental patterns of fishes
conserved across major tetrapod clades. Evol Dev 8:524536.
Seko Y, Azuma N, Takahashi Y, Makino H, Morito T, Muneta T,
Matsumoto K, Saito H, Sekiya I, Umezawa A. 2008. Human sclera
maintains common characteristics with cartilage throughout
evolution. PLoS One 3: e3709. DOI:10.1371/journal.pone.0003709.
Smith MM, Hall BK. 1990. Development and evolutionary origins of
vertebrate skeletogenic and odontogenic tissues. Biol Rev 65:
Stensio EA. 1950. La cavite labyrinthique, lossification sclerotique
et lorbite de Jagorina. In: George A, editor. Paleontologie et
Transformisme. Paris: Albin Michel. p 943.
Thompson H, Griffiths JS, Jeffery G, McGonnell IM. 2010. The retinal
pigment epithelium of the eye regulates the development of scleral
cartilage. Dev Biol 347:4032.
Underwood G. 1970. The eEye. In: Gans C, editor. Biology of the
reptilia. vol. 2. London, New York: Academic Press. p 198.
Walls GL. 1963. The vertebrate eye and its adaptive radiation.
New York: Hafner Publishing Group.
Watson TS. 1937. The acanthodian fishes. Philos Trans R Soc Lond B
Biol Sci 229:49146.
Zhu M, Yu X, Janvier P. 1999. A primitive fossil fish sheds light on the
origin of bony fishes. Nature 397:607610.
SCLERAL OSSICLE EVOLUTION 401
J. Exp. Zool. (Mol. Dev. Evol.)