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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.) 316:393–401, 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.) 316:393–401.

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

Hall, 2006a).

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

2011

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.

E-mail: [email protected]

ABSTRACT

J. Exp. Zool.(Mol. Dev. Evol.)316:393–401, 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.

FRANZ-ODENDAAL394

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


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 480–440 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.

1 5 presence, 0 5 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).

FRANZ-ODENDAAL396


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

endoskeletal capsule

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),

Janvier (’96)

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

Stensio (’50)



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 skeleton—the 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.

FRANZ-ODENDAAL398


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 480–440 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 (O’Steen 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



(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 480–440

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.

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